A region of the sex chromosome associated with population differences in diapause induction contains highly divergent alleles at clock genes

Abstract

Developmental plasticity describes the capacity of individuals with the same genotype to induce permanent change in a phenotype depending on a specific external input. One well‐studied example of adaptive developmental plasticity is the induction of facultative diapause in insects. Studies investigating the inheritance of diapause induction have suggested diverse genetic origins. However, only few studies have performed genome‐wide scans to identify genes affecting the induction decision. Here we compare two populations of the butterfly Pieris napi that differ in the propensity to enter diapause, and despite showing a low genome‐wide divergence, we identify a few genomic regions that show high divergence between populations. We then identified a single genomic region associated with diapause induction by genotyping diapausing and directly developing siblings from backcrosses of these populations. This region is located on the Z chromosome and contained three circadian clock genes, cycle, clock, and period. Additionally, period harbored the largest number of SNPs showing complete fixation between populations. We conclude that the heritable basis of between‐population variation in the plasticity that determines diapause induction resides on the Z chromosome, with the period gene being the prime candidate for the genetic basis of adaptive plasticity.

Moths passing in the night: Phenological and genomic divergences within a forest pest complex

“…Further, several of the Z-linked candidate loci were associated with antifreeze genes that may contribute to overwintering success. Sex chromosomes of other Lepidoptera have been found to house many adaptive loci associated with diapause (Fu et al, 2015;Pruisscher et al, 2018Pruisscher et al, , 2020, demonstrating their importance for rapid evolution of the trait. Indeed, diapause frequency is the only consistent phenotypic difference that separates C. o. biennis from other conifer-feeding Choristoneura.…”

Local adaptation of life cycles in a butterfly is associated with variation in several circadian clock genes

“…In total, only 12 outlier loci appeared to be located on the Z chromosome (Appendix : Table ). These included period , which is previously known to be Z‐linked in Lepidoptera (Pruisscher et al, 2020), but did not include any of the other loci showing a high F ST /low π signal. Hence, the results of the analyses did not appear to be primarily driven by sex‐linked variation.…”

“…Because sex-linked variation has been connected to diapause traits in other studies in Lepidoptera (Pruisscher et al, 2020), the combined set of outlier genes from the F ST /π and baypass (BF >20) analyses (n = 379) was tested for Z-linkage. Using blastp (Camacho et al, 2009), the amino acid sequences for the outlier gene models was cross-referenced against a database of all Z-chromosome gene sequences from a recent, chromosome-level assembly of the P. aegeria genome (Lohse et al, 2021 [version 1;awaiting peer review]).…”

“…Total = number of genes assigned a given GO term in the Pararge aegeria genome annotation; Outliers = number of genes assigned the same GO term in the outlier set; p = parent/child-adjusted Fisher p-value total, only 12 outlier loci appeared to be located on the Z chromosome (Appendix S1: Table S4). These included period, which is previously known to be Z-linked in Lepidoptera (Pruisscher et al, 2020), but did not include any of the other loci showing a high F ST /low π signal. Hence, the results of the analyses did not appear to be primarily driven by sex-linked variation.…”

Beyond genes-for-behaviour: the potential for genomics to resolve questions in avian brood parasitism

“…This could be done with association analyses, which measure the correlations between genotypes and either phenotypic traits (Genome-Wide Association Study, GWAS) or environmental variables (Gene-Environment Association, GEA, [119]). This could also be conducted using FST scans which identify genomic regions of high differentiation between populations from divergent environments or contrasting phenotypes [120]. We could also generate high-quality reference genomes and compare chromosome-level synteny across host species to identify e.g.…”