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

Abstract

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.

Salmo macrostigma(Teleostei, Salmonidae): Nothing more than a brown trout (S. trutta) lineage?

“…Phylogenomic methods to delimit taxon boundaries are challenging but have greatly improved in the past few years. Such methods can distinguish between structure associated with intraspecific variation and introgression from that resulting from speciation (Baumsteiger et al ., ; Mutanen et al ., ; Wagner et al ., ; Zarza et al ., ) and sometimes allow for a deep taxonomic reassessment of evolutionary units in challenging taxa (Papakostas et al ., ), or even reconciliation of morphological and molecular taxonomies in integrative studies (Dejaco et al ., ; Morard et al ., ). The Salmo genus is certainly one interesting case to consider because large scale integrative taxonomic studies are currently lacking.…”

Avian introgression in the genomic era

“…We found five studies on avian introgression that adopted the D-statistic to study introgression patterns in Zimmerius flycatchers , Corvus crows (Poelstra et al 2014), Darwin's Finches (Lamichhaney et al 2015), Aphelocoma jays (Zarza et al 2016), and Passer sparrows (Elgvin et al 2017). Most studies applied the D-statistic in the appropriate way (i.e.…”

Consequences of divergence and introgression for speciation in Andean cloud forest birds

“…Modern analyses have revealed “hidden” genetic introgression even among populations assumed to have diverged in an allopatric model, such as populations of subtropical birds found in different mountain ranges (Zarza et al. ). However, the influence of introgression on the divergence of traits important to speciation, such as plumage signals in birds, has rarely been studied in a comparative framework.…”

“…Specifically, I test whether allospecies pairs with pronounced plumage divergence have “hidden” histories of introgression (Huang ; Zarza et al. ) or whether they have been entirely isolated for prolonged periods of time as suggested by Winger and Bates ().…”

“…Rather, I assume that geographic isolation has played some role in divergence, and test how subsequent introgression has influenced differentiation in plumage. Specifically, I test whether allospecies pairs with pronounced plumage divergence have "hidden" histories of intro-gression (Huang 2016;Zarza et al 2016) or whether they have been entirely isolated for prolonged periods of time as suggested by .…”