Genomic signatures of relaxed disruptive selection associated with speciation reversal in whitefish

Abstract

BackgroundSpeciation reversal: the erosion of species differentiation via an increase in introgressive hybridization due to the weakening of previously divergent selection regimes, is thought to be an important, yet poorly understood, driver of biodiversity loss. Our study system, the Alpine whitefish (Coregonus spp.) species complex is a classic example of a recent postglacial adaptive radiation: forming an array of endemic lake flocks, with the independent origination of similar ecotypes among flocks. However, many of the lakes of the Alpine radiation have been seriously impacted by anthropogenic nutrient enrichment, resulting in a collapse in neutral genetic and phenotypic differentiation within the most polluted lakes. Here we investigate the effects of eutrophication on the selective forces that have shaped this radiation, using population genomics. We studied eight sympatric species assemblages belonging to five independent parallel adaptive radiations, and one species pair in secondary contact. We used AFLP markers, and applied FST outlier (BayeScan, Dfdist) and logistic regression analyses (MatSAM), to identify candidate regions for disruptive selection in the genome and their associations with adaptive traits within each lake flock. The number of outlier and adaptive trait associated loci identified per lake were then regressed against two variables (historical phosphorus concentration and contemporary oxygen concentration) representing the strength of eutrophication.ResultsWhilst we identify disruptive selection candidate regions in all lake flocks, we find similar trends, across analysis methods, towards fewer disruptive selection candidate regions and fewer adaptive trait/candidate loci associations in the more polluted lakes.ConclusionsWeakened disruptive selection and a concomitant breakdown in reproductive isolating mechanisms in more polluted lakes has lead to increased gene flow between coexisting Alpine whitefish species. We hypothesize that the resulting higher rates of interspecific recombination reduce either the number or extent of genomic islands of divergence surrounding loci evolving under disruptive natural selection. This produces the negative trend seen in the number of selection candidate loci recovered during genome scans of whitefish species flocks, with increasing levels of anthropogenic eutrophication: as the likelihood decreases that AFLP restriction sites will fall within regions of heightened genomic divergence and therefore be classified as FST outlier loci. This study explores for the first time the potential effects of human-mediated relaxation of disruptive selection on heterogeneous genomic divergence between coexisting species.

Managing cryptic biodiversity: Fine‐scale intralacustrine speciation along a benthic gradient in Alpine whitefish (Coregonusspp.)

“…Alpine whitefish with lower gill‐raker densities, on the other hand, have been shown to be more efficient at foraging for large benthic prey items (Lundsgaard‐Hansen, Matthews, Vonlanthen, Taverna, & Seehausen, 2013). These predictable differences in feeding efficiency are suggestive of fitness trade‐offs in gill‐raker number between the respective niches of coexisting Alpine whitefish species, corroborated by genetic evidence that within‐lake patterns of gill‐raker count variation are driven by divergent natural selection regimes in the Alpine and other whitefish radiations (Hudson et al., 2013; Præbel et al., 2013; Rogers & Bernatchez, 2007; Vonlanthen et al., 2009). Whitefish growth rate is a complex physiological trait impinging on many other aspects of the overall phenotype such as body shape.…”

Does eutrophication-driven evolution change aquatic ecosystems?

“…Altered resource availability (e.g. decreased macroinvertebrates and increased zooplankton biomass) may have additionally influenced the relative survival of hybrids [52]. The spawning time of some sympatric whitefish species also shifted towards greater overlap in some lakes during the period of high nutrients [53].…”

“…Known ecologically relevant differences among species include body size, growth rate, diet and depth-habitat. Reproductive isolation among members of lake radiations is maintained by differences in spawning depth, spawning season, possibly mate choice ( [49,50]; B. Lundsgaard-Hansen 2012, unpublished data) and natural selection against intermediate phenotypes [51,52].…”

Potential merger of ancient lineages in a passerine bird discovered based on evidence from host‐specific ectoparasites

“…; Hudson et al. ). Isolated lineages in their original, stable environment are likely to remain disjunct without such disturbances.…”

“…Despite many documented instances of introgression between vertebrate taxa in secondary contact, examples of complete lineage mergers, as indicated by total genetic mixing, are rare. The only genetically documented examples of complete lineage mergers in vertebrates, to our knowledge, involve recently diverged lake fish or tanagers (e.g., Taylor et al 2006;Vonlanthen et al 2012;Hudson et al 2013;Kleindorfer et al 2014). Other likely instances of complete genetic mixing of previously isolated lineages also have been described but have not been analyzed using genetic data (Rhymer and Simberloff 1996;Seehausen et al 1997).…”