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Mosaic genome evolution in a recent and rapid avian radiation

Abstract

Recent genomic analyses of evolutionary radiations suggest that ancestral or standing genetic variation may facilitate rapid diversification, particularly in cases involving convergence in ecological traits. Likewise, lateral transfer of alleles via hybridization may also facilitate adaptive convergence, but little is known about the role of ancestral variation in examples of explosive diversification that primarily involve the evolution of species recognition traits. Here, we show that genomic regions distinguishing sympatric species in an extraordinary radiation of small finches called munias (genus Lonchura) have phylogenetic histories that are discordant with each other, with the overall pattern of autosomal differentiation among species, and with sex-linked and mitochondrial components of the genome. Genome-wide data for 11 species sampled in Australia and Papua New Guinea indicate substantial autosomal introgression between sympatric species, but also identify a limited number of divergent autosomal regions, several of which overlap known colour genes (ASIPEDN3, IGSF11KITLG, MC1R and SOX10). Phylogenetic analysis of these outlier regions shows that different munia species have acquired unique combinations of alleles across a relatively small set of phenotypically relevant genes. Our results demonstrate that the recombination of ancestral genetic variation across multiple loci may be an important mechanism for generating phenotypic novelty and diversity.

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Acknowledgements

This research was supported by the National Geographic Society (8933-11), the National Science Foundation (DEB 1210810 and DEB 1446085) and by small grants from the American Ornithologists’ Union, American Museum of Natural History, American Society of Naturalists, Society for the Study of Evolution, Society of Systematic Biologists, Systematics Association and Linnean Society. The Departments of Environment and Conservation in Papua New Guinea and Western Australia provided permits for the fieldwork. We thank the Western Australian Museum and Commonwealth Scientific and Industrial Research Organisation for tissue loans. J. Robins at the National Research Institute facilitated our applications for permits and visas in Papua New Guinea. This work was conducted under Boston University’s Institutional Animal Care and Use Committee protocol number 10-011. We thank J. Berv, S. Billy, C. Kieswetter, J. Lewis, R. McKay, P. Saguba, T. Stryjewski and many others for assistance with fieldwork, and C. Balakrishnan, J. DaCosta, D. Irwin and C. Schneider for comments on the paper.

Author information

M.D.S. conceived the study. K.F.S., with limited assistance from M.D.S., completed the fieldwork, collected and prepared the specimens and collected all of the genomic data. The authors worked together on analysing the data and writing and approving the paper.

Competing interests

The authors declare no competing financial interests.

Correspondence to Katherine Faust Stryjewski or Michael D. Sorenson.

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Fig. 1: Geographic distributions and mtDNA phylogeny.
Fig. 2: Results of ddRAD-seq analyses.
Fig. 3: Co-ancestry matrix from fineRADstructure.
Fig. 4: Illustration of phylogenetic heterogeneity among genomic outlier regions.
Fig. 5: Mosaic distribution of alleles at outlier loci.