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.

Genome of an iconic Australian bird: High‐quality assembly and linkage map of the superb fairy‐wren (Malurus cyaneus)

“…This may be an artefact of the ability to detect syntenic blocks or variation in the rate of accumulating inversions along the different lineages. The Z chromosome was shown to have a higher number of inversions similar to other studies (Hooper & Price, , ) but only in the comparison using the 50‐kb syntenic block size. This difference between Z chromosome and autosomes is negligible with a conservative block size of 500 kb.…”

Mitonuclear Mate Choice: A Missing Component of Sexual Selection Theory?

“…They review evidence that inversions are frequently associated with both hybrid incompatibilities and mate preferences. In additionand consistent with the hypothesis that species recognition leads to selection for inversions and hence gene linkages -Hooper and Price [68] found that chromosomal inversions were more common in songbird species with sympatric congeners. Intriguingly in light of predictions of the mitonuclear mate choice, a disproportionate number of inversions in the songbird study were on the Z-chromosome.…”

“…Intriguingly in light of predictions of the mitonuclear mate choice, a disproportionate number of inversions in the songbird study were on the Z-chromosome. [68]…”

Chromosome Painting in Tyrant Flycatchers Confirms a Set of Inversions Shared by Oscines and Suboscines (Aves, Passeriformes)

“…As a matter of fact, a recent review has shown the occurrence of a large number of pericentric inversions in different orders of birds, highlighting their important effect on recombination suppression to justify their high occurrence [Hooper and Price, 2017]. Additionally, besides acting as a recombination suppressor, a pericentric inversion observed in the oscine white-throated sparrow ( Zonotrichia albicollis ) was associated with different behavioral patterns and phenotypic features [Thomas et al, 2008].…”