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

Hudson, Alan G.; Vonlanthen, Pascal; Bezault, Etienne; Seehausen, Ole (2013). Genomic signatures of relaxed disruptive selection associated with speciation reversal in whitefish. BMC evolutionary biology, 13(1), p. 108. BioMed Central 10.1186/1471-2148-13-108

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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.

Item Type:

Journal Article (Original Article)

Division/Institute:

08 Faculty of Science > Department of Biology > Institute of Ecology and Evolution (IEE) > Aquatic Ecology
08 Faculty of Science > Department of Biology > Institute of Ecology and Evolution (IEE)

UniBE Contributor:

Hudson, Alan; Bezault, Etienne and Seehausen, Ole

Subjects:

500 Science > 570 Life sciences; biology

ISSN:

1471-2148

Publisher:

BioMed Central

Language:

English

Submitter:

Marcel Häsler

Date Deposited:

29 Apr 2014 10:52

Last Modified:

14 Dec 2014 13:28

Publisher DOI:

10.1186/1471-2148-13-108

BORIS DOI:

10.7892/boris.44857

URI:

https://boris.unibe.ch/id/eprint/44857

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