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’.
Highlights
The evolution of reproductive isolation is necessary to initiate speciation
The vast majority of Choosiness-associated deletions, and all Choosiness-associated divergent tandem duplications, were fixed in one behavioural class and absent in the other. This frequency of fixed differences was replicated when populations were compared within behavioural classes in the Control Test, demonstrating that a pattern of population structure is captured by copy-number variation
Given that (i) there is established evidence of selection against hybridization in this hybrid zone, [54,55,56] (ii) behavioural classes do not share more genetic variation than the populations compared, and (iii) the expected pattern of copy-number displacement was observed in candidate olfactory receptor (OR) genes, the CNVs identified here clearly represent loci of interest at which future analyses could formally test for natural selection as a consequence of reinforcement
Summary
The evolution of reproductive isolation is necessary to initiate speciation. if speciation is considered complete only when gene flow is totally or almost-totally inhibited, reproductive isolation must evolve but reach a sufficient strength (‘complete’ reproductive isolation) [1]. We detected CNVs significantly and consistently differentiated in allele frequency between Choosy and Non-Choosy populations using a combination of read depth, read-pair orientation and insert size information, adapting the approach developed by Schrider et al [76,77] to detect copy-number variation from pooled data. This approach (detailed in electronic supplementary materials, figures S1–S3) is limited to the identification of multinucleotide deletions and tandem duplications. Enriched annotation terms were those supported by a p-value < 0.01 after adjustment for multiple testing using the Benjamini–Hochberg procedure implemented in DAVID
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