Testing Geology with Biology: Plate Tectonics and the Diversification of Microhylid Frogs in the Papuan Region.

Studies of the Papuan region have provided fundamental insights into the evolutionary processes generating its exceptional biodiversity, but the influence of geological processes merits further study. Lying at the junction of five tectonic plates, this region has experienced a turbulent geological history that has not only produced towering mountains allowing elevational specialization and island archipelagos with varying degrees of isolation promoting vicariance, but also active margins where land masses have collided and been subsequently rifted apart creating a mosaic of intermixed terranes with vastly different geological histories. Asterophryine frogs are a hyperdiverse clade representing half the world's microhylid diversity (over 360 species) centered on New Guinea and its satellite islands. We show that vicariance facilitated by geological history explains this far and wide distribution of a clade that should have poor dispersal abilities. We recovered a mainland tectonic unit, the East Papua Composite Terrane (EPCT), as the center of origin for Asterophryinae and no fewer than 71 instances of what appear to be long-distance dispersal events, 29 of which are between mainland regions, with 42 from the mainland to the islands, some presently as far as 200 km away from source populations over open ocean. Furthermore, we find strong support for a "Slow and Steady" hypothesis for the formation of the northern margin of New Guinea by many separate accretion events during the Miocene, over other major geological alternatives, consistent with the 20 M year age of the clade and arrival via the EPCT. In addition, the historical biogeography of our frogs strongly supports an affiliation of the Louisiade Archipelago and Woodlark Island with the Owen Stanley Range on the EPCT, and the recent proximity of the large New Britain Island. Our results show that Asterophryinae did not have to repeatedly and independently disperse across large ocean barriers to the offshore islands, against the predictions of island biogeography theory, but that the current distribution can be explained through vicariance and short-distance oceanic dispersal as historical land connections disappeared and islands slowly became separated from each other. We show that islands have a life history, changing in distance from other land masses, with consequent opportunities for dispersal, isolation, and cladogenesis of their biotas. More broadly, we can begin to see how the geological history of the Papuan region can result in the rapid accumulation and staggering number of extant species.

Molecular and phylogenetic datasets for the Asterophryinae frogs of New Guinea with additional data on lifestyle, geography, and elevation.

The data provided here are related to the article "Resolving the Deep Phylogeny: Implications for Early Adaptive Radiation, Cryptic, and Present-day Ecological Diversity of Papuan Microhylid Frogs" [1]. The dataset is based on 233 tissue samples of the subfamily Asteroprhyinae, with representatives from all recognized genera, in addition to three outgroup taxa. The sequence dataset contains over 2400 characters per sample for five genes: three nuclear (Seventh in Absentia (SIA), Brain Derived Neurotrophic Factor (BDNF), Sodium Calcium Exchange subunit-1 (NXC-1)), and two mitochondrial loci (Cytochrome oxidase b (CYTB), and NADH dehydrogenase subunit 4 (ND4)); and is 99% complete. New primers were designed for all loci and accession numbers for the raw sequence data are provided. The sequences are used with geological time calibrations to produce time-calibrated Bayesian inference (BI) and Maximum Likelihood (ML) phylogenetic reconstructions using BEAST2 and IQ-TREE. Lifestyle data (arboreal, scansorial, terrestrial, fossorial, semi-aquatic) were collected from the literature and field notes and used to infer ancestral character states for each lineage. Collection location and elevation data were used to verify sites where multiple species or candidate species co-occur. All sequence data, alignments, and associated metadata (voucher specimen number, species identification, type locality status, global positioning system [GPS] coordinates, elevation, site with species list, and lifestyle) as well as the code to produce all analyses and figures are provided.

Melanesia holds the world's most diverse and intact insular amphibian fauna.

Identifying hotspots of biological diversity is a key step in conservation prioritisation. Melanesia-centred on the vast island of New Guinea-is increasingly recognised for its exceptionally species-rich and endemic biota. Here we show that Melanesia has the world's most diverse insular amphibian fauna, with over 7% of recognised global frog species in less than 0.7% of the world's land area, and over 97% of species endemic. We further estimate that nearly 200 additional candidate species have been discovered but remain unnamed, pointing to a total fauna in excess of 700 species. Nearly 60% of the Melanesian frog fauna is in a lineage of direct-developing microhylids characterised by smaller distributions than co-occurring frog families, suggesting lineage-specific high beta diversity is a key driver of Melanesian anuran megadiversity. A comprehensive conservation status assessment further highlights geographic concentrations of recently described range-restricted threatened taxa that warrant urgent conservation actions. Nonetheless, by world standards, the Melanesian frog fauna is relatively intact, with 6% of assessed species listed as threatened and no documented extinctions; and thus it provides an unparalleled opportunity to understand and conserve a megadiverse and relatively intact insular biota.

Resolving the deep phylogeny: Implications for early adaptive radiation, cryptic, and present-day ecological diversity of Papuan microhylid frogs.

The microhylid frogs of the New Guinea region are the largest and most ecologically diverse subfamily (Asterophryinae) of one of the largest anuran families in the world and can live in communities of up to 20 species. While there has been recent progress in resolving the phylogenetic relationships of Asterophryinae, significant uncertainties remain, impeding further progress in understanding the evolution of microhabitat use, parental care, and life history variation in this group. In particular, the early divergences at the base of the tree remain unclear; as does the monophyly of some genera; and recent studies have discovered that species with wide geographic distribution are instead cryptic species complexes. In this study, we fortified geographic sampling of the largest previous phylogenetic effort by sequencing an additional 62 taxa and increased data quality and quantity by adding new layers of data vetting and by filling in previously incomplete loci to the five gene dataset (2 mitochondrial, 3 nuclear protein-coding genes) to obtain a dataset that is now 99% complete in over 2400 characters for 233 samples (205 taxa) of Asterophryinae and 3 outgroup taxa, and analyzed microhabitat use data for these taxa from field data and data collected from the literature. Importantly, our sampling includes complete community complements at 19 sites as well as representatives at over 80 sites across New Guinea and its offshore islands. We present a highly resolved molecular phylogeny which, for the first time, has over 95% of nodes supported (84% highly supported) whether using Maximum Likelihood or Bayesian Inference, allowing clarification of all genera (whether monophyletic or clearly not), their sister genera relationships, as well as an age estimate for the Asterophryinae at approximately 20MYA. Early generic diversification occurring between 17 and 12 MYA gave rise to a surprising diversity of about 18 genera as well as the 5 putative microhabitat types. Our tree reveals extensive cryptic diversity calling any widespread taxa into doubt, and clearly demonstrates that complex multispecies communities of Asterophryinae are ecologically diverse, are numerous, and of ancient origin across New Guinea. We discuss the implications of our phylogeny for explaining the explosive diversification of Asterophryinae as the result of adaptive radiation, niche conservatism, and non-adaptive radiation.

Geography-Dependent Horizontal Gene Transfer from Vertebrate Predators to Their Prey.

Horizontal transfer (HT) of genes between multicellular animals, once thought to be extremely rare, is being more commonly detected, but its global geographic trend and transfer mechanism have not been investigated. We discovered a unique HT pattern of Bovine-B (BovB) LINE retrotransposons in vertebrates, with a bizarre transfer direction from predators (snakes) to their prey (frogs). At least 54 instances of BovB HT were detected, which we estimate to have occurred across time between 85 and 1.3 Ma. Using comprehensive transcontinental sampling, our study demonstrates that BovB HT is highly prevalent in one geographical region, Madagascar, suggesting important regional differences in the occurrence of HTs. We discovered parasite vectors that may plausibly transmit BovB and found that the proportion of BovB-positive parasites is also high in Madagascar where BovB thus might be physically transported by parasites to diverse vertebrates, potentially including humans. Remarkably, in two frog lineages, BovB HT occurred after migration from a non-HT area (Africa) to the HT hotspot (Madagascar). These results provide a novel perspective on how the prevalence of parasites influences the occurrence of HT in a region, similar to pathogens and their vectors in some endemic diseases.

A global reptile assessment highlights shared conservation needs of tetrapods.

Comprehensive assessments of species' extinction risks have documented the extinction crisis1 and underpinned strategies for reducing those risks2. Global assessments reveal that, among tetrapods, 40.7% of amphibians, 25.4% of mammals and 13.6% of birds are threatened with extinction3. Because global assessments have been lacking, reptiles have been omitted from conservation-prioritization analyses that encompass other tetrapods4-7. Reptiles are unusually diverse in arid regions, suggesting that they may have different conservation needs6. Here we provide a comprehensive extinction-risk assessment of reptiles and show that at least 1,829 out of 10,196 species (21.1%) are threatened-confirming a previous extrapolation8 and representing 15.6 billion years of phylogenetic diversity. Reptiles are threatened by the same major factors that threaten other tetrapods-agriculture, logging, urban development and invasive species-although the threat posed by climate change remains uncertain. Reptiles inhabiting forests, where these threats are strongest, are more threatened than those in arid habitats, contrary to our prediction. Birds, mammals and amphibians are unexpectedly good surrogates for the conservation of reptiles, although threatened reptiles with the smallest ranges tend to be isolated from other threatened tetrapods. Although some reptiles-including most species of crocodiles and turtles-require urgent, targeted action to prevent extinctions, efforts to protect other tetrapods, such as habitat preservation and control of trade and invasive species, will probably also benefit many reptiles.

Elevation is a stronger predictor of morphological trait divergence than competition in a radiation of tropical lizards.

Adaptations for efficient performance are expected to shape animal morphology based on selection for microhabitat use and ecological forces. The presence of competitor species is predicted to cause niches to contract and enhance trait divergence. Therefore, increased species richness is expected to lead to greater trait divergence, and to result in reduced overlap and similarity between morphologies of sympatric species. We examined patterns of morphospace occupancy and partitioning in the skink fauna of New Guinea, the world's largest tropical island. Because skink species richness is largely decoupled from elevation in New Guinea, we could examine the effects of both factors (as proxies for competition and abiotic conditions), on morphospace occupancy and partitioning. We measured 1,860 specimens from 79 species of skinks throughout Papua New Guinea, and examined their morphospace occupancy in a spatial context. We calculated, for each assemblage within equal-area cells, the volume of morphospace occupied by all skinks, the mean volume occupied per species, and the mean distance and overlap between all species pairs. We then examined whether these metrics are related to species richness and elevation. Elevation is a stronger predictor of morphospace occupancy than species richness. As elevation increases, intraspecific variation decreases and morphologies become more similar to each other such that overall morphospace occupancy decreases. Highland skinks are, on average, smaller, thinner and shorter limbed than lowland species. We hypothesise that harsh climates in the New Guinea highland habitats impose strong selection on skinks to occupy specific areas of morphospace that facilitate efficient thermoregulation in suboptimal thermal conditions. We conclude that the effect of competition on trait divergence on a community and assemblage scale is eclipsed by abiotic selection pressures in these harsh environments.

Cryptic diversity and non-adaptive radiation of montane New Guinea skinks (Papuascincus; Scincidae).

New Guinea, the world's largest and highest tropical island, has a rich but poorly known biota. Papuascincus is a genus of skinks endemic to New Guinea's mountain regions, comprising two wide-ranging species and two species known only from their type series. The phylogeny of the genus has never been examined and the relationships among its species - as well as between it and closely related taxa - are hitherto unknown. We performed the first large-scale molecular-phylogenetic study of Papuascincus, including sampling across the genus' range in Papua New Guinea. We sequenced three mitochondrial and two nuclear markers from 65 specimens of Papuascincus and reconstructed their phylogenetic relationships. We also performed species-delimitation analyses, estimated divergence times and ancestral biogeography, and examined body-size evolution within the genus. Papuascincus was strongly supported as monophyletic. It began radiating during the mid-Miocene in the area now comprising the Central Cordillera of New Guinea, then dispersed eastward colonising the Papuan Peninsula. We found evidence of extensive cryptic diversity within the genus, with between nine and 20 supported genetic lineages. These were estimated using three methods of species delimitation and predominantly occur in allopatry. Distribution and body-size divergence patterns indicated that character displacement in size took place during the evolutionary history of Papuascincus. We conclude that the genus requires comprehensive taxonomic revision and likely represents a species-rich lineage of montane skinks.

Early insularity and subsequent mountain uplift were complementary drivers of diversification in a Melanesian lizard radiation (Gekkonidae: Cyrtodactylus).

Regions with complex geological histories present a major challenge for scientists studying the processes that have shaped their biotas. The history of the vast and biologically rich tropical island of New Guinea is particularly complex and poorly resolved. Competing geological models propose New Guinea emerged as a substantial landmass either during the Mid-Miocene or as recently as the Pliocene. Likewise, the estimated timing for the uplift of the high Central Cordillera, spanning the length of the island, differs across models. Here we investigate how early islands and mountain uplift have shaped the diversification and biogeography of Cyrtodactylus geckos. Our data strongly support initial colonisation and divergence within proto-Papuan islands in the Early- to Mid-Miocene, with divergent lineages and endemic diversity concentrated on oceanic island arcs in northern New Guinea and the formerly isolated East-Papuan Composite Terrane. At least four lineages are inferred to have independently colonised hill- and lower-montane forests, indicating that mountain uplift has also played a critical role in accumulating diversity, even in this predominantly lowland lineage. Our findings suggest that substantial land in northern New Guinea and lower-montane habitats date back well into the Miocene and that insular diversification and mountain colonisation have synergistically generated diversity in the geologically complex Papuan region.

The global distribution of tetrapods reveals a need for targeted reptile conservation.

The distributions of amphibians, birds and mammals have underpinned global and local conservation priorities, and have been fundamental to our understanding of the determinants of global biodiversity. In contrast, the global distributions of reptiles, representing a third of terrestrial vertebrate diversity, have been unavailable. This prevented the incorporation of reptiles into conservation planning and biased our understanding of the underlying processes governing global vertebrate biodiversity. Here, we present and analyse the global distribution of 10,064 reptile species (99% of extant terrestrial species). We show that richness patterns of the other three tetrapod classes are good spatial surrogates for species richness of all reptiles combined and of snakes, but characterize diversity patterns of lizards and turtles poorly. Hotspots of total and endemic lizard richness overlap very little with those of other taxa. Moreover, existing protected areas, sites of biodiversity significance and global conservation schemes represent birds and mammals better than reptiles. We show that additional conservation actions are needed to effectively protect reptiles, particularly lizards and turtles. Adding reptile knowledge to a global complementarity conservation priority scheme identifies many locations that consequently become important. Notably, investing resources in some of the world's arid, grassland and savannah habitats might be necessary to represent all terrestrial vertebrates efficiently.

Publisher Correction: The global distribution of tetrapods reveals a need for targeted reptile conservation.

In this Article originally published, owing to a technical error, the author 'Laurent Chirio' was mistakenly designated as a corresponding author in the HTML version, the PDF was correct. This error has now been corrected in the HTML version. Further, in Supplementary Table 3, the authors misspelt the surname of 'Danny Meirte'; this file has now been replaced.

Molecular phylogenetics and dating of the problematic New Guinea microhylid frogs (Amphibia: Anura) reveals elevated speciation rates and need for taxonomic reclassification.

Asterophryinae is a large monophyletic subfamily of Anurans containing over 300 species distributed across one of the world's most geologically active areas - New Guinea and its satellite islands, Australia and the Philippines. The tremendous ecological and morphological diversity of this clade, with apparent specializations for burrowing, terrestrial, semi-aquatic, and arboreal lifestyle, suggests an evolutionary process of adaptive radiation. Despite this spectacular diversity, this and many other questions of evolutionary processes have received little formal study because until now the phylogeny of this spececies-rich clade has remained uncertain. Here we reconstruct a phylogeny for Asterophryinae with greatly increased taxon and genetic sampling relative to prior studies. We use Maximum Likelihood and Bayesian Inference methods to produce the most robust and comprehensive phylogeny to date containing 155 species using 3 nuclear and 2 mitochondrial loci. We also perform a time calibration analysis to estimate the age of the clade. We find support for the monophyly of Asterophryinae as well as need for taxonomic reclassification of several genera. Furthermore, we find increased rates of speciation across the clade supporting the hypothesis of rapid radiation. Lastly, we found that adding taxa to the analysis produced more robust phylogenetic results over adding loci.

Ecological guild evolution and the discovery of the world's smallest vertebrate.

Living vertebrates vary drastically in body size, yet few taxa reach the extremely minute size of some frogs and teleost fish. Here we describe two new species of diminutive terrestrial frogs from the megadiverse hotspot island of New Guinea, one of which represents the smallest known vertebrate species, attaining an average body size of only 7.7 mm. Both new species are members of the recently described genus Paedophryne, the four species of which are all among the ten smallest known frog species, making Paedophryne the most diminutive genus of anurans. This discovery highlights intriguing ecological similarities among the numerous independent origins of diminutive anurans, suggesting that minute frogs are not mere oddities, but represent a previously unrecognized ecological guild.

Uncovering cryptic diversity in Aspidomorphus (Serpentes: Elapidae): evidence from mitochondrial and nuclear markers.

The Papuan region, comprising New Guinea and nearby islands, has a complex geological history that has fostered high levels of biodiversity and endemism. Unfortunately, much of this diversity remains undocumented. We examine the evolutionary relationships of the venomous snake genus Aspidomorphus (Elapidae: Hydrophiinae), a Papuan endemic, and document extensive cryptic lineage diversification. Between Aspidomorphus species we find 22.2-27.9% corrected cyt-b sequence divergence. Within species we find 17.7-23.7% maximum sequence divergence. These high levels of genetic divergence may have complicated previous phylogenetic studies, which have had difficulty placing Aspidomorphus within the subfamily Hydrophiinae. Compared to previous studies, we increase sampling within Hydrophiinae to include all currently recognized species of Aspidomorphus and increase species representation for the genera Demansia and Toxicocalamus. We confirm monophyly of Aspidomorphus and resolve placement of the genus utilizing a set of seven molecular markers (12S, 16S, cyt-b, ND4, c-mos, MyHC-2, and RAG-1); we find strong support for a sister-group relationship between Aspidomorphus and a Demansia/Toxicocalamus preussi clade. We also use one mitochondrial (cyt-b) and one nuclear marker (SPTBN1) to document deep genetic divergence within all currently recognized species of Aspidomorphus and discuss the Solomon Island Arc as a potential center of divergence in this species. Lastly, we find high levels of concordance between the mtDNA and nuDNA markers used for inter-species phylogenetic reconstruction.