A comparison of the association between large haplotype blocks under selection and the presence/absence of inversions.

Sangeet Lamichhaney,Leif Andersson

doi:10.1002/ece3.5094

Abstract

Inversions may contribute to ecological adaptation and phenotypic diversity, and with the advent of “second” and “third” generation sequencing technologies, the ability to detect inversion polymorphisms has been enhanced dramatically. A key molecular consequence of an inversion is the suppression of recombination allowing independent accumulation of genetic changes between alleles over time. This may lead to the development of divergent haplotype blocks maintained by balancing selection. Thus, divergent haplotype blocks are often considered as indicating the presence of an inversion. In this paper, we first review the features of a 7.7 Mb inversion causing the Rose‐comb phenotype in chicken, as a model for how inversions evolve and directly affect phenotypes. Second, we compare the genetic basis for alternative mating strategies in ruff and timing of reproduction in Atlantic herring, both associated with divergent haplotype blocks. Alternative male mating strategies in ruff are associated with a 4.5 Mb inversion that occurred about 4 million years ago. In fact, the ruff inversion shares some striking features with the Rose‐comb inversion such as disruption of a gene at one of the inversion breakpoints and generation of a new allele by recombination between the inverted and noninverted alleles. In contrast, inversions do not appear to be a major reason for the fairly large haplotype blocks (range 10–200 kb) associated with ecological adaptation in the herring. Thus, it is important to note that divergent haplotypes may also be maintained by natural selection in the absence of structural variation.

Highlights

An inversion represents the breakage of a chromosome at two points and reinsertion of the segment bound by the breakpoints in the reversed orientation (Sturtevant, 1921)
The 4.5 Mb inversion in ruff associated with alternate male mat‐ ing strategies is one of the several examples of “supergenes” maintained by inversions and associated with phenotypic poly‐ morphisms that has been reported in recent years
Other examples include a 400‐kb divergent chromosomal block controlling mim‐ icry in Heliconius butterfly (Joron et al, 2011), several megabase inversions showing genomic differentiation between migratory and nonmigratory ecotypes in Atlantic Cod (Berg et al, 2016; Kirubakaran et al, 2016; Sodeland et al, 2016) and a large inver‐ sion polymorphism (>100 MB) in white‐throated sparrow linked to variation in plumage, social behavior, and mate choice (Huynh, Maney, & Thomas, 2010)

Summary

| INTRODUCTION

An inversion represents the breakage of a chromosome at two points and reinsertion of the segment bound by the breakpoints in the reversed orientation (Sturtevant, 1921). An upregulated expression of this gene may explain the strikingly low levels of circulating tes‐ tosterone in Satellite and Faeder males (Kupper et al, 2015) This finding of how an ancestral chromosomal inversion can trigger an evolution of a large divergent haplotype (“supergene”) in ruff is consistent with recent findings in Heliconius (Jay et al, 2018) and Drosophila (Fuller, Leonard, Young, Schaeffer, & Phadnis, 2018). It is worth noting the striking similarities between the ruff and Rose‐comb inversions as regards gene inactivation at an inversion breakpoint and how new alleles with distinct phenotypes have emerged due to recombination between inverted and noninverted alleles. We have concluded that inversions are not a major reason for the presence of large haplotype blocks associated with ecological adaptation in Atlantic herring

| DISCUSSION

Findings

CONFLICT OF INTEREST