Museum genomics reveals the speciation history of Dendrortyx wood-partridges in the Mesoamerican highlands.

Natural history collections are increasingly valued as genomic resources. Their specimens reflect the combined efforts of collectors and curators over hundreds of years. For many rare or endangered species, specimens are the only readily available source of DNA. We leveraged specimens from a historical collection to study the evolutionary history of wood-partridges in the genus Dendrortyx. The three Dendrortyx species are found in the highlands of central Mexico and Central America south to Costa Rica. One of these species is endangered, and in general, Dendrortyx are secretive and poorly represented in tissue collections. We extracted DNA from historical museum specimens and sequenced ultraconserved elements (UCEs) and mitochondrial DNA (mtDNA) to assess their phylogeny and divergence times. Phylogenies built from hundreds to thousands of nuclear markers were well resolved and largely congruent with an mtDNA phylogeny. The divergence times revealed an unusually old avian divergence across the Isthmus of Tehuantepec in the Pliocene around 3.6 million years ago. Combined with other recent studies, our results challenge the general pattern that highland bird divergences in Mesoamerica are relatively young and influenced by the Pleistocene glacial cycles compared to the older divergences of reptiles and plants, which are thought to overlap more with periods of mountain formation. We also found evidence for monophyletic genetic lineages in mountain ranges within the widespread D. macroura, which should be investigated further with integrative taxonomic methods. Our study demonstrates the power of museum genomics to provide insight into the evolutionary histories of groups where modern samples are lacking.

Combining ultraconserved elements and mtDNA data to uncover lineage diversity in a Mexican highland frog (Sarcohyla; Hylidae).

Molecular studies have uncovered significant diversity in the Mexican Highlands, leading to the description of many new endemic species. DNA approaches to this kind of species discovery have included both mitochondrial DNA (mtDNA) sequencing and multilocus genomic methods. While these marker types have often been pitted against one another, there are benefits to deploying them together, as linked mtDNA data can provide the bridge between uncovering lineages through rigorous multilocus genomic analysis and identifying lineages through comparison to existing mtDNA databases. Here, we apply one class of multilocus genomic marker, ultraconserved elements (UCEs), and linked mtDNA data to a species complex of frogs (Sarcohyla bistincta, Hylidae) found in the Mexican Highlands. We generated data from 1,891 UCEs, which contained 1,742 informative SNPs for S. bistincta and closely related species and captured mitochondrial genomes for most samples. Genetic analyses based on both whole loci and SNPs agree there are six to seven distinct lineages within what is currently described as S. bistincta. Phylogenies from UCEs and mtDNA mostly agreed in their topologies, and the few differences suggested a more complex evolutionary history of the mtDNA marker. Our study demonstrates that the Mexican Highlands still hold substantial undescribed diversity, making their conservation a particularly urgent goal. The Trans-Mexican Volcanic Range stands out as a significant geographic feature in Sarcohyla and may have acted as a dispersal corridor for S. bistincta to spread to the north. Combining multilocus genomic data with linked mtDNA data is a useful approach for identifying potential new species and associating them with already described taxa, which will be especially important in groups with undescribed subadult phenotypes and cryptic species.

Hidden histories of gene flow in highland birds revealed with genomic markers.

Genomic studies are revealing that divergence and speciation are marked by gene flow, but it is not clear whether gene flow has played a prominent role during the generation of biodiversity in species-rich regions of the world where vicariance is assumed to be the principal mode by which new species form. We revisit a well-studied organismal system in the Mexican Highlands, Aphelocoma jays, to test for gene flow among Mexican sierras. Prior results from mitochondrial DNA (mtDNA) largely conformed to the standard model of allopatric divergence, although there was also evidence for more obscure histories of gene flow in a small sample of nuclear markers. We tested for these 'hidden histories' using genomic markers known as ultraconserved elements (UCEs) in concert with phylogenies, clustering algorithms and newer introgression tests specifically designed to detect ancient gene flow (e.g. ABBA/BABA tests). Results based on 4303 UCE loci and 2500 informative SNPs are consistent with varying degrees of gene flow among highland areas. In some cases, gene flow has been extensive and recent (although perhaps not ongoing today), whereas in other cases there is only a trace signature of ancient gene flow among species that diverged as long as 5 million years ago. These results show how a species complex thought to be a model for vicariance can reveal a more reticulate history when a broader portion of the genome is queried. As more organisms are studied with genomic data, we predict that speciation-with-bouts-of-gene-flow will turn out to be a common mode of speciation.