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Open Access Research article

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

Alan G Hudson123*, Pascal Vonlanthen12, Etienne Bezault124 and Ole Seehausen12

Author Affiliations

1 Division of Aquatic Ecology & Macroevolution, Institute of Ecology & Evolution, University of Bern, Baltzerstrasse 6, CH 3012 Bern, Switzerland

2 Department of Fish Ecology & Evolution, EAWAG Centre of Ecology, Evolution and Biogeochemistry, Seestrasse 79, CH 6047 Kastanienbaum, Switzerland

3 Department of Ecology & Environmental Science, Umeå University, SE 901 87 Umeå, Sweden

4 Department of Biology, Reed College, 3203 SE Woodstock Blvd, OR 97202 Portland, USA

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BMC Evolutionary Biology 2013, 13:108  doi:10.1186/1471-2148-13-108

Published: 30 May 2013

Abstract

Background

Speciation 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.

Results

Whilst 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.

Conclusions

Weakened 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.

Keywords:
Coregonus; Population genomics; Adaptive radiation; Speciation reversal; Relaxed selection; Heterogeneous genomic divergence; Ecological speciation; Speciation-with-gene-flow; Eutrophication; Divergence hitchhiking