Abstract
A common geographical pattern of genetic variation is the one-dimensional cline. Clines may be maintained by diversifying selection across a geographical gradient but can also reflect historical processes such as allopatry followed by secondary contact. To identify loci that may be undergoing diversifying selection, we examined the distribution of geographical variation patterns across the range of the killifish (Fundulus heteroclitus) in 310 loci, including microsatellites, allozymes, and single nucleotide polymorphisms. We employed two approaches to detect loci under strong diversifying selection. First, we developed an automated method to identify clinal variation on a per-locus basis and examined the distribution of clines to detect those that exhibited signifcantly steeper slopes. Second, we employed a classic -outlier method as a complementary approach. We also assessed performance of these techniques using simulations. Overall, latitudinal clines were detected in nearly half of all loci genotyped (i.e., all eight microsatellite loci, 12 of 16 allozyme loci and 44% of the 285 SNPs). With the exception of few outlier loci (notably mtDNA and malate dehydrogenase), the positions and slopes of Fundulus clines were statistically indistinguishable. The high frequency of latitudinal clines across the genome indicates that secondary contact plays a central role in the historical demography of this species. Our simulation results indicate that accurately detecting diversifying selection using genome scans is extremely difficult in species with a strong signal of secondary contact; neutral evolution under this history produces clines as steep as those expected under selection. Based on these results, we propose that demographic history can explain all clinal patterns observed in F. heteroclitus without invoking natural selection to either establish or maintain the pattern we observe today.
Highlights
Clinal variation is a common feature of terrestrial, freshwater [1,2] and marine species [3,4,5]
This study represents the first time that the relative contribution of neutral and non-neutral processes has been quantified in the classic genetic clines of the killifish Fundulus heteroclitus
This result raises real concern about the power of SNP genome scans to detect ‘loci that matter’ when a large portion of clines across the genome are generated by secondary contact
Summary
Clinal variation is a common feature of terrestrial, freshwater [1,2] and marine species [3,4,5]. This list includes Homo sapiens, whose geographic patterns of polymorphism are largely clinal [6]. Restricted dispersal can create seemingly adaptive clines at single loci [10], and historic geographic subdivision may establish clinal patterns that may persist for long periods of time [7,11] especially when population density or gene flow is low [12]
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