Speciation genomics and morphological evolution in an extraordinary avian radation, the Lonchura munias of New Guinea and Australia
Stryjewski, Katherine Faust
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Speciation, the evolution of morphologically, behaviorally and/or ecologically distinct lineages from a common ancestor, is the fundamental process generating biodiversity. The rapidly developing field of speciation genomics is challenging traditional views of speciation as a gradual, genome-wide process, and highlighting the role of divergent natural selection in the speciation process. This study investigates morphological evolution and the genomic architecture of speciation in a clade of 12 "munias" in the genus Lonchura, one of the most extraordinary cases of recent and rapid diversification in birds. With a diversity of plumage patterns and replicate examples of closely related species living in sympatry, this group is ideally suited for addressing fundamental questions about the genomics of speciation. In this study, I (1) test for evidence of character displacement between sympatric species using quantitative measurements of plumage coloration and morphology; (2) examine the structure of genome-wide variation using ddRAD-seq (double-digest Restriction Site Associated DNA sequencing); and (3) investigate the genomic structure of divergence using whole-genome sequencing. I find some evidence for character displacement, particularly in morphometrics and crown coloration. There is also a trend, however, for sympatric species to be more similar in coloration than allopatric species, particularly those that have come into contact more recently. Analysis of 7,043 ddRAD-seq loci reveals evidence of introgression among sympatric populations, with overall genomic variation corresponding more closely to geography than species identity. There is also substantial heterogeneity in genetic structure among mitochondrial, autosomal, and Z-linked markers. Finally, whole-genome sequencing reveals low overall genomic divergence while pinpointing "islands of differentiation" that exhibit elevated divergence between species. Two of these islands overlap genes known to be associated with coloration—Agouti signaling protein (ASIP) and Kit ligand (KITLG)—and allelic variation at these genes is associated with phenotypic traits. I also find evidence of a ~26 million base pair inversion on the Z chromosome, which groups the focal species differently than genome-wide variation. A strongly mosaic pattern of population structure among genomic regions supports a genic view of speciation, in which a small fraction of the genome is involved in the initial divergence of species.