Phylogeny-based conservation priorities for Australian freshwater fishes.

Conservation scientists are increasingly interested in the question of how extinction prunes the tree of life. This question is particularly important for Australian freshwater fishes because there is a broad mix of ∼300 old and young species, many of which are severely threatened. We used a complete species-level phylogeny of Australian freshwater fishes to examine phylogenetic nonrandomness of extinction risk. We computed the potential loss of phylogenetic diversity by simulating extinction across the tree under a pattern weighted based on International Union for Conservation of Nature extinction risk category and compared this loss to projected diversity loss under a random null model of extinction. Finally, we calculated EDGE (evolutionary distinctiveness, global endangerment) scores for 251 freshwater and 60 brackish species and compiled a list of high-priority species for conservation actions based on their extinction risk and evolutionary uniqueness. Extinction risk was not random and was clustered in both diversity cradles (recently diversifying, species-rich clades, such as Galaxiidae and Percichthyidae) and museums (older, species-poor groups, such as freshwater chondrichthyans). Clustered extinction made little difference to the average expected loss of phylogenetic diversity. However, the upper bound of loss was higher under a selective model of extinction, particularly when the counts of species lost were low. Thus, the loss of highly threatened species would diminish the tree of life more than a null model of randomly distributed extinction.  High priority species included both widely recognized and charismatic ones, such as the Queensland lungfish (Neoceratodus forsteri), river sharks, and freshwater sawfishes, and lesser-known species that receive less public attention, including the salamanderfish (Lepidogalaxias salamandroides), cave gudgeons, and many galaxiids, rainbowfishes, and pygmy perches.

Prioridades de Conservación Basadas en la Filogenia para Peces de Agua Dulce de Australia Resumen Los científicos de la conservación cada vez están más interesados en el tema de cómo la extinción poda al árbol de la vida. Esta cuestión es particularmente importante para los peces de agua dulce de Australia ya que existe una mezcla amplia de ∼300 especies antiguas y recientes, muchas de las cuales se encuentran seriamente amenazadas. Usamos una filogenia completa a nivel de especie de los peces de agua dulce de Australia para examinar la no aleatoriedad filogenética del riesgo de extinción. Computamos la pérdida potencial de la diversidad filogenética mediante la simulación de la extinción en todo el árbol bajo un patrón ponderado con base en la categoría de riesgo de extinción de la Unión Internacional para la Conservación de la Naturaleza y la comparamos con la pérdida proyectada de diversidad bajo un modelo aleatorio nulo de la extinción. Por último, calculamos los puntajes EDGE (peculiaridad evolutiva, riesgo global) para 251 especies de agua dulce y 60 especies de agua salobre y recopilamos una lista de especies de alta prioridad para las acciones de conservación basada en su riesgo de extinción y su singularidad evolutiva. El riesgo de extinción no fue aleatorio y estuvo agrupado tanto en cunas de diversidad (clados ricos en especies con diversificación reciente, como Galaxiidae y Percichthyidae) como en museos (grupos más viejos con pocas especies, como los condrictios de agua dulce). La extinción agrupada no trajo grandes diferencias para la pérdida promedio esperada de la diversidad filogenética. Sin embargo, el límite superior de la pérdida fue más alto bajo un modelo selectivo de extinción, particularmente cuando los conteos de especies perdidas fueron bajos. Por lo tanto, la pérdida de especies en grave peligro de extinción disminuiría el árbol de la vida más que un modelo nulo de extinción distribuida aleatoriamente. Las especies de mayor prioridad incluyeron tanto a las más conocidas y carismáticas, como el pez pulmonado de Queensland (Neoceratodus forsteri), los tiburones de río y los peces sierra de agua dulce, como a las especies menos conocidas que reciben menos atención del público, incluyendo al pez salamandra (Lepidogalaxias salamandroides), los gobios de las cuevas y a muchos galaxiidos, peces arcoiris y percas pigmeas.

Marine diversity patterns in Australia are filtered through biogeography.

Latitudinal diversity gradients are among the most striking patterns in nature. Despite a large body of work investigating both geographic and environmental drivers, biogeographical provinces have not been included in statistical models of diversity patterns. Instead, spatial studies tend to focus on species-area and local-regional relationships. Here, we investigate correlates of a latitudinal diversity pattern in Australian coastal molluscs. We use an online database of greater than 300 000 specimens and quantify diversity using four methods to account for sampling variation. Additionally, we present a biogeographic scheme using factor analysis that allows for both gradients and sharp boundaries between clusters. The factors are defined on the basis of species composition and are independent of diversity. Regardless of the measure used, diversity is not directly explained by combinations of abiotic variables. Instead, transitions between regions better explain the observed patterns. Biogeographic gradients can in turn be explained by environmental variables, suggesting that environmental controls on diversity may be indirect. Faunas within provinces are homogeneous regardless of environmental variability. Thus, transitions between provinces explain most of the variation in diversity because small-scale factors are dampened. This explanation contrasts with the species-energy hypothesis. Future work should more carefully consider biogeographic gradients when investigating diversity patterns.

The legacy of Eastern Mediterranean mountain uplifts: rapid disparity of phylogenetic niche conservatism and divergence in mountain vipers.

BACKGROUND: The orogeny of the eastern Mediterranean region has substantially affected ecological speciation patterns, particularly of mountain-dwelling species. Mountain vipers of the genus Montivipera are among the paramount examples of Mediterranean neo-endemism, with restricted ranges in the mountains of Anatolia, the Levant, Caucasus, Alborz, and Zagros. Here we explore the phylogenetic and ecological diversification of Montivipera to reconstruct its ecological niche evolution and biogeographic history. Using 177 sequences of three mitochondrial genes, a dated molecular phylogeny of mountain vipers was reconstructed. Based on 320 occurrence points within the entire range of the genus and six climatic variables, ecological niches were modelled and used to infer ancestral niche occupancy. In addition, the biogeographic history and ancestral states of the species were reconstructed across climate gradients. RESULTS: Dated phylogenetic reconstruction revealed that the ancestor of mountain vipers split into two major clades at around 12.18 Mya followed by multiple vicariance events due to rapid orogeny. Montivipera colonised coastal regions from a mountain-dwelling ancestor. We detected a highly complex ecological niche evolution of mountain vipers to temperature seasonality, a variable that also showed a strong phylogenetic signal and high contribution in niche occupation. CONCLUSION: Raising mountain belts in the Eastern Mediterranean region and subsequent remarkable changes in temperature seasonality have led to the formation of important centres of diversification and endemism in this biodiversity hotspot. High rates of niche conservatism, low genetic diversity, and segregation of ranges into the endemic distribution negatively influenced the adaptive capacity of mountain vipers. We suggest that these species should be considered as evolutionary significant units and priority species for conservation in Mediterranean mountain ecosystems.

The apparent exponential radiation of Phanerozoic land vertebrates is an artefact of spatial sampling biases.

There is no consensus about how terrestrial biodiversity was assembled through deep time, and in particular whether it has risen exponentially over the Phanerozoic. Using a database of 60 859 fossil occurrences, we show that the spatial extent of the worldwide terrestrial tetrapod fossil record itself expands exponentially through the Phanerozoic. Changes in spatial sampling explain up to 67% of the change in known fossil species counts, and these changes are decoupled from variation in habitable land area that existed through time. Spatial sampling therefore represents a real and profound sampling bias that cannot be explained as redundancy. To address this bias, we estimate terrestrial tetrapod diversity for palaeogeographical regions of approximately equal size. We find that regional-scale diversity was constrained over timespans of tens to hundreds of millions of years, and similar patterns are recovered for major subgroups, such as dinosaurs, mammals and squamates. Although the Cretaceous/Palaeogene mass extinction catalysed an abrupt two- to three-fold increase in regional diversity 66 million years ago, no further increases occurred, and recent levels of regional diversity do not exceed those of the Palaeogene. These results parallel those recovered in analyses of local community-level richness. Taken together, our findings strongly contradict past studies that suggested unbounded diversity increases at local and regional scales over the last 100 million years.

Publisher Correction: Open Science principles for accelerating trait-based science across the Tree of Life.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Open Science principles for accelerating trait-based science across the Tree of Life.

Synthesizing trait observations and knowledge across the Tree of Life remains a grand challenge for biodiversity science. Species traits are widely used in ecological and evolutionary science, and new data and methods have proliferated rapidly. Yet accessing and integrating disparate data sources remains a considerable challenge, slowing progress toward a global synthesis to integrate trait data across organisms. Trait science needs a vision for achieving global integration across all organisms. Here, we outline how the adoption of key Open Science principles-open data, open source and open methods-is transforming trait science, increasing transparency, democratizing access and accelerating global synthesis. To enhance widespread adoption of these principles, we introduce the Open Traits Network (OTN), a global, decentralized community welcoming all researchers and institutions pursuing the collaborative goal of standardizing and integrating trait data across organisms. We demonstrate how adherence to Open Science principles is key to the OTN community and outline five activities that can accelerate the synthesis of trait data across the Tree of Life, thereby facilitating rapid advances to address scientific inquiries and environmental issues. Lessons learned along the path to a global synthesis of trait data will provide a framework for addressing similarly complex data science and informatics challenges.

Reorganization of surviving mammal communities after the end-Pleistocene megafaunal extinction.

Large mammals are at high risk of extinction globally. To understand the consequences of their demise for community assembly, we tracked community structure through the end-Pleistocene megafaunal extinction in North America. We decomposed the effects of biotic and abiotic factors by analyzing co-occurrence within the mutual ranges of species pairs. Although shifting climate drove an increase in niche overlap, co-occurrence decreased, signaling shifts in biotic interactions. Furthermore, the effect of abiotic factors on co-occurrence remained constant over time while the effect of biotic factors decreased. Biotic factors apparently played a key role in continental-scale community assembly before the extinctions. Specifically, large mammals likely promoted co-occurrence in the Pleistocene, and their loss contributed to the modern assembly pattern in which co-occurrence frequently falls below random expectations.

Diversity dynamics of Phanerozoic terrestrial tetrapods at the local-community scale.

The fossil record provides one of the strongest tests of the hypothesis that diversity within local communities is constrained over geological timescales. Constraints to diversity are particularly controversial in modern terrestrial ecosystems, yet long-term patterns are poorly understood. Here we document patterns of local richness in Phanerozoic terrestrial tetrapods using a global data set comprising 145,332 taxon occurrences from 27,531 collections. We show that the local richness of non-flying terrestrial tetrapods has risen asymptotically since their initial colonization of land, increasing at most threefold over the last 300 million years. Statistical comparisons support phase-shift models, with most increases in local richness occurring: (1) during the colonization of land by vertebrates, concluding by the late Carboniferous; and (2) across the Cretaceous/Paleogene boundary. Individual groups, such as mammals, lepidosaurs and dinosaurs also experienced early increases followed by periods of stasis often lasting tens of millions of years. Mammal local richness abruptly tripled across the Cretaceous/Paleogene boundary, but did not increase over the next 66 million years. These patterns are consistent with the hypothesis that diversity is constrained at the local-community scale.

High diversity and rapid spatial turnover of integron gene cassettes in soil.

Integrons are genetic elements that promote rapid adaptation in bacteria by capturing exogenous, mobile gene cassettes. Recently, a subset of gene cassettes has facilitated the global spread of antibiotic resistance. However, outside clinical settings, very little is known about their diversity and spatial ecology. To address this question, we sequenced integron gene cassettes from soils sampled across Australia and Antarctica. We recovered 44 970 open reading frames that encoded 27 215 unique proteins, representing an order of magnitude more cassettes than previous sequencing efforts. We found that cassettes have extremely high local richness, significantly greater than previously predicted, with estimates ranging from 4000 to 18 000 unique cassettes per 0.3 g of soil. We show that cassettes have a heterogeneous distribution across space, and that they exhibit rapid turnover with distance. Similarity between samples drops to between 0.1% and 10% at distances of as little as 100 m. Together, these data provide key insights into the ecology and size of the gene cassette metagenome.

Limits to species richness in terrestrial communities.

Are communities limited by biotic interactions, or are they random draws from regional species pools? One way to tell is to compare total species counts in geographic regions to average counts in ecological samples falling within those regions. If species richness is limited regionally, then the relationship should be curvilinear even in a log-log space. Global sets of samples including trees and 10 groups of animals are analysed to test this hypothesis. Most relationships are indeed curvilinear. To explain these patterns, a simple model is proposed that invokes biotic interaction-limited speciation or immigration rates combined with extinction or extirpation rates that fall as the number of occupied patches increases. Local and regional richness come into balance as the rates trade off, causing global richness to also be limited. Surprisingly, however, the data for trees break the pattern, suggesting that the great adaptive radiation of seed plants may still be unfolding.

Effects of habitat disturbance on tropical forest biodiversity.

It is widely expected that habitat destruction in the tropics will cause a mass extinction in coming years, but the potential magnitude of the loss is unclear. Existing literature has focused on estimating global extinction rates indirectly or on quantifying effects only at local and regional scales. This paper directly predicts global losses in 11 groups of organisms that would ensue from disturbance of all remaining tropical forest habitats. The results are based on applying a highly accurate method of estimating species richness to 875 ecological samples. About 41% of the tree and animal species in this dataset are absent from disturbed habitats, even though most samples do still represent forests of some kind. The individual figures are 30% for trees and 8-65% for 10 animal groups. Local communities are more robust to disturbance because losses are partially balanced out by gains resulting from homogenization.

Pattern, process, inference and prediction in extinction biology.

Extinction is a key feature of the evolutionary history of life, and assessments of extinction risk are essential for the effective protection of biodiversity. The goal in assembling this special issue of Biology Letters was to highlight problems and questions at the research frontier of extinction biology, with an emphasis on recent developments in the methodology of inferring the patterns and processes of extinction from a background of often noisy and sparse data. In selecting topics, we sought to illustrate how extinction is not simply a self-evident phenomenon, but the subject of a dynamic and quantitatively rigorous field of natural science, with practical applications to conservation.

A comprehensive database of quality-rated fossil ages for Sahul's Quaternary vertebrates.

The study of palaeo-chronologies using fossil data provides evidence for past ecological and evolutionary processes, and is therefore useful for predicting patterns and impacts of future environmental change. However, the robustness of inferences made from fossil ages relies heavily on both the quantity and quality of available data. We compiled Quaternary non-human vertebrate fossil ages from Sahul published up to 2013. This, the FosSahul database, includes 9,302 fossil records from 363 deposits, for a total of 478 species within 215 genera, of which 27 are from extinct and extant megafaunal species (2,559 records). We also provide a rating of reliability of individual absolute age based on the dating protocols and association between the dated materials and the fossil remains. Our proposed rating system identified 2,422 records with high-quality ages (i.e., a reduction of 74%). There are many applications of the database, including disentangling the confounding influences of hypothetical extinction drivers, better spatial distribution estimates of species relative to palaeo-climates, and potentially identifying new areas for fossil discovery.

Climate change not to blame for late Quaternary megafauna extinctions in Australia.

Late Quaternary megafauna extinctions impoverished mammalian diversity worldwide. The causes of these extinctions in Australia are most controversial but essential to resolve, because this continent-wide event presaged similar losses that occurred thousands of years later on other continents. Here we apply a rigorous metadata analysis and new ensemble-hindcasting approach to 659 Australian megafauna fossil ages. When coupled with analysis of several high-resolution climate records, we show that megafaunal extinctions were broadly synchronous among genera and independent of climate aridity and variability in Australia over the last 120,000 years. Our results reject climate change as the primary driver of megafauna extinctions in the world's most controversial context, and instead estimate that the megafauna disappeared Australia-wide ∼13,500 years after human arrival, with shorter periods of coexistence in some regions. This is the first comprehensive approach to incorporate uncertainty in fossil ages, extinction timing and climatology, to quantify mechanisms of prehistorical extinctions.

Near-Stasis in the Long-Term Diversification of Mesozoic Tetrapods.

How did evolution generate the extraordinary diversity of vertebrates on land? Zero species are known prior to ~380 million years ago, and more than 30,000 are present today. An expansionist model suggests this was achieved by large and unbounded increases, leading to substantially greater diversity in the present than at any time in the geological past. This model contrasts starkly with empirical support for constrained diversification in marine animals, suggesting different macroevolutionary processes on land and in the sea. We quantify patterns of vertebrate standing diversity on land during the Mesozoic-early Paleogene interval, applying sample-standardization to a global fossil dataset containing 27,260 occurrences of 4,898 non-marine tetrapod species. Our results show a highly stable pattern of Mesozoic tetrapod diversity at regional and local levels, underpinned by a weakly positive, but near-zero, long-term net diversification rate over 190 million years. Species diversity of non-flying terrestrial tetrapods less than doubled over this interval, despite the origins of exceptionally diverse extant groups within mammals, squamates, amphibians, and dinosaurs. Therefore, although speciose groups of modern tetrapods have Mesozoic origins, rates of Mesozoic diversification inferred from the fossil record are slow compared to those inferred from molecular phylogenies. If high speciation rates did occur in the Mesozoic, then they seem to have been balanced by extinctions among older clades. An apparent 4-fold expansion of species richness after the Cretaceous/Paleogene (K/Pg) boundary deserves further examination in light of potential taxonomic biases, but is consistent with the hypothesis that global environmental disturbances such as mass extinction events can rapidly adjust limits to diversity by restructuring ecosystems, and suggests that the gradualistic evolutionary diversification of tetrapods was punctuated by brief but dramatic episodes of radiation.

The shape of terrestrial abundance distributions.

Ecologists widely accept that the distribution of abundances in most communities is fairly flat but heavily dominated by a few species. The reason for this is that species abundances are thought to follow certain theoretical distributions that predict such a pattern. However, previous studies have focused on either a few theoretical distributions or a few empirical distributions. I illustrate abundance patterns in 1055 samples of trees, bats, small terrestrial mammals, birds, lizards, frogs, ants, dung beetles, butterflies, and odonates. Five existing theoretical distributions make inaccurate predictions about the frequencies of the most common species and of the average species, and most of them fit the overall patterns poorly, according to the maximum likelihood-related Kullback-Leibler divergence statistic. Instead, the data support a low-dominance distribution here called the "double geometric." Depending on the value of its two governing parameters, it may resemble either the geometric series distribution or the lognormal series distribution. However, unlike any other model, it assumes both that richness is finite and that species compete unequally for resources in a two-dimensional niche landscape, which implies that niche breadths are variable and that trait distributions are neither arrayed along a single dimension nor randomly associated. The hypothesis that niche space is multidimensional helps to explain how numerous species can coexist despite interacting strongly.

Current extinction rates of reptiles and amphibians.

There is broad concern that a mass extinction of amphibians and reptiles is now underway. Here I apply an extremely conservative Bayesian method to estimate the number of recent amphibian and squamate extinctions in nine important tropical and subtropical regions. The data stem from a combination of museum collection databases and published site surveys. The method computes an extinction probability for each species by considering its sighting frequency and last sighting date. It infers hardly any extinction when collection dates are randomized and it provides underestimates when artificial extinction events are imposed. The method also appears to be insensitive to trends in sampling; therefore, the counts it provides are absolute minimums. Extinctions or severe population crashes have accumulated steadily since the 1970s and 1980s, and at least 3.1% of frog species have already disappeared. Based on these data and this conservative method, the best estimate of the global grand total is roughly 200 extinctions. Consistent with previous results, frog losses are heavy in Latin America, which has been greatly affected by the pathogenic chytrid fungus Batrachochytrium dendrobatidis. Extinction rates are now four orders-of-magnitude higher than background, and at least another 6.9% of all frog species may be lost within the next century, even if there is no acceleration in the growth of environmental threats.

A new twist on a very old binary similarity coefficient.

Pairwise similarity coefficients are downward biased when samples only record presences and sampling is partial. A simple but forgotten index proposed by Stephen Forbes in 1907 can help solve this problem. His original equation requires knowing the number of species absent in both samples that could have been present. It is proposed that this count should simply be ignored and that the coefficient should be adjusted using a simple heuristic correction. Four analyses show that the corrected equation outperforms the Dice and Simpson indices, which are highly correlated with many others. In two-sample simulations, similarity is almost always closer to the assumed value when the species pool size and sampling intensity are varied, regardless of whether the underlying abundance distribution is uniform, log-normal, or geometric. The index is also much more robust when sampling is unequal. An analysis of bat samples from peninsular Malaysia buttresses these conclusions. The corrected coefficient also indicates that local assemblages of North American mammals are random subsamples of larger species pools by returning similarity of values of around 1, and it suggests a more consistent relationship between biome-scale comparisons and local-scale comparisons. Finally, it yields a better-dispersed pattern when the biome-scale inventories are ordinated. If these results are generalizable, then the new and old equation should see wide application, potentially taking the place of the two most commonly used alternatives (the interrelated Dice and Jaccard indices) whenever sampling is incomplete.