An invasive lineage of sculpins, Cottus sp. (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups

Abstract

Fish abundance surveys in the Rhine system have shown in the past two decades that there is a rapid upriver invasion of a freshwater sculpin of the genus Cottus. These fish are found in habitats that are atypical for the known species Cottus gobio, which is confined to small cold streams within the Rhine drainage. Phylogeographic analysis based on mitochondrial haplotypes and diagnostic single nucleotide polymorphisms indicates that the invasive sculpins are hybrids between two old lineages from the River Scheldt drainage and the River Rhine drainage, although it is morphologically more similar to the Scheldt sculpins. Most importantly, however, the invasive population possesses a unique ecological potential that does not occur in either of the source populations from the Rhine or the Scheldt, which allows the colonization of new habitats that have previously been free of sculpins. Microsatellite analysis shows that the new lineage is genetically intermediate between the old lineages and that it forms a distinct genetic group across its whole expansion range. We conclude that hybridization between long separated groups has lead to the fast emergence of a new, adaptationally distinct sculpin lineage.

Figure 1

Colonization of rivers through invasive sculpins in the recent past. Data from regular fish abundance surveys in (a) the River Mosel and (b) the River Sieg are depicted for selected years. Open circles indicate the increasing range of invasive sculpins (as inferred from skin prickling) within main rivers, black circles represent the more or less static populations of non-prickled Rhine sculpins. The depicted length of the Mosel is approximately 200 km, the depicted length of the Sieg approx. 65 km, the double line depicts the Rhine.

Figure 2

Morphological and ecological analysis of sculpin samples. (a) Depiction of the five categories of spinelike scales covering the body (see §2) and (b) frequencies for all groups (size of circle represents frequencies found). (c) Differentiation in body shape among the three lineages. Each comprises a distinct cluster that separates along two CVA axes (axis 1: λ=0.13, χ²=941.6, df=48, p<0.01; axis 2: λ=0.62, χ²=215.3, df=23, p<0.01). (d) The shape change captured by the CVA axes plotted as vectors at 14 anatomical landmarks (depicted in upper panel) on deformation grids (middle panel: invasive sculpins vs Rhine sculpins; lower panel: invasive sculpins vs Scheldt sculpins). (e, f) Life history characters (age, fecundity, size) from reproducing females of Rhine sculpins (black circles), invasive sculpins (open circles) and Scheldt sculpins (black triangles).

Figure 3

Distribution of evolutionary lineages of sculpins around the River Rhine basin as inferred from a combined analysis of mt-haplotypes, nuclear SNPs and literature data. The numbers refer to the sampling sites of fish used in this study. Note that there are further populations of sculpins in the west, which represent different lineages but which are not relevant for this study and are therefore omitted for clarity. Several populations (marked yellow) in tributaries to the middle Rhine or River Main carry intogressed haplotypes of danubian origin but belong to the Rhine sculpin lineage according to nuclear data (see text).

Figure 4

Neighbour-joining trees of genetic distances (Nei's standard distance) among sculpin populations based on analysis of six microsatellite loci. (a) Tree based on six loci from 23 sampling sites and 14–48 individuals per site. The clustering is congruent with the combined SNP/haplotype inference as depicted in figure 3. Populations of stream sculpins are genetically more subdivided than invasive sculpins. (b) Tree based on 120 loci from five sampling sites and 12–48 individuals per site, representing the ancestral lineages and invasive sculpins. This shows that invasive sculpins are not particularly similar to either one of the presumed ancestral lineages on the genome level.