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.

Evidence for adaptive introgression of exons across a hybrid swarm in deer.

BACKGROUND: Secondary contact between closely related lineages can result in a variety of outcomes, including hybridization, depending upon the strength of reproductive barriers. By examining the extent to which different parts of the genome introgress, it is possible to infer the strength of selection and gain insight into the evolutionary trajectory of lineages. Following secondary contact approximately 8000 years ago in the Pacific Northwest, mule deer (Odocoileus hemionus hemionus) and black-tailed deer (O. h. columbianus) formed a hybrid swarm along the Cascade mountain range despite substantial differences in body size (up to two times) and habitat preference. In this study, we examined genetic population structure, extent of introgression, and selection pressures in freely interbreeding populations of mule deer and black-tailed deer using mitochondrial DNA sequences, 9 microsatellite loci, and 95 SNPs from protein-coding genes. RESULTS: We observed bi-directional hybridization and classified approximately one third of the 172 individuals as hybrids, almost all of which were beyond the F1 generation. High genetic differentiation between black-tailed deer and mule deer at protein-coding genes suggests that there is positive divergent selection, though selection on these loci is relatively weak. Contrary to predictions, there was not greater selection on protein-coding genes thought to be associated with immune function and mate choice. Geographic cline analyses were consistent across genetic markers, suggesting long-term stability (over hundreds of generations), and indicated that the center of the hybrid swarm is 20-30 km to the east of the Cascades ridgeline, where there is a steep ecological transition from wet, forested habitat to dry, scrub habitat. CONCLUSIONS: Our data are consistent with a genetic boundary between mule deer and black-tailed deer that is porous but maintained by many loci under weak selection having a substantial cumulative effect. The absence of clear reproductive barriers and the consistent centering of geographic clines at a sharp ecotone suggests that ecology is a driver of hybrid swarm dynamics. Adaptive introgression in this study (and others) promotes gene flow and provides valuable insight into selection strength on specific genes and the evolutionary trajectory of hybridizing taxa.

Phylogenetic evidence of historic mitochondrial introgression and cryptic diversity in the genus Pseudemoia (Squamata: Scincidae).

The Australian scincid genus Pseudemoia comprises six morphologically similar species restricted to temperate south-eastern Australia. Due to the high degree of morphological conservatism, phylogenetic relationships and taxonomic status within the Pseudemoia entrecasteauxii complex (comprising the nominal species P. entrecasteauxii, P. cryodroma, and P. pagenstecheri) remains unresolved. To further investigate the phylogenetic relationships and taxonomic status of Pseudemoia spp., and to test the hypothesis that P. cryodroma evolved from hybridization between P. entrecasteauxii and P. pagenstecheri, we sequenced one mitochondrial locus (ND4) and five nuclear loci (ß-globin, LGMN, PRLR, Rhodopsin, RPS8). While we find strong support for the monophyly of the P. entrecasteauxii complex, there exists marked incongruence between the mitochondrial and nuclear markers, particularly in regards to the high altitude specialist, P. cryodroma. The most parsimonious explanation of this discordance is historic mitochondrial introgression, although a hybrid origin for P. cryodroma cannot be completely rejected. Within P. pagenstecheri sensu lato, we identified a strongly supported, highly divergent yet morphologically cryptic lineage restricted to northern New South Wales. Although more weakly supported by the nuDNA, we also identified a second geographically distinct lineage of P. pagenstecheri s.l., which may warrant separate conservation management. Our study reveals a more complex evolutionary history of the genus Pseudemoia than previously appreciated and contributes to our understanding of the biogeography and evolution of Australian mesic zone fauna.

Selection and demography drive range-wide patterns of MHC-DRB variation in mule deer.

BACKGROUND: Standing genetic variation is important especially in immune response-related genes because of threats to wild populations like the emergence of novel pathogens. Genetic variation at the major histocompatibility complex (MHC), which is crucial in activating the adaptive immune response, is influenced by both natural selection and historical population demography, and their relative roles can be difficult to disentangle. To provide insight into the influences of natural selection and demography on MHC evolution in large populations, we analyzed geographic patterns of variation at the MHC class II DRB exon 2 locus in mule deer (Odocoileus hemionus) using sequence data collected across their entire broad range. RESULTS: We identified 31 new MHC-DRB alleles which were phylogenetically similar to other cervid MHC alleles, and one allele that was shared with white-tailed deer (Odocoileus virginianus). We found evidence for selection on the MHC including high dN/dS ratios, positive neutrality tests, deviations from Hardy-Weinberg Equilibrium (HWE) and a stronger pattern of isolation-by-distance (IBD) than expected under neutrality. Historical demography also shaped variation at the MHC, as indicated by similar spatial patterns of variation between MHC and microsatellite loci and a lack of association between genetic variation at either locus type and environmental variables. CONCLUSIONS: Our results show that both natural selection and historical demography are important drivers in the evolution of the MHC in mule deer and work together to shape functional variation and the evolution of the adaptive immune response in large, well-connected populations.

Identifying hybridization and admixture using SNPs: application of the DArTseq platform in phylogeographic research on vertebrates.

Next-generation sequencing (NGS) approaches are increasingly being used to generate multi-locus data for phylogeographic and evolutionary genetics research. We detail the applicability of a restriction enzyme-mediated genome complexity reduction approach with subsequent NGS (DArTseq) in vertebrate study systems at different evolutionary and geographical scales. We present two case studies using SNP data from the DArTseq molecular marker platform. First, we used DArTseq in a large phylogeographic study of the agamid lizard Ctenophorus caudicinctus, including 91 individuals and spanning the geographical range of this species across arid Australia. A low-density DArTseq assay resulted in 28 960 SNPs, with low density referring to a comparably reduced set of identified and sequenced markers as a cost-effective approach. Second, we applied this approach to an evolutionary genetics study of a classic frog hybrid zone (Litoria ewingii-Litoria paraewingi) across 93 individuals, which resulted in 48 117 and 67 060 SNPs for a low- and high-density assay, respectively. We provide a docker-based workflow to facilitate data preparation and analysis, then analyse SNP data using multiple methods including Bayesian model-based clustering and conditional likelihood approaches. Based on comparison of results from the DArTseq platform and traditional molecular approaches, we conclude that DArTseq can be used successfully in vertebrates and will be of particular interest to researchers working at the interface between population genetics and phylogenetics, exploring species boundaries, gene exchange and hybridization.