Department Fish Ecology and Evolution

Background: The European trout (Salmo trutta species complex) occurs across a very wide altitudinal range from lowland rivers to alpine streams. Historically, the major European river systems contained different, evolutionarily distinct trout lineages, and some of this genetic diversity has persisted in spite of extensive human-mediated translocations. We used AFLP-based genome scans to investigate the extent of potentially adaptive divergence among major drainages and along altitudinal gradients replicated in several rivers.
Results: The proportion of loci showing evidence of divergent selection was larger between drainages than along altitudinal transects within drainages. This suggests divergent selection is stronger between drainages, or adaptive divergence is constrained by gene flow among populations within drainages, although the latter could not be confirmed at a more local scale. Still, altitudinal divergence occurred and, at approximately 2% of the markers, parallel changes of the AFLP band frequencies with altitude were observed suggesting that altitude may well be an important source of divergent selection within rivers.
Conclusions: Our results indicate that adaptive genetic divergence is common both between major European river systems and along altitudinal gradients within drainages. Alpine trout appear to be a promising model system to investigate the relative roles of divergent selection and gene flow in promoting or preventing adaptation to climate gradients.

Species with a wide geographical distribution are often composed of distinct subgroups which may be adapted to their local environment. European trout (Salmo trutta species complex) provide an example of such a complex consisting of several genetically and ecologically distinct forms. However, trout populations are strongly influenced by human activities, and it is unclear to what extent neutral and adaptive genetic differences have persisted. We sampled 30 Swiss trout populations from heterogeneous environments along replicated altitudinal gradients in three major European drainages. More than 850 individuals were genotyped at 18 microsatellite loci which included loci diagnostic for evolutionary lineages and candidate markers associated with temperature tolerance, reproductive timing and immune defence. We find that the phylogeographic structure of Swiss trout populations has not been completely erased by stocking. Distinct genetic clusters corresponding to the different drainages could be identified, although nonindigenous alleles were clearly present, especially in the two Mediterranean drainages. We also still detected neutral genetic differentiation within rivers which was often associated with the geographical distance between populations. Five loci showed evidence of divergent selection between populations with several drainage-specific patterns. Lineage-diagnostic markers, a marker linked to a quantitative trait locus for upper temperature tolerance in other salmonids and a marker linked to the major histocompatibility class I gene were implicated in local adaptation and some patterns were associated with altitude. In contrast, tentative evidence suggests a signal of balancing selection at a second immune relevant gene (TAP2). Our results confirm the persistence of both neutral and potentially adaptive genetic differences between trout populations in the face of massive human-mediated dispersal.

Altitudinal gradients offer valuable study systems to investigate how adaptive genetic diversity is distributed within and between natural populations and which factors promote or prevent adaptive differentiation. The environmental clines along altitudinal gradients tend to be steep relative to the dispersal distance of many organisms, providing an opportunity to study the joint effects of divergent natural selection and gene flow. Temperature is one variable showing consistent altitudinal changes, and altitudinal gradients can therefore provide spatial surrogates for some of the changes anticipated under climate change. Here, we investigate the extent and patterns of adaptive divergence in animal populations along altitudinal gradients by surveying the literature for (i) studies on phenotypic variation assessed under common garden or reciprocal transplant designs and (ii) studies looking for signatures of divergent selection at the molecular level. Phenotypic data show that significant between-population differences are common and taxonomically widespread, involving traits such as mass, wing size, tolerance to thermal extremes and melanization. Several lines of evidence suggest that some of the observed differences are adaptively relevant, but rigorous tests of local adaptation or the link between specific phenotypes and fitness are sorely lacking. Evidence for a role of altitudinal adaptation also exists for a number of candidate genes, most prominently haemoglobin, and for anonymous molecular markers. Novel genomic approaches may provide valuable tools for studying adaptive diversity, also in species that are not amenable to experimentation.

Ecological speciation is defined as the emergence of reproductive isolation as a direct or indirect consequence of divergent ecological adaptation. Several empirical examples of ecological speciation have been reported in the literature which very often involve adaptation to biotic resources. In this review, we investigate whether adaptation to different thermal habitats could also promote speciation and try to assess the importance of such processes in nature. Our survey of the literature identified 16 animal and plant systems where divergent thermal adaptation may underlie (partial) reproductive isolation between populations or may allow the stable coexistence of sibling taxa. In many of the systems, the differentially adapted populations have a parapatric distribution along an environmental gradient. Isolation often involves extrinsic selection against locally maladapted parental or hybrid genotypes, and additional pre- or postzygotic barriers may be important. Together, the identified examples strongly suggest that divergent selection between thermal environments is often strong enough to maintain a bimodal genotype distribution upon secondary contact. What is less clear from the available data is whether it can also be strong enough to allow ecological speciation in the face of gene flow through reinforcement-like processes. It is possible that intrinsic features of thermal gradients or the genetic basis of thermal adaptation make such reinforcement-like processes unlikely but it is equally possible that pertinent systems are understudied. Overall, our literature survey highlights (once again) the dearth of studies that investigate similar incipient species along the continuum from initial divergence to full reproductive isolation and studies that investigate all possible reproductive barriers in a given system.