Morphological evolution and niche conservatism across a continental radiation of Australian blindsnakes.

Understanding how continental radiations are assembled across space and time is a major question in macroevolutionary biology. Here, we use a phylogenomic-scale phylogeny, a comprehensive morphological dataset and environmental niche models to evaluate the relationship between trait and environment, and assess the role of geography and niche conservatism in the continental radiation of Australian blindsnakes. This fossorial snake group comprises 47 described species and is widespread across various biomes on continental Australia. Although we expected blindsnakes to be morphologically conserved, we found considerable interspecific variation in all morphological traits we measured. Absolute body length is negatively correlated with mean annual temperature and body shape ratios are negatively correlated with soil compactness. We found that morphologically similar species are likely not a result of ecological convergence. Age-overlap correlation tests revealed niche similarity decreased with relative age of speciation events. We also found low geographical overlap across the phylogeny suggesting speciation is largely allopatric with low rates of secondary range overlap. Our study offers insights into the eco-morphological evolution of blindsnakes, and the potential for phylogenetic niche conservatism to influence continental scale radiations.

Evolutionary bursts drive morphological novelty in the world's largest skinks.

Animal phenotypes evolve and diverge as a result of differing selective pressures and drift. These processes leave unique signatures in patterns of trait evolution, impacting the tempo and mode of morphological macroevolution. While there is a broad understanding of the history of some organismal traits (e.g., body size), there is little consensus about the evolutionary mode of most others. This includes the relative contribution of prolonged (Darwinian gradualist) and episodic (Simpsonian jump) changes toward the evolution of novel morphologies. Here, we use new exon-capture and linear morphological datasets to investigate the tempo and mode of morphological evolution in Australo-Melanesian Tiliquini skinks. We generate a well-supported time-calibrated phylogenomic tree from ∼400 nuclear markers for more than 100 specimens, including undescribed diversity, and provide unprecedented resolution of the rapid Miocene diversification of these lizards. By collecting a morphological dataset that encompasses the lizard body plan (19 traits across the head, body, limb, and tail), we are able to identify that most traits evolve conservatively, but infrequent evolutionary bursts result in morphological novelty. These phenotypic discontinuities occur via rapid rate increases along individual branches, inconsistent with both gradualistic and punctuated equilibrial evolutionary modes. Instead, this "punctuated gradualism" has resulted in the rapid evolution of blue-tongued giants and armored dwarves in the ∼20 million years since colonizing Australia. These results outline the evolutionary pathway toward new morphologies and highlight the heterogeneity of evolutionary tempo and mode, even within individual traits.

Populating a Continent: Phylogenomics Reveal the Timing of Australian Frog Diversification.

The Australian continent's size and isolation make it an ideal place for studying the accumulation and evolution of biodiversity. Long separated from the ancient supercontinent Gondwana, most of Australia's plants and animals are unique and endemic, including the continent's frogs. Australian frogs comprise a remarkable ecological and morphological diversity categorized into a small number of distantly related radiations. We present a phylogenomic hypothesis based on an exon-capture dataset that spans the main clades of Australian myobatrachoid, pelodryadid hyloid, and microhylid frogs. Our time-calibrated phylogenomic-scale phylogeny identifies great disparity in the relative ages of these groups which vary from Gondwanan relics to recent immigrants from Asia and include arguably the continent's oldest living vertebrate radiation. This age stratification provides insight into the colonization of⁠, and diversification on, the Australian continent through deep time, during periods of dramatic climatic and community changes. Contemporary Australian frog diversity highlights the adaptive capacity of anurans, particularly in response to heat and aridity, and explains why they are one of the continent's most visible faunas.

Evolutionary models demonstrate rapid and adaptive diversification of Australo-Papuan pythons.

Lineages may diversify when they encounter available ecological niches. Adaptive divergence by ecological opportunity often appears to follow the invasion of a new environment with open ecological space. This evolutionary process is hypothesized to explain the explosive diversification of numerous Australian vertebrate groups following the collision of the Eurasian and Australian plates 25 Mya. One of these groups is the pythons, which demonstrate their greatest phenotypic and ecological diversity in Australo-Papua (Australia and New Guinea). Here, using an updated and near complete time-calibrated phylogenomic hypothesis of the group, we show that following invasion of this region, pythons experienced a sudden burst of speciation rates coupled with multiple instances of accelerated phenotypic evolution in head and body shape and body size. These results are consistent with adaptive radiation theory with an initial rapid niche-filling phase and later slow-down approaching niche saturation. We discuss these findings in the context of other Australo-Papuan adaptive radiations and the importance of incorporating adaptive diversification systems that are not extraordinarily species-rich but ecomorphologically diverse to understand how biodiversity is generated.

Population genomics and sexual signals support reproductive character displacement in Uperoleia (Anura: Myobatrachidae) in a contact zone.

When closely related species come into contact via range expansion, both may experience reduced fitness as a result of the interaction. Selection is expected to favour traits that minimize costly interspecies reproductive interactions (such as mismating) via a phenomenon called reproductive character displacement (RCD). Research on RCD frequently assumes secondary contact between species, but the geographical history of species interactions is often unknown. Population genomic data permit tests of geographical hypotheses about species origins and secondary contact through range expansion. We used population genomic data from single nucleotide polymorphisms (SNPs), mitochondrial sequence data, advertisement call data and morphological data to investigate a species complex of toadlets (Uperoleia borealis, U. crassa, U. inundata) from northern Australia. Although the three species of frogs were morphologically indistinguishable in our analysis, we determined that U. crassa and U. inundata form a single species (synonymized here) based on an absence of genomic divergence. SNP data identified the phylogeographical origin of U. crassa as the Top End, with subsequent westward invasion into the range of U. borealis in the Kimberley. We identified six F1 hybrids, all of which had the U. borealis mitochondrial haplotype, suggesting unidirectional hybridization. Consistent with the RCD hypothesis, U. borealis and U. crassa sexual signals differ more in sympatry than in allopatry. Hybrid males have intermediate calls, which probably reduces attractiveness to females. Integrating population genomic data, mitochondrial sequencing, morphology and behavioural approaches provides an unusually detailed collection of evidence for reproductive character displacement following range expansion and secondary contact.

Between a rock and a dry place: phylogenomics, biogeography, and systematics of ridge-tailed monitors (Squamata: Varanidae: Varanus acanthurus complex).

Genomic data are a powerful tool for the elucidation of evolutionary patterns at the population level and above. The combined analysis of genomic and morphological data can result in species delimitation hypotheses that reflect evolutionary history better than traditional taxonomy or any individual source of evidence. Here, we used thousands of single nucleotide polymorphisms, mitochondrial sequences, and comprehensive morphological data to characterize the evolutionary history of the ridge-tailed monitors in the Varanus acanthurus complex (V. acanthurus, V. baritji, and V. storri), a group of saxicolous lizards with a wide distribution in Australia, the driest vegetated continent. We found substantial genetic structure in the group and identify nine geographically clustered populations. Based on admixture patterns and species delimitation analyses we propose a taxonomic scheme that differs from current taxonomy. We consider V. acanthurus as monotypic, synonymize V. baritji with V. a. insulanicus (as a redefined V. insulanicus), elevate the subspecies of V. storri to full species (V. storri and V. ocreatus), and describe a new species from a previously identified center of endemism. The relationships among the species remain unresolved, likely as a result of fast speciation. Our study highlights the capability of large datasets to illuminate admixture patterns, biogeographic history, and species limits, even when phylogeny is not completely resolved. Furthermore, our results highlight the impact that the Cenozoic aridification of Australia had on saxicolous taxa and the role of mesic rocky escarpments as refugia. These habitats apparently allowed the persistence of lineages that became sources of colonization for arid environments.

Invasive chameleons released from predation display more conspicuous colors.

Conspicuous social and sexual signals are predicted to experience pronounced character release when natural selection via predation is relaxed. However, we have few good examples of this phenomenon in the wild and none in species with dynamic color change. Here, we show that Jackson's chameleons inadvertently introduced from Kenya to Hawaii (Oahu), where there are no coevolved, native lizard predators, experienced pronounced character release of color signals. Hawaiian chameleons displayed more conspicuous social color signals than Kenyan chameleons during male contests and courtship, were less cryptic in response to bird and snake predators, and showed greater change between display and antipredator color states. Hawaiian chameleon display colors were also more conspicuous in their local than ancestral habitats, consistent with local adaptation of social signals. These results demonstrate that relaxed predation pressure can result in character release of dynamic social signals in introduced species experiencing strong sexual selection.

Ontogenetic drivers of morphological evolution in monitor lizards and allies (Squamata: Paleoanguimorpha), a clade with extreme body size disparity.

BACKGROUND: Heterochrony, change in the rate or timing of development, is thought to be one of the main drivers of morphological evolution, and allometry, trait scaling patterns imposed by size, is traditionally thought to represent an evolutionary constraint. However, recent studies suggest that the ontogenetic allometric trajectories describing how organisms change as they grow may be labile and adaptive. Here we investigated the role of postnatal ontogenetic development in the morphological diversification of Paleoanguimorpha, the monitor lizards and allies, a clade with extreme body size disparity. We obtained linear and geometric morphometric data for more than 1,600 specimens belonging to three families and 60 species, representing ~ 72% of extant paleoanguimorph diversity. We used these data to undertake one of the largest comparative studies of ontogenetic allometry to date. RESULTS: Heterochrony is likely dictating morphological divergence at shallow evolutionary scales, while changes in the magnitude and direction of ontogenetic change are found mainly between major clades. Some patterns of ontogenetic variation and morphological disparity appear to reflect ontogenetic transitions in habitat use. Generally, juveniles are more similar to each other than adults, possibly because species that differ in ecology as adults are arboreal as juveniles. The magnitude of ontogenetic change follows evolutionary models where variation is constrained around an optimal value. Conversely, the direction of ontogenetic change may follow models with different adaptive optima per habitat use category or models where interspecific interactions influence its evolution. Finally, we found that the evolutionary rates of the ontogenetic allometric trajectories are phylogenetically variable. CONCLUSIONS: The attributes of ontogenetic allometric trajectories and their evolutionary rates are phylogenetically heterogeneous in Paleoanguimorpha. Both allometric constraints and ecological factors have shaped ontogeny in the group. Our study highlights the evolutionary lability and adaptability of postnatal ontogeny, and teases apart how different evolutionary shifts in ontogeny contribute to the generation of morphological diversity at different evolutionary scales.

A Smaller Habenula is Associated with Increasing Intensity of Sexual Selection.

The habenula is a small structure in the brain that acts as a relay station for neural information, helping to modulate behaviour in response to variable and unpredictable stimuli. Broadly, it is evolutionarily conserved in structure and connectivity across vertebrates and is the most prominent bilaterally asymmetric structure in the brain. Nonetheless, comparative evolutionary studies of the habenula are virtually non-existent. Here, we examine the volumes of the medial and lateral habenular subregions, in both hemispheres, across a group of Australian agamid lizards in the genus Ctenophorus. In males, we found bilaterally asymmetrical selection on the lateral habenula to become smaller with increasing intensity of sexual selection, possibly as a mechanism to increase aggressive responses. In females, we found bilaterally symmetrical selection on both the medial and lateral subregions to become smaller with increasing sexual selection. This is consistent with sexual selection increasing motivation to reproduce and the habenula's well-characterized role in controlling and modifying responses to rewarding stimuli. However, as there are currently no studies addressing habenular function in reptiles, it is difficult to draw more precise conclusions. As has happened recently in biomedical neuroscience, it is time for the habenula to receive greater attention in evolutionary neuroscience.

Competition and geography underlie speciation and morphological evolution in Indo-Australasian monitor lizards.

How biotic and abiotic factors act together to shape biological diversity is a major question in evolutionary biology. The recent availability of large datasets and development of new methodological approaches provide new tools to evaluate the predicted effects of ecological interactions and geography on lineage diversification and phenotypic evolution. Here, we use a near complete phylogenomic-scale phylogeny and a comprehensive morphological dataset comprising more than a thousand specimens to assess the role of biotic and abiotic processes in the diversification of monitor lizards (Varanidae). This charismatic group of lizards shows striking variation in species richness among its clades and multiple instances of endemic radiation in Indo-Australasia (i.e., the Indo-Australian Archipelago and Australia), one of Earth's most biogeographically complex regions. We found heterogeneity in diversification dynamics across the family. Idiosyncratic biotic and geographic conditions appear to have driven diversification and morphological evolution in three endemic Indo-Australasian radiations. Furthermore, incumbency effects partially explain patterns in the biotic exchange between Australia and New Guinea. Our results offer insight into the dynamic history of Indo-Australasia, the evolutionary significance of competition, and the long-term consequences of incumbency effects.

Rapid Radiation and Rampant Reticulation: Phylogenomics of South American Liolaemus Lizards.

Understanding the factors that cause heterogeneity among gene trees can increase the accuracy of species trees. Discordant signals across the genome are commonly produced by incomplete lineage sorting (ILS) and introgression, which in turn can result in reticulate evolution. Species tree inference using the multispecies coalescent is designed to deal with ILS and is robust to low levels of introgression, but extensive introgression violates the fundamental assumption that relationships are strictly bifurcating. In this study, we explore the phylogenomics of the iconic Liolaemus subgenus of South American lizards, a group of over 100 species mostly distributed in and around the Andes mountains. Using mitochondrial DNA (mtDNA) and genome-wide restriction site-associated DNA sequencing (RADseq; nDNA hereafter), we inferred a time-calibrated mtDNA gene tree, nDNA species trees, and phylogenetic networks. We found high levels of discordance between mtDNA and nDNA, which we attribute in part to extensive ILS resulting from rapid diversification. These data also reveal extensive and deep introgression, which combined with rapid diversification, explain the high level of phylogenetic discordance. We discuss these findings in the context of Andean orogeny and glacial cycles that fragmented, expanded, and contracted species distributions. Finally, we use the new phylogeny to resolve long-standing taxonomic issues in one of the most studied lizard groups in the New World.[Andes; ddRADSeq; introgression; lizards; mtDNA; reptiles; SNPs.].

Seen only once: an evolutionarily distinct species of Toadlet (Uperoleia: Myobatrachidae) from the Wessel Islands of northern Australia.

There is a high rate of recent species discovery in remote regions of northern Australia, especially for amphibians and reptiles. The Wessel Islands, located in the northeastern corner of the Northern Territory, has recently been identified as a region of high species and phylogenetic endemism based on samples collected during the sole reptile and amphibian survey there in 1993. Using a phylogenetic approach, we describe a new, evolutionarily distinct species of Uperoleia endemic to the Wessel Islands. This description is based on three specimens, one female and two juveniles, which represent the only confirmed vouchers of the species. Due to the low number of specimens, this new species cannot be diagnosed morphologically from other closely related Uperoleia, and nothing is currently known about the mating call or basic biology. The discovery of this species provides further evidence for the islands importance as an area of endemism and identifies an urgent need for further surveys to document the unique biological diversity of the Wessel Islands.

A return-on-investment approach for prioritization of rigorous taxonomic research needed to inform responses to the biodiversity crisis.

Global biodiversity loss is a profound consequence of human activity. Disturbingly, biodiversity loss is greater than realized because of the unknown number of undocumented species. Conservation fundamentally relies on taxonomic recognition of species, but only a fraction of biodiversity is described. Here, we provide a new quantitative approach for prioritizing rigorous taxonomic research for conservation. We implement this approach in a highly diverse vertebrate group-Australian lizards and snakes. Of 870 species assessed, we identified 282 (32.4%) with taxonomic uncertainty, of which 17.6% likely comprise undescribed species of conservation concern. We identify 24 species in need of immediate taxonomic attention to facilitate conservation. Using a broadly applicable return-on-investment framework, we demonstrate the importance of prioritizing the fundamental work of identifying species before they are lost.

A bird-like genome from a frog: Mechanisms of genome size reduction in the ornate burrowing frog, Platyplectrum ornatum.

The diversity of genome sizes across the tree of life is of key interest in evolutionary biology. Various correlates of variation in genome size, such as accumulation of transposable elements (TEs) or rate of DNA gain and loss, are well known, but the underlying molecular mechanisms driving or constraining genome size are poorly understood. Here, we study one of the smallest genomes among frogs characterized thus far, that of the ornate burrowing frog (Platyplectrum ornatum) from Australia, and compare it to other published frog and vertebrate genomes to examine the forces driving reduction in genome size. At ∼1.06 gigabases (Gb), the P. ornatum genome is like that of birds, revealing four major mechanisms underlying TE dynamics: reduced abundance of all major classes of TEs; increased net deletion bias in TEs; drastic reduction in intron lengths; and expansion via gene duplication of the repertoire of TE-suppressing Piwi genes, accompanied by increased expression of Piwi-interacting RNA (piRNA)-based TE-silencing pathway genes in germline cells. Transcriptomes from multiple tissues in both sexes corroborate these results and provide insight into sex-differentiation pathways in Platyplectrum Genome skimming of two closely related frog species (Lechriodus fletcheri and Limnodynastes fletcheri) confirms a reduction in TEs as a major driver of genome reduction in Platyplectrum and supports a macroevolutionary scenario of small genome size in frogs driven by convergence in life history, especially rapid tadpole development and tadpole diet. The P. ornatum genome offers a model for future comparative studies on mechanisms of genome size reduction in amphibians and vertebrates generally.

Phylogeography, historical demography and systematics of the world's smallest pythons (Pythonidae, Antaresia).

Advances from empirical studies in phylogeography, systematics and species delimitation highlight the importance of integrative approaches for quantifying taxonomic diversity. Genomic data have greatly improved our ability to discern both systematic diversity and evolutionary history. Here we combine analyses of mitochondrial DNA sequences, thousands of genome-wide SNPs and linear and geometric morphometrics on Antaresia, a clade of four currently recognised dwarf pythons from Australia and New Guinea (Antaresia childreni, A. stimsoni, A. maculosa and A. perthensis). Our integrative analyses of phylogenetics, population structure, species delimitation, historical demography and morphometrics revealed that the true evolutionary diversity is not well reflected in the current appraisal of the diversity of the group. We find that Antaresia childreni and A. stimsoni comprise a widespread network of populations connected by gene flow and without evidence of species-level divergence among them. However, A. maculosa shows considerable genetic structuring which leads us to recognise two subspecies in northeastern Australia and a new species in Torres Strait and New Guinea. These two contrasting cases of over and under estimation of diversity, respectively, illustrate the power of thorough integrative approaches into understanding evolution of biodiversity. Furthermore, our analyses of historical demographic patterns highlight the importance of the Kimberley, Pilbara and Cape York as origins of biodiversity in Australia.

Evidence that genetic compatibility underpins female mate choice in a monandrous amphibian.

Mate choice for genetic benefits remains controversial, largely because few studies have estimated the relative contributions of additive and non-additive sources of genetic variation to offspring fitness. Moreover, there remains a deficit of these estimates for species where female-mate preferences have been quantified in the wild, especially species characterized by monandry or monogamy. Here, we use artificial fertilization techniques combined with a cross-classified breeding design to simultaneously test for "good genes" and "compatible genes" benefits of mate choice in the monandrous red backed toadlet (Pseudophryne coriacea). In addition, we used a genomic approach to estimate effects of parental-genetic relatedness (assessed using 27, 768 single nucleotide polymorphisms) on offspring fitness. Our results revealed no significant additive genetic effects (sire effects), but highly significant non-additive genetic effects (sire × dam interaction effects), on fertilization success, survival during embryonic development, and hatching success. We also found significant associations between parental genetic similarity and offspring survival (whereby survival was higher when parents were more related), and significant positive relationships between fertilization success and embryo survival through to hatching. These results indicate that offspring viability is significantly influenced by the genetic compatibility of parental genotypes, that more related parents are more genetically compatible, and that gametes with greater compatibility at fertilization produce more viable offspring. More broadly, our findings provide new quantitative genetic evidence that genetic incompatibility underpins female mate preferences. Continued quantitative genetic assessment of the relative importance of good genes versus compatible genes is needed to ascertain the general importance of genetic benefits as a driver of female mate choice.

A Comprehensive Approach to Detect Hybridization Sheds Light on the Evolution of Earth's Largest Lizards.

Hybridization between species occurs more frequently in vertebrates than traditionally thought, but distinguishing ancient hybridization from other phenomena that generate similar evolutionary patterns remains challenging. Here, we used a comprehensive workflow to discover evidence of ancient hybridization between the Komodo dragon (Varanus komodoensis) from Indonesia and a common ancestor of an Australian group of monitor lizards known colloquially as sand monitors. Our data comprise $>$300 nuclear loci, mitochondrial genomes, phenotypic data, fossil and contemporary records, and past/present climatic data. We show that the four sand monitor species share more nuclear alleles with $V$. komodoensis than expected given a bifurcating phylogeny, likely as a result of hybridization between the latter species and a common ancestor of sand monitors. Sand monitors display phenotypes that are intermediate between their closest relatives and $V$. komodoensis. Biogeographic analyses suggest that $V$. komodoensis and ancestral sand monitors co-occurred in northern Australia. In agreement with the fossil record, this provides further evidence that the Komodo dragon once inhabited the Australian continent. Our study shows how different sources of evidence can be used to thoroughly characterize evolutionary histories that deviate from a treelike pattern, that hybridization can have long-lasting effects on phenotypes, and that detecting hybridization can improve our understanding of evolutionary and biogeographic patterns.[Biogeography; introgression; Komodo dragon; phylogenetic networks; phylogenomics; reticulation; Varanus.].

Phylogenomics, biogeography and taxonomic revision of New Guinean pythons (Pythonidae, Leiopython) harvested for international trade.

The large and enigmatic New Guinean pythons in the genus Leiopython are harvested from the wild to supply the international trade in pets. Six species are currently recognized (albertisii, biakensis, fredparkeri, huonensis, meridionalis, montanus) but the taxonomy of this group has been controversial. We combined analysis of 421 nuclear loci and complete mitochondrial genomes with morphological data to construct a detailed phylogeny of this group, understand their biogeographic patterns and establish the systematic diversity of this genus. Our molecular genetic data support two major clades, corresponding to L. albertisii and L. fredparkeri, but offer no support for the other four species. Our morphological data also only support two species. We therefore recognize L. albertisii and L. fredparkeri as valid species and place L. biakensis, L. meridionalis, L. huonensis and L. montanus into synonymy. We found that L. albertisii and L. fredparkeri are sympatric in western New Guinea; an atypical pattern compared to other Papuan species complexes in which the distributions of sister taxa are partitioned to the north and south of the island's central mountain range. For the purpose of conservation management, overestimation of species diversity within Leiopython has resulted in the unnecessary allocation of resources that could have been expended elsewhere. We strongly caution against revising the taxonomy of geographically widespread species groups when little or no molecular genetic data and only small morphological samples are available.

Phylogenomics of Monitor Lizards and the Role of Competition in Dictating Body Size Disparity.

Organismal interactions drive the accumulation of diversity by influencing species ranges, morphology, and behavior. Interactions vary from agonistic to cooperative and should result in predictable patterns in trait and range evolution. However, despite a conceptual understanding of these processes, they have been difficult to model, particularly on macroevolutionary timescales and across broad geographic spaces. Here, we investigate the influence of biotic interactions on trait evolution and community assembly in monitor lizards (Varanus). Monitors are an iconic radiation with a cosmopolitan distribution and the greatest size disparity of any living terrestrial vertebrate genus. Between the colossal Komodo dragon Varanus komodoensis and the smallest Australian dwarf goannas, Varanus length and mass vary by multiple orders of magnitude. To test the hypothesis that size variation in this genus was driven by character displacement, we extended existing phylogenetic comparative methods which consider lineage interactions to account for dynamic biogeographic history and apply these methods to Australian monitors and marsupial predators. Incorporating both exon-capture molecular and morphological data sets we use a combined evidence approach to estimate the relationships among living and extinct varaniform lizards. Our results suggest that communities of Australian Varanus show high functional diversity as a result of continent-wide interspecific competition among monitors but not with faunivorous marsupials. We demonstrate that patterns of trait evolution resulting from character displacement on continental scales are recoverable from comparative data and highlight that these macroevolutionary patterns may develop in parallel across widely distributed sympatric groups.[Character displacement; comparative methods; phylogenetics; trait evolution; Varanus.].