Abstract
Genetic variations in circadian clock genes may serve as molecular adaptations, allowing populations to adapt to local environments. Here, we carried out a survey of genetic variation in Drosophila cryptochrome (cry), the fly’s dedicated circadian photoreceptor. An initial screen of 10 European cry alleles revealed substantial variation, including seven non-synonymous changes. The SNP frequency spectra and the excessive linkage disequilibrium in this locus suggested that this variation is maintained by natural selection. We focused on a non-conservative SNP involving a leucine - histidine replacement (L232H) and found that this polymorphism is common, with both alleles at intermediate frequencies across 27 populations surveyed in Europe, irrespective of latitude. Remarkably, we were able to reproduce this natural observation in the laboratory using replicate population cages where the minor allele frequency was initially set to 10%. Within 20 generations, the two allelic variants converged to approximately equal frequencies. Further experiments using congenic strains, showed that this SNP has a phenotypic impact, with variants showing significantly different eclosion profiles. At the long term, these phase differences in eclosion may contribute to genetic differentiation among individuals, and shape the evolution of wild populations.
Highlights
The circadian clock consists of an evolutionarily conserved genetic network that drives the daily oscillations of a significant proportion of the transcriptome, in various organisms [1,2,3]
Of 10 natural cry alleles from various European wild populations (Table S1) revealed an extensive amount of genetic variation, including 21 silent single-nucleotide polymorphisms (SNPs) and 7 replacement SNPs, four of which mapped to the FAD binding domain of the protein (Fig. 1; Fig. S1)
L232H mapped to the protein surface, away from the FAD-binding domain of the protein, and unlikely to affect the redox status of the cofactor, which is thought to be important for the photoactivation of CRY [26,27]
Summary
The circadian clock consists of an evolutionarily conserved genetic network that drives the daily oscillations of a significant proportion of the transcriptome, in various organisms [1,2,3]. Wild populations in different environments are expected to show molecular adaptations of the clock to local conditions [5]. Because day-length and temperature change gradually along latitude, any allelic variation in clock genes that follows a latitudinal cline is a strong candidate for an adaptive polymorphism that is driven by natural selection. The threonineglycine repeat length polymorphism within the period gene of Drosophila melanogaster is a well-studied example of such a latitudinal cline in a clock gene [6]. This polymorphism is under balancing selection probably due to the different circadian temperature compensation properties that are determined by the various length alleles [5]
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