Abstract
Population differentiation can be driven in large part by natural selection, but selectively neutral evolution can play a prominent role in shaping patters of population divergence. The decomposition of the evolutionary history of populations into the relative effects of natural selection and selectively neutral evolution enables an understanding of the causes of population divergence and adaptation. In this study, we examined heterogeneous genomic divergence between alpine and lowland ecotypes of the allopolyploid plant, Anemone multifida. Using peak height and dominant AFLP data, we quantified population differentiation at non-outlier (neutral) and outlier loci to determine the potential contribution of natural selection and selectively neutral evolution to population divergence. We found 13 candidate loci, corresponding to 2.7% of loci, with signatures of divergent natural selection between alpine and lowland populations and between alpine populations (Fst = 0.074–0.445 at outlier loci), but neutral population differentiation was also evident between alpine populations (FST = 0.041–0.095 at neutral loci). By examining population structure at both neutral and outlier loci, we determined that the combined effects of selection and neutral evolution are associated with the divergence of alpine populations, which may be linked to extreme abiotic conditions and isolation between alpine sites. The presence of outlier levels of genetic variation in structured populations underscores the importance of separately analyzing neutral and outlier loci to infer the relative role of divergent natural selection and neutral evolution in population divergence.
Highlights
Population divergence and speciation have been driven in large part by the joint effects of neutral evolution and natural selection [1,2]
Amongst all alpine and lowland populations 13 loci (2.7%) were significant outliers amongst the dominant amplified fragment length polymorphism (AFLP) data, and nine were outliers (1.9%) based on peak height
Population divergence is in many cases caused by divergent natural selection in species that span different environments, but can be linked to or caused primarily by neutral evolution
Summary
Population divergence and speciation have been driven in large part by the joint effects of neutral evolution and natural selection [1,2]. Reductions in gene flow between populations due to divergent selection can enhance the impact of selectively neutral mechanisms of evolution (e.g. genetic drift), further accelerating differentiation between populations [6,7,8]. These isolating effects of adaptation can eventually lead to widespread genomic differentiation between populations or ecotypes, eventually leading to speciation [9,10,11,12]. Genetic drift can lead to the fixation or loss of alleles [21], while mutations are an important source of genetic diversity [22]
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