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. 2017 Sep;26(18):4712-4724.
doi: 10.1111/mec.14134. Epub 2017 Apr 28.

Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin

Stefan Dennenmoser  1   2 , Fritz J Sedlazeck  3 , Elzbieta Iwaszkiewicz  1 , Xiang-Yi Li  4 , Janine Altmüller  5 , Arne W Nolte  1   2
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Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin

Stefan Dennenmoser et al. Mol Ecol. 2017 Sep.

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.

Keywords: Cottidae; array-comparative genomic hybridization; digital droplet PCR; hybrid speciation; invasion genetics; structural mutations.

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Figures

Figure 1
Figure 1
Candidate copy‐number variations genes from aCGH analyses with significantly increased (a) and decreased (b) log2‐ratios in invasive Cottus (dark grey = invasive Cottus, light grey = C. perifretum, white = C. rhenanus)
Figure 2
Figure 2
Heatmap showing mapping results of genomic reads from 30 Cottus genomes against 1,005 repetitive elements. Colour‐coding represents the percentage of sum of reads (number of mapped reads per Mio reads) for each repetitive element. Coloured sidebars on the left indicate 208 repetitive elements with significantly higher numbers of mapped reads in invasive Cottus compared to the parental species (red), 12 elements with significantly lower numbers in invasive Cottus than in the parental species (orange), as well as repetitive elements that are significantly higher in C. rhenanus (light grey), and significantly lower in C. rhenanus (dark grey) compared to combined invasive Cottus and C. perifretum
Figure 3
Figure 3
Digital droplet PCR (ddPCR) validations of copy‐number variations candidates for three genes (a–c) and two repetitive elements (d, e). Box plots show copy‐number estimates for invasive Cottus (INV), C. perifretum (PER), C. rhenanus (RHEN) as well as two F2 offspring families from laboratory crosses between C. rhenanus and C. perifretum (BxWN = Bröl × Witte Nete; NxLB = Naaf × Larse Beek)
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