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 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.

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.

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 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.

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.].

Vast (but avoidable) underestimation of global biodiversity.

The number of species on Earth is highly uncertain. A recent study has suggested that there are less than 2 million prokaryotic species on Earth; this Formal Comment suggests instead that there are more likely hundreds of millions or billions of species, and that the majority of these are bacteria associated with insects and other animals.

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.

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.

Recent responses to climate change reveal the drivers of species extinction and survival.

Climate change may be a major threat to biodiversity in the next 100 years. Although there has been important work on mechanisms of decline in some species, it generally remains unclear which changes in climate actually cause extinctions, and how many species will likely be lost. Here, we identify the specific changes in climate that are associated with the widespread local extinctions that have already occurred. We then use this information to predict the extent of future biodiversity loss and to identify which processes may forestall extinction. We used data from surveys of 538 plant and animal species over time, 44% of which have already had local extinctions at one or more sites. We found that locations with local extinctions had larger and faster changes in hottest yearly temperatures than those without. Surprisingly, sites with local extinctions had significantly smaller changes in mean annual temperatures, despite the widespread use of mean annual temperatures as proxies for overall climate change. Based on their past rates of dispersal, we estimate that 57-70% of these 538 species will not disperse quickly enough to avoid extinction. However, we show that niche shifts appear to be far more important for avoiding extinction than dispersal, although most studies focus only on dispersal. Specifically, considering both dispersal and niche shifts, we project that only 16-30% of these 538 species may go extinct by 2070. Overall, our results help identify the specific climatic changes that cause extinction and the processes that may help species to survive.

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.

Do Alignment and Trimming Methods Matter for Phylogenomic (UCE) Analyses?

Alignment is a crucial issue in molecular phylogenetics because different alignment methods can potentially yield very different topologies for individual genes. But it is unclear if the choice of alignment methods remains important in phylogenomic analyses, which incorporate data from hundreds or thousands of genes. For example, problematic biases in alignment might be multiplied across many loci, whereas alignment errors in individual genes might become irrelevant. The issue of alignment trimming (i.e., removing poorly aligned regions or missing data from individual genes) is also poorly explored. Here, we test the impact of 12 different combinations of alignment and trimming methods on phylogenomic analyses. We compare these methods using published phylogenomic data from ultraconserved elements (UCEs) from squamate reptiles (lizards and snakes), birds, and tetrapods. We compare the properties of alignments generated by different alignment and trimming methods (e.g., length, informative sites, missing data). We also test whether these data sets can recover well-established clades when analyzed with concatenated (RAxML) and species-tree methods (ASTRAL-III), using the full data ($\sim $5000 loci) and subsampled data sets (10% and 1% of loci). We show that different alignment and trimming methods can significantly impact various aspects of phylogenomic data sets (e.g., length, informative sites). However, these different methods generally had little impact on the recovery and support values for well-established clades, even across very different numbers of loci. Nevertheless, our results suggest several "best practices" for alignment and trimming. Intriguingly, the choice of phylogenetic methods impacted the phylogenetic results most strongly, with concatenated analyses recovering significantly more well-established clades (with stronger support) than the species-tree analyses. [Alignment; concatenated analysis; phylogenomics; sequence length heterogeneity; species-tree analysis; trimming].

Species interactions have predictable impacts on diversification.

A fundamental goal of ecology is to reveal generalities in the myriad types of interactions among species, such as competition, mutualism and predation. Another goal is to explain the enormous differences in species richness among groups of organisms. Here, we show how these two goals are intertwined: we find that different types of species interactions have predictable impacts on rates of species diversification, which underlie richness patterns. On the basis of a systematic review, we show that interactions with positive fitness effects for individuals of a clade (e.g. insect pollination for plants) generally increase that clade's diversification rates. Conversely, we find that interactions with negative fitness effects (e.g. predation for prey, competition) generally decrease diversification rates. The sampled clades incorporate all animals and land plants, encompassing 90% of all described species across life. Overall, we show that different types of local-scale species interactions can predictably impact large-scale patterns of diversification and richness.

Sexual Dichromatism Is Decoupled from Diversification over Deep Time in Fishes.

AbstractSexually selected traits have long been thought to drive diversification, but support for this hypothesis has been persistently controversial. In fishes, sexually dimorphic coloration is associated with assortative mating and speciation among closely related species, as shown in classic studies. However, it is unclear whether these results can generalize to explain diversity patterns across ray-finned fishes, which contain the majority of vertebrate species and 96% of fishes. Here, we use phylogenetic approaches to test for an association between sexual dichromatism and diversification rates (speciation minus extinction) in ray-finned fishes. We assembled dichromatism data for 10,898 species, a data set of unprecedented size. We found no difference in diversification rates between monochromatic and dichromatic species when including all ray-finned fishes. However, at lower phylogenetic scales (within orders and families), some intermediate-sized clades did show an effect of dichromatism on diversification. Surprisingly, dichromatism could significantly increase or decrease diversification rates. Moreover, we found no effect in many of the clades initially used to link dichromatism to speciation in fishes (e.g., cichlids) or an effect only at shallow scales (within subclades). Overall, we show how the effects of dichromatism on diversification are highly variable in direction and restricted to certain clades and phylogenetic scales.

Multicellularity and sex helped shape the Tree of Life.

Across the Tree of Life, there are dramatic differences in species numbers among groups. However, the factors that explain the differences among the deepest branches have remained unknown. We tested whether multicellularity and sexual reproduction might explain these patterns, since the most species-rich groups share these traits. We found that groups with multicellularity and sexual reproduction have accelerated rates of species proliferation (diversification), and that multicellularity has a stronger effect than sexual reproduction. Patterns of species richness among clades are then strongly related to these differences in diversification rates. Taken together, these results help explain patterns of biodiversity among groups of organisms at the very broadest scales. They may also help explain the mysterious preponderance of sexual reproduction among species (the 'paradox of sex') by showing that organisms with sexual reproduction proliferate more rapidly.

Do mutualistic interactions last longer than antagonistic interactions?

Species interactions are crucial and ubiquitous across organisms. However, it remains unclear how long these interactions last over macroevolutionary timescales, and whether the nature of these interactions (mutualistic versus antagonistic) helps predict how long they persist. Here, we estimated the ages of diverse species interactions, based on phylogenies from 60 studies spanning the Tree of Life. We then tested if mutualistic interactions persist longer than antagonistic interactions. We found that the oldest mutualisms were significantly older than the oldest antagonisms across all organisms, and within plants, fungi, bacteria and protists. Surprisingly, this pattern was reversed in animals, with the oldest mutualisms significantly younger than the oldest antagonisms. We also found that many mutualisms were maintained for hundreds of millions of years (some greater than 1 billion years), providing strong evidence for the long-term stability of mutualisms and for niche conservatism in species interactions.

Weapon performance drives weapon evolution.

Many sexually selected traits function as weapons, and these weapons can be incredibly diverse. However, the factors underlying weapon diversity among species remain poorly understood, and a fundamental hypothesis to explain this diversity remains untested. Although weapons can serve multiple functions, an undeniably important function is their role in fights. Thus, a crucial hypothesis is that weapon diversification is driven by the evolution of weapon modifications that provide an advantage in combat (e.g. causing more damage). Here, we test this fighting-advantage hypothesis using data from 17 species of coreid bugs. We utilize the fact that male-male combat in coreids often results in detectable damage, allowing us to link different weapon morphologies to different levels of damage among species. We find that certain weapon morphologies inflict much more damage than others, strongly supporting the fighting-advantage hypothesis. Moreover, very different weapon morphologies can inflict similarly severe amounts of damage, leading to a weapon performance landscape with multiple performance peaks. This multi-peak pattern could potentially drive different lineages towards divergent weapon forms, further increasing weapon diversity among species. Overall, our results may help explain how sexually selected weapons have evolved into the diversity of forms seen today.

Why Are There So Many Flowering Plants? A Multiscale Analysis of Plant Diversification.

The causes of the rapid diversification and extraordinary richness of flowering plants (angiosperms) relative to other plant clades is a long-standing mystery. Angiosperms are only one among 10 major land plant clades (phyla) but include ∼90% of land plant species. However, most studies that have tried to identify which traits might explain the remarkable diversification of angiosperms have focused only on richness patterns within angiosperms and tested only one or a few traits at a single hierarchical scale. Here, we assemble a database of 31 diverse traits among 678 families and analyze relationships between traits and diversification rates across all land plants at three hierarchical levels (phylum, order, and family) using phylogenetic multiple regression. We find that most variation (∼85%) in diversification rates among major clades (phyla) is explained by biotically mediated fertilization (e.g., insect pollination) and clade-level geographic range size. Different sets of traits explain diversification at different hierarchical levels, with geographic range size dominating among families. Surprisingly, we find that traits related to local-scale species interactions (i.e., biotic fertilization) are particularly important for explaining diversification patterns at the deepest timescales, whereas large-scale geographic factors (i.e., clade-level range size) are more important at shallower timescales. This dichotomy might apply broadly across organisms.

Higher temperatures lower rates of physiological and niche evolution.

Understanding rates and patterns of change in physiological and climatic-niche variables is of urgent importance as many species are increasingly threatened by rising global temperatures. Here, we broadly test several fundamental hypotheses about physiological and niche evolution for the first time (with appropriate phylogenetic methods), using published data from 2059 vertebrate species. Our main results show that: (i) physiological tolerances to heat evolve more slowly than those to cold, (ii) the hottest climatic-niche temperatures change more slowly than the coldest climatic-niche temperatures, and (iii) physiological tolerances to heat and cold evolve more slowly than the corresponding climatic-niche variables. Physiological tolerances are significantly and positively related to the corresponding climatic-niche variables, but species often occur in climates outside the range of these tolerances. However, mismatches between climate and physiology do not necessarily mean that the climatic-niche data are misleading. Instead, some standard physiological variables used in vertebrates (i.e. critical thermal maxima and minima) may reflect when species are active (daily, seasonally) and their local-scale microhabitats (sun versus shade), rather than their large-scale climatic distributions.