Abstract
Evolutionary dynamics of structural genetic variation in lineages of hybrid origin is not well explored, although structural mutations may increase in controlled hybrid crosses. We therefore tested whether structural variants accumulate in a fish of recent hybrid origin, invasive Cottus, relative to both parental species Cottus rhenanus and Cottus perifretum. Copy‐number variation in exons of 10,979 genes was assessed using comparative genome hybridization arrays. Twelve genes showed significantly higher copy numbers in invasive Cottus compared to both parents. This coincided with increased expression for three genes related to vision, detoxification and muscle development, suggesting possible gene dosage effects. Copy number increases of putative transposons were assessed by comparative mapping of genomic DNA reads against a de novo assembly of 1,005 repetitive elements. In contrast to exons, copy number increases of repetitive elements were common (20.7%) in invasive Cottus, whereas decrease was very rare (0.01%). Among the increased repetitive elements, 53.8% occurred at higher numbers in C. perifretum compared to C. rhenanus, while only 1.4% were more abundant in C. rhenanus. This implies a biased mutational process that amplifies genetic material from one ancestor. To assess the frequency of de novo mutations through hybridization, we screened 64 laboratory‐bred F2 offspring between the parental species for copy‐number changes at five candidate loci. We found no evidence for new structural variants, indicating that they are too rare to be detected given our sampling scheme. Instead, they must have accumulated over more generations than we observed in a controlled cross.
Highlights
Hybridization can be an important driver of evolutionary change and may lead to homoploid hybrid speciation of animals and plants (Abbott et al, 2013; Mallet, 2007; Nolte & Tautz, 2010; Schumer, Rosenthal, & Andolfatto, 2014)
Copy-number variation in natural populations can contribute to the raw material for evolutionary change
The occurrence of high-frequency gene duplicates with potentially adaptive gene dosage effects in invasive Cottus is in line with such a scenario but appears to be relatively rare in this study
Summary
Hybridization can be an important driver of evolutionary change and may lead to homoploid hybrid speciation of animals and plants (Abbott et al, 2013; Mallet, 2007; Nolte & Tautz, 2010; Schumer, Rosenthal, & Andolfatto, 2014). The expected number of gene and transposon copies in a lineage of hybrid origin should correspond with the average of the copy number in the parental species (e.g., Kawakami, Dhakal, Katterhenry, Heatherington, & Ungerer, 2011; Scavetta & Tautz, 2010). The underlying mutational mechanisms are known from controlled hybrid crosses (e.g., Garcıa Guerreiro, 2014; McClintock, 1984; Scavetta & Tautz, 2010), few empirical studies have documented the evolutionary dynamics of copy-number variation and transposition in natural admixed lineages. To further explore the possibility that hybridization causes rapid evolution of de novo structural variants, we tested laboratory-raised F2 (selfed F1) C. rhenanus 9 C. perifretum crosses for copy-number changes of candidate genes and transposons that have increased in copy number in natural populations of invasive Cottus. We searched for associations between changes in gene copy number and gene expression in invasive Cottus to explore possible contributions of CNVs to phenotypic change
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