The role of copy-number variation in the reinforcement of sexual isolation between the two European subspecies of the house mouse

Abstract

Reinforcement has the potential to generate strong reproductive isolation through the evolution of barrier traits as a response to selection against maladaptive hybridization, but the genetic changes associated with this process remain largely unexplored. Building upon the increasing evidence for a role of structural variants in adaptation and speciation, we addressed the role of copy-number variation in the reinforcement of sexual isolation evidenced between the two European subspecies of the house mouse. We characterized copy-number divergence between populations of Mus musculus musculus that display assortative mate choice, and those that do not, using whole-genome resequencing data. Updating methods to detect deletions and tandem duplications (collectively: copy-number variants, CNVs) in Pool-Seq data, we developed an analytical pipeline dedicated to identifying genomic regions showing the expected pattern of copy-number displacement under a reinforcement scenario. This strategy allowed us to detect 1824 deletions and seven tandem duplications that showed extreme differences in frequency between behavioural classes across replicate comparisons. A subset of 480 deletions and four tandem duplications were specifically associated with the derived trait of assortative mate choice. These ‘Choosiness-associated’ CNVs occur in hundreds of genes. Consistent with our hypothesis, such genes included olfactory receptors potentially involved in the olfactory-based assortative mate choice in this system as well as one gene, Sp110 , that is known to show patterns of differential expression between behavioural classes in an organ used in mate choice—the vomeronasal organ. These results demonstrate that fine-scale structural changes are common and highly variable within species, despite being under-studied, and may be important targets of reinforcing selection in this system and others. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers

“…Progress will come from a combination of case studies of taxon pairs nearing complete isolation (see Stankowski et al [14], Yamasaki et al [15], Osborne et al [74] and North et al [29] in this theme issue), comparative approaches (e.g. de Vos et al [5] and Meyers et al [35] in this theme issue), theoretical studies highlighting what drives and hinders the evolution of strong RI (e.g.…”

“…The classical expectation is for postzygotic barriers (local adaptation or intrinsic incompatibility) to evolve first, followed by prezygotic barriers (in a trajectory where allopatric divergence is followed by secondary contact; see e.g. North et al [29] in this theme issue) but alternative scenarios have been proposed, as discussed e.g. by Coughlan & Matute [30] in this theme issue.…”

“…7. Reinforcement is a classical process in cases where some RI already exists, but it remains unclear how often, and how much it contributes to speciation (see North et al [29] in this theme issue). Does reinforcement complete RI following secondary contact?…”

“…Although the patterns of reinforcement are often observed at the phenotypic level, the genomic footprint of reinforcement is much less well understood and data are scarce [57,67] (box 1: Question 7). Focusing on copy-number variation detectable in paired-end sequencing data, North et al [29] test for the expected patterns of genomic divergence under a reinforcement scenario and show that these common, but understudied fine-scale structural variants make for strong candidate targets of reinforcing selection. While some 'adaptive coupling' processes have been well studied (especially classical reinforcement), others have not (box 1: Question 7).…”

Neurogenomic divergence during speciation by reinforcement of mating behaviors in chorus frogs (Pseudacris)

“…As predicted by theory [ 35 ], the evolution of reproductive isolation during reinforcement can result from structural changes at the genomic level [ 36 , 37 ]. Diverging species and populations are also likely to undergo differentiation of gene regulation pathways [ 38 , 39 ].…”