Hidden hotspots of amphibian biodiversity in China.

Identifying and protecting hotspots of endemism and species richness is crucial for mitigating the global biodiversity crisis. However, our understanding of spatial diversity patterns is far from complete, which severely limits our ability to conserve biodiversity hotspots. Here, we report a comprehensive analysis of amphibian species diversity in China, one of the most species-rich countries on Earth. Our study combines 20 y of field surveys with new molecular analyses of 521 described species and also identifies 100 potential cryptic species. We identify 10 hotspots of amphibian diversity in China, each with exceptional species richness and endemism and with exceptional phylogenetic diversity and phylogenetic endemism (based on a new time-calibrated, species-level phylogeny for Chinese amphibians). These 10 hotspots encompass 59.6% of China's described amphibian species, 49.0% of cryptic species, and 55.6% of species endemic to China. Only four of these 10 hotspots correspond to previously recognized biodiversity hotspots. The six new hotspots include the Nanling Mountains and other mountain ranges in South China. Among the 186 species in the six new hotspots, only 9.7% are well covered by protected areas and most (88.2%) are exposed to high human impacts. Five of the six new hotspots are under very high human pressure and are in urgent need of protection. We also find that patterns of richness in cryptic species are significantly related to those in described species but are not identical.

How many species will Earth lose to climate change?

Climate change may be an important threat to global biodiversity, potentially leading to the extinction of numerous species. But how many? There have been various attempts to answer this question, sometimes yielding strikingly different estimates. Here, we review these estimates, assess their disagreements and methodology, and explore how we might reach better estimates. Large-scale studies have estimated the extinction of ~1% of sampled species up to ~70%, even when using the same approach (species distribution models; SDMs). Nevertheless, worst-case estimates often converge near 20%-30% species loss, and many differences shrink when using similar assumptions. We perform a new review of recent SDM studies, which show ~17% loss of species to climate change under worst-case scenarios. However, this review shows that many SDM studies are biased by excluding the most vulnerable species (those known from few localities), which may lead to underestimating global species loss. Conversely, our analyses of recent climate change responses show that a fundamental assumption of SDM studies, that species' climatic niches do not change over time, may be frequently violated. For example, we find mean rates of positive thermal niche change across species of ~0.02°C/year. Yet, these rates may still be slower than projected climate change by ~3-4 fold. Finally, we explore how global extinction levels can be estimated by combining group-specific estimates of species loss with recent group-specific projections of global species richness (including cryptic insect species). These preliminary estimates tentatively forecast climate-related extinction of 14%-32% of macroscopic species in the next ~50 years, potentially including 3-6 million (or more) animal and plant species, even under intermediate climate change scenarios.

The causes of species richness patterns among clades.

Two major types of species richness patterns are spatial (e.g. the latitudinal diversity gradient) and clade-based (e.g. the dominance of angiosperms among plants). Studies have debated whether clade-based richness patterns are explained primarily by larger clades having faster rates of species accumulation (speciation minus extinction over time; diversification-rate hypothesis) or by simply being older (clade-age hypothesis). However, these studies typically compared named clades of the same taxonomic rank, such as phyla and families. This study design is potentially biased against the clade-age hypothesis, since clades of the same rank may be more similar in age than randomly selected clades. Here, we analyse the causes of clade-based richness patterns across the tree of life using a large-scale, time-calibrated, species-level phylogeny and random sampling of clades. We find that within major groups of organisms (animals, plants, fungi, bacteria, archaeans), richness patterns are most strongly related to clade age. Nevertheless, weaker relationships with diversification rates are present in animals and plants. These overall results contrast with similar large-scale analyses across life based on named clades, which showed little effect of clade age on richness. More broadly, these results help support the overall importance of time for explaining diverse types of species richness patterns.

How many species are there on Earth? Progress and problems.

How many species exist on Earth? Projections range from millions to trillions. A 2011 paper in PLOS Biology provided a comprehensive estimate of 9 million.

The radiation continuum and the evolution of frog diversity.

Most of life's vast diversity of species and phenotypes is often attributed to adaptive radiation. Yet its contribution to species and phenotypic diversity of a major group has not been examined. Two key questions remain unresolved. First, what proportion of clades show macroevolutionary dynamics similar to adaptive radiations? Second, what proportion of overall species richness and phenotypic diversity do these adaptive-radiation-like clades contain? We address these questions with phylogenetic and morphological data for 1226 frog species across 43 families (which represent >99% of all species). Less than half of frog families resembled adaptive radiations (with rapid diversification and morphological evolution). Yet, these adaptive-radiation-like clades encompassed ~75% of both morphological and species diversity, despite rapid rates in other clades (e.g., non-adaptive radiations). Overall, we support the importance of adaptive-radiation-like evolution for explaining diversity patterns and provide a framework for characterizing macroevolutionary dynamics and diversity patterns in other groups.

Accelerating local extinction associated with very recent climate change.

Climate change has already caused local extinction in many plants and animals, based on surveys spanning many decades. As climate change accelerates, the pace of these extinctions may also accelerate, potentially leading to large-scale, species-level extinctions. We tested this hypothesis in a montane lizard. We resurveyed 18 mountain ranges in 2021-2022 after only ~7 years. We found rates of local extinction among the fastest ever recorded, which have tripled in the past ~7 years relative to the preceding ~42 years. Further, climate change generated local extinction in ~7 years similar to that seen in other organisms over ~70 years. Yet, contrary to expectations, populations at two of the hottest sites survived. We found that genomic data helped predict which populations survived and which went extinct. Overall, we show the increasing risk to biodiversity posed by accelerating climate change and the opportunity to study its effects over surprisingly brief timescales.

Frog phylogeny: A time-calibrated, species-level tree based on hundreds of loci and 5,242 species.

Large-scale, time-calibrated phylogenies from supermatrix studies have become crucial for evolutionary and ecological studies in many groups of organisms. However, in frogs (anuran amphibians), there is a serious problem with existing supermatrix estimates. Specifically, these trees are based on a limited number of loci (15 or fewer), and the higher-level relationships estimated are discordant with recent phylogenomic estimates based on much larger numbers of loci. Here, we attempted to rectify this problem by generating an expanded supermatrix and combining this with data from phylogenomic studies. To assist in aligning ribosomal sequences for this supermatrix, we developed a new program (TaxonomyAlign) to help perform taxonomy-guided alignments. The new combined matrix contained 5,242 anuran species with data from 307 markers, but with 95% missing data overall. This dataset represented a 71% increase in species sampled relative to the previous largest supermatrix analysis of anurans (adding 2,175 species). Maximum-likelihood analyses generated a tree in which higher-level relationships (and estimated clade ages) were generally concordant with those from phylogenomic analyses but were more discordant with the previous largest supermatrix analysis. We found few obvious problems arising from the extensive missing data in most species. We also generated a set of 100 time-calibrated trees for use in comparative analyses. Overall, we provide an improved estimate of anuran phylogeny based on the largest number of combined taxa and markers to date. More broadly, we demonstrate the potential to combine phylogenomic and supermatrix analyses in other groups of organisms.

Selection on weapon allometry in the wild.

Allometry is the scaling relationship between a trait and body size. This relationship can often explain considerable morphological variation within and among species. Nevertheless, much remains unknown about the factors that underlie allometric patterns. For example, when different allometric relationships are observed amongst closely related species, these differences are regularly considered to be products of selection. However, directional selection on allometry (particularly the slope) has rarely been tested and observed in natural populations. Here, we investigate selection on the scaling relationship between weapon size and body size (i.e., weapon allometry) in a wild population of giant mesquite bugs, Pachylis neocalifornicus (previously Thasus neocalifornicus). Males in this species use their weapons (enlarged femurs) to compete with one another over access to resources and females. We found that large males with relatively large weapons successfully secured access to mates. However, we also found that small males with relatively small weapons could access mates as well. These two patterns together can increase the allometric slope of the sexually selected weapon, suggesting a straightforward process by which the allometric slope can evolve.

Macroevolution of sexually selected weapons: weapon evolution in chameleons.

The evolution of sexually selected traits is a major topic in evolutionary biology. However, large-scale evolutionary patterns in these traits remain understudied, especially those traits used in male-male competition (weapons sensu lato). Here, we analyze weapon evolution in chamaeleonid lizards, both within and between the sexes. Chameleons are an outstanding model system because of their morphological diversity (including 11 weapon types among ~220 species) and a large-scale time-calibrated phylogeny. We analyze these 11 traits among 165 species using phylogenetic methods, addressing many questions for the first time in any group. We find that all 11 weapons have each evolved multiple times and that weapon origins are generally more frequent than their losses. We find that almost all weapons have each persisted for >30 million years (and some for >65 million years). Across chameleon phylogeny, we identify both hotspots for weapon evolution (up to 10 types present per species) and coldspots (all weapons absent, many through loss). These hotspots are significantly associated with larger male body size, but are only weakly related to sexual-size dimorphism. We also find that weapon evolution is strongly correlated between males and females. Overall, these results provide a baseline for understanding large-scale patterns of weapon evolution within clades.

Redefining Possible: Combining Phylogenomic and Supersparse Data in Frogs.

The data available for reconstructing molecular phylogenies have become wildly disparate. Phylogenomic studies can generate data for thousands of genetic markers for dozens of species, but for hundreds of other taxa, data may be available from only a few genes. Can these two types of data be integrated to combine the advantages of both, addressing the relationships of hundreds of species with thousands of genes? Here, we show that this is possible, using data from frogs. We generated a phylogenomic data set for 138 ingroup species and 3,784 nuclear markers (ultraconserved elements [UCEs]), including new UCE data from 70 species. We also assembled a supermatrix data set, including data from 97% of frog genera (441 total), with 1-307 genes per taxon. We then produced a combined phylogenomic-supermatrix data set (a "gigamatrix") containing 441 ingroup taxa and 4,091 markers but with 86% missing data overall. Likelihood analysis of the gigamatrix yielded a generally well-supported tree among families, largely consistent with trees from the phylogenomic data alone. All terminal taxa were placed in the expected families, even though 42.5% of these taxa each had >99.5% missing data and 70.2% had >90% missing data. Our results show that missing data need not be an impediment to successfully combining very large phylogenomic and supermatrix data sets, and they open the door to new studies that simultaneously maximize sampling of genes and taxa.

Trait-based species richness: ecology and macroevolution.

Understanding the origins of species richness patterns is a fundamental goal in ecology and evolutionary biology. Much research has focused on explaining two kinds of species richness patterns: (i) spatial species richness patterns (e.g. the latitudinal diversity gradient), and (ii) clade-based species richness patterns (e.g. the predominance of angiosperm species among plants). Here, I highlight a third kind of richness pattern: trait-based species richness (e.g. the number of species with each state of a character, such as diet or body size). Trait-based richness patterns are relevant to many topics in ecology and evolution, from ecosystem function to adaptive radiation to the paradox of sex. Although many studies have described particular trait-based richness patterns, the origins of these patterns remain far less understood, and trait-based richness has not been emphasised as a general category of richness patterns. Here, I describe a conceptual framework for how trait-based richness patterns arise compared to other richness patterns. A systematic review suggests that trait-based richness patterns are most often explained by when each state originates within a group (i.e. older states generally have higher richness), and not by differences in transition rates among states or faster diversification of species with certain states. This latter result contrasts with the widespread emphasis on diversification rates in species-richness research. I show that many recent studies of spatial richness patterns are actually studies of trait-based richness patterns, potentially confounding the causes of these patterns. Finally, I describe a plethora of unanswered questions related to trait-based richness patterns.

Niche width predicts extinction from climate change and vulnerability of tropical species.

Climate change may be a major threat to global biodiversity, especially to tropical species. Yet, why tropical species are more vulnerable to climate change remains unclear. Tropical species are thought to have narrower physiological tolerances to temperature, and they have already experienced a higher estimated frequency of climate-related local extinctions. These two patterns suggest that tropical species are more vulnerable to climate change because they have narrower thermal niche widths. However, no studies have tested whether species with narrower climatic niche widths for temperature have experienced more local extinctions, and if these narrower niche widths can explain the higher frequency of tropical local extinctions. Here, we test these ideas using resurvey data from 538 plant and animal species from 10 studies. We found that mean niche widths among species and the extent of climate change (increase in maximum annual temperatures) together explained most variation (>75%) in the frequency of local extinction among studies. Surprisingly, neither latitude nor occurrence in the tropics alone significantly predicted local extinction among studies, but latitude and niche widths were strongly inversely related. Niche width also significantly predicted local extinction among species, as well as among and (sometimes) within studies. Overall, niche width may offer a relatively simple and accessible predictor of the vulnerability of populations to climate change. Intriguingly, niche width has the best predictive power to explain extinction from global warming when it incorporates coldest yearly temperatures.

Estimating Global Biodiversity: The Role of Cryptic Insect Species.

How many species are there on Earth and to what groups do these species belong? These fundamental questions span systematics, ecology, and evolutionary biology. Yet, recent estimates of overall global biodiversity have ranged wildly, from the low millions to the trillions. Insects are a pivotal group for these estimates. Insects make up roughly half of currently described extant species (across all groups), with ~1 million described species. Insect diversity is also crucial because many other taxa have species that may be unique to each insect host species, including bacteria, apicomplexan protists, microsporidian fungi, nematodes, and mites. Several projections of total insect diversity (described and undescribed) have converged on ~6 million species. However, these projections have not incorporated the morphologically cryptic species revealed by molecular data. Here, we estimate the extent of cryptic insect diversity. We perform a systematic review of studies that used explicit species-delimitation methods with multilocus data. We estimate that each morphology-based insect species contains (on average) 3.1 cryptic species. We then use these estimates to project the overall number of species on Earth and their distribution among major groups. Our estimates suggest that overall global biodiversity may range from 563 million to 2.2 billion species. [Biodiversity; cryptic species; insects; species delimitation; species richness.].

The origins of climate-diversity relationships and richness patterns in Chinese plants.

A major goal of ecology and evolutionary biology is to explain geographic patterns of species richness. Richness is often correlated with climatic variables. However, the processes underlying these climate-diversity relationships remain poorly understood. Two potential hypotheses to explain these relationships involve: (i) faster diversification rates (speciation minus extinction) in high-richness climates and (ii) earlier colonization of high-richness climates, allowing more time for speciation to build up richness. Few studies have tested these hypotheses directly, and most focused on animal clades with limited richness. In this study, we test these hypotheses in Chinese angiosperms, encompassing ~10% of Earth's plant species, using large-scale phylogenetic, climatic, and distributional data including 26,977 species. We find that climatic zones that were colonized earlier have higher species richness. By contrast, relationships between diversification rates and richness of climatic zones are often nonsignificant or negative. Our study reveals that even when richness is strongly correlated with climate, the underlying explanation may still be rooted in phylogenetic history. Thus, climate may not be a competing explanation for richness patterns relative to colonization times and diversification rates. We also show that the timing of colonization can be crucial for explaining richness patterns. Yet, many recent studies have ignored this explanation and instead have focused solely on rates of speciation and diversification as drivers of diversity gradients.

The evolution of reproductive modes and life cycles in amphibians.

Amphibians have undergone important evolutionary transitions in reproductive modes and life-cycles. We compare large-scale macroevolutionary patterns in these transitions across the three major amphibian clades: frogs, salamanders, and caecilians. We analyse matching reproductive and phylogenetic data for 4025 species. We find that having aquatic larvae is ancestral for all three groups and is retained by many extant species (33-44%). The most frequent transitions in each group are to relatively uncommon states: live-bearing in caecilians, paedomorphosis in salamanders, and semi-terrestriality in frogs. All three groups show transitions to more terrestrial reproductive modes, but only in caecilians have these evolved sequentially from most-to-least aquatic. Diversification rates are largely independent of reproductive modes. However, in salamanders direct development accelerates diversification whereas paedomorphosis decreases it. Overall, we find a widespread retention of ancestral modes, decoupling of trait transition rates from patterns of species richness, and the general independence of reproductive modes and diversification.

Population genomic analyses support sympatric origins of parapatric morphs in a salamander.

In numerous clades, divergent sister species have largely non-overlapping geographic ranges. This pattern presumably arises because species diverged in allopatry or parapatry, prior to a subsequent contact. Here, we provide population-genomic evidence for the opposite scenario: previously sympatric ecotypes that have spatially separated into divergent monomorphic populations over large geographic scales (reverse sympatric scenario). We analyzed a North American salamander (Plethodon cinereus) with two color morphs that are broadly sympatric: striped (redback) and unstriped (leadback). Sympatric morphs can show considerable divergence in other traits, and many Plethodon species are fixed for a single morph. Long Island (New York) is unusual in having many pure redback and leadback populations that are spatially separated, with pure redback populations in the west and pure leadbacks in the east. Previous work showed that these pure-morph populations were genetically, morphologically, and ecologically divergent. Here, we performed a coalescent-based analysis of new data from 88,696 single-nucleotide polymorphisms to address the origins of these populations. This analysis strongly supports the monophyly of Long Island populations and their subsequent divergence into pure redback and pure leadback populations. Taken together, these results suggest that the formerly sympatric mainland morphs separated into parapatric populations on Long Island, reversing the conventional speciation scenario.

Why are animals conspicuously colored? Evolution of sexual versus warning signals in land vertebrates.

Conspicuous colors (e.g., red, yellow, blue) have evolved numerous times across animals. But the function of this coloration can differ radically among species. Many species use this coloration as a sexual signal to conspecifics, whereas others use it as a warning signal to predators. Why do different species evolve conspicuous coloration in association with one function as opposed to the other? We address this question in terrestrial vertebrates (tetrapods) using phylogenetic approaches, and test whether day-night activities of species help determine these patterns. Using phylogenetic logistic regression, we found that conspicuous, sexually dimorphic coloration is significantly associated with diurnal lineages (e.g., many birds and lizards). By contrast, the evolution of warning signals was significantly associated with large-scale clades that were ancestrally nocturnal (e.g., snakes, amphibians), regardless of the current diel activity of species. Overall, we show that the evolution of conspicuous coloration as warning signals or sexual signals is influenced by the ecology of species, both recently and in the ancient past.

The origins of global biodiversity on land, sea and freshwater.

Many biodiversity studies focus on explaining high tropical species richness, but an equally dramatic yet understudied pattern involves the divergent richness of land, sea and freshwater. Here, we reveal the origins of these richness differences among habitats across animals and plants. Most plant and animal species are terrestrial, although these habitats cover only ~28% of Earth's surface. Marine habitats have fewer species over a larger area (~70%). Freshwater habitats have relatively high richness and exceptional phylogenetic diversity given their tiny area (2%). The relative richness of habitats is related to variation in diversification rates. Based on ancestral reconstructions of habitat, we find that most marine species are descended from marine ancestors and most terrestrial species from freshwater ancestors. Yet, most extant animal richness in freshwater is derived from terrestrial ancestors. Overall, our results reveal the origins of fundamental but neglected biodiversity patterns, and highlight the conservation importance of freshwater habitats.

Large-scale evolution of body temperatures in land vertebrates.

Body temperature is a crucial variable in animals that affects nearly every aspect of their lives. Here we analyze for the first time largescale patterns in the evolution of body temperatures across terrestrial vertebrates (tetrapods: including amphibians, mammals, birds and other reptiles). Despite the traditional view that endotherms (birds and mammals) have higher body temperatures than ectotherms, we find they are not significantly different. However, rates of body-temperature evolution are significantly different, with lower rates in endotherms than ectotherms, and the highest rates in amphibians. We find that body temperatures show strong phylogenetic signal and conservatism over 350 million years of evolutionary history in tetrapods, and some lineages appear to have retained similar body temperatures over time for hundreds of millions of years. Although body temperatures are often unrelated to climate in tetrapods, we find that body temperatures are significantly related to day-night activity patterns. Specifically, body temperatures are generally higher in diurnal species than nocturnal species, both across ectotherms and, surprisingly, across endotherms also. Overall, our results suggest that body temperatures are significantly linked to phylogeny and diel-activity patterns within and among tetrapod groups, rather than just climate and the endotherm-ectotherm divide.