Signatures of selection in mammalian clock genes with coding trinucleotide repeats: Implications for studying the genomics of high‐pace adaptation

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.

Evolutionary Response to Climate Change in Migratory Pied Flycatchers

“…An evolutionary response could have taken several routes seen in other taxa: first, the local population could have experienced selection on existing variation. Selection could have changed allele frequencies of genes involved in circannual rhythms and photoperiodic pathways [23,44], or modified transgenerational epigenetic effects [43,45]. Second, the population could have experienced introgression by earlier-timed immigrants [7].…”

Parallel evolution of gene classes, but not genes: Evidence from Hawai'ian honeycreeper populations exposed to avian malaria

“…Many authors have dealt with repetitive regions by removing them from analyses because they impede our ability to detect genes of interest; however, eliminating them from analysis negates the possibility of finding genes with these motifs that are of actual importance (Zhuang, Yang, Fevolden, & Cheng, ). For instance, genes that are important in adaptation may have repeat motifs that influence protein binding or gene expression (Gemayel, Cho, Boeynaems, & Verstrepen, ; Kashi & King, ; Prentice et al., ). In several instances, we detected genes (primarily beta‐defensin) of potential importance in this system within repetitive regions.…”

Spatial and environmental influences on selection in a clock gene coding trinucleotide repeat in Canada lynx (Lynx canadensis)

“…The candidate gene cTNR amplified in this study is within the NR1D1 gene. Primer design, optimization and amplification of this marker was conducted in Prentice, Bowman, Lalor et al (2017). We used the existing data set of NR1D1 genotypes and genotyped bobcat individuals and additional lynx from New Brunswick, Cape Breton Island, and Newfoundland according to the same protocol.…”

“…Species inhabiting seasonal environments often respond to photoperiod cues via circadian clocks (Goldman, 2001), making clock genes good candidates for characterizing the potential genetic responses of species to shifting seasonal conditions and novel environments (Kondratova et al., 2010). cTNRs have been observed in a number of clock genes, and emerging studies have begun to demonstrate the evolutionary and adaptive importance of clock gene cTNRs in a range of species (Johnsen et al., 2007; Liedvogel et al., 2009; O’Malley et al., 2010; Prentice, Bowman, Lalor et al., 2017).…”

“…Most interestingly, the NR1D1 gene has demonstrated involvement in circadian regulation of food entrainment (Delezie et al., 2016), and cold tolerance (Gerhart‐Hines et al., 2013). The cTNR within the NR1D1 gene has been previously shown to exhibit signatures of positive selection in Canada lynx (Prentice, Bowman, Lalor et al., 2017). Lynx are a suitable species for investigating selection on clock genes because they show high gene flow at neutral genetic markers across their mainland range (Row et al., 2012), and thus, spatial patterns in NR1D1 are likely to be due to selection rather than neutral processes such as dispersal and gene flow.…”