Latitudinal cline in allele length provides evidence for selection in a circadian rhythm gene

Abstract

Divergent natural selection across a heterogeneous landscape can drive the evolution of locally adapted populations in which phenotypic variation is fine‐tuned to the environment. At the molecular level, such processes can be inferred by identifying correlations between genetic variation and environmental variables. We demonstrate that allele length and allele frequency at a regulatory circadian rhythm gene, OtsClock1b, are highly correlated (R2 = 0.86, P = 1.25 × 10−5) with latitude (a surrogate for photoperiod) in kokanee, the freshwater resident form of sockeye salmon (Oncorhynchus nerka). Two OtsClock1b alleles were identified that differed in length by seven amino acids, with the frequency of the shorter allele increasing from 50% in southern British Columbia (49°N) to complete fixation in Alaska (62°N). No such associations were detected for neutral microsatellite loci. In addition, a kokanee population sampled from Kamchatka, Russia (55°N) fits within the North American latitudinal cline, suggesting that this pattern may be convergent across large longitudinal spatial scales. This correlation provides evidence that natural selection rather than demographic processes may drive the distribution of genetic variation at OtsClock1b in kokanee. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 869–877.

Geographic Variation of Plant Circadian Clock Function in Natural and Agricultural Settings

“…In D. littoralis , the rate at which the circadian rhythm damps out and eclosion becomes arrhythmic increases with latitude (Pittendrigh et al, 1991). A latitudinal cline in allele-length at the OtsClock1b locus was found in kokanee salmon populations in both North America and Russia (Lemay and Russello, 2014). A study of 52 human populations revealed a significant correlation between single nucleotide polymorphisms in circadian-regulated genes and latitude-derived difference between maximum and minimum photoperiod; this suggests that, following migration out of Africa, humans adapted to different latitudes in part through adjustments to their circadian clocks (Forni et al, 2014).…”

Adcyap1 polymorphism covaries with breeding latitude in a Nearctic migratory songbird, the Wilson's warbler (Cardellina pusilla)

“…; O'Malley and Banks ; O'Malley et al. ; Lemay and Russello ) and probably reflects local adaptation to different photoperiodic regimes (Kyriacou et al. ).…”

“…Polymorphism at a Clock polyglutamine-rich region (Poly-Q) has been reported both among and within populations (e.g., Johnsen et al 2007;O'Malley and Banks 2008;Liedvogel et al 2009;Caprioli et al 2012), and it may play a role in determining phenological responses by differentially affecting the timing of seasonal activities (Hayasaka et al 2002). At the amongpopulation level, a latitudinal cline in Clock allele size, with the frequency of longer alleles increasing along a southnorth gradient, has been documented in some migratory bird and fish species (Johnsen et al 2007;O'Malley and Banks 2008;O'Malley et al 2010;Lemay and Russello 2014) and probably reflects local adaptation to different photoperiodic regimes (Kyriacou et al 2008). However, such a latitudinal cline has not been detected in other studies (e.g., Dor et al 2012;O'Brien et al 2013).…”

Time scale matters: genetic analysis does not support adaptation‐by‐time as the mechanism for adaptive seasonal declines in kokanee reproductive life span

“…Across a broad latitudinal range, genetic differences in OtsClock1b were found among populations of Chinook salmon, coho salmon ( O. kisutch ), pink salmon ( O. gorbuscha ), and chum salmon ( O. keta , O'Malley and Banks; O'Malley et al. ), as well as kokanee (Lemay and Russello ). Moreover, RLS have never been shown to differ between seasonal runs or to vary systematically with latitude.…”

“…We also predicted differentiation at circadian-linked loci, because of their role in the regulation of seasonal timing. In salmon, OtsClock1b is one of two duplicated clock genes, and length polymorphisms of the PolyQ domain are known to vary among populations with distinct reproductive timing at different scales (O’Malley et al 2007 , 2010 ; O’Malley and Banks 2008 ), including in kokanee (Lemay and Russello 2014 ).…”