On the evolutionary history of Ephedra: Cretaceous fossils and extant molecules

Gnetales comprise three unusual genera of seed plants, Ephedra, Gnetum, and Welwitschia. Their extraordinary morphological diversity suggests that they are survivors of an ancient, more diverse group. Gnetalean antiquity is also supported by fossil data. Dispersed "ephedroid" (polyplicate) pollen first appeared in the Permian >250 million years ago (Myr), and a few megafossils document the presence of gnetalean features in the early Cretaceous. The Cretaceous welwitschioid seedling Cratonia cotyledon dates the split between Gnetum and Welwitschia to before 110 Myr. Ages and character evolution of modern diversity are, however, controversial, and, based on molecular data, it has recently been suggested that Ephedra is very young, only 8-32 Myr. Here, we present data on the evolutionary history of Ephedra. Fossil seeds from Buarcos, Portugal, unequivocally link one type of Cretaceous polyplicate pollen to Ephedra and document that plants with unique characters, including the peculiar naked male gametophyte, were established already in the Early Cretaceous. Clades in our molecular phylogeny of extant species correspond to geographical regions, with African species in a basal grade/clade. The study demonstrates extremely low divergence in both molecular and morphological characters in Ephedra. Features observed in the fossils are present in all major extant clades, showing that modern species have retained unique reproductive characters for >110 million years. A recent origin of modern species of Ephedra would imply that the Cretaceous Ephedra fossils discussed here were members of widespread, now extinct sister lineage(s), and that no morphological innovations characterized the second diversification.     

Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana

Dated molecular phylogenies are the basis for understanding species diversity and for linking changes in rates of diversification with historical events such as restructuring in developmental pathways, genome doubling, or dispersal onto a new continent. Valid fossil calibration points are essential to the accurate estimation of divergence dates, but for many groups of flowering plants fossil evidence is unavailable or limited. Arabidopsis thaliana, the primary genetic model in plant biology and the first plant to have its entire genome sequenced, belongs to one such group, the plant family Brassicaceae. Thus, the timing of A. thaliana evolution and the history of its genome have been controversial. We bring previously overlooked fossil evidence to bear on these questions and find the split between A. thaliana and Arabidopsis lyrata occurred about 13 Mya, and that the split between Arabidopsis and the Brassica complex (broccoli, cabbage, canola) occurred about 43 Mya. These estimates, which are two- to threefold older than previous estimates, indicate that gene, genomic, and developmental evolution occurred much more slowly than previously hypothesized and that Arabidopsis evolved during a period of warming rather than of cooling. We detected a 2- to 10-fold shift in species diversification rates on the branch uniting Brassicaceae with its sister families. The timing of this shift suggests a possible impact of the Cretaceous-Paleogene mass extinction on their radiation and that Brassicales codiversified with pierid butterflies that specialize on mustard-oil-producing plants.     

Co-occurrence of linguistic and biological diversity in biodiversity hotspots and high biodiversity wilderness areas

As the world grows less biologically diverse, it is becoming less linguistically and culturally diverse as well. Biologists estimate annual loss of species at 1,000 times or more greater than historic rates, and linguists predict that 50-90% of the world's languages will disappear by the end of this century. Prior studies indicate similarities in the geographic arrangement of biological and linguistic diversity, although conclusions have often been constrained by use of data with limited spatial precision. Here we use greatly improved datasets to explore the co-occurrence of linguistic and biological diversity in regions containing many of the Earth's remaining species: biodiversity hotspots and high biodiversity wilderness areas. Results indicate that these regions often contain considerable linguistic diversity, accounting for 70% of all languages on Earth. Moreover, the languages involved are frequently unique (endemic) to particular regions, with many facing extinction. Likely reasons for co-occurrence of linguistic and biological diversity are complex and appear to vary among localities, although strong geographic concordance between biological and linguistic diversity in many areas argues for some form of functional connection. Languages in high biodiversity regions also often co-occur with one or more specific conservation priorities, here defined as endangered species and protected areas, marking particular localities important for maintaining both forms of diversity. The results reported in this article provide a starting point for focused research exploring the relationship between biological and linguistic-cultural diversity, and for developing integrated strategies designed to conserve species and languages in regions rich in both.     

Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group

Since Darwin, biologists have been struck by the extraordinary diversity of teleost fishes, particularly in contrast to their closest “living fossil” holostean relatives. Hypothesized drivers of teleost success include innovations in jaw mechanics, reproductive biology and, particularly at present, genomic architecture, yet all scenarios presuppose enhanced phenotypic diversification in teleosts. We test this key assumption by quantifying evolutionary rate and capacity for innovation in size and shape for the first 160 million y (Permian–Early Cretaceous) of evolution in neopterygian fishes (the more extensive clade containing teleosts and holosteans). We find that early teleosts do not show enhanced phenotypic evolution relative to holosteans. Instead, holostean rates and innovation often match or can even exceed those of stem-, crown-, and total-group teleosts, belying the living fossil reputation of their extant representatives. In addition, we find some evidence for heterogeneity within the teleost lineage. Although stem teleosts excel at discovering new body shapes, early crown-group taxa commonly display higher rates of shape evolution. However, the latter reflects low rates of shape evolution in stem teleosts relative to all other neopterygian taxa, rather than an exceptional feature of early crown teleosts. These results complement those emerging from studies of both extant teleosts as a whole and their sublineages, which generally fail to detect an association between genome duplication and significant shifts in rates of lineage diversification.Numbering ∼29,000 species, teleost fishes account for half of modern vertebrate richness. In contrast, their holostean sister group, consisting of gars and the bowfin, represents a mere eight species restricted to the freshwaters of eastern North America (1). This stark contrast between teleosts and Darwin''s original “living fossils” (2) provides the basis for assertions of teleost evolutionary superiority that are central to textbook scenarios (3, 4). Classic explanations for teleost success include key innovations in feeding (3, 5) (e.g., protrusible jaws and pharyngeal jaws) and reproduction (6, 7). More recent work implicates the duplicate genomes of teleosts (8–10) as the driver of their prolific phenotypic diversification (8, 11–13), concordant with the more general hypothesis that increased morphological complexity and innovation is an expected consequence of genome duplication (14, 15).Most arguments for enhanced phenotypic evolution in teleosts have been asserted rather than demonstrated (8, 11, 12, 15, 16; but see ref. 17), and draw heavily on the snapshot of taxonomic and phenotypic imbalance apparent between living holosteans and teleosts. The fossil record challenges this neontological narrative by revealing the remarkable taxonomic richness and morphological diversity of extinct holosteans (Fig. 1) (18, 19) and highlights geological intervals when holostean taxonomic richness exceeded that of teleosts (20). This paleontological view has an extensive pedigree. Darwin (2) invoked a long interval of cryptic teleost evolution preceding the late Mesozoic diversification of the modern radiation, a view subsequently supported by the implicit (18) or explicit (19) association of Triassic–Jurassic species previously recognized as “holostean ganoids” with the base of teleost phylogeny. This perspective became enshrined in mid-20th century treatments of actinopterygian evolution, which recognized an early-mid Mesozoic phase dominated by holosteans sensu lato and a later interval, extending to the modern day, dominated by teleosts (4, 20, 21). Contemporary paleontological accounts echo the classic interpretation of modest teleost origins (22–24), despite a systematic framework that substantially revises the classifications upon which older scenarios were based (22–25). Identification of explosive lineage diversification in nested teleost subclades like otophysans and percomorphs, rather than across the group as a whole, provides some circumstantial neontological support for this narrative (26).Open in a separate windowFig. 1.Phenotypic variation in early crown neopterygians. (A) Total-group holosteans. (B) Stem-group teleosts. (C) Crown-group teleosts. Taxa illustrated to scale.In contrast to quantified taxonomic patterns (20, 23, 24, 27), phenotypic evolution in early neopterygians has only been discussed in qualitative terms. The implicit paleontological model of morphological conservatism among early teleosts contrasts with the observation that clades aligned with the teleost stem lineage include some of the most divergent early neopterygians in terms of both size and shape (Fig. 1) (see, for example, refs. 28 and 29). These discrepancies point to considerable ambiguity in initial patterns of phenotypic diversification that lead to a striking contrast in the vertebrate tree of life, and underpins one of the most successful radiations of backboned animals.Here we tackle this uncertainty by quantifying rates of phenotypic evolution and capacity for evolutionary innovation for the first 160 million y of the crown neopterygian radiation. This late Permian (Wuchiapingian, ca. 260 Ma) to Cretaceous (Albian, ca. 100 Ma) sampling interval permits incorporation of diverse fossil holosteans and stem teleosts alongside early diverging crown teleost taxa (Figs. 1 and ​and2A2A and Figs. S1 and ​andS2),S2), resulting in a dataset of 483 nominal species-level lineages roughly divided between the holostean and teleost total groups (Fig. 2B and Fig. S2). Although genera are widely used as the currency in paleobiological studies of fossil fishes (30; but see ref. 31), we sampled at the species level to circumvent problems associated with representing geological age and morphology for multiple congeneric lineages. We gathered size [both log-transformed standard length (SL) and centroid size (CS); results from both are highly comparable (Figs. S3 and ​andS4);S4); SL results are reported in the main text] and shape data (the first three morphospace axes arising from a geometric morphometric analysis) (Fig. 2A and Figs. S1) from species where possible. To place these data within a phylogenetic context, we assembled a supertree based on published hypotheses of relationships. We assigned branch durations to a collection of trees under two scenarios for the timescale of neopterygian diversification based on molecular clock and paleontological estimates. Together, these scenarios bracket a range of plausible evolutionary timelines for this radiation (Fig. 2B). We used the samples of trees in conjunction with our morphological datasets to test for contrasts in rates of, and capacity for, phenotypic change between different partitions of the neopterygian Tree of Life (crown-, total-, and stem-group teleosts, total-group holosteans, and neopterygians minus crown-group teleosts), and the sensitivity of these conclusions to uncertainty in both relationships and evolutionary timescale. Critically, these include comparisons of phenotypic evolution in early crown-group teleosts—those species that are known with certainty to possess duplicate genomes—with rates in taxa characterized largely (neopterygians minus crown teleosts) or exclusively (holosteans) by unduplicated genomes. By restricting our scope to early diverging crown teleost lineages, we avoid potentially confounding signals from highly nested radiations that substantially postdate both genome duplication and the origin of crown teleosts (26, 32). This approach provides a test of widely held assumptions about the nature of morphological evolution in teleosts and their holostean sister lineage.Open in a separate windowFig. 2.(A) Morphospace of Permian–Early Cretaceous crown Neopterygii. (B) One supertree subjected to our paleontological (Upper) and molecular (Lower) timescaling procedures to illustrate contrasts in the range of evolutionary timescales considered. Colors of points (A) and branches (B) indicate membership in major partitions of neopterygian phylogeny. Topologies are given in Datasets S4 and S5. See Dataset S6 for source trees.Open in a separate windowFig. S1.Morphospace of 398 Permian–Early Cretaceous Neopterygii. Three major axes of shape variation are presented. Silhouettes and accompanying arrows illustrate the main anatomical correlates of these principal axes, as described in Open in a separate windowFig. S2.Morphospace of 398 Permian–Early Cretaceous Neopterygii, illustrating the major clades of (A) teleosts and (B) holosteans.Open in a separate windowFig. S3.Comparisons of size rates between (A) holosteans and teleosts, (B) crown teleosts and all other neopterygians, (C) crown teleosts and stem teleosts, (D) crown teleosts and holosteans, and (E) stem teleosts and holosteans. Comparisons were made using the full-size SL dataset, a CS dataset, and a smaller SL dataset pruned to exactly match the taxon sampling of the CS dataset. Identical taxon sampling leads the CS and pruned SL datasets to yield near identical results. Although the larger SL dataset results often differ slightly, the overall conclusion from each pairwise comparison (i.e., which outcome is the most likely in an overall majority of trees) is identical in all but one comparison (E, under molecular timescales).Open in a separate windowFig. S4.Comparisons of size innovation between (A) holosteans and teleosts, (B) crown teleosts and all other neopterygians, (C) crown teleosts and stem teleosts, (D) crown teleosts and holosteans, and (E) stem teleosts and holosteans. Comparisons were made using the full-size SL dataset, a CS dataset, and a smaller SL dataset pruned to exactly match the taxon sampling of the CS dataset. Comparisons of size innovation are presented for K value distributions of the three datasets resemble each other closely.     

From the Cover: A Middle Eocene lowland humid subtropical “Shangri-La” ecosystem in central Tibet

Tibet’s ancient topography and its role in climatic and biotic evolution remain speculative due to a paucity of quantitative surface-height measurements through time and space, and sparse fossil records. However, newly discovered fossils from a present elevation of ∼4,850 m in central Tibet improve substantially our knowledge of the ancient Tibetan environment. The 70 plant fossil taxa so far recovered include the first occurrences of several modern Asian lineages and represent a Middle Eocene (∼47 Mya) humid subtropical ecosystem. The fossils not only record the diverse composition of the ancient Tibetan biota, but also allow us to constrain the Middle Eocene land surface height in central Tibet to ∼1,500 ± 900 m, and quantify the prevailing thermal and hydrological regime. This “Shangri-La”–like ecosystem experienced monsoon seasonality with a mean annual temperature of ∼19 °C, and frosts were rare. It contained few Gondwanan taxa, yet was compositionally similar to contemporaneous floras in both North America and Europe. Our discovery quantifies a key part of Tibetan Paleogene topography and climate, and highlights the importance of Tibet in regard to the origin of modern Asian plant species and the evolution of global biodiversity.

The Tibetan Plateau, once thought of as entirely the product of the India–Eurasia collision, is known to have had significant complex relief before the arrival of India early in the Paleogene (1–3). This large region, spanning ∼2.5 million km², is an amalgam of tectonic terranes that impacted Asia long before India’s arrival (4, 5), with each accretion contributing orographic heterogeneity that likely impacted climate in complex ways. During the Paleogene, the Tibetan landscape comprised a high (>4 km) Gangdese mountain range along the southern margin of the Lhasa terrane (2), against which the Himalaya would later rise (6), and a Tanghula upland on the more northerly Qiangtang terrane (7). Separating the Lhasa and Qiangtang blocks is the east–west trending Banggong-Nujiang Suture (BNS), which today hosts several sedimentary basins (e.g., Bangor, Nyima, and Lunpola) where >4 km of Cenozoic sediments have accumulated (8). Although these sediments record the climatic and biotic evolution of central Tibet, their remoteness means fossil collections have been hitherto limited. Recently, we discovered a highly diverse fossil assemblage in the Bangor Basin. These fossils characterize a luxuriant seasonally wet and warm Shangri-La forest that once occupied a deep central Tibetan valley along the BNS, and provide a unique opportunity for understanding the evolutionary history of Asian biodiversity, as well as for quantifying the paleoenvironment of central Tibet.^*Details of the topographic evolution of Tibet are still unclear despite decades of investigation (4, 5). Isotopic compositions of carbonates recovered from sediments in some parts of central Tibet have been interpreted in terms of high (>4 km) Paleogene elevations and aridity (9, 10), but those same successions have yielded isolated mammal (11), fish (12), plant (13–18), and biomarker remains (19) more indicative of a low (≤3-km) humid environment, but how low is poorly quantified. Given the complex assembly of Tibet, it is difficult to explain how a plateau might have formed so early and then remained as a surface of low relief during subsequent compression from India (20). Recent evidence from a climate model-mediated interpretation of palm fossils constrains the BNS elevation to below 2.3 km in the Late Paleogene (16), but more precise paleoelevation estimates are required. Further fossil discoveries, especially from earlier in the BNS sedimentary records, would document better the evolution of the Tibetan biota, as well as informing our understanding of the elevation and climate in an area that now occupies the center of the Tibetan Plateau.Our work shows that the BNS hosted a diverse subtropical ecosystem at ∼47 Ma, and this means the area must have been both low and humid. The diversity of the fossil flora allows us to 1) document floristic links to other parts of the Northern Hemisphere, 2) characterize the prevailing paleoclimate, and 3) quantify the elevation at which the vegetation grew. We propose that the “high and dry” central Tibet inferred from some isotope paleoaltimetry (9, 10) reflects a “phantom” elevated paleosurface (20) because fractionation over the bounding mountains allowed only isotopically light moist air to enter the valley, giving a false indication of a high elevation (21).     

Global variation in diversification rate and species richness are unlinked in plants

Species richness varies immensely around the world. Variation in the rate of diversification (speciation minus extinction) is often hypothesized to explain this pattern, while alternative explanations invoke time or ecological carrying capacities as drivers. Focusing on seed plants, the world’s most important engineers of terrestrial ecosystems, we investigated the role of diversification rate as a link between the environment and global species richness patterns. Applying structural equation modeling to a comprehensive distribution dataset and phylogenetic tree covering all circa 332,000 seed plant species and 99.9% of the world’s terrestrial surface (excluding Antarctica), we test five broad hypotheses postulating that diversification serves as a mechanistic link between species richness and climate, climatic stability, seasonality, environmental heterogeneity, or the distribution of biomes. Our results show that the global patterns of species richness and diversification rate are entirely independent. Diversification rates were not highest in warm and wet climates, running counter to the Metabolic Theory of Ecology, one of the dominant explanations for global gradients in species richness. Instead, diversification rates were highest in edaphically diverse, dry areas that have experienced climate change during the Neogene. Meanwhile, we confirmed climate and environmental heterogeneity as the main drivers of species richness, but these effects did not involve diversification rates as a mechanistic link, calling for alternative explanations. We conclude that high species richness is likely driven by the antiquity of wet tropical areas (supporting the “tropical conservatism hypothesis”) or the high ecological carrying capacity of warm, wet, and/or environmentally heterogeneous environments.

Species richness varies by several orders of magnitude from species-poor deserts to hyperdiverse tropical rainforests, but the mechanistic basis of this variation is hotly debated. Some explanations suggest that high species richness could be the result of more time to accumulate species (1, 2) or the ecological capacity to house many species (3, 4). There are, however, several prominent explanations that involve geographic variation in diversification rate, the net rate of speciation minus extinction (

From the Cover: Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution

How ecological and morphological diversity accrues over geological time has been much debated by paleobiologists. Evidence from the fossil record suggests that many clades reach maximal diversity early in their evolutionary history, followed by a decline in evolutionary rates as ecological space fills or due to internal constraints. Here, we apply recently developed methods for estimating rates of morphological evolution during the post-Paleozoic history of a major invertebrate clade, the Echinoidea. Contrary to expectation, rates of evolution were lowest during the initial phase of diversification following the Permo-Triassic mass extinction and increased over time. Furthermore, although several subclades show high initial rates and net decreases in rates of evolution, consistent with “early bursts” of morphological diversification, at more inclusive taxonomic levels, these bursts appear as episodic peaks. Peak rates coincided with major shifts in ecological morphology, primarily associated with innovations in feeding strategies. Despite having similar numbers of species in today’s oceans, regular echinoids have accrued far less morphological diversity than irregular echinoids due to lower intrinsic rates of morphological evolution and less morphological innovation, the latter indicative of constrained or bounded evolution. These results indicate that rates of evolution are extremely heterogenous through time and their interpretation depends on the temporal and taxonomic scale of analysis.Assessing how rates of morphological evolution have changed over geological time has been a major research goal of evolutionary paleobiologists since Westoll’s classic study of lungfish evolution (1). A common pattern to emerge from the fossil record is that many clades reach maximal morphological diversity early in their evolutionary history (2–4). This sort of pattern could be the result of an “early burst” of morphological diversification as taxa diverge followed by a slow-down in rates as ecological space becomes filled (5, 6). Internal constraint or long-term selective pressures could also limit overall disparity, leading to a slowdown in the rate of new trait acquisition over time (7, 8). However, only a small proportion of fossil disparity studies have also assessed changes in rates of evolution within lineages (e.g., along phylogenetic branches) thereby providing a more nuanced understanding of how this disparity came about (e.g., refs. 9–13). Simultaneously, decreasing rates in trait evolution have been difficult to detect using phylogenetic comparative data of extant taxa, because of low statistical power (14, 15), loss of signal through extinction (16), and inaccuracies in reconstructing ancestral nodes (17). Here we take advantage of recently developed methods for directly estimating per-lineage-million-year rates of evolution from phylogenies with both fossil and living taxa to test whether declining rates characterize the evolutionary history of a major clade of marine invertebrates, the echinoids.Since originating some 265 million years ago (18, 19), crown group echinoids have evolved to become ecologically and morphologically diverse in today’s oceans, and are an important component of both past and present marine ecosystems (e.g., refs. 20–22). However, analysis of how this diversity arose has either been based on taxonomic counts (e.g., ref. 23) or has adopted a morphometric approach where the requirement of a homologous set of landmarks limits taxonomic, temporal, and geographic scope (e.g., ref. 24). We use a discrete-character-based approach and a recent taxonomically comprehensive analysis of post-Paleozoic echinoids as our phylogenetic framework (25). This tree is almost entirely resolved (SI Appendix, Fig. S1) and branches may be scaled using the first appearance of each taxon in the fossil record (SI Appendix, Table S1). We tabulated the number of character state changes that occurred along each branch within ∼10-million-year time intervals spanning the Permian and post-Paleozoic (SI Appendix, Table S2), and divided this by the summed duration of branch lengths to compute a time series of per-lineage-million-year rates of morphological evolution. We accounted for uncertainty in phylogenetic structure, uncertainty in the timing of the first appearance of taxa, and uncertainty in the timing of character changes along each branch using a randomization approach (12). We also estimated rates within subclades, corroborating our findings by using likelihoods tests to determine whether some branches had higher rates than expected given rates across the entire tree. Finally, we compared rates of evolution through time with the structure of diversification within a character-defined morphospace, and looked for evidence of differences in evolutionary modes among subclades. The pattern that emerges is one of dynamic evolutionary change through time: Both rates and patterns of evolution vary temporally and across subclades, such that the overall pattern depends highly on the temporal and taxonomic scale of the analysis.     

Deep time diversity and the early radiations of birds

Reconstructing the history of biodiversity has been hindered by often-separate analyses of stem and crown groups of the clades in question that are not easily understood within the same unified evolutionary framework. Here, we investigate the evolutionary history of birds by analyzing three supertrees that combine published phylogenies of both stem and crown birds. Our analyses reveal three distinct large-scale increases in the diversification rate across bird evolutionary history. The first increase, which began between 160 and 170 Ma and reached its peak between 130 and 135 Ma, corresponds to an accelerated morphological evolutionary rate associated with the locomotory systems among early stem birds. This radiation resulted in morphospace occupation that is larger and different from their close dinosaurian relatives, demonstrating the occurrence of a radiation among early stem birds. The second increase, which started ∼90 Ma and reached its peak between 65 and 55 Ma, is associated with rapid evolution of the cranial skeleton among early crown birds, driven differently from the first radiation. The third increase, which occurred after ∼40 to 45 Ma, has yet to be supported by quantitative morphological data but gains some support from the fossil record. Our analyses indicate that the bird biodiversity evolution was influenced mainly by long-term climatic changes and also by major paleobiological events such as the Cretaceous–Paleogene (K–Pg) extinction.

The evolution of global biodiversity is a focal area of study in both evolutionary biology and paleontology, but its examination has been approached in different ways. Neontological studies reconstruct the history of biodiversity mainly by analyzing the tempo and mode of diversification based on molecular timetrees composed of extant species (1). By contrast, paleontologists normally measure past biodiversity by investigating morphological evolution and taxic diversity from the fossil record (2). This dichotomy in both methodology and data sources is best exemplified by recent studies on the evolution of bird biodiversity (the vernacular term “birds” is equivalent to the phylogenetic taxon “Avialae” in the present paper; see Methods and SI Appendix, Supplemental Text A). For example, the time-calibrated phylogeny of extant birds and related diversification rate analyses have revealed a rapid diversification of crown birds (equivalent to the phylogenetic taxon “Aves”) near the Cretaceous–Paleogene (K–Pg) boundary followed by a period of low-level net diversification rates starting about 50 Ma (3–5). Paleontological studies have revealed high morphological evolutionary rates both prior to and after the origin of Avialae (6–14), and an increased taxonomic diversity in the Early Cretaceous based on the known Mesozoic fossil record (15) (SI Appendix, Supplemental Text B). However, these results are not directly comparable and are difficult to be evaluated within the same evolutionary framework given that they are based on different evaluation parameters of bird diversity.     

Convergence,divergence, and parallelism in marine biodiversity trends: Integrating present-day and fossil data

Paleontological data provide essential insights into the processes shaping the spatial distribution of present-day biodiversity. Here, we combine biogeographic data with the fossil record to investigate the roles of parallelism (similar diversities reached via changes from similar starting points), convergence (similar diversities reached from different starting points), and divergence in shaping the present-day latitudinal diversity gradients of marine bivalves along the two North American coasts. Although both faunas show the expected overall poleward decline in species richness, the trends differ between the coasts, and the discrepancies are not explained simply by present-day temperature differences. Instead, the fossil record indicates that both coasts have declined in overall diversity over the past 3 My, but the western Atlantic fauna suffered more severe Pliocene−Pleistocene extinction than did the eastern Pacific. Tropical western Atlantic diversity remains lower than the eastern Pacific, but warm temperate western Atlantic diversity recovered to exceed that of the temperate eastern Pacific, either through immigration or in situ origination. At the clade level, bivalve families shared by the two coasts followed a variety of paths toward today’s diversities. The drivers of these lineage-level differences remain unclear, but species with broad geographic ranges during the Pliocene were more likely than geographically restricted species to persist in the temperate zone, suggesting that past differences in geographic range sizes among clades may underlie between-coast contrasts. More detailed comparative work on regional extinction intensities and selectivities, and subsequent recoveries (by in situ speciation or immigration), is needed to better understand present-day diversity patterns and model future changes.Biodiversity is spatially structured at many scales. Biogeographic realms and provinces, the partitioning of species among environments within biogeographic units, and genetic population structure within species are all manifestations of the ecological and evolutionary processes that generate and maintain diversity in terrestrial and marine systems. For most terrestrial and marine organisms, the first-order global diversity pattern is the latitudinal diversity gradient (LDG): the increase in the number of species and higher taxa from the poles to the tropics (1). This gradient, as seen today, has been shaped by a combination of origination, extinction, and past geographic shifts of taxa; all of these variables might differ among clades, functional groups, and land masses or ocean basins (2–7), even when the overall LDG is similar. Thus, a mechanistic understanding of the present-day LDG in general, and along specific equator−pole transects, for distinctive regional faunas, and for individual clades, cannot be divorced from its history.The need for historical data is underscored by the differences and similarities among related clades that broadly conform to the LDG. As in many evolutionary questions (8), process-based interpretations of similarities and differences in diversity at local and regional scales require separation of parallelism and convergence, and data on the timing and context of divergences. However, present-day data alone may not be able to determine whether similar latitudinal trends represent common histories—i.e., parallel diversity trajectories from similar starting points—or convergence from different starting points. Similarly, different latitudinal trends might reflect either long-standing contrasts or recent divergences driven by clade- or region-specific contrasts in origination, extinction, and/or range shifts. Thus, the pervasive emphasis on the approximate fit of taxonomic diversity trends (e.g., refs. 9–11) and biogeographic structure (e.g., ref. 12) to present-day environmental factors, and present-day similarities of diversity of a single clade in multiple regions (e.g., ref. 13), captures only part of the underlying story. Owing to difficulties in accurately quantifying extinction and the timing of most past distributional shifts, exclusively present-day data can be actively misleading when attempting to reconstruct biotic histories (14–17).Here we use intertidal and shelf-depth marine bivalves, a group with a well-documented LDG in modern oceans and a rich fossil record, to explore how an integrative approach can provide a direct, comparative window into the temporal and spatial dynamics of clades along the LDG. We do this by comparing two of the best-sampled coastlines, the Northern Hemisphere section of the American coasts (hereafter, E Pacific and W Atlantic), which show broadly similar LDGs that differ in detail and have different Late Cenozoic environmental and evolutionary histories. The differences between these coasts appear to involve all three components of diversity dynamics: origination, extinction, and spatial shifts. By focusing on the Pliocene bivalves in the two best-sampled temperate regions along each coast [California and the Carolinas−Virginia region (hereafter termed Virginia), both at ∼32°N–40°N], living at a time when extratropical temperatures were warmer and latitudinal temperature gradients gentler than today (18–20), we can begin to tease apart the complex roles of regional extinction and range expansion in shaping present-day patterns of species richness (hereafter termed diversity). For comparison, we summarized modern diversity within the same latitudinal bins, rather than using the natural provincial boundaries, to assess local extinctions from Pliocene to Recent.     

Molecules,morphology, and ecology indicate a recent,amphibious ancestry for echidnas

The semiaquatic platypus and terrestrial echidnas (spiny anteaters) are the only living egg-laying mammals (monotremes). The fossil record has provided few clues as to their origins and the evolution of their ecological specializations; however, recent reassignment of the Early Cretaceous Teinolophos and Steropodon to the platypus lineage implies that platypuses and echidnas diverged >112.5 million years ago, reinforcing the notion of monotremes as living fossils. This placement is based primarily on characters related to a single feature, the enlarged mandibular canal, which supplies blood vessels and dense electrosensory receptors to the platypus bill. Our reevaluation of the morphological data instead groups platypus and echidnas to the exclusion of Teinolophos and Steropodon and suggests that an enlarged mandibular canal is ancestral for monotremes (partly reversed in echidnas, in association with general mandibular reduction). A multigene evaluation of the echidna–platypus divergence using both a relaxed molecular clock and direct fossil calibrations reveals a recent split of 19–48 million years ago. Platypus-like monotremes (Monotrematum) predate this divergence, indicating that echidnas had aquatically foraging ancestors that reinvaded terrestrial ecosystems. This ecological shift and the associated radiation of echidnas represent a recent expansion of niche space despite potential competition from marsupials. Monotremes might have survived the invasion of marsupials into Australasia by exploiting ecological niches in which marsupials are restricted by their reproductive mode. Morphology, ecology, and molecular biology together indicate that Teinolophos and Steropodon are basal monotremes rather than platypus relatives, and that living monotremes are a relatively recent radiation.     

From the Cover: Between-country collaboration and consideration of costs increase conservation planning efficiency in the Mediterranean Basin

The importance of global and regional coordination in conservation is growing, although currently, the majority of conservation programs are applied at national and subnational scales. Nevertheless, multinational programs incur transaction costs and resources beyond what is required in national programs. Given the need to maximize returns on investment within limited conservation budgets, it is crucial to quantify how much more biodiversity can be protected by coordinating multinational conservation efforts when resources are fungible. Previous studies that compared different scales of conservation decision-making mostly ignored spatial variability in biodiversity threats and the cost of actions. Here, we developed a simple integrating metric, taking into account both the cost of conservation and threats to biodiversity. We examined the Mediterranean Basin biodiversity hotspot, which encompasses over 20 countries. We discovered that for vertebrates to achieve similar conservation benefits, one would need substantially more money and area if each country were to act independently as compared to fully coordinated action across the Basin. A fully coordinated conservation plan is expected to save approximately US$67 billion, 45% of total cost, compared with the uncoordinated plan; and if implemented over a 10-year period, the plan would cost ≈0.1% of the gross national income of all European Union (EU) countries annually. The initiative declared in the recent Paris Summit for the Mediterranean provides a political basis for such complex coordination. Surprisingly, because many conservation priority areas selected are located in EU countries, a partly coordinated solution incorporating only EU-Mediterranean countries is almost as efficient as the fully coordinated scenario.     

Landscape dynamics and diversification of the megadiverse South American freshwater fish fauna

Landscape dynamics are widely thought to govern the tempo and mode of continental radiations, yet the effects of river network rearrangements on dispersal and lineage diversification remain poorly understood. We integrated an unprecedented occurrence dataset of 4,967 species with a newly compiled, time-calibrated phylogeny of South American freshwater fishes—the most species-rich continental vertebrate fauna on Earth—to track the evolutionary processes associated with hydrogeographic events over 100 Ma. Net lineage diversification was heterogeneous through time, across space, and among clades. Five abrupt shifts in net diversification rates occurred during the Paleogene and Miocene (between 30 and 7 Ma) in association with major landscape evolution events. Net diversification accelerated from the Miocene to the Recent (c. 20 to 0 Ma), with Western Amazonia having the highest rates of in situ diversification, which led to it being an important source of species dispersing to other regions. All regional biotic interchanges were associated with documented hydrogeographic events and the formation of biogeographic corridors, including the Early Miocene (c. 23 to 16 Ma) uplift of the Serra do Mar and Serra da Mantiqueira and the Late Miocene (c. 10 Ma) uplift of the Northern Andes and associated formation of the modern transcontinental Amazon River. The combination of high diversification rates and extensive biotic interchange associated with Western Amazonia yielded its extraordinary contemporary richness and phylogenetic endemism. Our results support the hypothesis that landscape dynamics, which shaped the history of drainage basin connections, strongly affected the assembly and diversification of basin-wide fish faunas.

Geological and climatic events are widely believed to shape the biodiversity of continental biotas (1–3), yet we are only beginning to understand the nuanced ways in which individual geological and climatic events have contributed to evolutionary diversification (speciation minus extinction) across large spatial scales (4–7). South America harbors the most diverse fauna of continental freshwater fishes in the world (~5,750 species), providing unique opportunities to study the effects of geological history and river dynamics on diversification in obligate aquatic taxa (8, 9). Hydrogeographic processes, operating over tens of millions of years, have caused predictable changes in the geometry of river drainage networks, by isolating and merging portions of adjacent river basins and their connections to the sea, and by altering the physiochemical characteristics of water discharge (10, 11). Here, we evaluate the influence of major geological events on diversity patterns of obligate freshwater fishes of South America over the past 100 Ma, the time period over which hydrogeographic events shaped the origins of modern fluvial systems (4, 5, 12). We conducted the most comprehensive assessment of diversification in this group to date, using an extensive dataset on species geographic occurrences and a newly compiled, species-dense phylogeny of South American freshwater fishes (13). This new synthesis afforded us the opportunity to link unique hydrogeographic events with the spatial and temporal diversification and dispersal of individual fish clades.The historical dynamics of South American river basins and aquatic biotas were strongly shaped by four prominent geophysical events (Fig. 1) (11, 14). The first was the final separation of South America from Africa during the Late Cretaceous (c. 100 Ma). Between the Late Cretaceous and Early Paleogene (c. 100 to 55 Ma), river drainage patterns of South America were controlled by the location of the preexisting continental uplands (cratons and shields), ongoing uplift of the Andean cordilleras, super greenhouse climatic conditions characterized by high temperatures and precipitation, and dramatically fluctuating eustatic sea levels. As a result, most low-elevation coastal plains and interior structural basins were covered by nearshore marine habitats, and upland freshwater riverine and riparian habitats were intermittently isolated and connected (4, 15). During the Paleogene (c. 55 to 33 Ma), the Proto-Amazon-Orinoco river basin (Proto-Amazon basin, hereafter) drained the Sub-Andean Foreland basin, including much of northern South America and the northern La Plata region (Fig. 1 A and B; 5, 16).Open in a separate windowFig. 1.Bioregions, principle current landforms and sub-basins, and approximate chronology and location of the principal landscape evolution events that shaped the current drainage basins of South America and influenced the diversification of freshwater fishes. (A) Current river basins and geological formations mentioned in the text and the six bioregions proposed (detailed in SI Appendix). (B–E) Between 100 and 55 Ma, aquatic systems in South America were intermittently connected by multiple marine transgressions and regressions.Thus drainages across the continent during this time were intermittently connected by epicontinental seaways. During this time, the Proto-Amazon basin was the main drainage of northern South America, flowing through the sub-Andean foreland. At the same time, the Paraná and Paraguay basins (La Plata bioregion) represented major aquatic systems in South America (4, 5, 10, 11). Additional information about principal landforms controlling basin connectivity at each time interval and for each bioregion delineation appears in SI Appendix, Table S1.Second, intraplate compression and tectonic subduction along the Pacific margin during the Oligocene (c. 33 to 23 Ma) drove tectonic uplift of the Altiplano and Michicola Arch (c. 30 Ma) associated with formation of the Bolivian Orocline (17). These orogenic deformations intermittently isolated and connected rivers among the Western Amazonian, Upper Madeira, and Upper Paraguay sedimentary basins of the Sub-Andean Foreland, facilitating vicariance and biotic exchanges across their watershed divides (Fig. 1C; 4, 18–20). Third, tectonic reactivation and uplift of Serra do Mar and Serra da Mantiqueira ranges in southeastern Brazil during the Early Miocene (c. 23 to 16 Ma) re-routed some rivers from the La Plata basin directly to the Atlantic (Fig. 1D; 21, 22–24), isolating many terrestrial and aquatic species in the coastal basins of the Atlantic Forest. Also, at about this time (c. 23 to 10 Ma), the Pebas Megawetland extended over large areas of the modern Western Amazonia and Orinoco basins (Fig. 1D; 5, 7, 22–26). Fourth, the uplift of the Northern Andes during the Late Miocene and Pliocene (c. 10 to 4.5 Ma), which profoundly reorganized regional river drainage networks, isolated the modern Amazon, Orinoco, Magdalena, and Maracaibo river basins and connected the modern Western and Eastern Amazon basins, thereby forming the modern transcontinental Amazon River (Fig. 1E; 16, 27).Variation in connectivity and configuration of regional river networks resulting from these four major geological events strongly shaped diversity patterns of the Neotropical freshwater fish fauna (4, 12). In particular, river capture, in which a river drainage system is diverted from its historic bed to a neighboring bed, is a landscape evolution process that exerts a potent influence on diversification in obligate freshwater organisms, because it both severs existing and constructs new corridors of aquatic habitat among portions of adjacent drainage basins (18, 28). Because continental fishes are eco-physiologically restricted to freshwater habitats within drainage basins, watersheds represent natural dispersal barriers, as evidenced by the strong spatial concordance of geographic ranges in freshwater fish species with basin boundaries (28, 29). By isolating and connecting populations of aquatic taxa across watershed divides, river capture exerts complex effects on the diversity of freshwater organisms, for example by elevating extinction risk through geographic-range contraction, promoting speciation by genetic isolation and vicariance, and increasing biotic homogenization by dispersal and gene flow (16, 30–32).Although the role of geological events in shaping the evolution of rivers and freshwater diversity has long been recognized, the relative contributions of particular geological events remain poorly understood. Insights into their contributions can be gained only by studying diversity patterns at appropriate spatial, temporal, and taxonomic scales (28, 33–36). For instance, recent studies identified Western Amazonia as the center of Amazon fish diversity (high species richness, low phylogenetic diversity (PD), and high phylogenetic clustering, compared to Eastern Amazonia), with younger fish lineages dispersing progressively eastward across Amazonia after the formation of the modern transcontinental river c. 10 Ma (37–39). However, this interpretation did not consider the more ancient history of Neotropical fishes in the upland Brazilian and Guianas Shields, the formation of the modern lowland (< 250 m.a.s.l.) fauna in the Proto-Amazon basin, and the phenotypically and taxonomically modern composition of all the known Miocene paleo-ichthyofaunas (4, 40). Taking this deeper history into account, Pliocene and Pleistocene events may have served more as buffers against extinction than as drivers of speciation in the formation of Amazonian fish species diversity (Fig. 2; 15, 41). In fact, the most species-rich clades of Neotropical freshwater fishes are thought to have radiated during the Paleogene (c. 63 to 23 Ma) (4, 42, 43).Open in a separate windowFig. 2.Changes in the rates of net lineage diversification among South American freshwater fishes. Tips represent 2,523 fish species. (A) Branch colors indicate net lineage diversification rate estimated by BAMM, where red indicates highest and blue lowest diversification rates. Significant shifts in diversification rates are shown as pale green circles on the branches. Selected representative clades of Melanorivulus, Orestias, Ancistrini, Hypostomus, and Corydoras species are illustrated. The principal orders are represented by colored columns to the right of the tree tips. The timescale at the bottom is expressed in millions of years ago (Ma). Vertical dashed lines indicate timing of the main principal hydrogeographic events detailed in the inset legend on the left. (B) Rates-through-time plots based on BAMM estimations, considering all bioregions together (see Material and Methods for parametrization details). The shaded areas around the curves correspond to 95% CIs of the estimated rates. Dashed lines indicate the time period when most of shifts in diversification rates were estimated. (C) Rates-through-time plots considering the species present in each bioregion separately. Rates of diversification, speciation, and extinction were estimated mainly within crown taxa. The five photographs: Wikipedia Commons. *Ancistrini species of genera Hopliancistrus, Guyanancistrus, Pseudolithoxus, Lasiancistrus, Pseudancistrus, Panaque, and Pterygoplichthys.In the case of South American freshwater fishes, previous macroevolutionary studies have been hindered by the large number of species (~5,750), remote sampling localities, and logistical difficulties of gathering reliable data (8). Our new data on fish distributions, which we combine with a new, time-calibrated molecular phylogeny, offer powerful resources to study the role of geomorphological events and associated river captures in shaping fish diversity over longer time periods and larger spatial scales than has previously been attempted. In particular, we evaluate the prediction that the high diversity in Western Amazonia was influenced by biogeographical bridges formed across different aquatic systems and time periods, which led to both accelerated diversification rates and a role for Western Amazonia as a principal source of freshwater fish species for all of South America.     

Diversification of rhacophorid frogs provides evidence for accelerated faunal exchange between India and Eurasia during the Oligocene

The accretion of the Indian subcontinent to Eurasia triggered a massive faunal and floral exchange, with Gondwanan taxa entering into Asia and vice versa. The traditional view on the Indian–Asian collision assumes contact of the continental plates during the Early Eocene. Many biogeographic studies rely on this assumption. However, the exact mode and timing of this geological event is still under debate. Here we address, based on an extensive phylogenetic analysis of rhacophorid tree frogs, if there was already a Paleogene biogeographic link between Southeast Asia and India; in which direction faunal exchange occurred between India and Eurasia within the Rhacophoridae; and if the timing of the faunal exchange correlates with one of the recently suggested geological models. Rhacophorid tree frogs showed an early dispersal from India to Asia between 46 and 57 Ma, as reconstructed from the fossil record. During the Middle Eocene, however, faunal exchange ceased, followed by increase of rhacophorid dispersal events between Asia and the Indian subcontinent during the Oligocene that continued until the Middle Miocene. This corroborates recent geological models that argue for a much later final collision between the continental plates. We predict that the Oligocene faunal exchange between the Indian subcontinent and Asia, as shown here for rhacophorid frogs, also applies for other nonvolant organisms with an Indian–Asian distribution, and suggest that previous studies that deal with this faunal interchange should be carefully reinvestigated.     

Neutral theory as a predictor of avifaunal extinctions after habitat loss

The worldwide loss of natural habitats leads not only to the loss of habitat-endemic species but also to further and protracted extinctions in the reduced areas that remain. How rapid is this process? We use the neutral theory of biodiversity to answer this question, and we compare the results taken with observed rates of avifaunal extinctions. In the neutral model, we derive an exact solution for the rate of species loss in a closed community. The simple, closed-form solution exhibits hyperbolic decay of species richness with time, which implies a potentially rapid initial decline followed by much slower rates long term. Our empirical estimates of extinction times are based on published studies for avifaunal extinctions either on oceanic islands or in forest fragments, which span a total of six orders of magnitude in area. These estimates show that the time to extinction strongly depends on the area. The neutral-theory predictions agree well with observed rates over three orders of magnitude of area (between 100 and 100,000 ha) both for islands and forest fragments. Regarding the species abundance distribution, extinction times based on a broken-stick model led to better agreement with observation than if a log-series model was used. The predictions break down for very small or very large areas. Thus, neutrality may be an affordable assumption for some applications in ecology and conservation, particularly for areas of intermediate size.     

From the Cover: Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution

Fossils and molecular data are two independent sources of information that should in principle provide consistent inferences of when evolutionary lineages diverged. Here we use an alternative approach to genetic inference of species split times in recent human and ape evolution that is independent of the fossil record. We first use genetic parentage information on a large number of wild chimpanzees and mountain gorillas to directly infer their average generation times. We then compare these generation time estimates with those of humans and apply recent estimates of the human mutation rate per generation to derive estimates of split times of great apes and humans that are independent of fossil calibration. We date the human–chimpanzee split to at least 7–8 million years and the population split between Neanderthals and modern humans to 400,000–800,000 y ago. This suggests that molecular divergence dates may not be in conflict with the attribution of 6- to 7-million-y-old fossils to the human lineage and 400,000-y-old fossils to the Neanderthal lineage.     

The clinical patterns of myalgia in children with familial Mediterranean fever

OBJECTIVES: To study the frequency and clinical patterns of myalgia in a defined group of children with familial Mediterranean fever (FMF). METHODS: A prospective 4-year (September 1995-September 1999) study of children with FMF seen in the pediatric FMF clinic of Jordan University teaching hospital. Diagnosis of FMF was made according to published criteria. Once the diagnosis of FMF and myalgia was made, details about myalgia were collected by interview with the child and his/her parents and entered into a special study form. RESULTS: Of 264 children with FMF seen over the study period, 65 (25%) developed myalgia. Three clinical patterns of myalgia were identified: the spontaneous pattern, the exercise-induced pattern, and the protracted febrile myalgia syndrome (PFMS), seen in 8%, 81%, and 11% of patients, respectively. The three patterns differed in the severity of pain, height of fever, and duration of the episode. In 33 children with the exercise-induced myalgia, in which response to colchicine could be reliably assessed, a favorable response was achieved in 97%. Three children with the PFMS had a dramatic response to corticosteroids. CONCLUSIONS: Myalgia in children with FMF is common and can follow three different clinical patterns.     

Tolerance adaptation and precipitation changes complicate latitudinal patterns of climate change impacts

Global patterns of biodiversity and comparisons between tropical and temperate ecosystems have pervaded ecology from its inception. However, the urgency in understanding these global patterns has been accentuated by the threat of rapid climate change. We apply an adaptive model of environmental tolerance evolution to global climate data and climate change model projections to examine the relative impacts of climate change on different regions of the globe. Our results project more adverse impacts of warming on tropical populations due to environmental tolerance adaptation to conditions of low interannual variability in temperature. When applied to present variability and future forecasts of precipitation data, the tolerance adaptation model found large reductions in fitness predicted for populations in high-latitude northern hemisphere regions, although some tropical regions had comparable reductions in fitness. We formulated an evolutionary regional climate change index (ERCCI) to additionally incorporate the predicted changes in the interannual variability of temperature and precipitation. Based on this index, we suggest that the magnitude of climate change impacts could be much more heterogeneous across latitude than previously thought. Specifically, tropical regions are likely to be just as affected as temperate regions and, in some regions under some circumstances, possibly more so.     

Contrarian clade confirms the ubiquity of spatial origination patterns in the production of latitudinal diversity gradients

The latitudinal diversity gradient (LDG), wherein the number of species and higher taxa peaks in the tropics and decreases toward the poles, is the best-documented large-scale diversity pattern on Earth, but hypotheses explaining the standard LDG must also account for rare "contrarian" taxa that show diversity maxima outside of the tropics. For marine bivalves, one of the few groups that provide spatially explicit temporal data on a global scale, we show that a major contrarian group, the Anomalodesmata, unexpectedly exhibits the same large-scale dynamics as related clades having normal LDGs in two key respects. First, maxima in standing genus diversity and genus origination rates coincide spatially. Second, the strength of a clade's present-day LDG is significantly related to the proportion of its living genera that originated in the tropics during the late Cenozoic, with the contrarian gradient strength at both species and genus level predicted quantitatively by the values for the other clades. Geologic age distributions indicate that the anomalous LDG results from origination that is damped in the tropics rather than heightened in the temperate zones. The pervasive role of spatial origination patterns in shaping LDGs, regardless of the position of their diversity maxima, corroborates hypotheses based on clades showing standard gradients and underscores the insights that contrarian groups can provide into general principles of diversity dynamics.