Abstract
Climate change is predicted to affect the reproductive ecology of wildlife; however, we have yet to understand if and how species can adapt to the rapid pace of change. Clock genes are functional genes likely critical for adaptation to shifting seasonal conditions through shifts in timing cues. Many of these genes contain coding trinucleotide repeats, which offer the potential for higher rates of change than single nucleotide polymorphisms (SNPs) at coding sites, and, thus, may translate to faster rates of adaptation in changing environments. We characterized repeats in 22 clock genes across all annotated mammal species and evaluated the potential for selection on repeat motifs in three clock genes (NR1D1,CLOCK, and PER1) in three congeneric species pairs with different latitudinal range limits: Canada lynx and bobcat (Lynx canadensis and L. rufus), northern and southern flying squirrels (Glaucomys sabrinus and G. volans), and white‐footed and deer mouse (Peromyscus leucopus and P. maniculatus). Signatures of positive selection were found in both the interspecific comparison of Canada lynx and bobcat, and intraspecific analyses in Canada lynx. Northern and southern flying squirrels showed differing frequencies at common CLOCK alleles and a signature of balancing selection. Regional excess homozygosity was found in the deer mouse at PER1 suggesting disruptive selection, and further analyses suggested balancing selection in the white‐footed mouse. These preliminary signatures of selection and the presence of trinucleotide repeats within many clock genes warrant further consideration of the importance of candidate gene motifs for adaptation to climate change.
Highlights
The rapid pace of climate change is expected to profoundly alter the future phenology, range distribution, and physiology of wildlife (Bellard, Berteksmeier, Leadley, Thuiller, & Courchamp, 2012), with impacts on reproduction being of particular importance (Milligan, Holt, & Lloyd, 2009)
Understanding how standing genetic variation and genomic elements operating at higher rates of change contribute to adaptability will be important to estimate the relative roles of genetics, plasticity, and epigenetics in defining the “response capacity” or “adaptive potential” of species
If clock genes are under selection in our study species, we expect to observe at least one of the following: clines in allele frequencies within or between species pairs, differentiation of allele frequencies between species pairs, departures from Hardy–Weinberg equilibrium (HWE), divergent patterns of differentiation (FST) between neutral microsatellites and each candidate Coding trinucleotide repeats (cTNRs), and/or identification of our cTNR loci as outliers in comparison with neutral genetic population structure
Summary
The rapid pace of climate change is expected to profoundly alter the future phenology, range distribution, and physiology of wildlife (Bellard, Berteksmeier, Leadley, Thuiller, & Courchamp, 2012), with impacts on reproduction being of particular importance (Milligan, Holt, & Lloyd, 2009). (Hazlerigg, Ebling, & Johnston, 2005), suggesting that cTNRs within these genes may play a role in seasonally fine-tuning the circadian characteristics of species inhabiting higher latitudes These results suggest that environmental factors correlated with latitude (e.g., photoperiod) may be driving selection at cTNRs within clock genes that are critical for the seasonal adaptation of life-history strategies. Their higher rates of mutation propose a mechanism for the convergence of pole-ward allele sizes following climate-induced range expansion This is highly relevant to mammals, as many closely related species have evolved in complex and often isolated refugium patterns north or south of ice sheets during the Pleistocene (e.g., Shafer, Cullingham, Côté, & Coltman, 2010), allowing for the evolution of allelic repeat motifs specific to differential climatic conditions within an otherwise presumably conserved gene sequence. If clock genes are under selection in our study species, we expect to observe at least one of the following: clines in allele frequencies within or between species pairs, differentiation of allele frequencies between species pairs, departures from Hardy–Weinberg equilibrium (HWE), divergent patterns of differentiation (FST) between neutral microsatellites and each candidate cTNR, and/or identification of our cTNR loci as outliers in comparison with neutral genetic population structure
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