Linking species traits and demography to explain complex temperature responses across levels of organization

Microbial communities regulate ecosystem responses to climate change. However, predicting these responses is challenging because of complex interactions among processes at multiple levels of organization. Organismal traits that determine individual performance and ecological interactions are essential for scaling up environmental responses from individuals to ecosystems. We combine protist microcosm experiments and mathematical models to show that key traits—cell size, shape, and contents—each explain different aspects of species’ demographic responses to changes in temperature. These differences in species’ temperature responses have complex cascading effects across levels of organization—causing nonlinear shifts in total community respiration rates across temperatures via coordinated changes in community composition, equilibrium densities, and community–mean species mass in experimental protist communities that tightly match theoretical predictions. Our results suggest that traits explain variation in population growth, and together, these two factors scale up to influence community- and ecosystem-level processes across temperatures. Connecting the multilevel microbial processes that ultimately influence climate in this way will help refine predictions about complex ecosystem–climate feedbacks and the pace of climate change itself.

Climate regulates the organization, function, and dynamics of ecosystems (1, 2), yet predicting ecosystem responses to rapid environmental change remains a major challenge in ecology (3–5). This is partly due to the complexity of ecological systems, which involve processes at multiple levels of organization, from individuals to ecosystems (6). Forecasting ecosystem responses to climate change therefore hinges on understanding how novel environmental conditions influence processes at each level and how these simultaneous responses are linked across levels (2, 3, 7, 8).The processes that structure populations, communities, and ecosystems are ultimately determined by interactions between individual organisms and their biotic and abiotic environment (6, 7). Through their effects on individual performance, functional traits can influence population-, community-, and ecosystem-level properties like species presence and density, total biomass, species and functional diversity, primary productivity, and nutrient cycling (9–14). For example, it is well known that body size controls individual metabolic rates (15) and may interact with temperature (16–19) to influence population-level demographic characteristics like intrinsic growth rates and carrying capacities (19–21). At the community level, trait variation within and among species can influence competitive outcomes (22–24) and the strength and occurrence of trophic interactions (24–28), thus affecting community composition and dynamics. Therefore, traits are central to linking processes across levels of organization and predicting complex ecosystem responses to environmental variation (9, 10, 12). However, it is less clear how to truly scale up the effects of traits to predict their influence on processes at higher organizational levels, especially under climate change (9, 10, 12, 14, 29).Using traits to mechanistically link environmental conditions to ecological processes across levels of organization has been hailed as the “holy grail” of ecology (9, 30, 31). However, establishing these links empirically is remarkably challenging for multiple reasons. The main challenges are to determine 1) which trait—or combination of traits (including trade-offs)—is the most important driver of variation for each ecological process and 2) how these traits connect ecological responses to environmental change at multiple levels of organization. So, relevant functional traits must first be accurately quantified at the individual level. Trait variation must then be linked to variation in the demographic rates that determine population dynamics. Next, these responses must be considered in a community context to evaluate how trait-driven demographic variation affects the taxonomic and functional composition, species interactions, and dynamics of communities and their associated ecosystem consequences. Finally, all of these patterns—trait-driven shifts in species densities, community structure, and ecosystem functioning—must be characterized across environmental conditions, which is difficult or infeasible in most systems (32, 33).Microbial communities are key drivers of ecosystem responses to climate change (34–36) that also provide an opportunity to study environmental effects across levels of organization comprehensively in controlled laboratory conditions (32, 33, 37, 38). Indeed, microbial decomposers significantly influence nutrient flux and the global carbon cycle that ultimately determine the pace of climate change (36, 39). For example, bacteria and fungi store 41 times more carbon than the entire animal kingdom (40), while soil prokaryotic respiration alone releases 98 Pg ⋅ C ⋅ yr⁻¹ (41), representing one of the largest sources of atmospheric carbon emissions (42), which is expected to rise with global warming (43). The principal consumers of these microbial decomposers worldwide are a group of single-celled eukaryotes collectively known as protists (44, 45), which account for twice as much biomass as the entire animal kingdom globally (40). Predation by protists depresses microbial biomass, thus controlling total microbial respiration rates and, consequently, global carbon sequestration and nutrient flux (45–48). However, how this important biotic control on global ecosystem functioning may respond to rising temperatures is poorly understood (49). Protists can be studied in great detail in the laboratory and have proven to be a valuable tool for scaling up from individual species to study community- and ecosystem-level processes across environments (32, 49–54). Protists therefore provide a unique opportunity to understand the mechanisms connecting ecological processes across levels of organization while also informing how ongoing climate change may influence global nutrient cycling.Here, we combine laboratory experiments and mathematical modeling to examine how multiple protist traits jointly influence population-, community-, and ecosystem-level responses to temperature. We study 14 protist species that commonly cooccur in nature (55), span several orders of magnitude in body size, and play a variety of functional roles within microbial communities (producers, bacterivores, detritivores, grazers, and intraguild predators) (49, 55). Specifically, we ask, do protist traits inform how they will respond to changes in temperature at the population, community, and ecosystem levels? To answer this question, we measure key traits (Fig. 1) that are known to influence performance (15, 56–61) in source populations—hence prior to experimental manipulation—and then quantify population-, community-, and ecosystem-level responses to a range of temperatures. We find that body size, shape, and cellular contents are strongly, but distinctly, related to temperature-driven shifts in species demographic parameters controlling population growth and species interactions. We show that these differences in the temperature dependence of population demography scale up to determine how equilibrium densities, community network structure, species richness, and total system respiration rates change across temperatures in both theoretical and experimental communities. Our results show how links between multiple species traits and demographic parameters produce complex ecological responses to temperature, thus providing insights into how whole ecosystems might respond to a rapidly changing climate.Open in a separate windowFig. 1.Conceptual diagram showing traits and demographic characteristics of species (see

Morphological ghosts of introgression in Darwin’s finch populations

Many species of plants, animals, and microorganisms exchange genes well after the point of evolutionary divergence at which taxonomists recognize them as species. Genomes contain signatures of past gene exchange and, in some cases, they reveal a legacy of lineages that no longer exist. But genomic data are not available for many organisms, and particularly problematic for reconstructing and interpreting evolutionary history are communities that have been depleted by extinctions. For these, morphology may substitute for genes, as exemplified by the history of Darwin’s finches on the Galápagos islands of Floreana and San Cristóbal. Darwin and companions collected seven specimens of a uniquely large form of Geospiza magnirostris in 1835. The populations became extinct in the next few decades, partly due to destruction of Opuntia cactus by introduced goats, whereas Geospiza fortis has persisted to the present. We used measurements of large samples of G. fortis collected for museums in the period 1891 to 1906 to test for unusually large variances and skewed distributions of beak and body size resulting from introgression. We found strong evidence of hybridization on Floreana but not on San Cristóbal. The skew is in the direction of the absent G. magnirostris. We estimate introgression influenced 6% of the frequency distribution that was eroded by selection after G. magnirostris became extinct on these islands. The genetic residuum of an extinct species in an extant one has implications for its future evolution, as well as for a conservation program of reintroductions in extinction-depleted communities.

The classic, cladistic, view of the origin of biological diversity is a series of bifurcating processes with the products, species, remaining distinct as a result of genetic, behavioral, ecological, or geographical barriers to gene exchange (1, 2). Modern genomic data have necessitated a replacement of this view with a concept of networks in which lineages diverge but nonetheless exchange genes, especially in the early stages of diversification (3–10). Genomic data not only contain signatures of past gene exchange (9, 11–13)—the ghosts of introgression past—in some cases they reveal a legacy of lineages that no longer exist, for example in the phylogenies of bonobos (14, 15), dogs (16), cats (17), birds (18) and Homo sapiens (13). Persistence of introgressed genes for long periods of time implies either a slow rate of loss through random processes or selective retention (9, 19–25). The more genomic analyses are carried out, and the more refined they become, the more such “missing” history will be revealed, including our own (26). Studies of organisms for which fossils do not exist will profit the most.Can hybridization in the past be detected in the absence of genomic data? The question is important to ask because genomic data are not available for many organisms, such as rare, endangered, and protected species and those living in remote regions. Moreover, gene exchange may be difficult to detect between weakly differentiated species (27). Morphology may provide an answer. The signs of introgressive hybridization can be identified in the frequency distributions of continuously varying heritable traits (28–30). Hybrids are expected to be approximately intermediate between the parental species in body size, appendage size, and the size of trophic traits (but see ref. 31), and by back-crossing to one of the parental species they contribute to the proximal half of the frequency distribution. The result is a broader distribution of trait values of the recipient population that is skewed toward the donor population. If back-crossing is bidirectional, the frequency distributions of the two species should be skewed toward each other.Island populations of birds are good candidates to search for morphological evidence of past introgressive hybridization. Populations are often small and fluctuate in size, sex ratios are occasionally unbalanced, conspecific mates are then relatively scarce, and hybridization with related species may ensue (32–40). Darwin’s finches in the Galápagos archipelago are particularly suitable because there are many populations that vary in size. Indeed, introgressive hybridization is known from long-term field studies of individually marked birds (38, 41–47), and inferred from genetic data in other studies (48–50). In an earlier study we suggested that introgressive hybridization might occur when the population of one of two or more related species declines toward extinction, leaving a signature in the morphology of the surviving species (51). Geospiza fortis and Geospiza magnirostris on the southern islands of Floreana and San Cristóbal are an exemplary pair of species for testing this proposal. In 1835, Darwin, Fitzroy, and assistants collected seven specimens of a uniquely large form of G. magnirostris, five of them from Floreana, one from San Cristóbal, and the other probably from San Cristóbal (52). The populations became extinct, unobserved, in the next few decades, whereas G. fortis has persisted on both islands to the present. In clarifying the island of origin of each of the large specimens, Sulloway (52) assigned two other and much smaller specimens to San Cristóbal: one definitely and the other possibly to that island (S1 Appendix, section 1). Sulloway suggested one might be a hybrid between G. fortis and G. magnirostris, but did not comment on the other. We have since learned from a study of fossils that the large form of G. magnirostris was abundant on Floreana prior to human settlement in 1832 (53). San Cristóbal has a similar history of human settlement, introduction of goats, and habitat destruction (54, 55), but there are no reports of fossils.Thousands of specimens of Darwin’s finches were collected for museums after Darwin’s visit, more than 95% of them in the period 1888 to 1906 and most of the remainder afterward. All specimens of the ground finch genus Geospiza were measured and compared in a previous study (56). Included among them were almost 500 specimens of G. fortis from Floreana and close to 200 from San Cristóbal. Here we use the measurements to test for effects of introgression on the skewness of beak size and body size frequency distributions. To place the results in context, we compare these two populations with conspecific populations on other islands (44, 57), and large members of the population are genetically intermediate between small members and G. magnirostris (45). Lack of distinctiveness is also present in the frequency distributions on Santiago and Isabela. Pinzón and Seymour have suffered considerable habitat damage from introduced goats (54, 55), leading to the probable extinction of G. magnirostris. In view of uncertainty over the status of G. magnirostris, we have added G. fortis from these islands to the group of G. fortis populations known or suspected to have hybridized.Table 1.Occurrence of Geospiza fortis and G. magnirostris on Galápagos islands, and known or suspected hybridization

Pliocene reversal of late Neogene aridification

The Pliocene epoch (5.3–2.6 Ma) represents the most recent geological interval in which global temperatures were several degrees warmer than today and is therefore considered our best analog for a future anthropogenic greenhouse world. However, our understanding of Pliocene climates is limited by poor age control on existing terrestrial climate archives, especially in the Southern Hemisphere, and by persistent disagreement between paleo-data and models concerning the magnitude of regional warming and/or wetting that occurred in response to increased greenhouse forcing. To address these problems, here we document the evolution of Southern Hemisphere hydroclimate from the latest Miocene to the middle Pliocene using radiometrically-dated fossil pollen records preserved in speleothems from semiarid southern Australia. These data reveal an abrupt onset of warm and wet climates early within the Pliocene, driving complete biome turnover. Pliocene warmth thus clearly represents a discrete interval which reversed a long-term trend of late Neogene cooling and aridification, rather than being simply the most recent period of greater-than-modern warmth within a continuously cooling trajectory. These findings demonstrate the importance of high-resolution chronologies to accompany paleoclimate data and also highlight the question of what initiated the sustained interval of Pliocene warmth.Our knowledge of Pliocene climates is based predominantly on the rich marine sediment record (1), but understanding of Pliocene climates on land remains limited because the few existing terrestrial archives tend to have poor age control and are of short duration. This deficiency is no more evident than in paleovegetation records, which are integral to modeling Pliocene climates because vegetation is both a critical indicator of regional precipitation and also makes a large contribution to planetary albedo (2, 3). Several syntheses of Pliocene vegetation have been compiled (3, 4), but their value is hampered by substantial uncertainty surrounding the synchroneity of the records. For example, vegetation syntheses have focused on the Late Pliocene (the Piacenzian Age, 3.6–2.6 Ma) because this period is considered likely to be a closer biological and geological analog for future warming than the Early Pliocene (1, 5). However, only 6 of 32 Southern Hemisphere records interpreted by Salzmann et al. (4) as documenting the nature of Late Pliocene vegetation are both based on plant fossils and can confidently be assigned to the Late Pliocene; the remaining records have such poor chronologies that their possible ages range from Late Miocene to Early Pleistocene, or the records only infer the nature of vegetation indirectly from geomorphology or vertebrate fossils (SI Appendix, Table S1). As a result, current understanding of the response of Southern Hemisphere vegetation to Late Pliocene climates (2–4) may conflate the climate and vegetation history of ≥5 My of the late Cenozoic (Fig. 1), an interval that is characterized by global cooling (6) and, in subtropical- to midlatitudes, increasing aridity (7–10). This uncertainty is problematic for two reasons. First, it has become clear that the peak of Pliocene warmth globally was not generally within the Late Pliocene but occurred earlier, within the Early Pliocene (11). Second, largely because of a lack of continuous and well-dated records, the relationship between the longer-term cooling/aridification trend and Pliocene warmth remains unclear. Thus, was Pliocene warmth a discrete interruption of late Cenozoic cooling/aridification trends (6), or was the Pliocene merely an interval immediately preceding the abrupt steepening of these trends associated with the onset of extensive Northern Hemisphere glaciation (12, 13)?Open in a separate windowFig. 1.Conservative estimates of the age ranges of Southern Hemisphere vegetation records accepted by Salzmann et al. (3) as indicative of Late Pliocene (Piacenzian, 2.6–3.6 Ma) terrestrial vegetation. Sample code numbers are those used by Salzmann et al. Colors represent record type (pollen, wood, vertebrate, sediment). Bold colors indicate records clearly falling within the Late Pliocene, and faint colors indicate records either falling outside of the Late Pliocene or with broader age ranges. Of the 32 records, only 6 based on plant fossil data can be confidently assigned a Late Pliocene age. For Makapan, two age estimates are provided, reflecting uncertainty whether the record can be attributed to the Pliocene as a whole or to the Late Pliocene.To place the temporal evolution of Southern Hemisphere Pliocene vegetation and climate on a firmer chronological footing, we generated fossil pollen records from radiometrically dated speleothems (secondary cave carbonate deposits such as stalagmites and flowstones) from southern Australia. Pollen assemblages were extracted from samples collected in five caves on the Nullarbor Plain (Fig. 2 and SI Appendix, Fig. S1), a large (200,000 km²) karst province uplifted above sea level during the late Miocene (14). Consistent with its position in Southern Hemisphere subtropical latitudes, the Nullarbor Plain is currently semiarid, receiving mean annual precipitation (MAP) of ca. 180–270 mm (SI Appendix, Fig. S1), with a weak winter-maximum. Mean annual temperature is ∼18 °C. The vegetation is largely treeless chenopod shrubland, grading coastward into sparse, low open woodlands dominated by Acacia (Mimosaceae) or Eucalyptus (Myrtaceae). Nullarbor speleothems grew during the late Neogene (15) but negligible calcite speleothem growth occurs today. Recent development and refinement of the uranium-lead (U-Pb) chronometer has allowed high-precision geochronology of such ancient speleothem samples (15–18). Our fossil pollen record is composed of 13 polleniferous samples (out of 81 explored for pollen), the oldest dated at 5.59 ± 0.15 Ma, in the latest Miocene, and the youngest 0.41 ± 0.07 Ma, in the Middle Pleistocene (Open in a separate windowFig. 2.Locality map showing Nullarbor caves in southern Australia and sites mentioned in the text. The map was produced using Ocean Data View (odv.awi.de).

Table 1.

Age and pollen yield of Nullarbor speleothems

Resource colimitation governs plant community responses to altered precipitation

Ecological theory and evidence suggest that plant community biomass and composition may often be jointly controlled by climatic water availability and soil nutrient supply. To the extent that such colimitation operates, alterations in water availability caused by climatic change may have relatively little effect on plant communities on nutrient-poor soils. We tested this prediction with a 5-y rainfall and nutrient manipulation in a semiarid annual grassland system with highly heterogeneous soil nutrient supplies. On nutrient-poor soils, rainfall addition alone had little impact, but rainfall and nutrient addition synergized to cause large increases in biomass, declines in diversity, and near-complete species turnover. Plant species with resource-conservative functional traits (low specific leaf area, short stature) were replaced by species with resource-acquisitive functional traits (high specific leaf area, tall stature). On nutrient-rich soils, in contrast, rainfall addition alone caused substantial increases in biomass, whereas fertilization had little effect. Our results highlight that multiple resource limitation is a critical aspect when predicting the relative vulnerability of natural communities to climatically induced compositional change and diversity loss.Current and predicted climatic changes are expected to considerably alter the water balance experienced by terrestrial ecosystems. Climate change can lead to increases or decreases in mean annual rainfall, shifts in seasonal and annual rainfall variability, changes in the frequency and magnitude of extreme precipitation events, shifts from snow to rain, declining snowpack, and temperature-driven increases in the climatic water deficit (1–3). These water-related changes are expected to exert dramatic impacts on the primary productivity, species composition, trophic relationships, diversity, and ecosystem functioning of natural communities (4–8), especially in arid and semiarid ecosystems (9–11). Water-related climatic changes are expected to outweigh the direct effects of increased temperatures on many natural communities (12). Despite the pervasiveness of the projected ecological impacts of changed water availability, very little is known about the factors that make some natural communities more vulnerable or resistant than others (13, 14). An important step toward improving downscaled forecasts of climate change impacts on natural communities is to test explicit, theory-based predictions about the effects of altered water availability.Because water is a resource for plants, the concept of limiting resources is a potentially important principle for making successful predictions about altered water availability. Classically, “Liebig’s law of the minimum” suggests that plant productivity is limited by the single resource that is in scarcest supply relative to demand (15). This theory was developed for agricultural systems, and although its simple logic is appealing, its appropriateness to complex natural communities and ecosystems has been questioned (16, 17). Growing theory and evidence suggest a newer principle, namely that multiple scarce resources may act simultaneously and synergistically to limit plant community productivity (17–21). Interactions among multiple limiting resources are much more commonly found in factorial resource addition experiments than predicted by Liebig’s law (17, 20, 22). For example, water availability alone may have very little impact on primary productivity if nutrients are in short supply (23–26). Multiple biochemical and physical mechanisms may underlie such resource interactions. For example, nutrient ion solubility and microbial mediation of nutrient cycling are tightly linked to water availability (27, 28), providing likely mechanisms for positive synergisms between water and nutrient supply.One potential implication of the theory of multiple limiting resources is that where water and nutrients are jointly limiting to community productivity and composition, a given change in climate may have the strongest effects on fertile soils and the weakest effects where soil fertility is low. A variety of evidence is consistent with this prediction (29). For example, effects of experimental warming and drought were lower in an infertile limestone grassland than in a fertile ex-cultivated grassland (13, 30); post-Pleistocene vegetation change was less pronounced on infertile peridotite than in forests on fertile granitic substrates (31); and in our study system, both experimental watering (25, 32) and ambient variation in annual precipitation (33, 34) had less effect on grasslands on serpentine soils than on more productive grasslands on sedimentary soils. If these contrasting plant community responses to climate are attributable to colimitation by water and nutrients, then several important implications follow. First, the endemic-rich plant communities found on nutrient-poor soils worldwide (35) may be relatively secure in the face of climate change. Second, communities on low-nutrient soils may be exceptionally vulnerable to biodiversity loss under the synergistic impacts of climate change and anthropogenic nutrient addition (17).Water and nutrient colimitation has yet to be tested as a cause for variable responses of natural communities to climate change. In conducting such a test, an additional factor that must be considered is the prevalence on unproductive soils of plant species with “resource-conservative” functional traits (e.g., short stature, low specific leaf area, and low tissue nitrogen concentration). Such traits confer tolerance to low nutrients at the cost of low maximal growth rates under resource-rich conditions (36–38). The prevalence of species with resource-conservative traits, rather than (or in addition to) nutrient limitation itself, may limit the responses of species and communities on infertile soils to altered water availability. Conversely, the dominance of species having the opposite (“resource-demanding,” “fast growing”) functional traits might render communities in fertile habitats more responsive to both water and nutrient addition. The theory of functional trait syndromes also enables predictions about how communities will change if nutrient and water addition coincides with the arrival of propagules of species with fast-growing functional traits. The expected result is a disproportionate loss of species with resource-conservative traits that are characteristic of unique endemic-rich floras of many low-nutrient substrates around the world (35, 39).In a 5-y field experiment, we used factorial additions of water and full-spectrum (macro- and micro) nutrients to test whether nutrient addition would render the most unproductive and diverse communities more sensitive to water, as predicted under resource colimitation. Alternatively, the responsiveness of these communities to water might remain constrained by the absence of species with “fast-growing” functional trait syndromes. Our experimental system is a semiarid annual grassland in which fertile sedimentary soils and infertile (N- and Ca-poor) serpentine soils are interspersed over short distances (Fig. S1). Previous work showed that water addition alone had little effect on grassland communities on the infertile soils (25, 32), whereas fertilization alone had stronger effects (40–42). In this study, we examined a gradient comprising three habitats: “harsh serpentine” grassland with coarse rocky soils, high native diversity, and very low biomass; “lush serpentine” grassland with fine-textured alluvial soils and intermediate biomass and species composition; and “nonserpentine” grassland with sedimentary soils and high biomass of mainly exotic species (Open in a separate windowFig. S1.Figure of 131 experimental plots which were distributed among multiple alternating areas of harsh and lush serpentine grassland and two areas of nonserpentine grassland within a roughly 12-ha site. Water was brought to the area by an irrigation system consisting of nine watering lines that passed through multiple patches of the three grassland habitats. Color codes: red, harsh serpentine grasslands; green, lush serpentine grasslands; blue, nonserpentine grasslands. C, control; F, fertilization; FW, fertilization and watering; W, watering.

Table S1.

Soil and plant community variables (means ± SE) illustrating differences among harsh, lush, and nonserpentine grassland habitats

Isotopic signals of summer denitrification in a northern hardwood forested catchment

Despite decades of measurements, the nitrogen balance of temperate forest catchments remains poorly understood. Atmospheric nitrogen deposition often greatly exceeds streamwater nitrogen losses; the fate of the remaining nitrogen is highly uncertain. Gaseous losses of nitrogen to denitrification are especially poorly documented and are often ignored. Here, we provide isotopic evidence (δ¹⁵N_NO3 and δ¹⁸O_NO3) from shallow groundwater at the Hubbard Brook Experimental Forest indicating extensive denitrification during midsummer, when transient, perched patches of saturation developed in hillslopes, with poor hydrological connectivity to the stream, while streamwater showed no isotopic evidence of denitrification. During small rain events, precipitation directly contributed up to 34% of streamwater nitrate, which was otherwise produced by nitrification. Together, these measurements reveal the importance of denitrification in hydrologically disconnected patches of shallow groundwater during midsummer as largely overlooked control points for nitrogen loss from temperate forest catchments.Many forested catchments export far less nitrogen (N) in streamwater than they receive in atmospheric deposition (1, 2). The rest of the deposited N may accumulate in vegetation or soil organic matter, or be lost in gaseous form. Losses of N to denitrification, the microbial reduction of aqueous nitrate (NO₃⁻) to nitrous oxide (N₂O, a greenhouse gas) and N₂ gas, are extremely difficult to measure due to the difficulty in directly measuring N₂ fluxes and due to the high degree of spatiotemporal variability in redox conditions and substrate sources (3). Many past studies using a range of measurements (streamwater nitrate isotopic composition, the acetylene block technique, N₂O emissions, and mass balance calculations) have concluded that denitrification in temperate forests is highly uncertain or generally unimportant (e.g., refs. 4–8).Nitrogen budgets are particularly perplexing in the northern hardwood forests at the Hubbard Brook Experimental Forest (HBEF) in the White Mountains of New Hampshire, USA, where atmospheric deposition has supplied 6–8 kg N ha⁻¹⋅yr⁻¹ for half a century, a rate ∼5–10 times preindustrial levels (7–10). Accumulation of N in plant biomass ceased in the early 1990s (10, 11), while streamwater inorganic N export from catchments across the HBEF and nearby streams decreased to <1 kg N ha⁻¹⋅yr⁻¹, for reasons that remain elusive (9, 10, 12). These N flux measurements imply increasingly important roles for N gas loss or storage in soil organic matter. However, both processes are so difficult to quantify that the fate, drivers, and consequences of the “missing” N remain unknown, at the HBEF and elsewhere (8–10, 12).Measurement of the dual isotopic composition of NO₃⁻ (δ¹⁵N_NO3 and δ¹⁸O_NO3) provides a powerful tool to identify NO₃⁻ sources and to infer its loss to denitrification (13–16). Values of δ¹⁸O_NO3 differ greatly between NO₃⁻ in precipitation and NO₃⁻ produced by nitrification (refs. 13–16, Table S1), which is the microbial oxidation of NH₄⁺ to NO₃⁻. Measurements of δ¹⁸O_NO3 have enabled detection of direct contributions of precipitation NO₃⁻ to streamwater (Table S1), especially during snowmelt, when catchments often release large quantities of NO₃⁻ (7, 8). However, past δ¹⁸O_NO3 measurements show that nitrification—not precipitation—supplies the vast majority of NO₃⁻ in streamwater at the HBEF (10, 17, 18) and other forested catchments (refs. 14 and 19, Table S1).Nitrate isotopic composition reflects not only NO₃⁻ sources but also fractionation from a range of processes (14, 20). During denitrification, heterotrophic microbes consume organic carbon using NO₃⁻ as an electron acceptor under low-oxygen conditions, in a 5:4 molar ratio of carbon:NO₃⁻. If NO₃⁻ is not replenished or consumed by other processes, denitrification progressively enriches both ¹⁸O and ¹⁵N in the residual NO₃⁻, with an O:N fractionation ratio of 0.4–0.7 in the field (14, 20, 21) and up to 1.0 in laboratory studies (22). The fractionation ratio is the slope of the relationship between δ¹⁸O_NO3 and δ¹⁵N_NO3. Dual isotopic enrichment and these enrichment ratios provide evidence of denitrification. Dual isotope analysis of NO₃⁻ has provided evidence for denitrification in large aquifers (e.g., ref. 20) and in drainage waters receiving heavy agricultural N loads (e.g., refs. 21 and 23), whereas recent catchment studies in a subtropical forest (15) and a warm Mediterranean grassland (24) have reported isotopic evidence of denitrification in soil or groundwater. However, dozens of past studies of stream δ¹⁸O_NO3 and δ¹⁵N_NO3 in naturally vegetated temperate and boreal catchments (refs. 14 and 19, Table S1), including the HBEF (10, 17), have revealed little if any isotopic evidence of denitrification.To investigate the role of denitrification at the HBEF, we measured NO₃⁻ isotopic composition throughout watershed 3 (WS3), a hydrologic reference catchment drained by Paradise Brook within the HBEF (Fig. 1), during the first two weeks of July 2011, close to the warmest part of the year (Fig. S1). Sampling encompassed nine shallow groundwater wells, a seep, and 19 stream sites along Paradise Brook and its tributaries. The shallow groundwater wells accessed water from saturated soil within the solum above the C horizon at depths between 30 and 115 cm. Three of the nine wells were close to (<2 m) or within the perennial stream channel; the other six were more distal (≥4 m) and upgradient from the perennial channel. Four rain events occurred during the sampling period (0.8–12.3 mm, 26.8 mm total); all contained NO₃⁻ and NH₄⁺ concentrations that exceeded those in streamwater and groundwater by an order of magnitude (Fig. 2 A and B). Nitrogen export over the study period amounted to 0.006 ± 0.003 kg N ha⁻¹, consisting of 24% NO₃⁻, 13% NH₄⁺, and 63% dissolved organic nitrogen (DON). Streamflow over the sampling period (5.3 mm) exported less than 2% of rainfall N input (0.335 ± 0.087 kg N ha⁻¹). The remaining 98% was retained within the catchment or lost via denitrification. If this 98% were denitrified in soil or shallow groundwater, it gives a maximum denitrification rate of 5.0 (3.6–6.4) kg N ha⁻¹ if extrapolated over the growing season. Although this figure represents the maximum loss of N to denitrification, recent extrapolations of N₂ and N₂O flux measurements from soil cores from the HBEF found denitrification rates during the growing season higher than previous estimates and equal to or higher than atmospheric deposition while follow-up measurements found rates ranging from 4–10 kg N ha⁻¹⋅y⁻¹ at HBEF (25).Open in a separate windowFig. 1.Location of HBEF in the northeast United States (Top Right), showing HBEF watersheds 1–9 (Bottom Right) and watershed 3 (WS3; Left). WS3 shows drainage network comprising Paradise Brook and tributary channels, with sampling locations from the weir (triangle), streams (filled circles), wells (empty circles; including wells ≥4 m from surface streamflow in July 2011 (JD05, JD17, JD18, JD19, JD29, JD30) and those <2 m (R12, east bank; R13 in-stream; R14, west bank) and a seep (dash). Contour interval is 3 m; elevation range is 537–732 m.

Table 1.

Concentrations of NO₃⁻, NH₄⁺, DON, and DOC (μM), and δ¹⁵N_NO3 and δ¹⁸O_NO3 of water samples from watershed 3, Hubbard Brook Experimental Forest, New Hampshire July 2011

The evolution of social parasitism in Formica ants revealed by a global phylogeny

Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 172 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed a global phylogeny of Formica ants. The genus originated in the Old World ∼30 Ma ago and dispersed multiple times to the New World and back. Within Formica, obligate dependent colony-founding behavior arose once from a facultatively polygynous common ancestor practicing independent and facultative dependent colony foundation. Temporary social parasitism likely preceded or arose concurrently with obligate dependent colony founding, and dulotic social parasitism evolved once within the obligate dependent colony-founding clade. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from a facultative parasitic background in socially polymorphic organisms. In contrast to permanently socially parasitic ants in other genera, the high parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.

The complex societies of eusocial insects are vulnerable to exploitation by social parasites that depend on their host colonies for survival and reproduction without contributing to colony maintenance and brood care (1–4). Social parasitism is common among eusocial Hymenoptera and evolved independently in distantly related lineages, including bees, wasps, and ants (3–8). Many studies on social parasitism have focused on the evolution of cooperation and conflict in colonies of eusocial insects and on coevolutionary arms race dynamics between hosts and parasites (9–12). However, the evolutionary origins of social parasitism and the coevolutionary factors causing speciation and thereby contributing to the high diversity of social parasite species in eusocial insects are not well understood (13, 14). Comparative evolutionary studies of social parasites are promising, because they are expected to provide insights into the conditions associated with a behavioral change from cooperative eusociality to exploitative social parasitism as well as into the consequences of the life history transitions on speciation and biological diversification.Social parasitism is a life history strategy that evolved at least 60 times in ants, and more than 400 socially parasitic species are known from six distantly related subfamilies (4). Despite the high diversity, three main life history strategies can be recognized across social parasites: 1) temporary, 2) dulotic, and 3) permanent social parasitism (1, 3, 15–21). The queens of temporary socially parasitic ant species invade the host nest and kill the resident queen(s), and the host workers raise the parasite’s offspring (16). In the absence of an egg-laying host queen, the host workforce is gradually replaced until the colony is composed solely of the temporary social parasite species. The queens of dulotic social parasites start their colony life cycle as temporary social parasites, and once sufficient parasitic workers have been reared, they conduct well-organized raids of nearby host nests to capture their brood (22). Some brood is eaten, but most workers eclose in the parasite’s nest and contribute to the workforce of the colony. By contrast, most permanent social parasite (i.e., inquiline) species are tolerant of the host queen, allowing her to continuously produce host workers, whereas the inquiline queens focus their reproductive effort on sexual offspring (1, 13). Inquilines obligately depend on their hosts and most inquiline species lost their worker caste entirely (1, 18, 19, 23).The evolutionary origins of social parasitism have been debated since Darwin’s On the Origin of Species by Means of Natural Selection (24). Entomologists have long noticed that ant social parasites and their hosts are close relatives (15, 16, 25–29), an observation subsequently referred to as “Emery’s rule” (30). Strictly interpreted, Emery’s rule postulates a sister group relationship between host and parasite, whereas a less restrictive or “loose” interpretation signifies for example a congeneric, but not necessarily a sister taxon relationship (13, 31–33). Consequently, two competing hypotheses were developed for explaining the speciation mechanisms of social parasites: 1) The interspecific hypothesis proposes that host and social parasite evolved reproductive isolation in allopatry, whereas 2) the intraspecific hypothesis postulates that the social parasite evolved directly from its host in sympatry (3, 13, 18, 20, 21, 31–37). Empirical studies of temporary, dulotic, and host queen-intolerant workerless ant social parasites generally provide support for the interspecific hypothesis (14, 38–48), whereas recent phylogenetic studies lend support to the intraspecific hypothesis for queen-tolerant inquilines (33, 36, 49–51). In some cases, host shifts, secondary speciation events of hosts and/or parasites, and extinctions obscure the original evolutionary conditions under which social parasitism originated (52–54).To explore the origin and evolution of diverse socially parasitic life histories in eusocial insects, we reconstructed the evolutionary history of the Holarctic ant genus Formica. Formica ants are ideally suited for comparative studies of social parasitism because the genus has the highest number of social parasite species in any ant genus (84 of 172; Fig. 1 and ​and2).2). In addition, colonies of Formica species vary significantly in colony-founding behavior as well as in nest and colony structures, providing an opportunity to explore the interplay between colony organization and life history at the origin of social parasitism. Some Formica species use independent colony foundation (ICF), when new colonies are started by a single queen (i.e., haplometrosis) or a group of cooperating queens (i.e., pleometrosis). Queens of other species rely on dependent colony founding (DCF), cooperating with groups of conspecific workers to found a new colony (i.e., budding) or invading an existing heterospecific colony as a temporary social parasite (TSP) or a permanent social parasite (PSP) (1, 56–62). In contrast to other studies (63), we regard TSP as a form of DCF because the socially parasitic queen relies on the social environment of the host for colony founding and rearing of the first brood. Furthermore, Formica colonies can have a single or multiple functional queens (monogyny vs. polygyny) and comprise one (monodomous) or multiple (polydomous) to thousands of interconnected physical nests covering a large area (supercolonial) (64).Table 1.Diversity of social parasites in the genus Formica compared to all other ants

Transoceanic drift and the domestication of African bottle gourds in the Americas

Bottle gourd (Lagenaria siceraria) was one of the first domesticated plants, and the only one with a global distribution during pre-Columbian times. Although native to Africa, bottle gourd was in use by humans in east Asia, possibly as early as 11,000 y ago (BP) and in the Americas by 10,000 BP. Despite its utilitarian importance to diverse human populations, it remains unresolved how the bottle gourd came to be so widely distributed, and in particular how and when it arrived in the New World. A previous study using ancient DNA concluded that Paleoindians transported already domesticated gourds to the Americas from Asia when colonizing the New World [Erickson et al. (2005) Proc Natl Acad Sci USA 102(51):18315–18320]. However, this scenario requires the propagation of tropical-adapted bottle gourds across the Arctic. Here, we isolate 86,000 base pairs of plastid DNA from a geographically broad sample of archaeological and living bottle gourds. In contrast to the earlier results, we find that all pre-Columbian bottle gourds are most closely related to African gourds, not Asian gourds. Ocean-current drift modeling shows that wild African gourds could have simply floated across the Atlantic during the Late Pleistocene. Once they arrived in the New World, naturalized gourd populations likely became established in the Neotropics via dispersal by megafaunal mammals. These wild populations were domesticated in several distinct New World locales, most likely near established centers of food crop domestication.In independent centers of plant domestication worldwide, distinct suites of food crops tend to emerge from native flora under human selection. An exception to this is the bottle gourd (Lagenaria siceraria, Cucurbitaceae), which is native to Africa, but was used by diverse human cultures not only in Africa, but also across Eurasia, the Pacific Islands, and the New World during pre-Columbian times (1–4). Although bottle gourd fruits are edible, they are used by humans mostly for other purposes, including as lightweight, durable containers, fishnet floats, and musical instruments (5). This variety of utilitarian applications likely explains why bottle gourds are so globally pervasive.In the New World, bottle gourds appear in archaeological contexts as early as 10,000 BP (6) (9). Bottle gourds were long proposed to have arrived in the Americas via long-range dispersal on ocean currents (10–13). However, an analysis of DNA from living and archaeological gourds suggested that the bottle gourd may have been transported into the New World by the first colonizing humans (6). In this scenario, the bottle gourd, like the dog (14), crossed the Bering Land Bridge with colonizing humans already in its domestic form, making the bottle gourd one of the earliest domesticated species (1, 6).

Table 1.

Archaeological samples and associated AMS radiocarbon dates for gourd rind fragments used in this study

Combining two strategies to improve perfusion and drug delivery in solid tumors

Blood perfusion in tumors can be significantly lower than that in the surrounding normal tissue owing to the leakiness and/or compression of tumor blood vessels. Impaired perfusion reduces oxygen supply and results in a hypoxic microenvironment. Hypoxia promotes tumor progression and immunosuppression, and enhances the invasive and metastatic potential of cancer cells. Furthermore, poor perfusion lowers the delivery of systemically administered drugs. Therapeutic strategies to improve perfusion include reduction in vascular permeability by vascular normalization and vascular decompression by alleviating physical forces (solid stress) inside tumors. Both strategies have shown promise, but guidelines on how to use these strategies optimally are lacking. To this end, we developed a mathematical model to guide the optimal use of these strategies. The model accounts for vascular, transvascular, and interstitial fluid and drug transport as well as the diameter and permeability of tumor vessels. Model simulations reveal an optimal perfusion region when vessels are uncompressed, but not very leaky. Within this region, intratumoral distribution of drugs is optimized, particularly for drugs 10 nm in diameter or smaller and of low binding affinity. Therefore, treatments should modify vessel diameter and/or permeability such that perfusion is optimal. Vascular normalization is more effective for hyperpermeable but largely uncompressed vessels (e.g., glioblastomas), whereas solid stress alleviation is more beneficial for compressed but less-permeable vessels (e.g., pancreatic ductal adenocarcinomas). In the case of tumors with hyperpermeable and compressed vessels (e.g., subset of mammary carcinomas), the two strategies need to be combined for improved treatment outcomes.Perfused vessels are necessary for enabling adequate oxygenation and distribution of systemically administered drugs in solid tumors. However, perfusion rates in some regions of a tumor can be significantly lower than that in the peritumor normal tissue, leading to hypoxia, low pH, and inadequate drug delivery. Impaired blood perfusion in tumors could result from (i) excessive fluid loss from the vasculature to the interstitial space owing to vessel hyperpermeability (Fig. 1A), (ii) increased resistance to fluid flow caused by vessel tortuosity, and (iii) reduced effective cross-sectional area for blood flow due to vessel compression (Fig. 1C) (1, 2). Vessel hyperpermeability and tortuosity can be lowered using judicious doses of antiangiogenic agents (1, 3–6). Fig. 1 A and B shows a schematic of how vascular normalization can improve perfusion by improving the structure and composition of the vessel wall, and Open in a separate windowFig. 1.Schematic of therapeutic strategies to improve tumor perfusion. (A) Abnormalities in interendothelial junctions, pericyte coverage, and/or basement membrane lead to hyperpermeability of tumor blood vessels and excessive fluid leakage that slows down blood flow. (B) Vascular normalization fortifies the vessel wall, resulting in smaller interendothelial gaps (“pores”) and improved perfusion. (C) Structural components of the tumor microenvironment exert forces on blood vessels, resulting in vessel compression and reduced blood flow. (D) Alleviation of these forces by selective depletion of tumor constituents (e.g., cells or extracellular matrix) can decompress the vessels and improve vessel perfusion. BM, basement membrane; CC, cancer and/or stromal cell; EC, endothelial cell; ECM, extracellular matrix; PC, pericyte.

Table 1.

Studies showing vascular normalization improves perfusion measured as improved oxygenation

Early hominin auditory ossicles from South Africa

The middle ear ossicles are only rarely preserved in fossil hominins. Here, we report the discovery of a complete ossicular chain (malleus, incus, and stapes) of Paranthropus robustus as well as additional ear ossicles from Australopithecus africanus. The malleus in both early hominin taxa is clearly human-like in the proportions of the manubrium and corpus, whereas the incus and stapes resemble African and Asian great apes more closely. A deep phylogenetic origin is proposed for the derived malleus morphology, and this may represent one of the earliest human-like features to appear in the fossil record. The anatomical differences found in the early hominin incus and stapes, along with other aspects of the outer, middle, and inner ear, are consistent with the suggestion of different auditory capacities in these early hominin taxa compared with modern humans.The middle ear ossicles have historically played a prominent role in paleontological studies because the appearance of the three bone ossicular chain is considered a defining feature of the emergence of mammals (1, 2). The evolutionary transformation of the malleus and incus, which once formed part of the lower jaw, represents a profound modification of both the feeding and auditory apparatuses and had important implications for the sensory ecology of early mammals (3), including primates (4). However, surprisingly little is known of the auditory ossicles in our early human ancestors because they are among the rarest hominin fossils recovered (5–11). Nevertheless, their study holds great potential as an avenue of inquiry into the evolutionary relationships among fossil taxa, as well as aspects of their sensory perception.In humans, the embryological origins of each of the three ear bones have been thoroughly studied. These tiny bones are fully formed at birth (12, 13) and, unlike other bones of the skeleton, generally do not remodel after about the first year of life (14). The ear ossicles then, in some ways, remain “relic” embryonic bones throughout life, and their evolutionarily conservative nature makes them particularly suitable for phylogenetic analysis (15–17). Comparative genomic studies have revealed changes during the course of our evolutionary history in several genes related to the development of the auditory structures (18) and hearing (19), and previous studies of the inner ear in early hominins have provided insights into their taxonomic relationships and locomotion (20).A few anatomical differences in the ear ossicles of fossil hominins have been reported previously (6–11). Among early hominins, the incus in Paranthropus robustus (SK 848) was argued to show a highly derived articular facet morphology, revealing profound differences from living hominids (7, 21). In contrast, the stapes of Australopithecus africanus (Stw 151) appears similar to African apes in showing generally small metric dimensions, including the size of the footplate (8). We report here on a complete right ossicular chain (malleus, incus, and stapes) (22) (SI Appendix, SI Text S1). This represents an exceptional case of preservation in the human fossil record because to date only two late Pleistocene Neanderthal specimens are reported to preserve a complete ossicular chain (10, 11). In addition, a left malleus and partial right stapes were removed from a specimen attributed to Australopithecus africanus (Stw 255) from Sterkfontein (South Africa) (SI Appendix, SI Text S1). These discoveries allow for a direct comparison of the ear ossicles between these two early hominin taxa, and for comparison with previously reported early hominin specimens (SpecimenOssiclesTaxonSiteReferenceSK 848IncusP. robustusSwartkransRef. 7SKW 18Malleus, incus, stapesP. robustusSwartkransPresent studyStw 151StapesA. africanusSterkfonteinRef. 8Stw 255Malleus, stapesA. africanusSterkfonteinPresent studyOpen in a separate window     

COS-derived GPP relationships with temperature and light help explain high-latitude atmospheric CO2 seasonal cycle amplification

In the Arctic and Boreal region (ABR) where warming is especially pronounced, the increase of gross primary production (GPP) has been suggested as an important driver for the increase of the atmospheric CO₂ seasonal cycle amplitude (SCA). However, the role of GPP relative to changes in ecosystem respiration (ER) remains unclear, largely due to our inability to quantify these gross fluxes on regional scales. Here, we use atmospheric carbonyl sulfide (COS) measurements to provide observation-based estimates of GPP over the North American ABR. Our annual GPP estimate is 3.6 (2.4 to 5.5) PgC · y⁻¹ between 2009 and 2013, the uncertainty of which is smaller than the range of GPP estimated from terrestrial ecosystem models (1.5 to 9.8 PgC · y⁻¹). Our COS-derived monthly GPP shows significant correlations in space and time with satellite-based GPP proxies, solar-induced chlorophyll fluorescence, and near-infrared reflectance of vegetation. Furthermore, the derived monthly GPP displays two different linear relationships with soil temperature in spring versus autumn, whereas the relationship between monthly ER and soil temperature is best described by a single quadratic relationship throughout the year. In spring to midsummer, when GPP is most strongly correlated with soil temperature, our results suggest the warming-induced increases of GPP likely exceeded the increases of ER over the past four decades. In autumn, however, increases of ER were likely greater than GPP due to light limitations on GPP, thereby enhancing autumn net carbon emissions. Both effects have likely contributed to the atmospheric CO₂ SCA amplification observed in the ABR.

Gross primary production (GPP) is the total amount of carbon that is taken up from the atmosphere and converted to sugars by plants during photosynthesis. It is the primary source of organic matter production on Earth. GPP is also central to the carbon cycle and for understanding carbon feedbacks to climate. Currently, it exceeds ecosystem respiration (ER) and controls the overall direction of land carbon sequestration on a global scale, thus having a cooling effect on climate. However, carbon cycle–based terrestrial feedbacks in the future have substantial uncertainties and therefore represent one of the largest uncertainties in climate projections (1). A large source of this uncertainty stems from our inability to quantify GPP at large spatial scales and our incomplete understanding of the sensitivity of GPP to rising atmospheric CO₂ concentrations and air temperature (2, 3).In the Arctic and Boreal regions, where climate warming has been magnified by more than a factor of 2 relative to other regions of the globe (4, 5), the growth of GPP is thought to have contributed to an increase in the atmospheric CO₂ mole fraction seasonal cycle amplitude (SCA) observed over the northern high latitudes (6, 7), either due to an earlier onset or lengthening of the growing season (6, 8, 9) or enhanced carbon uptake (7, 10), although increased respiration (11, 12) and transport from midlatitudes (13, 14) also contribute.Despite the vital role of GPP in the carbon cycle, climate, and food systems, its magnitudes and trends over the Arctic and Boreal regions are poorly known. Annual GPP estimated from terrestrial ecosystem models (TEMs) and machine learning methods (15, 16) differ by as much as a factor of 6 (Fig. 1 and SI Appendix, Fig. S1). Given this large uncertainty, the current capability for constraining GPP on regional scales remains very limited. No direct GPP measurements can be made at scales larger than at a leaf level, because the basic process of GPP, which extracts CO₂ from the atmosphere, is countered by the production of CO₂ for respiration. Although large-scale GPP estimates have been made by machine learning methods (15, 16), light-use efficiency models (17), empirical models (18), and terrestrial biogeochemical process models (19–21) that have been trained on small-scale net CO₂ fluxes measured by eddy covariance towers, they substantially differ in mean magnitude, interannual variability, trends, and spatial distributions of inferred GPP (22–24). Satellite remote-sensing measurements of solar-induced chlorophyll fluorescence (SIF) and near-infrared reflectance of vegetation (NIRv) have been strongly linked to GPP on regional and global seasonal scales (25–28). However, GPP estimates based on scaling of SIF and NIRv can be limited by inconsistent and poorly constrained scaling factors among different plant functional types (29) or can be biased from interferences of clouds and aerosols in retrievals (30).Open in a separate windowFig. 1.Regional GPP for the North American ABR, estimated from bottom-up terrestrial models participating in Multiscale Synthesis and Terrestrial Model Intercomparison Project (MsTMIP) (dashed lines), FluxCom (cyan squares with solid lines), FluxSat (green triangles with solid lines), and SiB4 (red circles with solid lines) and our top-down atmospheric COS inversions (dark gray shading indicates the 2.5th to 97.5th of our best inversion ensemble estimates, whereas the light gray shading denotes the range of our best ensemble estimates plus 2σ uncertainties from each inversion). The North American ABR is indicated in B. (A) Annual GPP estimates between 2000 and 2019. (B) Multiyear average seasonal cycle of GPP from MsTMIP (2008–2010), FluxSat (2001–2019), FluxCom (2001–2018), SiB4 (2009–2013), and this study (2009–2013). (C) Spatial distribution of GPP in July 2010 from three selected TEMs (LPJ-wsl, SiB4, and DLEM) and average GPP from July in 2009 to 2013 derived from COS-based inversions. The spatial distribution of GPP from other TEMs is shown in SI Appendix, Fig. S12.Table 1.Annual COS fluxes and GPP over the North American ABR, estimated from process-based bottom-up approaches and our atmosphere-based top-down method

From the Cover: Sex-specific ornament evolution is a consistent feature of climatic adaptation across space and time in dragonflies

Adaptation to different climates fuels the origins and maintenance of biodiversity. Detailing how organisms optimize fitness for their local climates is therefore an essential goal in biology. Although we increasingly understand how survival-related traits evolve as organisms adapt to climatic conditions, it is unclear whether organisms also optimize traits that coordinate mating between the sexes. Here, we show that dragonflies consistently adapt to warmer climates across space and time by evolving less male melanin ornamentation—a mating-related trait that also absorbs solar radiation and heats individuals above ambient temperatures. Continent-wide macroevolutionary analyses reveal that species inhabiting warmer climates evolve less male ornamentation. Community-science observations across 10 species indicate that populations adapt to warmer parts of species’ ranges through microevolution of smaller male ornaments. Observations from 2005 to 2019 detail that contemporary selective pressures oppose male ornaments in warmer years; and our climate-warming projections predict further decreases by 2070. Conversely, our analyses show that female ornamentation responds idiosyncratically to temperature across space and time, indicating the sexes evolve in different ways to meet the demands of the local climate. Overall, these macro- and microevolutionary findings demonstrate that organisms predictably optimize their mating-related traits for the climate just as they do their survival-related traits.

Dating back to Darwin (1) and Wallace (2), biologists have long hypothesized that much of the Earth’s biodiversity was forged by adaptation to different climates. Characterizing how organisms respond to climatic factors, like temperature, is therefore an enduring goal in biology, which has become even more crucial due to the ongoing climate crisis (3). To date, researchers have uncovered many ways that organisms improve survival in their local climates through the evolution of traits such as physiological tolerance (4), life cycle timing (5), and body size (6). However, recent work reveals that climatic adaptation can also involve optimizing mating and reproduction in addition to survival (7). The evolution of sexual traits that coordinate mating could therefore be an important way that plants and animals improve fitness in their local climate from one generation to the next. Nevertheless, despite >95% of eukaryotic taxa engaging in sexual reproduction, it is unclear if sexual characters are a dimension of the phenotype that organisms typically optimize for the climate (3, 8–10).One type of sexual trait that could often be involved in climatic adaptation is ornamental coloration, which many animals use to attract mates and intimidate rivals. As the dark and/or saturated colors used in many ornaments absorb solar radiation and lead to heating, the demands of warmer climates could force animals to evolve smaller or less saturated ornaments (9, 11, 12). Alternatively, because tropical species are frequently more ornately colored than their temperate relatives, some researchers have suggested that adaptation to warmer climates may instead favor more exaggerated ornamentation (13). By understanding how ornamental coloration responds to selective pressures in different climates, we can begin to resolve if the evolution of sexual traits is indeed a major feature of how organisms adapt to the climate (3, 10).Testing if ornaments respond predictably to climatic factors across multiple lineages and/or timescales is one approach to assessing ornament evolution’s role in climatic adaptation (14, 15). If, for example, selective pressures in warmer climates require the evolution of less exaggerated ornamentation, then we should observe that animals inhabiting hotter environments consistently evolve less ornamental color regardless of timescale or historical contingencies (e.g., differing genetic backgrounds, or genetic drift) (14). Dragonflies and damselflies are well suited for such tests because they possess ornamental wing melanization that varies within and among species (16). Males with greater wing melanization typically attract more mates and ward off territorial rivals, and both sexes use these ornaments to signal their species’ identity to con- and heterospecifics (16). Though these advantages in courtship and rival intimidation often favor greater ornamentation, wing melanization can also heat individuals >2 °C (11, 12, 17). Such heating may provide modest locomotor benefits under cool conditions (11), but it can damage wing tissue, reduce male fighting ability and territorial defense, and even cause death under warm conditions (11, 17). In contrast, because females mainly spend their time foraging in cooler and/or more shaded microhabitats to maximize fecundity (16), their wing melanization may rarely cause overheating. These sex-specific thermal consequences for both reproduction and survival suggest that dragonflies should adapt to their local climates across space and time through the evolution of ornamental wing melanization in males but not necessarily in females (11, 12). We tested this hypothesis by exploring how male and female ornaments have responded to climatic differences across the macroevolutionary, microevolutionary, and contemporary history of Nearctic dragonflies.To first evaluate if selective pressures in different climates have favored ornament evolution across macroevolutionary timescales, we tested if Nearctic dragonfly species inhabiting warmer ranges are less likely to have evolved wing melanization than those inhabiting cooler ranges. Using field guides, community-science observations, and >387,900 occurrence records from the Global Biodiversity Information Facility (https://www.gbif.org), we compiled phenotypic and climatic data for 319 Nearctic species (Fig. 1 A and B). After controlling for shared evolutionary history, we found sex-specific patterns of ornament evolution among climates. Species with warmer ranges are indeed less likely to have male wing melanization than species with cooler ranges (β ± SE = −0.078 ± 0.024, 95% CIs = −0.162 to −0.035; Fig. 1C). Species with the darkest patches of male wing melanization also tend to have the coolest ranges (β ± SE = −0.010 ± 0.004, 95% CIs = −0.017 to −0.003). However, interspecific patterns for female wing melanization contrasted starkly with these patterns for males. Species with warmer ranges have a somewhat higher probability of female wing melanization, though the trend is not different from zero (β ± SE = 0.027 ± 0.016, 95% CIs = −0.008 to 0.068; Fig. 1D). There is also no relationship between the temperature of a species’ range and the darkness of its female wing melanization (β ± SE = −0.006 ± 0.004, 95% CIs = −0.012 to 0.001). Thus, the evolution of male, but not female, wing melanization is a component of how dragonflies respond to climatic differences over long timescales.Open in a separate windowFig. 1.Macroevolution of dragonfly wing melanization in relation to temperature. (A) Nearctic dragonfly phylogeny. Filled tips indicate the presence of male (green) and female (purple) wing melanization. (B) Dragonfly species across the Nearctic. (C and D) Probability of males (C) and females (D) possessing wing melanization. Tick marks are species (n = 319), and lines are from phylogenetic logistic regressions.These macroevolutionary findings indicate that selective pressures in warmer climates have favored less male, but not female, ornamentation among Nearctic dragonfly species. However, most dragonfly species are much older than their current geographic distributions (16). Thus, as is true in many studies of ancient lineages, these biogeographic patterns probably stem from both ecological filtering and adaptation. For instance, following the Last Glacial Maximum, species may have recolonized regions where the climatic conditions did not make male ornamentation too costly (i.e., ecological filtering) (12). Additionally, because ornamentation is quite evolutionarily labile (18), these macroevolutionary patterns likely also arise from adaptation to local climates. The relative contributions of colonization and adaptation to interspecific ornament variation cannot yet be disentangled for this group or for many other ancient clades. Nevertheless, if adaptation to local climatic conditions has led species to evolve differing ornamentation over long timescales, then it should also entail ornament evolution across shorter timescales—such as those separating populations within the same species.To evaluate if populations consistently adapt to their local climates via ornament evolution, we next tested for parallel shifts in ornament size across the ranges of 10 widely distributed Nearctic dragonfly species (14) (Fig. 2). Here, we measured the proportion of melanized wing area on >2,700 dragonfly observations from the community-science platform iNaturalist (https://www.inaturalist.org) (19). Despite some of these species being separated by >100 My of evolution, we found that their constituent populations exhibit remarkably parallel responses in their male, but not female, ornamentation. Within 7 of the 10 species, males in warmer regions had significantly less wing melanization than their counterparts in cooler areas (Fig. 2A and SI Appendix, Table S1). Consequently, when averaging across all 10 species’ responses, male wing melanization tended to decrease as local temperatures increased (β ± SE = −0.064 ± 0.031 SD per 1 °C; 95% CIs = −0.127 to −0.001). Because developing at warmer temperatures does not induce male dragonflies to express less ornamentation (20), genetic differences among populations are more likely to underlie these parallel responses than phenotypic plasticity alone. In contrast to the patterns in males, females possessed significantly less wing melanization in warmer climates for only 3 out of 10 species (Fig. 2A and SI Appendix, Table S1). As a result, the average female response to temperature across the 10 species was indistinguishable from 0 (β ± SE = −0.006 ± 0.024 SD per 1 °C; 95% CIs = −0.054 to 0.042). Thus, mirroring macroevolutionary patterns among species, the differing selective pressures among climates also favor consistent patterns of sex-specific ornament evolution within species (Fig. 2B). In particular, these sex-specific responses within species result in male ornaments being 25.8 ± 2.0% larger than female ornaments in the coolest parts of North America, on average, but only 2.0 ± 3.3% larger in the warmest areas.Open in a separate windowFig. 2.Parallel evolution of wing melanization in response to mean annual temperature (MAT) within dragonfly species. (A) Graphs show species’ relationships for males (green) and females (purple). Points are individuals (n = 2,718), and lines are fitted from linear mixed-effects models. Asterisks indicate significant declines. (B) Average within-species SD change wing melanization (± SE) for 1 °C increase.Across timescales ranging from >150 My to only dozens of millennia, our results show that dragonflies consistently adapt to their climate via sex-specific evolution of wing melanization. However, climatic projections indicate North America could warm >4.5 °C by 2070 (21). The ornament evolution that previously facilitated adaptation over thousands of years may therefore need to occur over fewer than 100 generations unless alternative responses can be employed. Two such alternatives to rapid ornament evolution are shifts in species’ distributions and phenologies (22). For instance, more-ornamented species could lessen the threat of overheating by tracking northward shifts of cooler temperatures. When we incorporated each species’ ornamentation into a recently published analysis of range shifts among 65 European dragonflies (23), however, we found that species with male ornamentation have not moved further northward than species without it (difference in northward range shifts ± SE = 10.50 ± 24.33 km, 95% CIs = −37.19 to 58.18). More-ornamented species could also alleviate the risk of overheating by shifting phenology to defend territories in cooler times of day or to reproduce in cooler times of year (22). Though we cannot rule out this possibility, it is notable that such phenological shifts, if they occur, have not enabled males to possess greater ornamentation in warmer climates over the previous >150 My. Rapid ornament evolution may therefore be necessary to avoid overheating as our planet’s climate changes (24).To evaluate how natural and sexual selection might alter ornamentation as the Earth warms, we tested if the 10 widely distributed dragonfly species (Fig. 2) possessed less wing melanization in years that were warmer than the Northern Hemisphere’s long-term average (mean temperature anomaly). Our analyses show that, from 2005 to 2019, species averaged less wing melanization in warmer years for males but not females (males: β ± SE = −0.263 ± 0.103 SD per 1 °C, 95% CIs = −0.513 to −0.005; females: β ± SE = −0.118 ± 0.146 SD per 1 °C, 95% CIs = −0.418 to 0.181; Fig. 3). However, since males and females responded more similarly to each other across annual variation than geographic variation, the estimated extent of sexual dimorphism was only modestly more male biased in cold years (16.0 ± 1.5%) than in warm years (14.5 ± 1.9%). Nonetheless, these results collectively reveal that male ornaments were smallest in this century’s warmest years. By contrast, our analyses show that the extent of wing melanization did not exhibit a net decrease across the 15-y timespan for either sex nor was it related to the previous year’s temperature (SI Appendix, Table S8). The temporal patterns in ornament size therefore likely emerge from processes operating within generations rather than across generations. As dragonflies do not develop less wing melanization when reared under warmer conditions (20), a probable explanation for this within-generation effect is that selection in warmer years consistently reduces the number of highly ornamented individuals in breeding populations.Open in a separate windowFig. 3.Wing melanization shifts with interannual temperature variation. (A) Lines show fitted relationship (with 95% CIs) between wing melanization (SD relative to mean) and the Northern Hemisphere’s yearly temperature anomaly from 2005 to 2019 (n = 2,620). (B) Estimated-marginal mean wing melanization (with 95% CIs) for 2005 to 2019. The sexes’ points are offset horizontally to reduce overlap.Since selective pressures in warmer years appear to favor less ornamented males, we estimated how wing melanization might shift as North America warms over the next several decades. Based on the best- and worst-case scenarios for climatic warming (21), we used the current geographic relationship between ornamentation and temperature to forecast the amount of wing melanization each species should possess in 2070 for the coolest third, thermal midpoint, and warmest third of its range (21, 24) (SI Appendix, Table S3). Our projections indicate that, on average, species’ male wing melanization will decline 0.205 to 0.328 SD by 2070 (SI Appendix, Table S3)—a modest loss of only up to 0.007 SD per generation. In contrast, species’ female wing melanization will not need to change significantly (SI Appendix, Table S3). The breeder’s equation can illuminate the plausibility of dragonflies losing this much male wing melanization each generation to match yearly warming of 0.09 °C (4.5 °C/50 y) (24). Assuming that phenotypic selection underlies the interannual ornament variation we observed (Fig. 3B), selection in each generation will favor, on average, 0.024 SD less male wing melanization than it did in the previous generation (−0.263 SD ornamentation °C⁻¹ × 0.09 °C Y⁻¹). For male ornamentation to keep pace with this intensity of selection each generation, heritability would need to average 0.277 ± 0.111. This h² is similar to the estimated mean for all adult traits in animals [h² = 0.247 ± 0.032 (25)] and smaller than the estimated mean for melanin-based traits in insects (h² = 0.463 ± 0.114; see SI Appendix). Because the capacity for rapid responses to climatic warming is often limited along other phenotypic axes [e.g., physiological tolerance (4, 26, 27)], the modest projected responses and moderate requisite heritability of male wing melanization suggest that ornament evolution could be an important component of climatic adaptation in the coming years.Table 1.Average forecasted shifts (± SE), and 95% prediction intervals, that will be necessary for dragonflies to optimize their wing melanization to the climatic conditions of 2070 across North America

Revisiting Darwin's conundrum reveals a twist on the relationship between phylogenetic distance and invasibility

A key goal of invasion biology is to identify the factors that favor species invasions. One potential indicator of invasiveness is the phylogenetic distance between a nonnative species and species in the recipient community. However, predicting invasiveness using phylogenetic information relies on an untested assumption: that both biotic resistance and facilitation weaken with increasing phylogenetic distance. We test the validity of this key assumption using a mathematical model in which a novel species is introduced into communities with varying ecological and phylogenetic relationships. Contrary to what is generally assumed, we find that biotic resistance and facilitation can either weaken or intensify with phylogenetic distance, depending on the mode of interspecific interactions (phenotype matching or phenotype differences) and the resulting evolutionary trajectory of the recipient community. Thus, we demonstrate that considering the mechanisms that drive phenotypic divergence between native and nonnative species can provide critical insight into the relationship between phylogenetic distance and invasibility.Invasive species are a major cause of concern due to their large ecological, social, and economic consequences (1–3). In principle, future invasions could be avoided by preventing introductions of potential invaders into susceptible communities. Thus, research has focused on identifying the characteristics that predispose species to becoming invasive (4–7) and the properties that make communities susceptible to invasion (8, 9). Although generalities have been elusive, one approach that has recently been gaining interest is using phylogenetic distance (time since cladogenesis) between nonnative species and species in the recipient community as an indicator of invasion potential.Darwin was the first to suggest that the probability of establishment by introduced species depends on their relatedness to native species (10). However, as Darwin noted, the ecological similarity of related species can have opposing effects on their potential for coexistence (“Darwin’s naturalization conundrum”). On the one hand, establishment in regions with close relatives should be facilitated by favorable abiotic conditions and the presence of suitable prey, hosts, and mutualists (Fig. 1A). On the other hand, establishment in these regions should be inhibited by competition with the relatives themselves and exploitation by shared natural enemies (Fig. 1B). Citing observations by Alphonse de Candolle and Asa Gray that naturalized species are more frequently from nonnative genera, Darwin concluded that competition was the dominant factor and relatedness to native species should reduce establishment success (“Darwin’s naturalization hypothesis”).Open in a separate windowFig. 1.Conventional predictions for the relationship between phylogenetic distance and establishment probability. (A) Abiotic conditions, mutualists, and resource species (e.g., prey and hosts) are expected to favor establishment of related species. As time t since cladogenesis increases, these favorable effects decline, leading to reduced probability of establishment. (B) Competitors and natural enemies are expected to disfavor establishment of related species. As time since cladogenesis increases, these unfavorable effects decline, leading to increased probability of establishment.However, recent studies using statistical models, molecular phylogenetics, and experimental community assembly have revealed that the correlation between relatedness and establishment probability can be positive, negative, or zero (11). More fundamentally, doubt has been cast on the key assumption underlying both Darwin’s intuitive arguments and contemporary research: that the effects of native species are strongest when phylogenetic distance to the nonnative species is low (Fig. 1) (12). Although this assumption is supported by studies showing that the presence of closely related species in a community increases competition (13), attack by natural enemies (14–18), and visitation by mutualists (19), a number of recent studies demonstrate the opposite, i.e., that distantly related species can experience more intense competition (12, 20) and herbivory (21).

Table 1.

The effect of phylogenetic relatedness on the probability of establishment by nonnative species

Phytoplankton adapt to changing ocean environments

Model projections indicate that climate change may dramatically restructure phytoplankton communities, with cascading consequences for marine food webs. It is currently not known whether evolutionary change is likely to be able to keep pace with the rate of climate change. For simplicity, and in the absence of evidence to the contrary, most model projections assume species have fixed environmental preferences and will not adapt to changing environmental conditions on the century scale. Using 15 y of observations from Station CARIACO (Carbon Retention in a Colored Ocean), we show that most of the dominant species from a marine phytoplankton community were able to adapt their realized niches to track average increases in water temperature and irradiance, but the majority of species exhibited a fixed niche for nitrate. We do not know the extent of this adaptive capacity, so we cannot conclude that phytoplankton will be able to adapt to the changes anticipated over the next century, but community ecosystem models can no longer assume that phytoplankton cannot adapt.During the last several decades, global land temperature has increased by ∼0.3 °C per decade (1), and a further increase in global mean air temperatures of 1.1–6.4 °C is expected by 2100 (2). The warming of the oceans is resulting in spatially variable changes in sea surface temperature (3, 4), salinity, mixed-layer depth, and the distribution of nutrients. Ocean time series sampled on a monthly basis document intra- and interannual changes in physical forcing and biogeochemistry, providing crucial data for formulating ecosystem models and characterizing how ecosystems respond to climate change (5, 6). We have very high confidence that climate change during the last several decades has influenced the abundance, phenology, and geographic ranges for a wide assortment of species (7–10). Further increases in global temperature may result in significant and nonreversible changes to many populations and communities (11, 12). If dispersal rates are rapid relative to the rate of evolutionary adaptation, changes in climate will result in local species being displaced by nonresident species from a regional pool of species that are better adapted to the new conditions (13). When modelers project changes in biotic communities under climate change scenarios, they generally assume that each species has a genetically determined fixed environmental niche and that species’ spatial and temporal distributions will be determined by environmental conditions (14–17). A recent model of this type predicts a loss of a third of tropical phytoplankton strains by 2100 with a ∼2 °C increase in mean temperature (11); however, paleoecological studies indicate organisms may be much more resilient to climate change than these types of models suggest (18, 19).Local populations may be able to acclimate physiologically and then adapt through evolutionary change to gradual climate shifts. We do not know the constraints or timescales required for phytoplankton to adapt to changes in environmental conditions anticipated over the next century. Phytoplankton species have short generation times and large population sizes, so they may be particularly able to adapt to rapid climate change (20, 21). In addition, temperature response curves measured in the laboratory show that phytoplankton usually have the fastest growth rates at or slightly below the mean temperature of the environment they were isolated from, suggesting that natural populations are adapted to their local environment (15, 22), although some species have niches that do not reflect the environmental conditions from which they were isolated (23). Evolutionary experiments in the laboratory indicate that phytoplankton species have the capacity to evolve over hundreds to thousands of generations in response to single environmental factors; specifically, changes in CO₂ concentration or temperature (24–29). Laboratory evolution experiments do not replicate either the highly dynamic marine environment or the trajectory of climate change, so it is necessary to look to see how phytoplankton evolve in the field. Theoretical studies show that species will evolve to maximize their geometric mean fitness in temporally varying environments, so evolutionary change is expected even if decadal-scale changes in average environmental conditions are smaller than interannual variation in those same conditions (29). Here we explicitly test whether phytoplankton species niches are stable or are able to adapt to simultaneous changes in several different environmental conditions over a decadal scale, using ocean time-series data. The answer to this question is essential for modelers attempting to predict biotic responses to changes in climate.We quantify the realized niche for 67 dominant phytoplankton species (30) from Station CARIACO (Carbon Retention in a Colored Ocean) from the CARIACO Ocean Time-Series Program, using the MaxEnt method (31), which ignores species abundance and only relies on the conditions under which a species is present to describe the habitat of the species. We define the realized niche as the hypervolume of environmental conditions under which each species persists (32) and estimate the range of conditions for each species from a 15-y time series with monthly sampling. The MaxEnt method provides a robust estimate of the realized niche and is insensitive to the challenges posed by the detection of species at low abundance (33). During the 15 y from 1996 to 2011, there was a gradual warming of about 1 °C, an increase in average irradiance, and a decrease in nitrate concentration in the upper mixed layer (0–30 m) at Station CARIACO (34). These are regional changes resulting from the movement of the Inter-Tropical Convergence Zone (35). We divided the time series into an early, cooler period and a late, warmer period and examined the stability of the realized niches of phytoplankton species between these two periods (Fig. 1 and Open in a separate windowFig. 1.Monthly environmental conditions averaged over the upper mixed layer (1, 7, 15, and 25 m depth) from the CARIACO Ocean Time-Series Program: temperature (°C), irradiance (mol⋅m^–2⋅d^–1), and nitrate concentration (µmol⋅L^–1). The vertical dotted line is drawn at the boundary (January 1, 2004) between the cool and warm periods. The straight lines are linear regressions: temperature = (24.6 ± 0.3) + (0.09 ± 0.03) t, R² = 0.05, P < 0.005; irradiance = (18.1 ± 0.9) + (0.05 ± 0.11) t, R²= 0.001, P = 0.65; nitrate = (1.06 ± 0.14) – (0.045 ± 0.017) t, R² = 0.04, P = 0.03, where t is time in years since January 1, 1996, errors are one SE, and the shaded region is the 95% confidence interval on the line. The R² is very low because of the tremendous interannual variation relative to the trend.

Table 1.

Shift in mean niche tracks changes in environmental conditions

Early Lapita skeletons from Vanuatu show Polynesian craniofacial shape: Implications for Remote Oceanic settlement and Lapita origins

With a cultural and linguistic origin in Island Southeast Asia the Lapita expansion is thought to have led ultimately to the Polynesian settlement of the east Polynesian region after a time of mixing/integration in north Melanesia and a nearly 2,000-y pause in West Polynesia. One of the major achievements of recent Lapita research in Vanuatu has been the discovery of the oldest cemetery found so far in the Pacific at Teouma on the south coast of Efate Island, opening up new prospects for the biological definition of the early settlers of the archipelago and of Remote Oceania in general. Using craniometric evidence from the skeletons in conjunction with archaeological data, we discuss here four debated issues: the Lapita–Asian connection, the degree of admixture, the Lapita–Polynesian connection, and the question of secondary population movement into Remote Oceania.The first human settlement of Vanuatu is indicated by the Lapita culture, whose earliest signature appears in the northwestern Melanesian islands toward the end of the interval 3,470–3,250 y B.P. or slightly later (1). The Lapita culture is defined by a set of artifacts including highly decorated pottery displaying a distinctive design system, long-distance exchanges of raw material and finished items, translocations of plants and animals, and the initial incursion of humans into the pristine island environments of Remote Oceania to the east of the main Solomon chain between 3,000 and 2,800 y B.P. (1, 2). In Vanuatu, as in the rest of Remote Oceania, Lapita quickly evolved, within 200–300 y, into distinctive local cultures in conjunction with increased population size and sedentism by the end of the Lapita period (3).The question of the biological nature of the Lapita populations is routinely approached with data collected from protohistoric/historic or extant populations used as proxies. Analysis of skull morphology and morphometrics of protohistoric/historic populations from Oceania shows a geographical pattern of variation, separating northern and southern Melanesia from western and eastern Polynesia (4–6). More generally, the results indicate two contrasting divisions, an Australo-Melanesian pole comprising groups from the western part of Remote Oceania (Island Melanesia) and an Asian pole including groups from the (far) eastern part of Remote Oceania (Polynesia). This pattern suggests separate origins for the indigenous inhabitants of these two regions. Evidence from inherited genetic markers indicates that the populations living today in Vanuatu and generally in the region first settled by Lapita groups share a common origin in an area that encompasses Island South East Asia, the north coast of New Guinea, and the Bismarck Archipelago (7–13). These populations display haplogroups attributed both to the Pleistocene settlement of the northern Melanesian/Near Oceanic region and to the Lapita diaspora, with chronological estimates based on genetic data. Geographical variations in haplotype frequencies distinguish the western part of the initial Lapita region from the eastern part, with a smaller diversity in the eastern populations in what is today Western Polynesia.Studies on Lapita skeletal morphology (14–20). In a recent biodistance study of mandibles from Watom (New Britain), Pietrusewsky et al. (16) conclude that “expectation that skeletons associated with the Lapita Cultural Complex, Early or Late Lapita, biologically resemble the modern-day inhabitants of Remote Oceania is not supported” and challenge “the prevailing orthodox view that the origin of Polynesians is associated with Lapita culture.” However, whether the few analyzed individuals represent initial “Lapita people” is open to question. Because they postdate the initial appearance of the Lapita culture in the region (20), they may actually reflect subsequent gene flow and migratory events within the Melanesian region, saying more “about the contemporary indigenous inhabitants of eastern Melanesia than … about the ancestors of the Polynesians,” as noted by Pietrusewsky et al. (18). Alternatively, the possibility that these late Lapita and (immediately) post-Lapita individuals derive directly from the initial “Lapita population” is not excluded, because heterogeneity among the early populations of the region and among the Lapita groups themselves might be expected (21–23).

Table S1.

List of Lapita specimens known so far

Disentangling the last 1,000 years of human–environment interactions along the eastern side of the southern Andes (34–52°S lat.)

Researchers have long debated the degree to which Native American land use altered landscapes in the Americas prior to European colonization. Human–environment interactions in southern South America are inferred from new pollen and charcoal data from Laguna El Sosneado and their comparison with high-resolution paleoenvironmental records and archaeological/ethnohistorical information at other sites along the eastern Andes of southern Argentina and Chile (34–52°S). The records indicate that humans, by altering ignition frequency and the availability of fuels, variously muted or amplified the effects of climate on fire regimes. For example, fire activity at the northern and southern sites was low at times when the climate and vegetation were suitable for burning but lacked an ignition source. Conversely, abundant fires set by humans and infrequent lightning ignitions occurred during periods when warm, dry climate conditions coincided with ample vegetation (i.e., fuel) at midlatitude sites. Prior to European arrival, changes in Native American demography and land use influenced vegetation and fire regimes locally, but human influences were not widely evident until the 16th century, with the introduction of nonnative species (e.g., horses), and then in the late 19th century, as Euro-Americans targeted specific resources to support local and national economies. The complex interactions between past climate variability, human activities, and ecosystem dynamics at the local scale are overlooked by approaches that infer levels of land use simply from population size or that rely on regionally composited data to detect drivers of past environmental change.

Understanding the contribution of people in shaping landscape history through their use of fire is a fundamental component of human–environment research and critical for conservation and land-management strategies that seek to maintain elements of pre-European ecosystem dynamics into the future (1, 2). In North and South America, discussions centered around this topic have become increasingly nuanced, acknowledging that the interactions between climate, human activity, and ecosystem dynamics are complex and vary at different temporal and spatial scales (e.g., refs. 3 and 4). In most ecosystems, fire is the dominant type of natural disturbance, but fire has also long been used by humans to facilitate hunting, forest clearance, resource enhancement, and defense. Such strategies have increased ignitions and altered the length and timing of fire seasons (1), but less clear in many regions is the contribution of human-set fires in shaping climate–vegetation dynamics over time.A long-term perspective on fire comes largely from paleoecological and archaeological records that span millennia, although interpretation of these data are often confounded by the uneven distribution of records and their low sampling resolution, poor chronological control, and unclear spatial inference. Ethnographic and historical accounts provide additional information on anthropogenic burning, but they generally describe Native American activities following the spread of European diseases and attendant population declines; the introduction of livestock, crops, and horses; and the cultural changes following genocide and enforced confinement (5–8). These accounts may not be representative of longer patterns of use.The forest–steppe boundary on the eastern side of the Andes in southern South America is one of the sharpest ecotones on Earth and shaped by a combination of climate, fire, and human activity (9). Although many studies along the ecotone have focused on the long-term fire and vegetation history (10–12) and recent human–fire interactions (13, 14), relatively little is known about the ecosystem dynamics of the region during the transition from Native American to Euro-American land use practices in the last 1,000 y. This gap in knowledge stems from the short duration of most tree-ring records of fire (spanning a few centuries), the paucity of archaeological data to connect with historical and ethnographic information, and the low temporal and spatial resolution of paleoecological records during this time span.To address these shortcomings, we present high-resolution pollen, charcoal, and lithological records from Laguna El Sosneado in Mendoza Province, Argentina, to describe the late-Holocene vegetation and fire history in a location with abundant archaeological sites. We compared the ecological history of the last 1,000 y at this and three other sites (Laguna Portezuelo, Lago Mosquito, and Río Rubens Bog) along the east side of the Andes from latitude 34–52°S. These four sites were selected because of their well-constrained age-depth models, exceptionally high-resolution pollen and charcoal records for the last ∼1,000 y, and varying degrees of Native American and Euro-American land use (Fig. 1 and Open in a separate windowFig. 1.Map of southern South America showing vegetation zones based on refs. 19–21, lightning frequency (2010 to 2020, strikes km⁻² y⁻¹) (22), and locations of the high-resolution paleoecological sites discussed in the text and in Site nameLatitude (°S)Longitude (°W)Elevation (m)Temperature (°C)^*Precipitation (mm y⁻¹)^*Vapor pressure (hPa)Age constraint (last 1,000 y)Median resolution (y sample⁻¹)^†Pre-European vegetationSourceLaguna El Sosneado34.869.921105.65243.63Pollen = 24 Charcoal = 8Grass-, shrub-steppePresent workLaguna Portezuelo37.971.017307.26184.54Pollen = 16 Charcoal = 16Steppe with patches of AraucariaNanavati et al. (15)Lago Mosquito42.571.45606.86975.35Pollen = 19 Charcoal = 6Austrocedrus chilensis- Nothofagus dombeyi woodland and steppePresent work, Whitlock et al. (16)Río Rubens Bog52.071.92206.73896.210Pollen = 16 Charcoal = 18Open N. antarctica and N. pumilio forest and steppeHuber and Markgraf (17) Markgraf and Huber (12)Open in a separate window*Annual median values (1901 to 2018) from CRU 4.05 0.5° grid cells (18).^†Estimated from ∼1,000 cal y BP to the core top.     

Predator-induced maternal effects determine adaptive antipredator behaviors via egg composition

In high-risk environments with frequent predator encounters, efficient antipredator behavior is key to survival. Parental effects are a powerful mechanism to prepare offspring for coping with such environments, yet clear evidence for adaptive parental effects on offspring antipredator behaviors is missing. Rapid escape reflexes, or “C-start reflexes,” are a key adaptation in fish and amphibians to escape predator strikes. We hypothesized that mothers living in high-risk environments might induce faster C-start reflexes in offspring by modifying egg composition. Here, we show that offspring of the cichlid fish Neolamprologus pulcher developed faster C-start reflexes and were more risk averse if their parents had been exposed to cues of their most dangerous natural predator during egg production. This effect was mediated by differences in egg composition. Eggs of predator-exposed mothers were heavier with higher net protein content, and the resulting offspring were heavier and had lower igf-1 gene expression than control offspring shortly after hatching. Thus, changes in egg composition can relay multiple putative pathways by which mothers can influence adaptive antipredator behaviors such as faster escape reflexes.

Nongenetically transmitted maternal effects can exert modifications in offspring phenotype, leading to individual variation (1) that natural selection can act on (2–4). Maternal effects may act to transfer signals or cues that affect the development of offspring phenotypes persistently (via the deposition of hormones, nutrients, or maternal RNA into eggs), and these effects can even carry over to multiple generations (5, 6). It has been hypothesized that via maternal effects in the prenatal stage, mothers can shape offspring phenotype to prepare them for the environment they are likely to encounter after birth (2, 7, 8). These adaptive maternal effects should only evolve if the mother can reliably forecast the offspring environment (9, 10).Predation risk is one of the most significant environmental factors affecting life history and individual fitness (11, 12) as well as population dynamics (13) and social structure (14, 15), so one might expect that in dangerous environments mothers prepare their offspring via maternal effects to effectively cope with predation risk. Efficient antipredator behaviors are key for survival because they allow quick and highly flexible responses to unpredictable predator attacks. Therefore, one should expect predator-induced maternal effects on offspring antipredator behavior to be widespread. However, compared to well-established morphological [e.g., neck helmets in Daphnia (16)] and physiological [e.g., glucocorticoids (17)] maternal effects influencing offspring survival, the adaptive value of maternal effects on offspring behavior is yet unclear (SI Appendix, Table S1) for three main reasons: 1) Previous studies did not evaluate the adaptive value of the reported antipredator behavior in the face of real predation threat (18–21). 2) The changes in offspring behavior induced by maternal exposure to predation threat were either maladaptive (22, 23) or they had no detectable effect on predator evasion (17, 24). For instance, in three-spine stickleback (Gasterosteus aculeatus), offspring of mothers exposed to predator cues tended to shoal closer together (17) but did so only before but not during or after an attack. Additionally, they were more often victims of predator attacks, probably because they were less vigilant (22), and they had deficits in learning abilities (25). 3) Offspring from predator-exposed mothers may show reduced mobility compared to offspring from unexposed control mothers [e.g., in spider mites, Tetranychus urticae (23, 26), and crickets, Gryllus pennsylvanicus (27)]; however, when offspring performed these putatively adaptive antipredator behavior, this involved high opportunity costs, such as reduced foraging time (15, 20) (details reviewed in SI Appendix, Table S1).Thus, despite the general interest in studying maternal effects on antipredator behavior, we are currently lacking clear evidence for adaptive antipredator behavior in offspring that has been induced by maternal effects. Ideally, a test for such effects should focus on behaviors that 1) have been proven to aid predator evasion and 2) do not inflict considerable opportunity costs (e.g., costs on foraging). Fast-start escape responses such as the “C-start” reflexes of fish (28) fulfill these conditions perfectly. These reflexes are very short, in the range of a few seconds to immediately escape the predator, thus inflicting virtually no opportunity costs on time-consuming vital activities such as foraging. In fish, C-start reflexes are governed by a single action potential determining not only whether an escape response will occur but also the direction of the escape. These reflexes are elicited by the giant Mauthner neurons or “M-cells” located in the hindbrain (29). When the functioning of M-cells in zebrafish larvae prey was experimentally disabled, predators had a three times higher capture success (30). Moreover, in white-tailed damselfish (Pomacentrus chrysurus), out of 18 morphological, physiological, and behavioral parameters, C-start response latencies to an experimental startle stimulus explained best the long-term survival of juveniles (31). However, despite the obvious adaptive value of escape reflexes for prey survival, it is yet unknown whether they can be modulated by maternal effects.We hypothesized that mothers living in high-risk environments might induce faster C-start reflexes in offspring, which would render unequivocal evidence for adaptive predator-induced maternal effects on offspring behavior. While generally, parental effects may be conveyed to offspring by parental behavior (32–35) or by the modification of gametes (17, 36–38), in this study, we hypothesized that the maternal effects on offspring evasion behavior are transmitted through the eggs if mothers are exposed to predator cues during egg maturation. Consequently, we further hypothesized that treatment differences in these offspring will manifest already in the egg and fry stage. We performed two experiments to investigate predator-induced maternal effects on escape behavior and its putative underlying mechanisms in a cooperatively breeding vertebrate, the cichlid fish Neolamprologus pulcher. In these fish, young of recent clutches delay dispersal from the natal territory greatly beyond the time of independence from parental care and help raise the offspring of a dominant breeder pair, thereby often forgoing their own reproduction. Maternal effects enhancing offspring survival and antipredator behavior will primarily increase the direct fitness of parents, but in this species, selection of maternal effects might be further strengthened via positive feedback on maternal fitness because all surviving offspring stay at the natal territory as alloparental brood care helpers at least until they are sexually mature.If the maternal exposure to predators results in specific antipredator adaptations, we predicted 1) that offspring from predator-exposed female N. pulcher will exhibit faster C-start reflex responses (17) with a higher total protein content and with more steroids and other lipids owing to their role in offspring growth (39) and antipredator responses (40). 3) Larger eggs should result in larger offspring (41). A larger size of offspring is considered an important adaptation to evade gape-size limited predation (42), which is strong particularly in small juvenile N. pulcher, and it enhances the burst swim speed (42). 4) The larger offspring size from parents exposed to predation threat should be accompanied by a higher expression of genes of the somatotropic axis in these offspring (Number in textCategoryTraitPredictions for offspring from predator-exposed parentsAntipredator adaptations(1)BehaviorOnset of C-start reflexFaster(2)Egg traitEgg weightHigher (17)Total protein contentHigher (39)Metabolite compositionHigher deposition of steroidal compounds and metabolites related to the somatotropic and stress axis (17)(3)Size/growthOffspring size at fry stageLarger (41, 100)Growth until 3 moFaster (100)(4)Gene expressionExpression of three key somatotropic genes: igf-1, ghr, and igf-2Higher (indicating higher growth) (100)General stress responsiveness(5)BehaviorSeek shelterMore readily immediately after threat and generally more often(6)Gene expressionExpression of grLower, as it is involved in negative feedback on hypothalamic-pituitary-adrenal/interrenal (HPA/HPI) stress responses (101)Expression of mrHigher, as membrane-bound MRs boost initial stress responses (101)Open in a separate windowAlternatively, although not mutually exclusively, maternal predator exposure may lead to an enhanced general stress responsiveness in offspring. If this were the case, 5) we should expect offspring to be generally more anxious (e.g., to seek shelter more readily and often; see 相似文献   

Biome boundary maintained by intense belowground resource competition in world’s thinnest-rooted plant community

Recent findings point to plant root traits as potentially important for shaping the boundaries of biomes and for maintaining the plant communities within. We examined two hypotheses: 1) Thin-rooted plant strategies might be favored in biomes with low soil resources; and 2) these strategies may act, along with fire, to maintain the sharp boundary between the Fynbos and Afrotemperate Forest biomes in South Africa. These biomes differ in biodiversity, plant traits, and physiognomy, yet exist as alternative stable states on the same geological substrate and in the same climate conditions. We conducted a 4-y field experiment to examine the ability of Forest species to invade the Fynbos as a function of growth-limiting nutrients and belowground plant–plant competition. Our results support both hypotheses: First, we found marked biome differences in root traits, with Fynbos species exhibiting the thinnest roots reported from any biome worldwide. Second, our field manipulation demonstrated that intense belowground competition inhibits the ability of Forest species to invade Fynbos. Nitrogen was unexpectedly the resource that determined competitive outcome, despite the long-standing expectation that Fynbos is severely phosphorus constrained. These findings identify a trait-by-resource feedback mechanism, in which most species possess adaptive traits that modify soil resources in favor of their own survival while deterring invading species. Our findings challenge the long-held notion that biome boundaries depend primarily on external abiotic constraints and, instead, identify an internal biotic mechanism—a selective feedback among traits, plant–plant competition, and ecosystem conditions—that, along with contrasting fire regime, can act to maintain biome boundaries.

Recent findings (1) have demonstrated striking differences in plant rooting strategies across biomes worldwide, spawning the hypothesis that belowground competition for soil resources may be critical for maintaining biome boundaries (1, 2). This idea differs fundamentally from the historical notion that biomes primarily are delineated by extrinsic abiotic factors such as climate, geological parent material, or topography (3–8), or the more recent recognition that aboveground plant adaptations can promote fire-determined plant communities (9, 10).Belowground competition introduces a biotic mechanism that is intrinsic to the plant community, emerges from plant–plant contest for resources, and may help explain the puzzling observation that biome boundaries can persist independent of climate–geological factors (4, 10).Of central importance is Ma et al.’s (1) recent observation that root traits that are associated with resource uptake appear to differ across biomes with differing soil resource dynamics. Specifically, Ma et al. hypothesized that thin-rooted plant strategies may be favored in biomes with permanently or seasonally low soil resources. They reasoned that, in those conditions, natural selection would favor absorptive roots [i.e., first-order roots (1, 11)] with low diameter and high specific root length (i.e., root length per unit photosynthetic carbon invested), which, in turn, are traits that allow high root surface area and efficient exploration of resource-poor soils. Conversely, thick roots and low specific root length may remain competitive traits in biomes with abundant soil resources, despite reduced root surface area and less efficient soil exploration.Here we test Ma et al.’s hypothesis (1) using a unique study of root traits and plant–plant resource competition across the boundary of two distinct biomes within the Cape Floristic Region of South Africa: Fynbos and Afrotemperate Forest. We show in Fig. 1 and 12, 13), by slow decomposition and nutrient recycling (14), and by low stores of soil organic matter (15). In contrast, the Afrotemperate Forest biome is defined by a substantial accumulation of soil organic matter and organic-bound nutrients, which, in turn, supports high rates of plant–soil–nutrient recycling. Based on Ma et al.’s hypothesis, we would expect that these sharp differences in soil resource conditions would result in divergent belowground root traits across the biome boundary.Open in a separate windowFig. 1.Sharp differences in biodiversity, aboveground plant traits, and ecosystem properties across the South African Fynbos–Forest boundary. (A) Two neighboring biomes of the Cape Floristic Region—the Fynbos (62) and the Afrotemperate Forest (63)—form a sharp boundary despite perching on the same geological parent material (39). (B) Biodiversity: The hyperdiverse Fynbos harbors >7,000 plant species, of which the majority are endemic to South Africa (64). The Afrotemperate Forest, on the other hand, contains >450 species with less endemism (63). (C) Aboveground plant traits: Fynbos species generally possess thick and small leaves with a high carbon-to-nitrogen (C:N) ratio while Afrotemperate Forest species display thinner and larger leaves with a lower C:N ratio. In addition, Fynbos plant species possess traits that either enhance (e.g., waxes) or resist (e.g., thick bark) fire. For example, Fynbos vegetation contains high concentrations of flammable organic compounds (e.g., crude fat content) that can facilitate very hot fires (65). In contrast, Afrotemperate Forest species tend to be sensitive to fire and possess traits that suppress fire (e.g., high water content). (D) Ecosystem properties: Fynbos soils are exceedingly poor in soil carbon, nitrogen, and phosphorus contents. In contrast, the Afrotemperate Forest soil is characterized by a developed layer rich in carbon, nitrogen, and phosphorus, which facilitates active cycling of nutrients between plant and soil pools (66, 67).Table 1.Comparison of neighboring Fynbos and Afrotemperate Forest

Children across societies enforce conventional norms but in culturally variable ways

Individuals in all societies conform to their cultural group’s conventional norms, from how to dress on certain occasions to how to play certain games. It is an open question, however, whether individuals in all societies actively enforce the group’s conventional norms when others break them. We investigated third-party enforcement of conventional norms in 5- to 8-y-old children (n = 376) from eight diverse small-scale and large-scale societies. Children learned the rules for playing a new sorting game and then, observed a peer who was apparently breaking them. Across societies, observer children intervened frequently to correct their misguided peer (i.e., more frequently than when the peer was following the rules). However, both the magnitude and the style of interventions varied across societies. Detailed analyses of children’s interactions revealed societal differences in children’s verbal protest styles as well as in their use of actions, gestures, and nonverbal expressions to intervene. Observers’ interventions predicted whether their peer adopted the observer’s sorting rule. Enforcement of conventional norms appears to be an early emerging human universal that comes to be expressed in culturally variable ways.

Norms regulate how members of a group ought to behave and enable social cohesion, coordination, and large-scale cooperation (1–3). Compliance with norms depends, among other things, on formal and informal mechanisms for sanctioning those who deviate from established norms (4–6). To date, the study of how group members in different societies sanction each other in informal ways has primarily focused on third-party enforcement of social and moral norms,^* including fairness norms about resource distribution (9–14), cooperative norms in cattle raids (15, 16), ownership norms (17), and norms against harming others (17, 18). Violations of social and moral norms impact others in significant ways and so, often evoke strong emotional reactions and enforcement against violators (19).Social and moral norm violations, however, do not represent the full range of norm violations that people encounter in their everyday lives (20). Societies also have a plethora of conventional norms: rules that determine how people ought to dress, greet each other, eat, play certain games, and behave in certain public fora like funerals or weddings (21). In contrast to moral and social norms, conventional norms coordinate behavior in arbitrary ways and within some constraints (22), can be altered by consensus or authorities (8, 23). For example, shaking hands, bumping fists, or bowing to each other all achieve the same goal of coordinating how we greet each other. The reason why we follow one rule or the other is because this is how “we” do things as a group. As conventional norms involve conformity mostly for its own sake, they present an ideal test case for the extent to which different communities informally sanction or tolerate rule transgressions.Some studies have found that young children actively enforce conventional norms by protesting, correcting others, or reminding them of the rules, even as uninvolved third parties (24–32). However, this research has been carried out exclusively with children from middle-class families in Europe and North America, and there exists, to date, no systematic cross-cultural study on conventional norm enforcement and its intercultural variability. There is some indication that children’s reasoning about conventional rules differs between societies (33, 34). Moreover, studies with adults have found cross-national variation in ratings about norm compliance and tolerance of deviant behaviors (i.e., so-called “loose” and “tight” cultures) (35) as well as in judgements about how to respond appropriately to conventional norm violations (i.e., metanorms about sanctions) (20). These previous studies, however, used ratings or judgements of hypothetical scenarios and provide only limited insight into actual behavior—children and adults may think that conventional norms should be enforced in a certain way but may not take the risk of actually sanctioning others. In addition, these studies have mostly taken place in urban, large-scale societies, and there is evidence from cross-cultural research on costly third-party enforcement of fairness norms that use of informal sanctions increases with community size (12, 14), likely because small-scale communities often rely on other mechanisms such as direct reciprocity and reputation management (36). It is an open question whether small-scale communities also engage in less third-party enforcement of conventional norms than large, urban populations, and it is possible that egalitarian hunter-gatherer communities may be particularly tolerant of conventional transgressions (37) and not show any enforcement.We, therefore, conducted a comprehensive study with 376 (5- to 8-y-old) children from eight diverse small- and large-scale societies (SI Appendix). The study included children from three urban locations on three different continents (South America, Europe, Asia) and from five rural locations on two continents (South America, Africa). The sites differed substantially in community sizes, ranging from rural dwellings of a few hundred people to cities with millions of inhabitants; in the languages spoken; and in their economic activities, including wage labor, agriculture, and (recently sedentized) hunter-gatherers. This resulted in a maximally diverse sample (13, 38–40) and ensured diversity in both rural and urban locations, avoiding simplistic dichotomies of urban Global North vs. rural Global South (41). Children were slightly older than children in previous norm enforcement studies in Europe (28, 30) but fell within the age range in which societal differences in normative behaviors such as sharing behavior and respect for ownership emerge (38–40, 42, 43).Table 1.Overview of participants and societies in the study