Evolutionary legacies in contemporary tetrapod imperilment.

The Tree of Life will be irrevocably reshaped as anthropogenic extinctions continue to unfold. Theory suggests that lineage evolutionary dynamics, such as age since origination, historical extinction filters and speciation rates, have influenced ancient extinction patterns - but whether these factors also contribute to modern extinction risk is largely unknown. We examine evolutionary legacies in contemporary extinction risk for over 4000 genera, representing ~30,000 species, from the major tetrapod groups: amphibians, birds, turtles and crocodiles, squamate reptiles and mammals. We find consistent support for the hypothesis that extinction risk is elevated in lineages with higher recent speciation rates. We subsequently test, and find modest support for, a primary mechanism driving this pattern: that rapidly diversifying clades predominantly comprise range-restricted, and extinction-prone, species. These evolutionary patterns in current imperilment may have important consequences for how we manage the erosion of biological diversity across the Tree of Life.

Hydrothermal physiology and climate vulnerability in amphibians.

Concerns over the consequences of global climate change for biodiversity have spurred a renewed interest in organismal thermal physiology. However, temperature is only one of many environmental axes poised to change in the future. In particular, hydrologic regimes are also expected to shift concurrently with temperature in many regions, yet our understanding of how thermal and hydration physiology jointly affect performance and fitness is still limited for most taxonomic groups. Here, we investigated the relationship between functional performance, hydration state and temperature in three ecologically distinct amphibians, and compare how temperature and water loss can concurrently limit activity under current climate conditions. We found that performance was maintained across a broad range of hydration states in all three species, but then declines abruptly after a threshold of 20-30% mass loss. This rapid performance decline was accelerated when individuals were exposed to warmer temperatures. Combining our empirical hydrothermal performance curves with species-specific biophysical models, we estimated that dehydration can increase restrictions on species' activity by up to 60% compared to restriction by temperature alone. These results illustrate the importance of integrating species' hydration physiology into forecasts of climate vulnerability, as omitting this axis may significantly underestimate the effects of future climate change on Earth's biological diversity.

Clustered versus catastrophic global vertebrate declines.

Recent analyses have reported catastrophic global declines in vertebrate populations1,2. However, the distillation of many trends into a global mean index obscures the variation that can inform conservation measures and can be sensitive to analytical decisions. For example, previous analyses have estimated a mean vertebrate decline of more than 50% since 1970 (Living Planet Index2). Here we show, however, that this estimate is driven by less than 3% of vertebrate populations; if these extremely declining populations are excluded, the global trend switches to an increase. The sensitivity of global mean trends to outliers suggests that more informative indices are needed. We propose an alternative approach, which identifies clusters of extreme decline (or increase) that differ statistically from the majority of population trends. We show that, of taxonomic-geographic systems in the Living Planet Index, 16 systems contain clusters of extreme decline (comprising around 1% of populations; these extreme declines occur disproportionately in larger animals) and 7 contain extreme increases (around 0.4% of populations). The remaining 98.6% of populations across all systems showed no mean global trend. However, when analysed separately, three systems were declining strongly with high certainty (all in the Indo-Pacific region) and seven were declining strongly but with less certainty (mostly reptile and amphibian groups). Accounting for extreme clusters fundamentally alters the interpretation of global vertebrate trends and should be used to help to prioritize conservation efforts.

Ecological constraints associated with genome size across salamander lineages.

Salamanders have some of the largest, and most variable, genome sizes among the vertebrates. Larger genomes have been associated with larger cell sizes, lower metabolic rates, and longer embryonic and larval durations in many different taxonomic groups. These life-history traits are often important for dictating fitness under different environmental conditions, suggesting that a species' genome size may have the potential to constrain its ecological distribution. We test how genome size varies with the ephemerality of larval habitat across the salamanders, predicting that species with larger genomes will be constrained to more permanent habitats that permit slower development, while species with smaller genomes will be more broadly distributed across the gradient of habitat ephemerality. We found that salamanders with larger genomes are almost exclusively associated with permanent aquatic habitats. In addition, the evolutionary transition rate between permanent and ephemeral larval habitats is much higher in salamander lineages with smaller genome sizes. These patterns suggest that genome size may act as an evolutionary constraint on the ecological habitats of salamanders, restricting those species with large genomes and slower development to habitats with permanent sources of water.

Amphibian species traits, evolutionary history and environment predict Batrachochytrium dendrobatidis infection patterns, but not extinction risk.

The fungal pathogen Batrachochytrium dendrobatidis (B. dendrobatidis) has emerged as a major agent of amphibian extinction, requiring conservation intervention for many susceptible species. Identifying susceptible species is challenging, but many aspects of species biology are predicted to influence the evolution of host resistance, tolerance, or avoidance strategies towards disease. In turn, we may expect species exhibiting these distinct strategies to differ in their ability to survive epizootic disease outbreaks. Here, we test for phylogenetic and trait-based patterns of B. dendrobatidis infection risk and infection intensity among 302 amphibian species by compiling a global data set of B. dendrobatidis infection surveys across 95 sites. We then use best-fit models that associate traits, taxonomy and environment with B. dendrobatidis infection risk and intensity to predict host disease mitigation strategies (tolerance, resistance, avoidance) for 122 Neotropical amphibian species that experienced epizootic B. dendrobatidis outbreaks, and noted species persistence or extinction from these events. Aspects of amphibian species life history, habitat use and climatic niche were consistently linked to variation in B. dendrobatidis infection patterns across sites around the world. However, predicted B. dendrobatidis infection risk and intensity based on site environment and species traits did not reveal a consistent pattern between the predicted host disease mitigation strategy and extinction outcome. This suggests that either tolerant or resistant species may have no advantage in ameliorating disease during epizootic events, or that other factors drive the persistence of amphibian populations during chytridiomycosis outbreaks. These results suggest that using a trait-based approach may allow us to identify species with resistance or tolerance to endemic B. dendrobatidis infections, but that this approach may be insufficient to ultimately identify species at risk of extinction from epizootics.

Linking speciation to extinction: Diversification raises contemporary extinction risk in amphibians.

Many of the traits associated with elevated rates of speciation, including niche specialization and having small and isolated populations, are similarly linked with an elevated risk of extinction. This suggests that rapidly speciating lineages may also be more extinction prone. Empirical tests of a speciation-extinction correlation are rare because assessing paleontological extinction rates is difficult. However, the modern biodiversity crisis allows us to observe patterns of extinction in real time, and if this hypothesis is true then we would expect young clades that have recently diversified to have high contemporary extinction risk. Here, we examine evolutionary patterns of modern extinction risk across over 300 genera within one of the most threatened vertebrate classes, the Amphibia. Consistent with predictions, rapidly diversifying amphibian clades also had a greater share of threatened species. Curiously, this pattern is not reflected in other tetrapod classes and may reflect a greater propensity to speciate through peripheral isolation in amphibians, which is partly supported by a negative correlation between diversification rate and mean geographic range size. This clustered threat in rapidly diversifying amphibian genera means that protecting a small number of species can achieve large gains in preserving amphibian phylogenetic diversity. Nonindependence between speciation and extinction rates has many consequences for patterns of biodiversity and how we may choose to conserve it.