A latitudinal cline in the Chinook salmon (Oncorhynchus tshawytscha) Clock gene: Evidence for selection on PolyQ length variants

Coastal Oregon Marine Experiment Station, Department of Fisheries and Wildlife, Hatfield Marine Science Center, Oregon State University, Newport, OR 97365, USA.
Proceedings of the Royal Society B: Biological Sciences (Impact Factor: 5.29). 09/2008; 275(1653):2813-21. DOI: 10.1098/rspb.2008.0524
Source: PubMed

ABSTRACT A critical seasonal event for anadromous Chinook salmon (Oncorhynchus tshawytscha) is the time at which adults migrate from the ocean to breed in freshwater. We investigated whether allelic variation at the circadian rhythm genes, OtsClock1a and OtsClock1b, underlies genetic control of migration timing among 42 populations in North America. We identified eight length variants of the functionally important polyglutamine repeat motif (PolyQ) of OtsClock1b while OtsClock1a PolyQ was highly conserved. We found evidence of a latitudinal cline in average allele length and frequency of the two most common OtsClock1b alleles. The shorter 335 bp allele increases in frequency with decreasing latitude while the longer 359 bp allele increases in frequency at higher latitudes. Comparison to 13 microsatellite loci showed that 335 and 359 bp deviate significantly from neutral expectations. Furthermore, a hierarchical gene diversity analysis based on OtsClock1b PolyQ variation revealed that run timing explains 40.9 per cent of the overall genetic variance among populations. By contrast, an analysis based on 13 microsatellite loci showed that run timing explains only 13.2 per cent of the overall genetic variance. Our findings suggest that length polymorphisms in OtsClock1b PolyQ may be maintained by selection and reflect an adaptation to ecological factors correlated with latitude, such as the seasonally changing day length.

  • Source
    • "), strongly suggests purifying selection arising from functional constraint (Hurst 2002). Comparative study of clock-gene variation across members of a biological community is an alternative to single species studies of local adaptation and geographic variation in seasonal timing (e.g., O'Malley and Banks 2008a "
    [Show abstract] [Hide abstract]
    ABSTRACT: Genetic determinants of seasonal reproduction are not fully understood but may be important predictors of organism responses to climate change. We used a comparative approach to study the evolution of seasonal timing within a fish community in a natural common garden setting. We tested the hypothesis that allelic length variation in the PolyQ domain of a circadian rhythm gene, Clock1a, corresponded to interspecific differences in seasonal reproductive timing across 5 native and 1 introduced cyprinid fishes (n = 425 individuals) that co-occur in the Rio Grande, NM, USA. Most common allele lengths were longer in native species that initiated reproduction earlier (Spearman's r = -0.70, P = 0.23). Clock1a allele length exhibited strong phylogenetic signal and earlier spawners were evolutionarily derived. Aside from length variation in Clock1a, all other amino acids were identical across native species, suggesting functional constraint over evolutionary time. Interestingly, the endangered Rio Grande silvery minnow (Hybognathus amarus) exhibited less allelic variation in Clock1a and observed heterozygosity was 2- to 6-fold lower than the 5 other (nonimperiled) species. Reduced genetic variation in this functionally important gene may impede this species' capacity to respond to ongoing environmental change.
    The Journal of heredity 02/2014; DOI:10.1093/jhered/esu008 · 1.97 Impact Factor
  • Source
    • "Importantly, genetic variation was extremely low in the polyQ repeat region of the Clock gene (OtsClock1b) and Cry2b (Fig. 3). The polyQ repeat region of Clock is related to migration timing in various taxa from fish (O'Malley and Banks 2008; O'Malley et al. 2010a) to birds (e.g. Liedvogel et al. 2009; Caprioli et al. 2012). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Though genetic diversity is necessary for population persistence in rapidly changing environments, little is known about how climate-warming influences patterns of intra-population genetic variation. For a pink salmon population experiencing increasing temperatures, we used temporal genetic data (microsatellite = 1993, 2001, 2009; allozyme = 1979, 1981, 1983) to quantify the genetic effective population size (Ne) and genetic divergence due to differences in migration timing and to estimate whether these quantities have changed over time. We predicted that temporal trends toward earlier migration timing and a corresponding loss of phenotypic variation would decrease genetic divergence based on migration timing and Ne. We observed significant genetic divergence based on migration timing and genetic heterogeneity between early- and late-migrating fish. There was also some evidence for divergent selection between early- and late-migrating fish at circadian rhythm genes, but results varied over time. Estimates of Ne from multiple methods were large (>1200) and Ne/Nc generally exceeded 0.2. Despite shifts in migration timing and loss of phenotypic variation, there was no evidence for changes in within-population genetic divergence or Ne over the course of this study. These results suggest that in instances of population stability, genetic diversity may be resistant to climate-induced changes in migration timing.
    Evolutionary Applications 07/2013; 6(5). DOI:10.1111/eva.12066 · 4.57 Impact Factor
  • Source
    • "Recent work in a blue tit population has demonstrated phenotypic correlates of variation in Clock genotype, showing females, but not males, with fewer poly-Q repeats at the variable Clock locus to breed earlier in the season (Liedvogel et al. 2009). The pattern found for within-population variation at the variable Clock locus in blue tits matches predictions derived from earlier results in birds, fish and insects, which revealed associations between Clock genotype and latitude across populations concordant with latitudinal variation in the timing of reproduction (Tauber and Kyriacou 2005, Johnsen et al. 2007, O'Malley and Banks 2008). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Studies of a range of taxa, including birds, have revealed latitudinal clines in allele length at the conserved Clock locus, a gene with known influences on behaviour and physiology. Such clines might reflect adaptation to seasonal variation, a suggestion supported by a recent within-population analysis of blue tits Cyanistes caeruleus, which found associations between Clock genotype and timing of breeding in females. To test the generality of this pattern, we sequenced the polymorphic poly-Q locus of the Clock gene in 521 female great tits Parus major, which were selected based on possession of extreme breeding phenotypes. In total, we identified five alleles with one allele accounting for 96% of allelic diversity in the sample set. Overall variability at the poly-Q locus was very low, and the spatial distribution of Clock alleles across Wytham was highly homogenous. Our data further provide no evidence for a connection between Clock genotype and reproductive timing phenotype in female great tits; further, we found no effect of Clock genotype on reproductive success. Hence, these results are in contrast to the pattern found for the sympatric blue tit population inhabiting the same woodlands, suggesting that phenotypic effects of Clock are not general in passerine birds.
    Journal of Avian Biology 08/2010; 41(5):543 - 550. DOI:10.1111/j.1600-048X.2010.05055.x · 2.24 Impact Factor
Show more