Museum skins enable identification of introgression associated with cytonuclear discordance.

Increased sampling of genomes and populations across closely related species has revealed that levels of genetic exchange during and after speciation are higher than previously thought. One obvious manifestation of such exchange is strong cytonuclear discordance, where the divergence in mitochondrial DNA (mtDNA) differs from that for nuclear genes more (or less) than expected from differences between mtDNA and nuclear DNA (nDNA) in population size and mutation rate. Given genome-scale datasets and coalescent modelling, we can now confidently identify cases of strong discordance and test specifically for historical or recent introgression as the cause. Using population sampling, combining exon capture data from historical museum specimens and recently collected tissues we showcase how genomic tools can resolve complex evolutionary histories in the brachyotis group of rock-wallabies (Petrogale). In particular, applying population and phylogenomic approaches we can assess the role of demographic processes in driving complex evolutionary patterns and assess a role of ancient introgression and hybridisation. We find that described species are well supported as monophyletic taxa for nDNA genes, but not for mtDNA, with cytonuclear discordance involving at least four operational taxonomic units (OTUs) across four species which diverged 183-278 kya. ABC modelling of nDNA gene trees supports introgression during or after speciation for some taxon pairs with cytonuclear discordance. Given substantial differences in body size between the species involved, this evidence for gene flow is surprising. Heterogenous patterns of introgression were identified but do not appear to be associated with chromosome differences between species. These and previous results suggest that dynamic past climates across the monsoonal tropics could have promoted reticulation among related species.

The macroevolutionary singularity of snakes.

Snakes and lizards (Squamata) represent a third of terrestrial vertebrates and exhibit spectacular innovations in locomotion, feeding, and sensory processing. However, the evolutionary drivers of this radiation remain poorly known. We infer potential causes and ultimate consequences of squamate macroevolution by combining individual-based natural history observations (>60,000 animals) with a comprehensive time-calibrated phylogeny that we anchored with genomic data (5400 loci) from 1018 species. Due to shifts in the dynamics of speciation and phenotypic evolution, snakes have transformed the trophic structure of animal communities through the recurrent origin and diversification of specialized predatory strategies. Squamate biodiversity reflects a legacy of singular events that occurred during the early history of snakes and reveals the impact of historical contingency on vertebrate biodiversity.

Speciation across biomes: Rapid diversification with reproductive isolation in the Australian delicate mice.

Phylogeographic studies of continental clades, especially when combined with palaeoclimate modelling, provide powerful insight into how environment drives speciation across climatic contexts. Australia, a continent characterized by disparate modern biomes and dynamic climate change, provides diverse opportunity to reconstruct the impact of past and present environments on diversification. Here, we use genomic-scale data (1310 exons and whole mitogenomes from 111 samples) to investigate Pleistocene diversification, cryptic diversity, and secondary contact in the Australian delicate mice (Hydromyini: Pseudomys), a recent radiation spanning almost all Australian environments. Across northern Australia, we find no evidence for introgression between cryptic lineages within Pseudomys delicatulus sensu lato, with palaeoclimate models supporting contraction and expansion of suitable habitat since the last glacial maximum. Despite multiple contact zones, we also find little evidence of introgression at a continental scale, with the exception of a potential hybrid zone in the mesic biome. In the arid zone, combined insights from genetic data and palaeomodels support a recent expansion in the arid specialist P. hermannsburgensis and contraction in the semi-arid P. bolami. In the face of repeated secondary contact, differences in sperm morphology and chromosomal rearrangements are potential mechanisms that maintain species boundaries in these recently diverged species. Additionally, we describe the western delicate mouse as a new species and recommend taxonomic reinstatement of the eastern delicate mouse. Overall, we show that speciation in an evolutionarily young and widespread clade has been driven by environmental change, and potentially maintained by divergence in reproductive morphology and chromosome rearrangements.

Population genomic diversity and structure in the golden bandicoot: a history of isolation, extirpation, and conservation.

Using genetic information to develop and implement conservation programs is vital for maintaining biodiversity and ecosystem resilience. Evaluation of the genetic variability within and among remnant populations can inform management of both natural and translocated populations to maximise species' adaptive potential, mitigate negative impacts of inbreeding, and subsequently minimise risk of extinction. Here we use reduced representation sequencing to undertake a genetic assessment of the golden bandicoot (Isoodon auratus), a threatened marsupial endemic to Australia. The currently recognised taxon consists of three subspecies distributed among multiple natural and translocated populations. After confirming the genetic distinctiveness of I. auratus from two closely related taxa, I. fusciventer and I. macrourus, we identified four genetic clusters within I. auratus. These clusters exhibited substantial genetic differentiation (pairwise FST values ranging from 0.18 to 0.65, pairwise DXY ranging from 0.1 to 0.168), reflecting long-term isolation of some populations on offshore islands and the influence of genetic drift. Mainland natural populations in the Kimberley region had the highest genetic diversity and the largest contribution to overall allelic and gene diversity compared to both natural and translocated island populations. A population translocated to Guluwuru Island in the Northern Territory had the lowest genetic diversity. Our data suggest that island populations can appear genetically unique due to genetic drift and this needs to be taken into account when considering genetic diversity in conservation efforts to maintain overall genetic diversity of the species. We effectively demonstrate how genomic information can guide practical conservation planning, especially when declining species are represented by multiple isolated populations.

Genetic mixing in conservation translocations increases diversity of a keystone threatened species, Bettongia lesueur.

Translocation programmes are increasingly being informed by genetic data to monitor and enhance conservation outcomes for both natural and established populations. These data provide a window into contemporary patterns of genetic diversity, structure and relatedness that can guide managers in how to best source animals for their translocation programmes. The inclusion of historical samples, where possible, strengthens monitoring by allowing assessment of changes in genetic diversity over time and by providing a benchmark for future improvements in diversity via management practices. Here, we used reduced representation sequencing (ddRADseq) data to report on the current genetic health of three remnant and seven translocated boodie (Bettongia lesueur) populations, now extinct on the Australian mainland. In addition, we used exon capture data from seven historical mainland specimens and a subset of contemporary samples to compare pre-decline and current diversity. Both data sets showed the significant impact of population founder source (whether multiple or single) on the genetic diversity of translocated populations. Populations founded by animals from multiple sources showed significantly higher genetic diversity than the natural remnant and single-source translocation populations, and we show that by mixing the most divergent populations, exon capture heterozygosity was restored to levels close to that observed in pre-decline mainland samples. Relatedness estimates were surprisingly low across all contemporary populations and there was limited evidence of inbreeding. Our results show that a strategy of genetic mixing has led to successful conservation outcomes for the species in terms of increasing genetic diversity and provides strong rationale for mixing as a management strategy.

Notes from the taxonomic disaster zone: Evolutionary drivers of intractable species boundaries in an Australian lizard clade (Scincidae: Ctenotus).

Genomic-scale datasets, sophisticated analytical techniques, and conceptual advances have disproportionately failed to resolve species boundaries in some groups relative to others. To understand the processes that underlie taxonomic intractability, we dissect the speciation history of an Australian lizard clade that arguably represents a "worst-case" scenario for species delimitation within vertebrates: the Ctenotus inornatus species group, a clade beset with decoupled genetic and phenotypic breaks, uncertain geographic ranges, and parallelism in purportedly diagnostic morphological characters. We sampled hundreds of localities to generate a genomic perspective on population divergence, structure, and admixture. Our results revealed rampant paraphyly of nominate taxa in the group, with lineages that are either morphologically cryptic or polytypic. Isolation-by-distance patterns reflect spatially continuous differentiation among certain pairs of putative species, yet genetic and geographic distances are decoupled in other pairs. Comparisons of mitochondrial and nuclear gene trees, tests of nuclear introgression, and historical demographic modelling identified gene flow between divergent candidate species. Levels of admixture are decoupled from phylogenetic relatedness; gene flow is often higher between sympatric species than between parapatric populations of the same species. Such idiosyncratic patterns of introgression contribute to species boundaries that are fuzzy while also varying in fuzziness. Our results suggest that "taxonomic disaster zones" like the C. inornatus species group result from spatial variation in the porosity of species boundaries and the resulting patterns of genetic and phenotypic variation. This study raises questions about the origin and persistence of hybridizing species and highlights the unique insights provided by taxa that have long eluded straightforward taxonomic categorization.

Linking life history to landscape for threatened species conservation in a multiuse region.

Landscape-scale conservation that considers metapopulation dynamics will be essential for preventing declines of species facing multiple threats to their survival. Toward this end, we developed a novel approach that combines occurrence records, spatial-environmental data, and genetic information to model habitat, connectivity, and patterns of genetic structure and link spatial attributes to underlying ecological mechanisms. Using the threatened northern quoll (Dasyurus hallucatus) as a case study, we applied this approach to address the need for conservation decision-making tools that promote resilient metapopulations of this threatened species in the Pilbara, Western Australia, a multiuse landscape that is a hotspot for biodiversity and mining. Habitat and connectivity were predicted by different landscape characteristics. Whereas habitat suitability was overwhelmingly driven by terrain ruggedness, dispersal was facilitated by proximity to watercourses. Although there is limited evidence for major physical barriers in the Pilbara, areas with high silt and clay content (i.e., alluvial and hardpan plains) showed high resistance to dispersal. Climate subtlety shaped distributions and patterns of genetic turnover, suggesting the potential for local adaptation. By understanding these spatial-environmental associations and linking them to life-history and metapopulation dynamics, we highlight opportunities to provide targeted species management. To support this, we have created habitat, connectivity, and genetic uniqueness maps for conservation decision-making in the region. These tools have the potential to provide a more holistic approach to conservation in multiuse landscapes globally.

La conservación a nivel del paisaje que incluye las dinámicas metapoblacionales será esencial para prevenir la declinación de especies con múltiples amenazas a su supervivencia. Enfocados en este fin, desarrollamos una estrategia novedosa que combina los registros presenciales, datos espacio-ambientales e información genética para modelar la conectividad de hábitat y los patrones de estructura genética y conectar los atributos espaciales con los mecanismos ecológicos subyacentes. Usamos al cuol del norte (Dasyurus hallucatus) como estudio de caso para aplicar esta estrategia y abordar la necesidad de herramientas de decisión en la conservación que promuevan metapoblaciones resilientes de esta especie en la Pilbara de Australia Occidental, un paisaje multiusos que es un punto caliente para la biodiversidad y la minería. Diferentes características del paisaje pronosticaron la conectividad y el hábitat. Mientras que la escabrosidad del terreno causó enormemente la idoneidad del hábitat, la dispersión estuvo propiciada por la proximidad a los cauces. Aunque hay evidencias limitadas de barreras físicas importantes en la Pilbara, las áreas con un contenido elevado de limo y arcilla (es decir, planicies aluviales y de alio) mostraron una gran resistencia a la dispersión. La matización climática determinó la distribución y los patrones del recambio genético, lo que sugiere un potencial para la adaptación local. Si entendemos estas asociaciones espacio-ambientales y las conectamos con las dinámicas metapoblacionales y de historia de vida, podemos resaltar las oportunidades para proporcionar un manejo focalizado de la especie. Para respaldar esto hemos creado mapas de hábitat, conectividad y singularidad genética para las decisiones de conservación en la región. Estas herramientas tienen el potencial de proporcionar una estrategia más holística para la conservación en los paisajes multiusos de todo el mundo.

Initiation of speciation across multiple dimensions in a rock-restricted, tropical lizard.

Population isolation and concomitant genetic divergence, resulting in strong phylogeographical structure, is a core aspect of speciation initiation. If and how speciation then proceeds and ultimately completes depends on multiple factors that mediate reproductive isolation, including divergence in genomes, ecology and mating traits. Here we explored these multiple dimensions in two young (Plio-Pleistocene) species complexes of gekkonid lizards (Heteronotia) from the Kimberley-Victoria River regions of tropical Australia. Using mitochondrial DNA screening and exon capture phylogenomics, we show that the rock-restricted Heteronotia planiceps exhibits exceptional fine-scale phylogeographical structure compared to the codistributed habitat generalist Heteronotia binoei. This indicates pervasive population isolation and persistence in the rock-specialist, and thus a high rate of speciation initiation across this geographically complex region, with levels of genomic divergence spanning the "grey zone" of speciation. Proximal lineages of H. planiceps were often separated by different rock substrates, suggesting a potential role for ecological isolation; however, phylogenetic incongruence and historical introgression were inferred between one such pair. Ecomorphological divergence among lineages within both H. planiceps and H. binoei was limited, except that limestone-restricted lineages of H. planiceps tended to be larger than rock-generalists. By contrast, among-lineage divergence in the chemical composition of epidermal pore secretions (putative mating trait) exceeded ecomorphology in both complexes, but with less trait overlap among lineages in H. planiceps. This system-particularly the rock-specialist H. planiceps-highlights the role of multidimensional divergence during incipient speciation, with divergence in genomes, ecomorphology and chemical signals all at play at very fine spatial scales.

New Guinea uplift opens ecological opportunity across a continent.

Sahul unites the world's largest and highest tropical island and the oldest and most arid continent on the backdrop of dynamic environmental conditions. Massive geological uplift in New Guinea is predicted to have acted as a species pump from the late Miocene onward, but the impact of this process on biogeography and diversification remains untested across Sahul as a whole. To address this, we reconstruct the assembly of a recent and diverse radiation of rodents (Murinae: Hydromyini) spanning New Guinea, Australia, and oceanic islands. Using phylogenomic data from 270 specimens, including many recently extinct and highly elusive species, we find that the orogeny and expansion of New Guinea opened ecological opportunity and triggered diversification across a continent. After a single over-water colonization from Asia ca. 8.5 Ma, ancestral Hydromyini were restricted to the tropical rainforest of proto-New Guinea for 3.5 million years. Following a shift in diversification coincident with the orogeny of New Guinea ca. 5 Ma and subsequent colonization of Australia, transitions between geographic regions (n = 24) and biomes (n = 34) become frequent. Recurrent over-water colonization between mainland and islands demonstrate how islands can play a substantial role in the assembly of continental fauna. Our results are consistent with a model of increased ecological opportunity across Sahul following major geological uplift in New Guinea ca. 5 Ma, with sustained diversification facilitated by over-water colonization from the Pleistocene to present. We show how geological processes, biome transitions, and over-water colonization collectively drove the diversification of an expansive continental radiation.

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.

Composition of a chemical signalling trait varies with phylogeny and precipitation across an Australian lizard radiation.

The environment presents challenges to the transmission and detection of animal signalling systems, resulting in selective pressures that can drive signal divergence amongst populations in disparate environments. For chemical signals, climate is a potentially important selective force because factors such as temperature and moisture influence the persistence and detection of chemicals. We investigated an Australian lizard radiation (Heteronotia) to explore relationships between a sexually dimorphic chemical signalling trait (epidermal pore secretions) and two key climate variables: temperature and precipitation. We reconstructed the phylogeny of Heteronotia with exon capture phylogenomics, estimated phylogenetic signal in amongst-lineage chemical variation and assessed how chemical composition relates to temperature and precipitation using multivariate phylogenetic regressions. High estimates of phylogenetic signal indicate that the composition of epidermal pore secretions varies amongst lineages in a manner consistent with Brownian motion, although there are deviations to this, with stark divergences coinciding with two phylogenetic splits. Accounting for phylogenetic non-independence, we found that amongst-lineage chemical variation is associated with geographic variation in precipitation but not temperature. This contrasts somewhat with previous lizard studies, which have generally found an association between temperature and chemical composition. Our results suggest that geographic variation in precipitation can affect the evolution of chemical signalling traits, possibly influencing patterns of divergence amongst lineages and species.

Genetic and Ecogeographic Controls on Species Cohesion in Australia's Most Diverse Lizard Radiation.

AbstractSpecies vary extensively in geographic range size and climatic niche breadth. If range limits are primarily determined by climatic factors, species with broad climatic tolerances and those that track geographically widespread climates should have large ranges. However, large ranges might increase the probability of population fragmentation and adaptive divergence, potentially decoupling climatic niche breadth and range size. Conversely, ecological generalism in large-ranged species might lead to higher gene flow across climatic transitions, increasing species' cohesion and thus decreasing genetic isolation by distance (IBD). Focusing on Australia's iconic Ctenotus lizard radiation, we ask whether species range size scales with climatic niche breadth and the degree of population isolation. To this end, we infer independently evolving operational taxonomic units (OTUs), their geographic and climatic ranges, and the strength of IBD within OTUs based on genome-wide loci from 722 individuals spanning 75 taxa. Large-ranged OTUs were common and had broader climatic niches than small-ranged OTUs; thus, large ranges do not appear to simply result from passive tracking of widespread climatic zones. OTUs with larger ranges and broader climatic niches showed relatively weaker IBD, suggesting that large-ranged species might possess intrinsic attributes that facilitate genetic cohesion across large distances and varied climates. By influencing population divergence and persistence, traits that affect species cohesion may play a central role in large-scale patterns of diversification and species richness.

Limited Introgression between Rock-Wallabies with Extensive Chromosomal Rearrangements.

Chromosome rearrangements can result in the rapid evolution of hybrid incompatibilities. Robertsonian fusions, particularly those with monobrachial homology, can drive reproductive isolation amongst recently diverged taxa. The recent radiation of rock-wallabies (genus Petrogale) is an important model to explore the role of Robertsonian fusions in speciation. Here, we pursue that goal using an extensive sampling of populations and genomes of Petrogale from north-eastern Australia. In contrast to previous assessments using mitochondrial DNA or nuclear microsatellite loci, genomic data are able to separate the most closely related species and to resolve their divergence histories. Both phylogenetic and population genetic analyses indicate introgression between two species that differ by a single Robertsonian fusion. Based on the available data, there is also evidence for introgression between two species which share complex chromosomal rearrangements. However, the remaining results show no consistent signature of introgression amongst species pairs and where evident, indicate generally low introgression overall. X-linked loci have elevated divergence compared with autosomal loci indicating a potential role for genic evolution to produce reproductive isolation in concert with chromosome change. Our results highlight the value of genome scale data in evaluating the role of Robertsonian fusions and structural variation in divergence, speciation, and patterns of molecular evolution.

Environmental resistance and habitat quality influence dispersal of the saltwater crocodile.

Landscape genetics commonly focuses on the effects of environmental resistance on animal dispersal patterns, but there is an emerging focus on testing environmental effects on emigration and settlement choices. In this study, we used landscape genetics approaches to quantify dispersal patterns in the world's largest crocodilian, the saltwater crocodile (Crocodylus porosus), and demonstrated environmental influences on three processes that comprise dispersal: emigration, movement and settlement. We found that both environmental resistance and properties of the source and destination catchments (proportion of breeding habitat) were important factors influencing observed dispersal events. Our habitat quality variables related to hypotheses about resource competition and represented the ratio of breeding habitat (which limits carrying capacity), suggesting that competition for habitat influences emigration and settlement choices, together with the strong effect of environmental resistance to movement (where high-quality habitat was associated with greatest environmental permeability). Approximately 42% of crocodiles were migrants from populations other than their sampling locations and some outstandingly productive populations had a much higher proportion of emigration rather than immigration. The distance most commonly travelled between source and destination was 150-200 km although a few travelled much longer distances, up to 600-700 km. Given the extensive dispersal range, individual catchments or hydrographic regions that combine two or three adjacent catchments are an appropriate scale for population management.

The Evolution of Comparative Phylogeography: Putting the Geography (and More) into Comparative Population Genomics.

Comparative population genomics is an ascendant field using genomic comparisons between species to draw inferences about forces regulating genetic variation. Comparative phylogeography, by contrast, focuses on the shared lineage histories of species codistributed geographically and is decidedly organismal in perspective. Comparative phylogeography is approximately 35 years old, and, by some metrics, is showing signs of reduced growth. Here, we contrast the goals and methods of comparative population genomics and comparative phylogeography and argue that comparative phylogeography offers an important perspective on evolutionary history that succeeds in integrating genomics with landscape evolution in ways that complement the suprageographic perspective of comparative population genomics. Focusing primarily on terrestrial vertebrates, we review the history of comparative phylogeography, its milestones and ongoing conceptual innovations, its increasingly global focus, and its status as a bridge between landscape genomics and the process of speciation. We also argue that, as a science with a strong "sense of place," comparative phylogeography offers abundant "place-based" educational opportunities with its focus on geography and natural history, as well as opportunities for collaboration with local communities and indigenous peoples. Although comparative phylogeography does not yet require whole-genome sequencing for many of its goals, we conclude that it nonetheless plays an important role in grounding our interpretation of genetic variation in the fundamentals of geography and Earth history.

Temperature predicts the rate of molecular evolution in Australian Eugongylinae skinks.

Temperature differences over time and space have been hypothesized to cause variation in the rate of molecular evolution of species, but empirical evidence is mixed. To further test this hypothesis, we utilized a large exon-capture sequence data of Australian Eugongylinae skinks, exemplifying a radiation of temperature-sensitive ectotherms spanning a large latitudinal gradient. The association between temperature (and other species traits) and long-term substitution rate was assessed based on 1268 sequenced exons of 44 species pairs from the Eugongylinae subfamily using regression analyses. Temperature is the strongest, positively correlated predictor of variation in substitution rate across the Australian Eugongylinae. It explains 45% of variation in synonymous substitution rate, and 11% after controlling for all the other factors. Synonymous substitution rate is also negatively associated with body size, with a 6% variation explained by body size after controlling for the effects of temperature. Other factors are not associated with synonymous substitution rate after controlling for temperature. Overall, this study points to temperature as a strong predictor of the molecular evolution rate in the Eugongylinae subfamily, and demonstrates the power of large-scale exonic data to identify correlates of the rate of molecular evolution.

Museum Genomics.

Natural history collections are invaluable repositories of biological information that provide an unrivaled record of Earth's biodiversity. Museum genomics-genomics research using traditional museum and cryogenic collections and the infrastructure supporting these investigations-has particularly enhanced research in ecology and evolutionary biology, the study of extinct organisms, and the impact of anthropogenic activity on biodiversity. However, leveraging genomics in biological collections has exposed challenges, such as digitizing, integrating, and sharing collections data; updating practices to ensure broadly optimal data extraction from existing and new collections; and modernizing collections practices, infrastructure, and policies to ensure fair, sustainable, and genomically manifold uses of museum collections by increasingly diverse stakeholders. Museum genomics collections are poised to address these challenges and, with increasingly sensitive genomics approaches, will catalyze a future era of reproducibility, innovation, and insight made possible through integrating museum and genome sciences.

Predictors of phylogeographic structure among codistributed taxa across the complex Australian monsoonal tropics.

Differences in the geographic scale and depth of phylogeographic structure across codistributed taxa can reveal how microevolutionary processes such as population isolation and persistence drive diversification. In turn, environmental heterogeneity, species' traits, and historical biogeographic barriers may influence the potential for isolation and persistence. Using extensive SNP data and a combination of population genetic summary statistics and landscape genomic analyses, we explored predictors of the scale and depth of phylogeographic structure in codistributed lizard taxa from the topographically and climatically complex monsoonal tropics (AMT) of Australia. We first resolved intraspecific lineages and then tested whether genetic divergence across space within lineages is related to isolation by distance, resistance and/or environment and whether these factors differ across genera or between rock-related versus habitat generalist taxa. We then tested whether microevolutionary processes within lineages explain differences in the geographic scale and depth of intraspecific phylogeographic lineages. The results indicated that landscape predictors of phylogeographic structure differ between taxa. Within lineages, there was prevalent isolation by distance, but the strength of isolation by distance is independent of the taxonomic family, habitat specialization, and climate. Isolation by environment is the strongest predictor of landscape-scale genetic divergence for all taxa, with both temperature and precipitation acting as limiting factors. The strength of isolation by distance does not predict the geographic scale of the phylogeographic structure. However, more localized lineages had higher mean individual heterozygosity and less negative Tajima's D. This result implies that finer-scale phylogeographic structuring within species is associated with larger and more stable populations and, hence, persistence.

Museum genomics reveals the rapid decline and extinction of Australian rodents since European settlement.

Australia has the highest historically recorded rate of mammalian extinction in the world, with 34 terrestrial species declared extinct since European colonization in 1788. Among Australian mammals, rodents have been the most severely affected by these recent extinctions; however, given a sparse historical record, the scale and timing of their decline remain unresolved. Using museum specimens up to 184 y old, we generate genomic-scale data from across the entire assemblage of Australian hydromyine rodents (i.e., eight extinct species and their 42 living relatives). We reconstruct a phylogenomic tree for these species spanning ∼5.2 million years, revealing a cumulative total of 10 million years (>10%) of unique evolutionary history lost to extinction within the past ∼150 y. We find no evidence for reduced genetic diversity in extinct species just prior to or during decline, indicating that their extinction was extremely rapid. This suggests that populations of extinct Australian rodents were large prior to European colonization, and that genetic diversity does not necessarily protect species from catastrophic extinction. In addition, comparative analyses suggest that body size and biome interact to predict extinction and decline, with larger species more likely to go extinct. Finally, we taxonomically resurrect a species from extinction, Gould's mouse (Pseudomys gouldii Waterhouse, 1839), which survives as an island population in Shark Bay, Western Australia (currently classified as Pseudomys fieldi Waite, 1896). With unprecedented sampling across a radiation of extinct and living species, we unlock a previously inaccessible historical perspective on extinction in Australia. Our results highlight the capacity of collections-based research to inform conservation and management of persisting species.

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.