Shape based assignment tests suggest transgressive phenotypes in natural sculpin hybrids (Teleostei, Scorpaeniformes, Cottidae)

Abstract

Background: Hybridization receives attention because of the potential role that it may play in generating evolutionary novelty. An explanation for the emergence of novel phenotypes is given by transgressive segregation, which, if frequent, would imply an important evolutionary role for hybridization. This process is still rarely studied in natural populations as samples of recent hybrids and their parental populations are needed. Further, the detection of transgressive segregation requires phenotypes that can be easily quantified and analysed. We analyse variability in body shape of divergent populations of European sculpins (Cottus gobio complex) as well as natural hybrids among them.

Results: A distance-based method is developed to assign unknown specimens to known groups based on morphometric data. Apparently, body shape represents a highly informative set of characters that parallels the discriminatory power of microsatellite markers in our study system. Populations of sculpins are distinct and "unknown" specimens can be correctly assigned to their source population based on body shape. Recent hybrids are intermediate along the axes separating their parental groups but display additional differentiation that is unique and coupled with the hybrid genetic background.

Conclusion: There is a specific hybrid shape component in natural sculpin hybrids that can be best explained by transgressive segregation. This inference of how hybrids differ from their ancestors provides basic information for future evolutionary studies. Furthermore, our approach may serve to assign candidate specimens to their source populations based on morphometric data and help in the interpretation of population differentiation.

Figure 1

Differentiation of ancestral populations and hybrid intermediacy. Invasive sculpins separate from all stream sculpins along the first CV axis. Sculpin populations from Stream Broel and Stream Naaf separate along the second CV axis. BI hybrids form an intermediate group between their parental populations. Distance based assignment based on these two axes correctly identifies pure candidates while a majority of BI hybrids are wrongly assigned to one of the parental groups with which they overlap.

Figure 2

Extreme phenotypic values indicate a hybrid shape component. BI Hybrids are, on average, not intermediate along the third CV axis and may occupy extreme values relative to their parental populations. The parental populations as well as stream Naaf sculpins display little differentiation along the third CV axis. An inclusion of this hybrid specific shape component in distance based assignment increases the power to correctly identify hybrids more than two fold.

Figure 3

Landmark configuration and displacement vectors that distinguish groups of sculpins. Fourteen Landmarks were chosen to analyse variability in sculpin body shape (top). CVA was used to identify axes along which different groups can be discriminated based on the relative position of landmarks to a reference. The shape change captured by these axes can be visualized as relative displacement vectors for each landmark on a deformation grid. CV axis 1 separates invasive sculpins from all stream sculpins and axis 2 further separates two populations of stream sculpins. CV axis 3 captures the shape component that is unique to recent hybrids. While the deformation along CV axes 1 and 2 can be expressed in terms of inflation or compression of body parts, the hybrid specific shape change appears to be less balanced.