Sea spray aerosol concentration modulated by sea surface temperature

Natural aerosols in pristine regions form the baseline used to evaluate the impact of anthropogenic aerosols on climate. Sea spray aerosol (SSA) is a major component of natural aerosols. Despite its importance, the abundance of SSA is poorly constrained. It is generally accepted that wind-driven wave breaking is the principle governing SSA production. This mechanism alone, however, is insufficient to explain the variability of SSA concentration at given wind speed. The role of other parameters, such as sea surface temperature (SST), remains controversial. Here, we show that higher SST promotes SSA mass generation at a wide range of wind speed levels over the remote Pacific and Atlantic Oceans, in addition to demonstrating the wind-driven SSA production mechanism. The results are from a global scale dataset of airborne SSA measurements at 150 to 200 m above the ocean surface during the NASA Atmospheric Tomography Mission. Statistical analysis suggests that accounting for SST greatly enhances the predictability of the observed SSA concentration compared to using wind speed alone. Our results support implementing SST into SSA source functions in global models to better understand the atmospheric burdens of SSA.

Over two-thirds of the Earth is covered by the ocean. The material exchange between the ocean and the atmosphere affects the balance of the Earth’s energy on a global scale (1). Sea spray aerosol (SSA) is the major particulate material directly emitted from the ocean. Studies have shown that SSA dominates the aerosol mass in the marine boundary layer (MBL). Such dominance renders SSA an important player in climate change (2). However, the exact processes by which the SSA is introduced to the atmosphere still remains to be learned, making the SSA budget highly uncertain (3).It is generally established that SSA is produced by mechanical processes (4–6). Wind stress induces breaking waves that entrain bubbles into the surface ocean (7). Film and jet drops formed during bubble bursting are the main sources of SSA particles (8). The wind-driven mechanism is supported by the positive correlation between wind speed and SSA concentration from field observations (9, 10). Therefore, wind speed is used as the sole parameter to characterize SSA in many models (1, 4, 11).In addition to wind speed, sea surface temperature (SST) may play a large role in SSA production (12–15). SST affects the drop formation process by modifying the physical properties of the surface ocean water. An increase of SST reduces the kinematic viscosity and surface tension of the ocean, thereby enhancing the entrainment efficiency and rising speed of bubbles (12, 16). As a result, the number size distribution of the bubbles may change, leading to varying SSA properties (14, 15, 17).Limited laboratory and field studies regarding the effects of SST on SSA production have shown disparate results. Some argue that SSA production is independent of SST (18) or suppressed by increasing SST (14, 15, 19, 20) from 0 to 10 °C, while other laboratory (12, 21–23) and field measurements (3, 5) suggest that SSA production increases monotonically with water temperature. Furthermore, recent observations in the remote Atlantic Ocean shows that increasing SST enhances the modal mean diameter of SSA (24). On the other hand, model simulations have demonstrated that incorporating SST into SSA source functions generally improves the SSA prediction (3, 25, 26). The inconsistency in the previous work suggests that the impacts of SST on SSA formation remain unclear.In this study, we conducted unprecedented aircraft measurements of SSA concentration on a global scale during the Atmospheric Tomography Mission (ATom). These measurements consist of a series of flights spanning three seasons (summer, fall, and winter) over remote oceans (Fig. 1 and SI Appendix, Fig. S1). Our observations again confirm that wind speed is the dominant factor controlling the concentration of SSA. Further, we show that increasing SST enhances the mass concentration of SSA.Open in a separate windowFig. 1.Flight tracks during ATom2. The color indicates the flight altitude. The size of the markers represents the sea salt number fraction. The inset in the bottom right shows the vertical profile of sea salt number fraction. The flight tracks during ATom3 and ATom4 are similar to ATom2.     

Seasonal drought events in tropical East Asia over the last 60,000 y

The cause of seasonal hydrologic changes in tropical East Asia during interstadial/stadial oscillations of the last glaciation remains controversial. Here, we show seven seasonal drought events that occurred during the relatively warm interstadials by phytolith and pollen records. These events are significantly manifested as high percentages of bilobate phytoliths and are consistent with the large zonal sea-surface temperature (SST) gradient from the western to eastern tropical Pacific, suggesting that the reduction in seasonal precipitation could be interpreted by westward shifts of the western Pacific subtropical high triggered by changes of zonal SST gradient over the tropical Pacific and Hadley circulation in the Northern Hemisphere. Our findings highlight that both zonal and meridional ocean–atmosphere circulations, rather than solely the Intertropical Convergence Zone or El Niño-Southern Oscillation, controlled the hydrologic changes in tropical East Asia during the last glaciation.

The tropics are home to regions of central importance to global hydrologic cycles. As an important hydrological parameter, seasonal precipitation underwent profound changes in the tropical oceans and their adjacent continents on different timescales during the last glaciation (1). However, the features and mechanisms that caused seasonal precipitation changes during interstadial/stadial oscillations of the last glacial–interglacial cycle in tropical regions remain controversial (2). Two contrasting hypotheses were proposed to explain these changes. Both of these hypotheses involve interactions between the meridional Hadley and zonal Walker circulations as well as changes in sea-surface temperature (SST) (3).The first hypothesis invokes tropical SST changes in response to a slowdown of the Atlantic Meridional Overturning Circulation (AMOC) triggered by large iceberg discharges in the North Atlantic during the stadials (4, 5) and the resulting shift of the intertropical convergence zone (ITCZ). This AMOC-forced southward movement of the ITCZ caused antiphase changes in seasonal rainfall between north and south of the equator in the tropical Pacific and its adjacent continents on the millennium scale (6–9). The second hypothesis attributes the changes in the tropical atmosphere–ocean dynamics stimulated by tropical SST changes (e.g., El Niño-Southern Oscillation, ENSO) (10, 11) as the cause of seasonal heavy/light rainfall in the eastern/western tropical Pacific during the Heinrich stadials (12).However, most of the evidence supporting these two hypotheses comes from the Atlantic (13) and the tropical Pacific (1, 12, 14). Limited evidence is from tropical continents, and particularly little evidence is available from terrestrial tropical East Asia, where the mechanisms responsible for seasonal precipitation changes are still under debate. Although the oxygen isotopes of stalagmites on land have been viewed as one of the most robust East Asian summer monsoon records, the interpretation of speleothem δ¹⁸O in China remains controversial (15–17). Therefore, to demonstrate these hypotheses, both unique research sites, which could simultaneously receive continental and tropical ocean signals, and unambiguous proxies, which could reflect annual and seasonal precipitation, are urgently needed.The core studied in this paper is located at Huguangyan Maar Lake (HML) in Guangdong, southern coast of China (110°17′ E, 21°9′ N, 23 m above sea level) (Fig. 1). This region is closely influenced by Hadley circulation (HC) over the continent and Walker circulation (WC) over the tropical Pacific (18, 19), as well as the related changes in the western Pacific subtropical high (WPSH) (19, 20). Here, we present two sets of proxy datasets. One proxy is the phytolith record, a reliable indicator for the evaluation of seasonal–annual Poaceae in ecosystems (21, 22); and Poaceae taxa are more sensitive than arboreal taxa in revealing seasonal hydrological changes (21, 22). The other proxy is the pollen record, which is an indicator of annual precipitation and reflects the general paleoclimate features at low latitudes in East Asia (23–29). Therefore, based on the two contrasting proxies, the successive 60,000-y phytolith and pollen sequences in this study could substantially reveal the mechanism of regional seasonal precipitation changes during stadials/interstadials since the last glacial period in northern tropical East Asia.Open in a separate windowFig. 1.Geographical and climatological settings of study site and region. (A) Topographic map from ENVI 5.1 showing the location of study site (red star, Huguangyan Maar Lake, HML) in south China and seasonal positions of ITCZ (30). (B) Schematic map showing the settings of atmospheric circulations and SSTs in the tropical Pacific. Black solid circles indicate cores mentioned in this paper: 1 = MD98-2181, 2 = ODP806B, 3 = MD02-2529, 4 = ME0005A-24JC, 5 = ODP846, 6 = TR163-22, and 7 = TR163-19. Colors are annual mean SSTs from the period 1981–2010 obtained from https://psl.noaa.gov.     

The impact of identity by descent on fitness and disease in dogs

Domestic dogs have experienced population bottlenecks, recent inbreeding, and strong artificial selection. These processes have simplified the genetic architecture of complex traits, allowed deleterious variation to persist, and increased both identity-by-descent (IBD) segments and runs of homozygosity (ROH). As such, dogs provide an excellent model for examining how these evolutionary processes influence disease. We assembled a dataset containing 4,414 breed dogs, 327 village dogs, and 380 wolves genotyped at 117,288 markers and data for clinical and morphological phenotypes. Breed dogs have an enrichment of IBD and ROH, relative to both village dogs and wolves, and we use these patterns to show that breed dogs have experienced differing severities of bottlenecks in their recent past. We then found that ROH burden is associated with phenotypes in breed dogs, such as lymphoma. We next test the prediction that breeds with greater ROH have more disease alleles reported in the Online Mendelian Inheritance in Animals (OMIA). Surprisingly, the number of causal variants identified correlates with the popularity of that breed rather than the ROH or IBD burden, suggesting an ascertainment bias in OMIA. Lastly, we use the distribution of ROH across the genome to identify genes with depletions of ROH as potential hotspots for inbreeding depression and find multiple exons where ROH are never observed. Our results suggest that inbreeding has played a large role in shaping genetic and phenotypic variation in dogs and that future work on understudied breeds may reveal new disease-causing variation.

The unique demographic and selective history of dogs has enabled the persistence of deleterious variation, simplified genetic architecture of complex traits, and caused an increase in both runs of homozygosity (ROH) and identity-by-descent (IBD) segments within breeds (1–6). Specifically, the average F_ROH was ∼0.3 in dogs (7), compared to 0.005 in humans, computed from the 1000 Genomes populations (8). The large amount of the genome in ROH in dogs, combined with a wealth of genetic variation and phenotypic data (2, 5, 7, 9–11), allow us to test how ROH and IBD influence complex traits and fitness (Fig. 1). Furthermore, many of the deleterious alleles within dogs likely arose relatively recently within a breed, and dogs tend to share similar disease pathways and genes with humans (4, 12, 13), increasing their relevance for complex traits in humans.Open in a separate windowFig. 1.Potential mechanisms for associations between ROH and phenotypes that depend on recessive mutations. If a recessive deleterious mutation is nonlethal (blue), it may lead to ROH correlating with disease, while lethal (red) recessive mutations will cause a depletion of ROH.Despite IBD segments and ROH being ubiquitous in genomes, the extent to which they affect the architecture of complex traits as well as reproductive fitness has remained elusive. Given that ROH are formed by inheritance of the same ancestral chromosome from both parents, there is a much higher probability of the individual to become homozygous for a deleterious recessive variant (8, 14), leading to a reduction in fitness. This prediction was verified in recent work in nonhuman mammals that has shown that populations suffering from inbreeding depression tend to have an increase in ROH (15, 16). ROH in human populations are enriched for deleterious variants (8, 14, 17). However, the extent to which ROH impact phenotypes remains unclear. For example, several studies have associated an increase in ROH with complex traits in humans (18–23), though some associations remain controversial (24–28). Determining how ROH and IBD influence complex traits and fitness could provide a mechanism for differences in complex-trait architecture across populations that vary in their burden of IBD and ROH.Here, we use IBD segments and ROH from 4,741 breed dogs and village dogs, and 380 wolves to determine the recent demographic history of dogs and wolves and establish a connection between recent inbreeding and deleterious variation associated with both disease and inbreeding depression. This comprehensive dataset contains genotype data from 172 breeds of dog, village dogs from 30 countries, and gray wolves from British Colombia, North America, and Europe. We test for an association with the burden of ROH and case-control status for a variety of complex traits. Remarkably, we also find that the number of disease-associated causal variants identified in a breed is positively correlated with breed popularity rather than burden of IBD or ROH in the genome, suggesting ascertainment biases also exist in databases of dog disease mutations and that many breeds of dog are understudied. Lastly, we identify multiple loci that may be associated with inbreeding depression by examining localized depletions of ROH across dog genomes.     

From the Cover: Neurophysiological coordination of duet singing

Coordination of behavior for cooperative performances often relies on linkages mediated by sensory cues exchanged between participants. How neurophysiological responses to sensory information affect motor programs to coordinate behavior between individuals is not known. We investigated how plain-tailed wrens (Pheugopedius euophrys) use acoustic feedback to coordinate extraordinary duet performances in which females and males rapidly take turns singing. We made simultaneous neurophysiological recordings in a song control area “HVC” in pairs of singing wrens at a field site in Ecuador. HVC is a premotor area that integrates auditory feedback and is necessary for song production. We found that spiking activity of HVC neurons in each sex increased for production of its own syllables. In contrast, hearing sensory feedback produced by the bird’s partner decreased HVC activity during duet singing, potentially coordinating HVC premotor activity in each bird through inhibition. When birds sang alone, HVC neurons in females but not males were inhibited by hearing the partner bird. When birds were anesthetized with urethane, which antagonizes GABAergic (γ-aminobutyric acid) transmission, HVC neurons were excited rather than inhibited, suggesting a role for GABA in the coordination of duet singing. These data suggest that HVC integrates information across partners during duets and that rapid turn taking may be mediated, in part, by inhibition.

Animals routinely rely on sensory feedback for the control of their own behavior. In cooperative performances, such sensory feedback can include cues produced by other participants (1–8). For example, in interactive vocal communication, including human speech, individuals take turns vocalizing. This “turn taking” is a consequence of each participant responding to auditory cues from a partner (4–6, 9, 10). The role of such “heterogenous” (other-generated) feedback in the control of vocal turn taking and other cooperative performances is largely unknown.Plain-tailed wrens (Pheugopedius euophrys) are neotropical songbirds that cooperate to produce extraordinary duet performances but also sing by themselves (Fig. 1A) (4, 10, 11). Singing in plain-tailed wrens is performed by both females and males and used for territorial defense and other functions, including mate guarding and attraction (1, 11–16). During duets, female and male plain-tailed wrens take turns, alternating syllables at a rate of between 2 and 5 Hz (Fig. 1A) (4, 11).Open in a separate windowFig. 1.Neural control of solo and duet singing in plain-tailed wrens. (A) Spectrogram of a singing bout that included male solo syllables (blue line, top) followed by a duet. Solo syllables for both sexes (only male solo syllables are shown here) are sung at lower amplitudes than syllables produced in duets. Note that the smeared appearance of wren syllables in spectrograms reflects the acoustic structure of plain-tailed wren singing. (B and C) Each bird has a motor system that is used to produce song and sensory systems that mediate feedback. (B) During solo singing, the bird hears its own song, which is known as autogenous feedback (orange). (C) During duet singing, each bird hears both its own singing and the singing of its partner, known as heterogenous feedback (green). The key difference between solo and duet singing is heterogenous feedback that couples the neural systems of the two birds. This coupling results in changes in syllable amplitude and timing in both birds.There is a categorical difference between solo and duet singing. In solo singing, the singing bird receives only autogenous (hearing its own vocalization) feedback (Fig. 1B). The partner may hear the solo song if it is nearby, a heterogenous (other-generated) cue. In duet singing, birds receive both heterogenous and autogenous feedback as they alternate syllable production (Fig. 1C). Participants use heterogenous feedback during duet singing for precise timing of syllable production (4, 11). For example, when a male temporarily stops participating in a duet, the duration of intersyllable intervals between female syllables increases (4), showing an effect of heterogenous feedback on the timing of syllable production.How does the brain of each wren integrate heterogenous acoustic cues to coordinate the precise timing of syllable production between individuals during duet performances? To address this question, we examined neurophysiological activity in HVC, a nucleus in the nidopallium [an analogue of mammalian cortex (17, 18)]. HVC is necessary for song learning, production, and timing in species of songbirds that do not perform duets (19–24). Neurons in HVC are active during singing and respond to playback of the bird’s own learned song (25–27). In addition, recent work has shown that HVC is also involved in vocal turn taking (19).To examine the role of heterogenous feedback in the control of duet performances, we compared neurophysiological activity in HVC when female or male wrens sang solo syllables with syllables sung during duets. Neurophysiological recordings were made in awake and anesthetized pairs of wrens at the Yanayacu Biological Station and Center for Creative Studies on the slopes of the Antisana volcano in Ecuador. We found that heterogenous cues inhibited HVC activity during duet performances in both females and males, but inhibition was only observed in females during solo singing.     

Dimensions of invasiveness: Links between local abundance,geographic range size,and habitat breadth in Europe’s alien and native floras

Understanding drivers of success for alien species can inform on potential future invasions. Recent conceptual advances highlight that species may achieve invasiveness via performance along at least three distinct dimensions: 1) local abundance, 2) geographic range size, and 3) habitat breadth in naturalized distributions. Associations among these dimensions and the factors that determine success in each have yet to be assessed at large geographic scales. Here, we combine data from over one million vegetation plots covering the extent of Europe and its habitat diversity with databases on species’ distributions, traits, and historical origins to provide a comprehensive assessment of invasiveness dimensions for the European alien seed plant flora. Invasiveness dimensions are linked in alien distributions, leading to a continuum from overall poor invaders to super invaders—abundant, widespread aliens that invade diverse habitats. This pattern echoes relationships among analogous dimensions measured for native European species. Success along invasiveness dimensions was associated with details of alien species’ introduction histories: earlier introduction dates were positively associated with all three dimensions, and consistent with theory-based expectations, species originating from other continents, particularly acquisitive growth strategists, were among the most successful invaders in Europe. Despite general correlations among invasiveness dimensions, we identified habitats and traits associated with atypical patterns of success in only one or two dimensions—for example, the role of disturbed habitats in facilitating widespread specialists. We conclude that considering invasiveness within a multidimensional framework can provide insights into invasion processes while also informing general understanding of the dynamics of species distributions.

Human socioeconomic activities are altering species’ global distributions, bridging natural dispersal barriers through the accidental and intentional relocation of organisms, and opening opportunities for them to expand into new regions beyond their historic native ranges (1). The outcome of any given introduction event, however, is dependent on ecological and stochastic processes, and many introduced alien species fail to establish and persist (2, 3). Even species that do achieve persistent, self-sustaining populations (i.e., become naturalized sensu ref. 4) show varying degrees of success (i.e., invasiveness) in newly occupied regions. This has been true for natural colonization events throughout Earth’s history [e.g., on islands (5, 6) and during continental biotic interchanges (7–9)] and is certainly the case for the ongoing surge of human-mediated introductions (10–12). Disentangling the factors that lead to invasion success provides an opportunity not only for anticipating and mediating future anthropogenic invasions but also for better understanding the dynamics underlying natural range expansions (13).Quantifying a species’ success in invading the alien range is complex, a fact reflected in the diverse criteria applied by different authorities when deciding whether or not to classify naturalized species as invasive (14). Recent efforts have therefore recognized that invasiveness cannot be captured by a single metric but rather encompasses multiple aspects of ecological success and impact (15, 16). Some proposed metrics, such as spread rate and socioeconomic impacts, are difficult to quantify for large numbers of species (4, 17). However, Rabinowitz’s three-dimensional scheme for characterizing the rarity or commonness of species in their native distributions (18, 19) has been successfully co-opted as a valuable perspective for better understanding the success of alien species (16, 20, 21). Applied in the context of introduced species, this framework recognizes the potential for established aliens to vary along at least three demographic dimensions of invasiveness: 1) in local abundance within the naturalized range, 2) in geographic range size or extent of the naturalized range, and 3) in habitat breadth in the naturalized range (16). We subsequently distinguish these metrics as dimensions of invasiveness when measured in the naturalized distributions of alien species and dimensions of commonness when measured in species native distributions.Considering invasiveness within a multidimensional framework is particularly important if species vary independently among different dimensions (16, 21). Such a scenario opens the possibility for aliens to achieve invasion success in many different ways (Fig. 1). In other words, there could exist different forms of invasiveness, similar to the different forms of rarity or commonness originally proposed by Rabinowitz (19). On the other hand, theoretical concepts and empirical examples suggest correlations between Rabinowitz’s dimensions of commonness among species in their native distributions (6, 22, 23). For example, a positive relationship between local abundance and extent of geographic occurrence or range size has been documented at various scales for numerous taxa (24–26), including plants (24, 27–31), with niche breadth proposed as a linking mechanism (24, 26, 32). If the processes that generate these patterns in native distributions act similarly in species alien distributions, some of the forms of invasiveness outlined in Fig. 1 should be less likely to occur than others. More specifically, if the invasiveness dimensions are correlated, species should vary from excelling (abundant, widespread, generalists; form AWG in Fig. 1) to performing poorly (scarce, restricted, specialists; form 0 in Fig. 1) in all three invasiveness dimensions (33). On the other hand, these macroecological patterns are not without exception, and a recent assessment found little support for correlations among commonness dimensions in Europe’s native flora (34). Alien distributions may further differ because aliens vary in their residence time, and particularly recently introduced species may be in disequilibrium and still increasing along one or more of the invasiveness dimensions (21, 35–37). In line with these alternatives, a continuum from overall poor invaders to species succeeding in all three dimensions has been documented for the regional alien flora of French grassland communities (20), while associations among dimensions were found to be low for the herbaceous alien flora of Southeast Australia (16). The correspondence among different invasiveness dimensions at broader geographic scales has yet to be assessed.Open in a separate windowFig. 1.Conceptual diagram outlining the eight different forms of invasiveness depending on success in zero, one, two, or three dimensions of invasiveness (based on refs. 16, 18, and 20). Forms of invasiveness within the cyan polygon are associated with high naturalized abundance, within the magenta polygon with widespread naturalized geographic extent, and within the yellow polygon with high naturalized habitat breadth. The overlap between magenta and cyan is blue, between cyan and yellow is green, between magenta and yellow is red, and between all three is black. The forms of invasiveness are comparable to analogous forms of commonness used to describe species in their native distributions, and we refer to the same abbreviations in both cases.Functional traits play a role in mediating invasion processes, but efforts to identify characteristics of successful invaders have generally resulted in few or inconsistent associations (38, 39). However, distinguishing between different components of invasiveness may provide additional clarity if each is influenced by different traits or if the same trait has contrasting effects on different dimensions (15, 16, 21, 40, 41). For example, many plant traits are associated with general trade-offs between rapid growth (i.e., acquisitive growth strategies) versus stress tolerance and survival (i.e., conservative growth strategies) (42–44), and one can hypothesize scenarios where these divergent strategies are associated with success in different dimensions of invasiveness (40, 41). Another example are specialized adaptations for long-distance dispersal that may promote rapid range expansion, both in extent and into new habitats, but likely do not provide any advantages that would influence local abundances (45, 46). For habitat specialists, their specific habitat associations may additionally be important for determining whether or not they become widespread (31).A number of hypotheses for invasion success additionally emphasizes the importance of unique ecological dynamics that emerge when species are decoupled from constraints experienced in their native environments (47). For example, because species are able to occupy unfilled niches where introduced [i.e., Darwin’s naturalization hypothesis (48, 49)] or because they leave behind important herbivores, competitors, or pathogens that limit populations in the native distribution [i.e., enemy release (50, 51)]. These mechanisms may be less likely when species expand into areas near the native range, for example, during natural range expansions or intracontinental introductions, as the alien individuals are more likely to encounter conditions similar to those that limited their native distribution compared to species introduced from further abroad (e.g., those with extracontinental origins) (52–54).Here, we combine vegetation plot data covering Europe (55) with databases of alien and native distributions (56, 57), plant traits (58, 59), and historical dates of introduction (60) to provide a comprehensive assessment of multidimensional invasion success for the European alien seed plant flora. First, we test for correlations among local abundance, geographic extent, and habitat breadth of alien species in their naturalized distributions and classify species into one of the eight forms of invasiveness (Fig. 1). We ask whether some forms of invasiveness rarely occur and specifically whether species tend to fit along a continuum ranging from generally poor invaders to super invaders—species excelling in all three dimensions. In addition, we compare relationships among dimensions of invasiveness to those among dimensions of commonness measured for Europe’s native flora, assessing similarities and differences in patterns of distribution between contexts. Next, we explore likely drivers of each invasiveness dimension, testing whether the year of first alien occurrence in Europe, functional traits related to ecological strategies, specialized adaptations for long-distance dispersal, habitat associations, and region of origin explain different forms of invasion success.     

Paleocene latitude of the Kohistan–Ladakh arc indicates multistage India–Eurasia collision

We report paleomagnetic data showing that an intraoceanic Trans-Tethyan subduction zone existed south of the Eurasian continent and north of the Indian subcontinent until at least Paleocene time. This system was active between 66 and 62 Ma at a paleolatitude of 8.1 ± 5.6 °N, placing it 600–2,300 km south of the contemporaneous Eurasian margin. The first ophiolite obductions onto the northern Indian margin also occurred at this time, demonstrating that collision was a multistage process involving at least two subduction systems. Collisional events began with collision of India and the Trans-Tethyan subduction zone in Late Cretaceous to Early Paleocene time, followed by the collision of India (plus Trans-Tethyan ophiolites) with Eurasia in mid-Eocene time. These data constrain the total postcollisional convergence across the India–Eurasia convergent zone to 1,350–2,150 km and limit the north–south extent of northwestern Greater India to <900 km. These results have broad implications for how collisional processes may affect plate reconfigurations, global climate, and biodiversity.

Classically, the India–Eurasia collision has been considered to be a single-stage event that occurred at 50–55 million years ago (Ma) (1, 2). However, plate reconstructions show thousands of kilometers of separation between India and Eurasia at the inferred time of collision (3, 4). Accordingly, the northern extent of Greater India was thought to have protruded up to 2,000 km relative to present-day India (5, 6) (Fig. 1). Others have suggested that the India–Eurasia collision was a multistage process that involved an east–west trending Trans-Tethyan subduction zone (TTSZ) situated south of the Eurasian margin (7–9) (Fig. 1). Jagoutz et al. (9) concluded that collision between India and the TTSZ occurred at 50–55 Ma, and the final continental collision occurred between the TTSZ and Eurasia at 40 Ma (9, 10). This model reconciles the amount of convergence between India and Eurasia with the observed shortening across the India–Eurasia collision system with the addition of the Kshiroda oceanic plate. Additionally, the presence of two subduction systems can explain the rapid India–Eurasia convergence rates (up to 16 mm a⁻¹) that existed between 135 and 50 Ma (9), as well as variations in global climate in the Cenozoic (11).Open in a separate windowFig. 1.The first panel is an overview map of tectonic structure of the Karakoram–Himalaya–Tibet orogenic system. Blue represents India, red represents Eurasia, and the Kohistan–Ladakh arc (KLA) is shown in gray. The different shades of blue highlight the deformed margin of the Indian plate that has been uplifted to form the Himalayan belt, and the zones of darker red within the Eurasian plate highlight the Eurasian continental arc batholith. Thick black lines denote the suture zones which separate Indian and Eurasian terranes. The tectonic summary panels illustrate the two conflicting collision models and their differing predictions of the location of the Kohistan–Ladakh arc. India is shown in blue, Eurasia is shown in red, and the other nearby continents are shown in gray. Active plate boundaries are shown with black lines, and recently extinct boundaries are shown with gray lines. Subduction zones are shown with triangular tick marks.While the existence of the TTSZ in the Cretaceous is not disputed, the two conflicting collision models make distinct predictions about its paleolatitude in Late Cretaceous to Paleocene time; these can be tested using paleomagnetism. In the single-stage collision model, the TTSZ amalgamated with the Eurasian margin prior to ∼80 Ma (12) at a latitude of ≥20 °N (13, 14). In contrast, in the multistage model, the TTSZ remained near the equator at ≤10 °N, significantly south of Eurasia, until collision with India (9) (Fig. 1).No undisputed paleomagnetic constraints on the location of the TTSZ are available in the central Himalaya (15–17). Westerweel et al. (18) showed that the Burma Terrane, in the eastern Himalaya, was part of the TTSZ and was located near the equator at ∼95 Ma, but they do not constrain the location of the TTSZ in the time period between 50 and 80 Ma, which is required to test the two collision hypotheses. In the western Himalaya, India and Eurasia are separated by the Bela, Khost, and Muslimbagh ophiolites and the 60,000 km² intraoceanic Kohistan Ladakh arc (19, 20) (Fig. 1). These were obducted onto India in the Late Cretaceous to Early Paleocene (19), prior to the closure of the Eocene to Oligocene Katawaz sedimentary basin (20) (Fig. 1). The Kohistan–Ladakh arc contacts the Eurasian Karakoram terrane in the north along the Shyok suture and the Indian plate in the south along the Indus suture (21) (Fig. 1). Previous paleomagnetic studies suggest that the Kohistan–Ladakh arc formed as part of the TTSZ near the equator in the early Cretaceous but provide no information on its location after 80 Ma (22–25). While pioneering, these studies lack robust age constraints, do not appropriately average paleosecular variation of the geodynamo, and do not demonstrate that the measured magnetizations have not been reset during a subsequent metamorphic episode.     

A solution to a sex ratio puzzle in Melittobia wasps

The puzzling sex ratio behavior of Melittobia wasps has long posed one of the greatest questions in the field of sex allocation. Laboratory experiments have found that, in contrast to the predictions of theory and the behavior of numerous other organisms, Melittobia females do not produce fewer female-biased offspring sex ratios when more females lay eggs on a patch. We solve this puzzle by showing that, in nature, females of Melittobia australica have a sophisticated sex ratio behavior, in which their strategy also depends on whether they have dispersed from the patch where they emerged. When females have not dispersed, they lay eggs with close relatives, which keeps local mate competition high even with multiple females, and therefore, they are selected to produce consistently female-biased sex ratios. Laboratory experiments mimic these conditions. In contrast, when females disperse, they interact with nonrelatives, and thus adjust their sex ratio depending on the number of females laying eggs. Consequently, females appear to use dispersal status as an indirect cue of relatedness and whether they should adjust their sex ratio in response to the number of females laying eggs on the patch.

Sex allocation has produced many of the greatest success stories in the study of social behaviors (1–4). Time and time again, relatively simple theory has explained variation in how individuals allocate resources to male and female reproduction. Hamilton’s local mate competition (LMC) theory predicts that when n diploid females lay eggs on a patch and the offspring mate before the females disperse, the evolutionary stable proportion of male offspring (sex ratio) is (n − 1)/2n (Fig. 1) (5). A female-biased sex ratio is favored to reduce competition between sons (brothers) for mates and to provide more mates (daughters) for those sons (6–8). Consistent with this prediction, females of >40 species produce female-biased sex ratios and reduce this female bias when multiple females lay eggs on the same patch (higher n; Fig. 1) (9). The fit of data to theory is so good that the sex ratio under LMC has been exploited as a “model trait” to study the factors that can constrain “perfect adaptation” (4, 10–13).Open in a separate windowFig. 1.LMC. The sex ratio (proportion of sons) is plotted versus the number of females laying eggs on a patch. The bright green dashed line shows the LMC theory prediction for the haplodiploid species (5, 39). A more female-biased sex ratio is favored in haplodiploids because inbreeding increases the relative relatedness of mothers to their daughters (7, 32). Females of many species adjust their offspring sex ratio as predicted by theory, such as the parasitoid Nasonia vitripennis (green diamonds) (82). In contrast, the females of several Melittobia species, such as M. australica, continue to produce extremely female-biased sex ratios, irrespective of the number of females laying eggs on a patch (blue squares) (15).In stark contrast, the sex ratio behavior of Melittobia wasps has long been seen as one of the greatest problems for the field of sex allocation (3, 4, 14–21). The life cycle of Melittobia wasps matches the assumptions of Hamilton’s LMC theory (5, 15, 19, 21). Females lay eggs in the larvae or pupae of solitary wasps and bees, and then after emergence, female offspring mate with the short-winged males, who do not disperse. However, laboratory experiments on four Melittobia species have found that females lay extremely female-biased sex ratios (1 to 5% males) and that these extremely female-biased sex ratios change little with increasing number of females laying eggs on a patch (higher n; Fig. 1) (15, 17–20, 22). A number of hypotheses to explain this lack of sex ratio adjustment have been investigated and rejected, including sex ratio distorters, sex differential mortality, asymmetrical male competition, and reciprocal cooperation (15–18, 20, 22–26).We tested whether Melittobia’s unusual sex ratio behavior can be explained by females being related to the other females laying eggs on the same patch. After mating, some females disperse to find new patches, while some may stay at the natal patch to lay eggs on previously unexploited hosts (Fig. 2). If females do not disperse, they can be related to the other females laying eggs on the same host (27–31). If females laying eggs on a host are related, this increases the extent to which relatives are competing for mates and so can favor an even more female-biased sex ratio (28, 32–35). Although most parasitoid species appear unable to directly assess relatedness, dispersal behavior could provide an indirect cue of whether females are with close relatives (36–38). Consequently, we predict that when females do not disperse and so are more likely to be with closer relatives, they should maintain extremely female-biased sex ratios, even when multiple females lay eggs on a patch (28, 35).Open in a separate windowFig. 2.Host nest and dispersal manners of Melittobia. (A) Photograph of the prepupae of the leaf-cutter bee C. sculpturalis nested in a bamboo cane and (B) a diagram showing two ways that Melittobia females find new hosts. The mothers of C. sculpturalis build nursing nests with pine resin consisting of individual cells in which their offspring develop. If Melittobia wasps parasitize a host in a cell, female offspring that mate with males inside the cell find a different host on the same patch (bamboo cane) or disperse by flying to other patches.We tested whether the sex ratio of Melittobia australica can be explained by dispersal status in a natural population. We examined how the sex ratio produced by females varies with the number of females laying eggs on a patch and whether or not they have dispersed before laying eggs. To match our data to the predictions of theory, we developed a mathematical model tailored to the unique population structure of Melittobia, where dispersal can be a cue of relatedness. We then conducted a laboratory experiment to test whether Melittobia females are able to directly access the relatedness to other females and adjust their sex ratio behavior accordingly. Our results suggest that females are adjusting their sex ratio in response to both the number of females laying eggs on a patch and their relatedness to the other females. However, relatedness is assessed indirectly by whether or not they have dispersed. Consequently, the solution to the puzzling behavior reflects a more-refined sex ratio strategy.     

From the Cover: Evidence from South Africa for a protracted end-Permian extinction on land

Earth’s largest biotic crisis occurred during the Permo–Triassic Transition (PTT). On land, this event witnessed a turnover from synapsid- to archosauromorph-dominated assemblages and a restructuring of terrestrial ecosystems. However, understanding extinction patterns has been limited by a lack of high-precision fossil occurrence data to resolve events on submillion-year timescales. We analyzed a unique database of 588 fossil tetrapod specimens from South Africa’s Karoo Basin, spanning ∼4 My, and 13 stratigraphic bin intervals averaging 300,000 y each. Using sample-standardized methods, we characterized faunal assemblage dynamics during the PTT. High regional extinction rates occurred through a protracted interval of ∼1 Ma, initially co-occurring with low origination rates. This resulted in declining diversity up to the acme of extinction near the Daptocephalus–Lystrosaurus declivis Assemblage Zone boundary. Regional origination rates increased abruptly above this boundary, co-occurring with high extinction rates to drive rapid turnover and an assemblage of short-lived species symptomatic of ecosystem instability. The “disaster taxon” Lystrosaurus shows a long-term trend of increasing abundance initiated in the latest Permian. Lystrosaurus comprised 54% of all specimens by the onset of mass extinction and 70% in the extinction aftermath. This early Lystrosaurus abundance suggests its expansion was facilitated by environmental changes rather than by ecological opportunity following the extinctions of other species as commonly assumed for disaster taxa. Our findings conservatively place the Karoo extinction interval closer in time, but not coeval with, the more rapid marine event and reveal key differences between the PTT extinctions on land and in the oceans.

Mass extinctions are major perturbations of the biosphere resulting from a wide range of different causes including glaciations and sea level fall (1), large igneous provinces (2), and bolide impacts (3, 4). These events caused permanent changes to Earth’s ecosystems, altering the evolutionary trajectory of life (5). However, links between the broad causal factors of mass extinctions and the biological and ecological disturbances that lead to species extinctions have been difficult to characterize. This is because ecological disturbances unfold on timescales much shorter than the typical resolution of paleontological studies (6), particularly in the terrestrial record (6–8). Coarse-resolution studies have demonstrated key mass extinction phenomena including high extinction rates and lineage turnover (7, 9), changes in species richness (10), ecosystem instability (11), and the occurrence of disaster taxa (12). However, finer time resolutions are central to determining the association and relative timings of these effects, their potential causal factors, and their interrelationships. Achieving these goals represents a key advance in understanding the ecological mechanisms of mass extinctions.The end-Permian mass extinction (ca. 251.9 Ma) was Earth’s largest biotic crisis as measured by taxon last occurrences (13–15). Large outpourings from Siberian Trap volcanism (2) are the likely trigger of calamitous climatic changes, including a runaway greenhouse effect and ocean acidification, which had profound consequences for life on land and in the oceans (16–18). An estimated 81% of marine species (19) and 89% of tetrapod genera became extinct as established Permian ecosystems gave way to those of the Triassic. In the ocean, this included the complete extinction of reef-forming tabulate and rugose corals (20, 21) and significant losses in previously diverse ammonoid, brachiopod, and crinoid families (22). On land, many nonmammalian synapsids became extinct (16), and the glossopterid-dominated floras of Gondwana also disappeared (23). Stratigraphic sequences document a global “coral gap” and “coal gap” (24, 25), suggesting reef and forest ecosystems were rare or absent for up to 5 My after the event (26). Continuous fossil-bearing deposits documenting patterns of turnover across the Permian–Triassic transition (PTT) on land (27) and in the oceans (28) are geographically widespread (29, 30), including marine and continental successions that are known from China (31, 32) and India (33). Continental successions are known from Russia (34), Australia (35), Antarctica (36), and South Africa’s Karoo Basin (Fig. 1 and 37–40), the latter providing arguably the most densely sampled and taxonomically scrutinized (41–43) continental record of the PTT. The main extinction has been proposed to occur at the boundary between two biostratigraphic zones with distinctive faunal assemblages, the Daptocephalus and Lystrosaurus declivis assemblage zones (Fig. 1), which marks the traditional placement of the Permian–Triassic geologic boundary [(37) but see ref. 44]. Considerable research has attempted to understand the anatomy of the PTT in South Africa (38, 39, 45–52) and to place it in the context of biodiversity changes across southern Gondwana (53, 54) and globally (29, 31, 32, 44, 47, 55).Open in a separate windowFig. 1.Map of South Africa depicting the distribution of the four tetrapod fossil assemblage zones (Cistecephalus, Daptocephalus, Lystrosaurus declivis, Cynognathus) and our two study sites where fossils were collected in this study (sites A and B). Regional lithostratigraphy and biostratigraphy within the study interval are shown alongside isotope dilution–thermal ionization mass spectrometry dates retrieved by Rubidge et al., Botha et al., and Gastaldo et al. (37, 44, 80). The traditional (dashed red line) and associated PTB hypotheses for the Karoo Basin (37, 44) are also shown. Although traditionally associated with the PTB, the Daptocephalus–Lystrosaurus declivis Assemblage Zone boundary is defined by first appearances of co-occurring tetrapod assemblages, so its position relative to the three PTB hypotheses is unchanged. The Ripplemead member (*) has yet to be formalized by the South African Committee for Stratigraphy.Decades of research have demonstrated the richness of South Africa’s Karoo Basin fossil record, resulting in hundreds of stratigraphically well-documented tetrapod fossils across the PTT (37, 39, 56). This wealth of data has been used qualitatively to identify three extinction phases and an apparent early postextinction recovery phase (39, 45, 51). Furthermore, studies of Karoo community structure and function have elucidated the potential role of the extinction and subsequent recovery in breaking the incumbency of previously dominant clades, including synapsids (11, 57). Nevertheless, understanding patterns of faunal turnover and recovery during the PTT has been limited by the scarcity of quantitative investigations. Previous quantitative studies used coarsely sampled data (i.e., assemblage zone scale, 2 to 3 Ma time intervals) to identify low species richness immediately after the main extinction, potentially associated with multiple “boom and bust” cycles of primary productivity based on δ¹³C variation during the first 5 My of the Triassic (41, 58). However, many details of faunal dynamics in this interval remain unknown. Here, we investigate the dynamics of this major tetrapod extinction at an unprecedented time resolution (on the order of hundreds of thousands of years), using sample-standardized methods to quantify multiple aspects of regional change across the Cistecephalus, Daptocephalus, and Lystrosaurus declivis assemblage zones.     

The high-affinity immunoglobulin receptor FcγRI potentiates HIV-1 neutralization via antibodies against the gp41 N-heptad repeat

The HIV-1 gp41 N-heptad repeat (NHR) region of the prehairpin intermediate, which is transiently exposed during HIV-1 viral membrane fusion, is a validated clinical target in humans and is inhibited by the Food and Drug Administration (FDA)-approved drug enfuvirtide. However, vaccine candidates targeting the NHR have yielded only modest neutralization activities in animals; this inhibition has been largely restricted to tier-1 viruses, which are most sensitive to neutralization by sera from HIV-1–infected individuals. Here, we show that the neutralization activity of the well-characterized NHR-targeting antibody D5 is potentiated >5,000-fold in TZM-bl cells expressing FcγRI compared with those without, resulting in neutralization of many tier-2 viruses (which are less susceptible to neutralization by sera from HIV-1–infected individuals and are the target of current antibody-based vaccine efforts). Further, antisera from guinea pigs immunized with the NHR-based vaccine candidate (ccIZN36)₃ neutralized tier-2 viruses from multiple clades in an FcγRI-dependent manner. As FcγRI is expressed on macrophages and dendritic cells, which are present at mucosal surfaces and are implicated in the early establishment of HIV-1 infection following sexual transmission, these results may be important in the development of a prophylactic HIV-1 vaccine.

Membrane fusion between HIV-1 and host cells is mediated by the viral envelope glycoprotein (Env), a trimer consisting of the gp120 and gp41 subunits. Upon interaction with cellular receptors, Env undergoes a dramatic conformational change and forms the prehairpin intermediate (PHI) (1–3), in which the fusion peptide region at the amino terminus of gp41 inserts into the cell membrane. In the PHI, the N-heptad repeat (NHR) region of gp41 is exposed and forms a stable, three-stranded α-helical coiled coil. Subsequently, the PHI resolves when the NHR and the C-heptad repeat (CHR) regions of gp41 associate to form a trimer-of-hairpins structure that brings the viral and cell membranes into proximity, facilitating membrane fusion (Fig. 1).Open in a separate windowFig. 1.HIV-1 membrane fusion. The surface protein of the HIV-1 envelope is composed of the gp120 and gp41 subunits. After Env binds to cell-surface receptors, gp41 inserts into the host cell membrane and undergoes a conformational change to form the prehairpin intermediate. The N-heptad repeat (orange) region of gp41 is exposed in the PHI and forms a three-stranded coiled coil. To complete viral fusion, the PHI resolves to a trimer-of-hairpins structure in which the C-heptad repeat (blue) adopts a helical conformation and binds the NHR region. Fusion inhibitors such as enfuvirtide bind the NHR, preventing viral fusion by inhibiting formation of the trimer of hairpins (1–3). The membrane-proximal external region (red) is located adjacent to the transmembrane (TM) region of gp41.The NHR region of the PHI is a validated therapeutic target in humans: the Food and Drug Administration (FDA)-approved drug enfuvirtide binds the NHR and inhibits viral entry into cells (4, 5). Various versions of the three-stranded coiled coil formed by the NHR have been created and used as vaccine candidates in animals (6–10). The neutralization potencies of these antisera, as well as those of anti-NHR monoclonal antibodies (mAbs) (11–15), are modest and mostly limited to HIV-1 isolates that are highly sensitive to antibody-mediated neutralization [commonly referred to as tier-1 viruses (16)]. These results have led to skepticism about the PHI as a vaccine target.Earlier studies showed that the neutralization activities of mAbs that bound another region of gp41, the membrane-proximal external region (MPER) (Fig. 1), were enhanced as much as 5,000-fold in cells expressing FcγRI (CD64) (17, 18), an integral membrane protein that binds the Fc portion of immunoglobulin G (IgG) molecules with high (nanomolar) affinity (19, 20). This effect was not attributed to phagocytosis and occurred when the cells were preincubated with antibody and washed before adding virus (17, 18). Since the MPER is a partially cryptic epitope that is not fully exposed until after Env engages with cellular receptors (21, 22), these results suggest that by binding the Fc region, FcγRI provides a local concentration advantage for MPER mAbs at the cell surface that enhances viral neutralization (17, 18). While not expressed on T cells, FcγRI is expressed on macrophages and dendritic cells (23), which are present at mucosal surfaces and are implicated in sexual HIV-1 transmission and the early establishment of HIV-1 infection (22–34).Here we investigated whether FcγRI expression also potentiates the neutralizing activity of antibodies targeting the NHR, since that region, like the MPER, is preferentially exposed during viral fusion. We found that D5, a well-characterized anti-NHR mAb (11, 12), inhibits HIV-1 infection ∼5,000-fold more potently in TZM-bl cells expressing FcγRI (TZM-bl/FcγRI cells) than in TZM-bl cells that do not. Further, while antisera from guinea pigs immunized with (ccIZN36)₃, an NHR-based vaccine candidate (7), displayed weak neutralizing activity in TZM-bl cells, they exhibited enhanced neutralization in TZM-bl/FcγRI cells, including against some tier-2 HIV-1 isolates that are more resistant to antibody-mediated neutralization (16) and that serve as benchmarks for antibody-based vaccine efforts. These results indicate that FcγRI can play an important role in neutralization by antibodies that target the PHI. Since these receptors are expressed on cells prevalent at mucosal surfaces thought to be important for sexual HIV-1 transmission, our results motivate vaccine strategies that harness this potentiating effect.     

Heading perception depends on time-varying evolution of optic flow

There is considerable support for the hypothesis that perception of heading in the presence of rotation is mediated by instantaneous optic flow. This hypothesis, however, has never been tested. We introduce a method, termed “nonvarying phase motion,” for generating a stimulus that conveys a single instantaneous optic flow field, even though the stimulus is presented for an extended period of time. In this experiment, observers viewed stimulus videos and performed a forced-choice heading discrimination task. For nonvarying phase motion, observers made large errors in heading judgments. This suggests that instantaneous optic flow is insufficient for heading perception in the presence of rotation. These errors were mostly eliminated when the velocity of phase motion was varied over time to convey the evolving sequence of optic flow fields corresponding to a particular heading. This demonstrates that heading perception in the presence of rotation relies on the time-varying evolution of optic flow. We hypothesize that the visual system accurately computes heading, despite rotation, based on optic acceleration, the temporal derivative of optic flow.

James Gibson first remarked that the instantaneous motion of points on the retina (Fig. 1A) can be formally described as a two-dimensional (2D) field of velocity vectors called the “optic flow field” (or “optic flow”) (1). Such optic flow, caused by an observer’s movement relative to the environment, conveys information about self-motion and the structure of the visual scene (1–15). When an observer translates in a given direction along a straight path, the optic flow field radiates from a point in the image with zero velocity, or singularity, called the focus of expansion (Fig. 1B). It is well known that under such conditions, one can accurately estimate one’s “heading” (i.e., instantaneous direction of translation in retinocentric coordinates) by simply locating the focus of expansion (SI Appendix). However, if there is angular rotation in addition to translation (by moving along a curved path or by a head or eye movement), the singularity in the optic flow field will be displaced such that it no longer corresponds to the true heading (Fig. 1 C and D). In this case, if one estimates heading by locating the singularity, the estimate will be biased away from the true heading. This is known as the rotation problem (14).Open in a separate windowFig. 1.Projective geometry, the rotation problem, time-varying optic flow, and the optic acceleration hypothesis. (A) Viewer-centered coordinate frame and perspective projection. Because of motion between the viewpoint and the scene, a 3D surface point traverses a path in 3D space. Under perspective projection, the 3D path of this point projects onto a 2D path in the image plane (retina), the temporal derivative of which is called image velocity. The 2D velocities associated with all visible points define a dense 2D vector field called the optic flow field. (B–D) Illustration of the rotation problem. (B) Optic flow for pure translation (1.5-m/s translation speed, 0° heading, i.e., heading in the direction of gaze). Optic flow singularity (red circle) corresponds to heading (purple circle). (C) Pure rotation, for illustrative purposes only and not corresponding to any experimental condition (2°/s rightward rotation). (D) Translation + rotation (1.5 m/s translation speed, 0° heading, 2°/s rightward rotation). Optic flow singularity (red circle) is displaced away from heading (purple circle). (E) Three frames from a video depicting movement along a circular path with the line-of-sight initially perpendicular to a single fronto-parallel plane composed of black dots. (F) Time-varying evolution of optic flow. The first optic flow field reflects image motion between the first and second frames of the video. The second optic flow field reflects image motion between the second and third frames of the video. For this special case (circular path), the optic flow field evolves (and the optic flow singularity drifts) only due to the changing depth of the environment relative to the viewpoint. (G) Illustration of the optic acceleration hypothesis. Optic acceleration is the derivative of optic flow over time (here, approximated as the difference between the second and first optic flow fields). The singularity of the optic acceleration field corresponds to the heading direction. Acceleration vectors autoscaled for visibility.Computer vision researchers and vision scientists have developed a variety of algorithms that accurately and precisely extract observer translation and rotation from optic flow, thereby solving the rotation problem. Nearly all of these rely on instantaneous optic flow (i.e., a single optic flow field) (4, 9, 16–25) with few exceptions (26–29). However, it is unknown whether these algorithms are commensurate with the neural computations underlying heading perception.The consensus of opinion in the experimental literature is that human observers can estimate heading (30, 31) from instantaneous optic flow, in the absence of additional information (5, 10, 15, 32–34). Even so, there are reports of systematic biases in heading perception (11); the visual consequences of rotation (eye, head, and body) can bias heading judgments (10, 15, 35–37), with the amount of bias typically proportional to the magnitude of rotation. Other visual factors, such as stereo cues (38, 39), depth structure (8, 10, 40–43), and field of view (FOV) (33, 42–44) can modulate the strength of these biases. Errors in heading judgments have been reported to be greater when eye (35–37, 45, 46) or head movements (37) are simulated versus when they are real, which has been taken to mean that observers require extraretinal information, although there is also evidence to the contrary (10, 15, 33, 40, 41, 44, 47–50). Regardless, to date no one has tested whether heading perception (even with these biases) is based on instantaneous optic flow or on the information available in how the optic flow field evolves over time. Some have suggested that heading estimates rely on information accumulated over time (32, 44, 51), but no one has investigated the role of time-varying optic flow without confounding it with stimulus duration (i.e., the duration of evidence accumulation).In this study, we employed an application of an image processing technique that ensured that only a single optic flow field was available to observers, even though the stimulus was presented for an extended period of time. We called this condition “nonvarying phase motion” or “nonvarying”: The phases of two component gratings comprising each stationary stimulus patch shifted over time at a constant rate, causing a percept of motion in the absence of veridical movement (52). Phase motion also eliminated other cues that may otherwise have been used for heading judgments, including image point trajectories (15, 32) and their spatial compositions (i.e., looming) (53, 54). For nonvarying phase motion, observers exhibited large biases in heading judgments in the presence of rotation. A second condition, “time-varying phase motion,” or “time-varying,” included acceleration by varying the velocity of phase motion over time to match the evolution of a sequence of optic flow fields. Doing so allowed observers to compensate for the confounding effect of rotation on optic flow, making heading perception nearly veridical. This demonstrates that heading perception in the presence of rotation relies on the time-varying evolution of optic flow.     

Plant species richness at archaeological sites suggests ecological legacy of Indigenous subsistence on the Colorado Plateau

Humans have both intentional and unintentional impacts on their environment, yet identifying the enduring ecological legacies of past small-scale societies remains difficult, and as such, evidence is sparse. The present study found evidence of an ecological legacy that persists today within an semiarid ecosystem of western North America. Specifically, the richness of ethnographically important plant species is strongly associated with archaeological complexity and ecological diversity at Puebloan sites in a region known as Bears Ears on the Colorado Plateau. A multivariate model including both environmental and archaeological predictors explains 88% of the variation in ethnographic species richness (ESR), with growing degree days and archaeological site complexity having the strongest effects. At least 31 plant species important to five tribal groups (Navajo, Hopi, Zuni, Ute Mountain Ute, and Apache), including the Four Corners potato (Solanum jamesii), goosefoot (Chenopodium sp.), wolfberry (Lycium pallidum), and sumac (Rhus trilobata), occurred at archaeological sites, despite being uncommon across the wider landscape. Our results reveal a clear ecological legacy of past human behavior: even when holding environmental variables constant, ESR increases significantly as a function of past investment in habitation and subsistence. Consequently, we suggest that propagules of some species were transported and cultivated, intentionally or not, establishing populations that persist to this day. Ensuring persistence will require tribal input for conserving and restoring archaeo-ecosystems containing “high-priority” plant species, especially those held sacred as lifeway medicines. This transdisciplinary approach has important implications for resource management planning, especially in areas such as Bears Ears that will experience greater visitation and associated impacts in the near future.

Local resource abundance is important for determining where in a given landscape humans decide to live. Nearby water, game, soil, and plants provide readily available wild resources for foraging and conditions that allow for cultivation (1–5). However, humans also modify their surrounding environments in order to increase the abundance and diversity of local plant (6–11) and animal (12–15) resources. Such “human niche construction” is a hallmark of ancient and modern societies (16, 17), having positive and negative impacts on global biodiversity while possibly creating enduring ecological legacies (18–21). This may be especially true for more sedentary and dense populations (22, 4) that are more likely to find investment worthwhile (23) and to produce unintentional impacts. Thus, variation in contemporary ecological diversity may in part reflect past land use dynamics and, therefore, be revealed through coupled archaeological and ecological research (24–33).Coupled ecological and archaeological research has led to the discovery of altered patterns of succession resulting from 1) forest clearing and changes in canopy light regime (34, 35), 2) alterations of soil especially linked to food refuse (36, 37), 3) changes in fire regimes (38, 39), and, more rarely, 4) the importation of plant propagules from distant sites of collection (40, 41). Identifying such long-lost dynamics between humans and landscapes can inform conservation aimed at restoring site-specific artifacts, features, and the associated resource base past and present, here termed “archaeo-ecosystems” (42, 43). This would greatly facilitate cross-cultural management of public lands (44) in ways that promote Indigenous health, cultural reclamation, and sovereignty (7, 45). The linkages, however, between ecological legacies, archaeo-ecosystem restoration and cross-cultural management have yet to be systematically tested or practically applied.Here, we offer a formal evaluation of this archaeo-ecosystem approach by using paired archaeological and ecological survey data focused on Puebloan occupation of a region known as Bears Ears on the Colorado Plateau in southeastern Utah (Fig. 1). Puebloan populations modified their environment by constructing terraces and check dams, developing blinds and wing traps, importing exogenous species, and setting fires (4, 22, 46), but investments were not uniform across the region. We test the hypothesis that locations with greater investment indicated by larger and more complex archaeological sites should today have higher richness of culturally significant plant species, here termed ethnographic species richness (ESR), as an enduring legacy of past investment. Our study expands previous work on ecological legacies by using field surveys to develop an explanatory model applied to 265 sites across one million acres of semiarid public lands. It documents the occurrence of uncommon and ethnographically significant plant species associated with those sites and infuses traditional ecological knowledge into proposed management actions for conserving these archaeo-ecosystems. Controlling for underlying environmental variation, our results indicate that past human habitation increases the diversity of plant species important for Indigenous subsistence.Open in a separate windowFig. 1.Location of Bears Ears National Monument in southeastern Utah. The predicted ESR at 265 known archaeological sites across the original and reduced monument boundaries and surrounding region are shown.     

A rate threshold mechanism regulates MAPK stress signaling and survival

Cells are exposed to changes in extracellular stimulus concentration that vary as a function of rate. However, how cells integrate information conveyed from stimulation rate along with concentration remains poorly understood. Here, we examined how varying the rate of stress application alters budding yeast mitogen-activated protein kinase (MAPK) signaling and cell behavior at the single-cell level. We show that signaling depends on a rate threshold that operates in conjunction with stimulus concentration to determine the timing of MAPK signaling during rate-varying stimulus treatments. We also discovered that the stimulation rate threshold and stimulation rate-dependent cell survival are sensitive to changes in the expression levels of the Ptp2 phosphatase, but not of another phosphatase that similarly regulates osmostress signaling during switch-like treatments. Our results demonstrate that stimulation rate is a regulated determinant of cell behavior and provide a paradigm to guide the dissection of major stimulation rate dependent mechanisms in other systems.

All cells employ signal transduction pathways to respond to physiologically relevant changes in extracellular stressors, nutrient levels, hormones, morphogens, and other stimuli that vary as functions of both concentration and rate in healthy and diseased states (1–7). Switch-like “instantaneous” changes in the concentrations of stimuli in the extracellular environment have been widely used to show that the strength of signaling and overall cellular response are dependent on the stimulus concentration, which in many cases needs to exceed a certain threshold (8, 9). Previous studies have shown that the rate of stimulation can also influence signaling output in a variety of pathways (10–17) and that stimulation profiles of varying rates can be used to probe underlying signaling pathway circuitry (4, 18, 19). However, it is still not clear how cells integrate information conveyed by changes in both the stimulation rate and concentration in determining signaling output. It is also not clear if cells require stimulation gradients to exceed a certain rate in order to commence signaling.Recent investigations have demonstrated that stimulation rate can be a determining factor in signal transduction. In contrast to switch-like perturbations, which trigger a broad set of stress-response pathways, slow stimulation rates activate a specific response to the stress applied in Bacillus subtilis cells (10). Meanwhile, shallow morphogen gradient stimulation fails to activate developmental pathways in mouse myoblast cells in culture, even when concentrations sufficient for activation during pulsed treatment are delivered (12). These observations raise the possibility that stimulation profiles must exceed a set minimum rate or rate threshold to achieve signaling activation. Although such rate thresholds would help cells decide if and how to respond to dynamic changes in stimulus concentration, the possibility of signaling regulation by a rate threshold has never been directly investigated in any system. Further, no study has experimentally examined how stimulation rate requirements impact cell phenotype or how cells molecularly regulate the stimulation rate required for signaling activation. As such, the biological significance of any existing rate threshold regulation of signaling remains unknown.The budding yeast Saccharomyces cerevisiae high osmolarity glycerol (HOG) pathway provides an ideal model system for addressing these issues (Fig. 1A). The evolutionarily conserved mitogen-activated protein kinase (MAPK) Hog1 serves as the central signaling mediator of this pathway (20–22). It is well established that instantaneous increases in osmotic stress concentration induce Hog1 phosphorylation, activation, and translocation to the nucleus (18, 21, 23–30). Activated Hog1 governs the majority of the cellular osmoadaptation response that enables cells to survive (23, 31, 32). Multiple apparently redundant MAPK phosphatases dephosphorylate and inactivate Hog1, which, along with the termination of upstream signaling after adaptation, results in its return to the cytosol (Fig. 1A) (23, 25, 26, 33–39). Because of this behavior, time-lapse analysis of Hog1 nuclear enrichment in single cells has proven an excellent and sensitive way to monitor signaling responses to dynamic stimulation patterns in real time (18, 27–30, 40, 41). Further, such assays have been readily combined with traditional growth and molecular genetic approaches to link observed signaling responses with cell behavior and signaling pathway architecture (27–29).Open in a separate windowFig. 1.Hog1 signaling and cell survival are sensitive to the rate of preconditioning osmotic stress application. (A) Schematic of the budding yeast HOG response. (B) Preconditioning protection assay workflow indicating the first stress treatments to a final concentration of 0.4 M NaCl (Left), high-stress exposure (Middle), and colony formation readout (Right). (C) High-stress survival as a function of each first treatment relative to the untreated first stress condition. Bars and errors are means and SD from three biological replicates. *Statistically significant by Kolmogorov–Smirnov test (P < 0.05). NS = not significant. (D) Treatment concentration over time. (E) Treatment rate over time for quadratic and pulse treatment. The rate for the pulse is briefly infinite (blue vertical line) before it drops to 0. (F) Hog1 nuclear localization during the treatments depicted in D and E. (Inset) Localization pattern in the quadratic-treated sample. Lines represent means and shaded error represents the SD from three to four biological replicates.Here, we use systematically designed osmotic stress treatments imposed at varying rates of increase to show that a rate threshold condition regulates yeast high-stress survival and Hog1 MAPK signaling. We demonstrate that only stimulus profiles that satisfy both this rate threshold condition and a concentration threshold condition result in robust signaling. We go on to show that the protein tyrosine phosphatase Ptp2, but not the related Ptp3 phosphatase, serves as a major rate threshold regulator. By expressing PTP2 under the control of a series of different enhancer–promoter DNA constructs, we demonstrate that changes in the level of Ptp2 expression can alter the stimulation rate required for signaling induction and survival. These findings establish rate thresholds as a critical and regulated component of signaling biology akin to concentration thresholds.     

Developmental influence on evolutionary rates and the origin of placental mammal tooth complexity

Development has often been viewed as a constraining force on morphological adaptation, but its precise influence, especially on evolutionary rates, is poorly understood. Placental mammals provide a classic example of adaptive radiation, but the debate around rate and drivers of early placental evolution remains contentious. A hallmark of early dental evolution in many placental lineages was a transition from a triangular upper molar to a more complex upper molar with a rectangular cusp pattern better specialized for crushing. To examine how development influenced this transition, we simulated dental evolution on “landscapes” built from different parameters of a computational model of tooth morphogenesis. Among the parameters examined, we find that increases in the number of enamel knots, the developmental precursors of the tooth cusps, were primarily influenced by increased self-regulation of the molecular activator (activation), whereas the pattern of knots resulted from changes in both activation and biases in tooth bud growth. In simulations, increased activation facilitated accelerated evolutionary increases in knot number, creating a lateral knot arrangement that evolved at least ten times on placental upper molars. Relatively small increases in activation, superimposed on an ancestral tritubercular molar growth pattern, could recreate key changes leading to a rectangular upper molar cusp pattern. Tinkering with tooth bud geometry varied the way cusps initiated along the posterolingual molar margin, suggesting that small spatial variations in ancestral molar growth may have influenced how placental lineages acquired a hypocone cusp. We suggest that development could have enabled relatively fast higher-level divergence of the placental molar dentition.

Whether developmental processes bias or constrain morphological adaptation is a long-standing question in evolutionary biology (1–4). Many of the distinctive features of a species derive from pattern formation processes that establish the position and number of anatomical structures (5). If developmental processes like pattern formation are biased toward generating only particular kinds of variation, adaptive radiations may often be directed along developmental–genetic “lines of least resistance” (2, 4, 6, 7). Generally, the evolutionary consequences of this developmental bias have been considered largely in terms of how it might influence the pattern of character evolution (e.g., refs. 1, 2, 8–10). But development could also influence evolutionary rates by controlling how much variation is accessible to natural selection in a given generation (11).For mammals, the dentition is often the only morphological system linking living and extinct species (12). Correspondingly, tooth morphology plays a crucial role in elucidating evolutionary relationships, time calibrating phylogenetic trees, and reconstructing adaptive responses to past environmental change (e.g., refs. 13–15). One of the most pervasive features of dental evolution among mammals is an increase in the complexity of the tooth occlusal surface, primarily through the addition of new tooth cusps (16, 17). These increases in tooth complexity are functionally and ecologically significant because they enable more efficient mechanical breakdown of lower-quality foods like plant leaves (18).Placental mammals are the most diverse extant mammalian group, comprising more than 6,000 living species spread across 19 extant orders, and this taxonomic diversity is reflected in their range of tooth shapes and dietary ecologies (12). Many extant placental orders, especially those with omnivorous or herbivorous ecologies (e.g., artiodactyls, proboscideans, rodents, and primates), convergently evolved a rectangular upper molar cusp pattern from a placental ancestor with a more triangular cusp pattern (19–21). This resulted from separate additions in each lineage of a novel posterolingual cusp, the "hypocone'''' [sensu (19)], to the tritubercular upper molar (Fig. 1), either through modification of a posterolingual cingulum (“true” hypocone) or another posterolingual structure, like a metaconule (pseudohypocone) (19). The fossil record suggests that many of the basic steps in the origin of this rectangular cusp pattern occurred during an enigmatic early diversification window associated with the divergence and early radiation of several placental orders (20, 21; Fig. 1). However, there remains debate about the rate and pattern of early placental divergence (22–24). On the one hand, most molecular phylogenies suggest that higher-level placental divergence occurred largely during the Late Cretaceous (25, 26), whereas other molecular phylogenies and paleontological analyses suggest more rapid divergence near the Cretaceous–Paleogene (K–Pg) boundary (21, 24, 27–29). Most studies agree that ecological opportunity created in the aftermath of the K–Pg extinction probably played an important role in ecomorphological diversification within the placental orders (30, 31). But exactly how early placentals acquired the innovations needed to capitalize on ecological opportunity remains unclear. Dental innovations, especially those which facilitated increases in tooth complexity, may have been important because they would have promoted expansion into plant-based dietary ecologies left largely vacant after the K–Pg extinction event (32).Open in a separate windowFig. 1.Placental mammal lineages separately evolved complex upper molar teeth with a rectangular cusp pattern composed of two lateral pairs of cusps from a common ancestor with a simpler, triangular cusp pattern. Many early relatives of the extant placental orders, such as Eritherium, possessed a hypocone cusp and a more rectangular primary cusp pattern. Examples of complex upper molars are the following: Proboscidea, the gomphothere Anancus; Rodentia, the wood mouse Apodemus; and Artiodactyla, the suid Nyanzachoerus.Mammalian tooth cusps form primarily during the “cap” and “bell” stage of dental development, when signaling centers called enamel knots establish the future sites of cusp formation within the inner dental epithelium (33, 34). The enamel knots secrete molecules that promote proliferation and changes in cell–cell adhesion, which facilitates invagination of the dental epithelium into an underlying layer of mesenchymal cells (34, 35). Although a range of genes are involved in tooth cusp patterning (36–38), the basic dynamics can be effectively modeled using reaction–diffusion models with just three diffusible morphogens: an activator, an inhibitor, and a growth factor (39–41). Candidate activator genes in mammalian tooth development include Bmp4, Activin A, Fgf20, and Wnt genes, whereas potential inhibitors include Shh and Sostdc, and Fgf4 and Bmp2 have been hypothesized to act as growth factors (38, 40–43). In computer models of tooth development, activator molecules up-regulated in the underlying mesenchyme stimulate differentiation of overlying epithelium into nondividing enamel knot cells. These in turn secrete molecules that inhibit further differentiation of epithelium into knot cells, while also promoting cell proliferation that creates the topographic relief of the cusp (40). Although many molecular, cellular, and physical processes have the potential to influence cusp formation, and thereby tooth complexity (35, 37), parameters that control the strength and conductance of the activator and inhibitor signals, the core components of the reaction–diffusion cusp patterning mechanism (39, 40) are likely to be especially important.Here, we integrate a previous computer model of tooth morphogenesis called ToothMaker (41), with simulations of trait evolution and data from the fossil record (Fig. 2), to examine the developmental origins of tooth complexity in placental mammals. Specifically, we ask the following: 1) What developmental processes can influence how many cusps form? 2) How might these developmental processes influence the evolution of tooth cusp number, especially rates? And 3) what developmental changes may have been important in the origins of the fourth upper molar cusp, the hypocone, in placental mammal evolution?Open in a separate windowFig. 2.Workflow for simulations of tooth complexity evolution. (A) Tooth shape is varied for five signaling and growth parameters in ToothMaker. (B) From an ancestral state, each parameter is varied in 2.5% increments up to a maximum of ± 50% of the ancestral state. (C) Tooth complexity and enamel knot (EK) pattern were quantified for each parameter combination. Tooth complexity was measured using cusp number/EK number and OPC. ToothMaker and placental upper second molars were classified into categories based on EK/cusp pattern. (D) The parameter space was populated with pattern and tooth complexity datums to build a developmental landscape. (E) Tooth complexity evolution was simulated on each developmental landscape. (F) Resulting diversity and pattern of tooth complexity was compared with placental mammal molar diversity.     

Modulation of immune cell reactivity with cis-binding Siglec agonists

Inflammatory pathologies caused by phagocytes lead to numerous debilitating conditions, including chronic pain and blindness due to age-related macular degeneration. Many members of the sialic acid-binding immunoglobulin-like lectin (Siglec) family are immunoinhibitory receptors whose agonism is an attractive approach for antiinflammatory therapy. Here, we show that synthetic lipid-conjugated glycopolypeptides can insert into cell membranes and engage Siglec receptors in cis, leading to inhibitory signaling. Specifically, we construct a cis-binding agonist of Siglec-9 and show that it modulates mitogen-activated protein kinase (MAPK) signaling in reporter cell lines, immortalized macrophage and microglial cell lines, and primary human macrophages. Thus, these cis-binding agonists of Siglecs present a method for therapeutic suppression of immune cell reactivity.

Sialic acid-binding immunoglobulin (IgG)-like lectins (Siglecs) are a family of immune checkpoint receptors that are on all classes of immune cells (1–5). Siglecs bind various sialoglycan ligands and deliver signals to the immune cells that report on whether the target is healthy or damaged, “self” or “nonself.” Of the 14 human Siglecs, 9 contain cytosolic inhibitory signaling domains. Accordingly, engagement of these inhibitory Siglecs by sialoglycans suppresses the activity of the immune cell, leading to an antiinflammatory effect. In this regard, inhibitory Siglecs have functional parallels with the T cell checkpoint receptors CTLA-4 and PD-1 (6–9). As with these clinically established targets for cancer immune therapy, there has been a recent surge of interest in antagonizing Siglecs to potentiate immune cell reactivity toward cancer (10). Conversely, engagement of Siglecs with agonist antibodies can suppress immune cell reactivity in the context of antiinflammatory therapy. This approach has been explored to achieve B cell suppression in lupus patients by agonism of CD22 (Siglec-2) (11, 12), and to deplete eosinophils for treatment of eosinophilic gastroenteritis by agonism of Siglec-8 (13). Similarly, a CD24 fusion protein has been investigated clinically as a Siglec-10 agonist for both graft-versus-host disease and viral infection (14, 15).Traditionally, Siglec ligands have been studied as functioning in trans, that is, on an adjacent cell (16–18), or as soluble clustering agents (9, 19). In contrast to these mechanisms of action, a growing body of work suggests that cis ligands for Siglecs (i.e., sialoglycans that reside on the same cell membrane) cluster these receptors and maintain a basal level of inhibitory signaling that increases the threshold for immune cell activation. Both Bassik and coworkers (20) and Wyss-Coray and coworkers (21) have linked the depletion of cis Siglec ligands with increased activity of macrophages and microglia, and other studies have shown that a metabolic blockade of sialic acid renders phagocytes more prone to activation (22).Synthetic ligands are a promising class of Siglec agonists (17, 23, 24). Many examples rely on clustering architectures (e.g., sialopolymers, nanoparticles, liposomes) to induce their effect (19, 23–26). Indeed, we have previously used glycopolymers to study the effects of Siglec engagement in trans on natural killer (NK) cell activity (16). We and other researchers have employed glycopolymers (16, 23), glycan-remodeling enzymes (27, 28), chemical inhibitors of glycan biosynthesis (22), and mucin overexpression constructs (29, 30) to modulate the cell-surface levels of Siglec ligands. However, current approaches lack specificity for a given Siglec.We hypothesized that Siglec-specific cis-binding sialoglycans displayed on immune cell surfaces could dampen immune cell activity with potential therapeutic applications. Here we test this notion with the synthesis of membrane-tethered cis-binding agonists of Siglec-9 (Fig. 1). Macrophages and microglia widely express Siglec-9 and are responsible for numerous pathologies including age-related inflammation (31), macular degeneration (32), neural inflammation (33), and chronic obstructive pulmonary disease (34). We designed and developed a lipid-linked glycopolypeptide scaffold bearing glycans that are selective Siglec-9 ligands (pS9L-lipid). We show that pS9L-lipid inserts into macrophage membranes, binds Siglec-9 specifically and in cis, and induces Siglec-9 signaling to suppress macrophage activity. By contrast, a lipid-free soluble analog (pS9L-sol) binds Siglec-9 but does not agonize Siglec-9 or modulate macrophage activity. Membrane-tethered glycopolypeptides are thus a potential therapeutic modality for inhibiting phagocyte activity.Open in a separate windowFig. 1.Lipid-tethered glycopolypeptides cluster and agonize Siglecs in cis on effector cells. (A) Immune cells express activating receptors that stimulate inflammatory signaling. (B) Clustering of Siglec-9 by cis-binding agonists stimulates inhibitory signaling that quenches activation.     

From the Cover: Transgenic cotton and sterile insect releases synergize eradication of pink bollworm a century after it invaded the United States

Invasive organisms pose a global threat and are exceptionally difficult to eradicate after they become abundant in their new habitats. We report a successful multitactic strategy for combating the pink bollworm (Pectinophora gossypiella), one of the world’s most invasive pests. A coordinated program in the southwestern United States and northern Mexico included releases of billions of sterile pink bollworm moths from airplanes and planting of cotton engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt). An analysis of computer simulations and 21 y of field data from Arizona demonstrate that the transgenic Bt cotton and sterile insect releases interacted synergistically to reduce the pest’s population size. In Arizona, the program started in 2006 and decreased the pest’s estimated statewide population size from over 2 billion in 2005 to zero in 2013. Complementary regional efforts eradicated this pest throughout the cotton-growing areas of the continental United States and northern Mexico a century after it had invaded both countries. The removal of this pest saved farmers in the United States $192 million from 2014 to 2019. It also eliminated the environmental and safety hazards associated with insecticide sprays that had previously targeted the pink bollworm and facilitated an 82% reduction in insecticides used against all cotton pests in Arizona. The economic and social benefits achieved demonstrate the advantages of using agricultural biotechnology in concert with classical pest control tactics.

Invasive life forms pose a major global threat and are especially difficult to eradicate after they become widespread and abundant in their new habitats (1–4). The pink bollworm (Pectinophora gossypiella), one of the world’s most invasive insects, is a voracious lepidopteran pest of cotton that was first detected in the United States in 1917 (5–8). For most of the past century, it was particularly destructive in the southwestern United States, including Arizona, where its larvae fed almost exclusively on cotton, consuming the seeds inside bolls and disrupting lint production (6, 8). In 1969, its peak seasonal density at an Arizona study site was 1.8 million larvae per hectare (ha), which translates to over 200 billion larvae in the 126,000 ha of cotton planted statewide that year (9, 10). In 1990, this pest cost Arizona cotton growers $48 million, including $32 million damage to cotton despite $16 million spent for insecticides sprayed to control it (11). In several field trials, mass releases of sterile pink bollworm moths to mate with wild moths reduced progeny production somewhat, yet did not suppress established populations because the sterile moths did not sufficiently outnumber the wild moths (6, 12–14).Pink bollworm control was revolutionized in 1996 by the introduction of cotton genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt). Bt proteins kill some major insect pests yet are not toxic to most nontarget organisms, including people and many beneficial insects (15–17). Transgenic Bt cotton helped to reduce the total annual cost of pink bollworm damage and insecticide treatments to $32 million in the United States (18). Although Bt cotton kills essentially 100% of susceptible pink bollworm larvae (19–21), this pest rapidly evolved resistance to Bt proteins in laboratory selection experiments in Arizona and in Bt cotton fields in India (20–24). To delay the evolution of resistance to Bt cotton, farmers in Arizona planted “refuges” of non-Bt cotton that yielded abundant susceptible moths to mate with the rare resistant moths emerging from Bt cotton (Fig. 1A). The refuge strategy, which has been mandated in the United States and many other countries, but was not adopted widely by farmers in India, helped preserve pink bollworm susceptibility to Bt cotton in Arizona from 1996 to 2005 (24).Open in a separate windowFig. 1.Management strategies. (A) The refuge strategy is the primary approach adopted worldwide to delay the evolution of pest resistance to Bt crops and was used in Arizona from 1996 to 2005. Refuges of non-Bt cotton planted near Bt cotton produce abundant susceptible moths (blue) to mate with the rare resistant moths (red) emerging from Bt cotton. If the inheritance of resistance to Bt cotton is recessive, as in pink bollworm, the heterozygous offspring from matings between resistant and susceptible moths die when they feed on Bt cotton bolls as larvae (24). (B) Bt cotton and sterile moth releases were used together in Arizona from 2006 to 2014 as part of a multitactic program to eradicate the pink bollworm. Susceptible sterile moths (brown) were released from airplanes to mate with the rare resistant moths emerging from Bt cotton. The few progeny produced by such matings (48) are expected to be heterozygous for resistance and to die when they feed on Bt cotton bolls as larvae.As part of a coordinated, multitactic effort to eradicate the pink bollworm from the southwestern United States and northern Mexico, a new strategy largely replacing refuges with mass releases of sterile pink bollworm moths was initiated in Arizona during 2006 (Fig. 1B; 24–27). To enable this novel strategy, the US Environmental Protection Agency granted a special exemption from the refuge requirement, which allowed Arizona cotton growers to plant up to 100% of their cotton with Bt cotton (28). We previously reported data from 1998 to 2009 showing that this innovative strategy sustained susceptibility of pink bollworm to Bt cotton while reducing the pest’s population density (25). Here, to test the idea of eradicating pink bollworm with the combination of Bt cotton and sterile releases, we conducted computer simulations and analyzed field data collected in Arizona from 1998 to 2018.     

Stable metal anodes enabled by a labile organic molecule bonded to a reduced graphene oxide aerogel

Metallic anodes (lithium, sodium, and zinc) are attractive for rechargeable battery technologies but are plagued by an unfavorable metal–electrolyte interface that leads to nonuniform metal deposition and an unstable solid–electrolyte interphase (SEI). Here we report the use of electrochemically labile molecules to regulate the electrochemical interface and guide even lithium deposition and a stable SEI. The molecule, benzenesulfonyl fluoride, was bonded to the surface of a reduced graphene oxide aerogel. During metal deposition, this labile molecule not only generates a metal-coordinating benzenesulfonate anion that guides homogeneous metal deposition but also contributes lithium fluoride to the SEI to improve Li surface passivation. Consequently, high-efficiency lithium deposition with a low nucleation overpotential was achieved at a high current density of 6.0 mA cm⁻². A Li|LiCoO₂ cell had a capacity retention of 85.3% after 400 cycles, and the cell also tolerated low-temperature (−10 °C) operation without additional capacity fading. This strategy was applied to sodium and zinc anodes as well.

Rechargeable batteries based on metal anodes including lithium (Li), sodium (Na), and zinc (Zn) show great promise in achieving high energy density (1–3). Unfortunately, the electrochemical interface of the metal anodes is not favorable for metal deposition. Metal nucleation is inhomogeneous at the surface, leading to the growth of metal dendrites (4–7) and the formation of an unstable solid–electrolyte interphase (SEI) that is incapable of protecting metals from the side reactions with the electrolyte (8–12).Substantial efforts have been devoted to stabilizing the interface of metal anodes, especially for Li metal. These include the design of artificial protective layers (13–17), alternative electrolytes (18–24), and sacrificial additives (25–30) to stabilize the metal–electrolyte interface, the development of mechanically robust coatings (31–34) to block Li dendrite growth, and the use of structured scaffolds to host dendrite-free Li deposition by reducing local current densities (35–43). However, the performance of metal anodes remains poor under high-current or low-temperature conditions. This is because the inhomogeneous Li nucleation and unstable SEI problems have not been well addressed, and these problems at the interface are even exacerbated under critical operating conditions, especially high-current densities and low temperatures (5, 6, 44).Toward this end, we report a simple molecular approach for regulating the electrochemical interface of metal anodes, which enables even Li deposition and stable SEI formation in a conventional electrolyte. This was realized by bonding a labile organic molecule, benzenesulfonyl fluoride (BSF), to a reduced graphene oxide (rGO) aerogel surface as the Li anode host (Fig. 1A). During Li deposition, BSF molecules electrochemically decompose at the interface and generate benzenesulfonate anions bonded to the rGO aerogel (Fig. 1B). The conjugated anions have a strong binding affinity for Li, serving as lithiophilic sites on the rGO surface to synergistically induce homogeneous Li nucleation of Li on the rGO surface. At the same time, BSF molecules contribute LiF to the SEI layer, which facilitates Li surface passivation (Fig. 1C). As a result, high-efficiency (99.2%) Li deposition was achieved at a Li deposition amount of 6.0 mAh cm⁻² and a current density of 6.0 mA cm⁻²; the barrier to Li nucleation was markedly reduced, as evidenced by the low nucleation overpotentials at high-current density (6.0 mA cm⁻²) or at a low temperature (−10 °C). A 400-cycle life with a capacity retention of 83.6% was achieved for a Li|LiCoO₂ (LCO) cell in a conventional carbonate electrolyte. Moreover, with the organic molecule-tuned interface, the Li|LCO cell can be stably cycled at a low operating temperature (−10 °C). This approach was applied to Na and Zn metal anodes as well.Open in a separate windowFig. 1.Illustration of a stable interface for Li deposition using a labile organic molecule, benzenesulfonyl fluoride (BSF). (A) Covalently bonded BSF on the rGO aerogel surface. (B) In situ generation of a lithiophilic conjugated anion (benzenesulfonate) and LiF on the surface during Li deposition. (C) Li nucleation preferentially occurs at the conjugated anion sites owing to the strong Li binding affinity, which leads to uniform Li deposition. In addition, the LiF that is formed is in the SEI layer and passivates the Li surface.