Chromosomal inversion differences correlate with range overlap in passerine birds

Abstract

Chromosomal inversions evolve frequently but the reasons for this remain unclear. We used cytological descriptions of 411 species of passerine birds to identify large pericentric inversion differences between species, based on the position of the centromere. Within 81 small clades comprising 284 of the species, we found 319 differences on the 9 largest autosomes combined, 56 on the Z chromosome, and 55 on the W chromosome. We also identified inversions present within 32 species. Using a new fossil-calibrated phylogeny, we examined the phylogenetic, demographic and genomic context in which these inversions have evolved. The number of inversion differences between closely related species is consistently predicted by whether the ranges of species overlap, even when time is controlled for as far as is possible. Fixation rates vary across the autosomes, but inversions are more likely to be fixed on the Z chromosome than the average autosome. Variable mutagenic input alone (estimated by chromosome size, map length, GC content or repeat density) cannot explain the differences between chromosomes in the number of inversions fixed. Together, these results support a model in which inversions increase because of their effects on recombination suppression in the face of hybridization. Other factors associated with hybridization may also contribute, including the possibility that inversions contain incompatibility alleles, making taxa less likely to collapse following secondary contact.

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Fig. 1: History of pericentric inversion evolution across greenfinches in the genus Chloris.
Fig. 2: Pericentric inversion fixation rate variation on the autosomes and Z chromosome combined across the Passeriformes.
Fig. 3: Pericentric inversion fixation rate within small clades and between sisters.

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Acknowledgements

We thank N. S. Bulatova, B. S. W. Chang, E. J. de Lucca, G. Semenov, P. Tang, I. M. Ventura, Y. Wu and the University of Chicago Library for their help in accessing cytological studies not available online; S. G. Dubay, K. Supriya and A. E. White for their assistance with statistical analyses and figure aesthetics; and A. Hipp, R. Hudson, M. Kronforst and M. Przeworski for their comments on the manuscript. Tissue materials for species without data on GenBank generously came from the Kansas University Biodiversity Institute and Natural History Museum (KU), the Field Museum of Natural History (FMNH) and the Australian National Wildlife Collection (ANWC). A. E. Johnson provided original artwork of the Chloris greenfinches used in Fig. 1.

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D.M.H. collected the data, ran the analyses and wrote the manuscript, all with input from T.D.P. Supported in part by an NSF Doctoral Dissertation Improvement Grant (DDIG1601323) to T.D.P. and D.M.H.

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Correspondence to Daniel M. Hooper.

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Hooper, D.M., Price, T.D. Chromosomal inversion differences correlate with range overlap in passerine birds. Nat Ecol Evol 1, 1526–1534 (2017). https://doi.org/10.1038/s41559-017-0284-6

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