Abstract
Understanding how genes shape phenotypes is essential to assess the evolutionary potential of a trait. Identifying the genes underlying quantitative behavioral or life-history traits has, however, proven to be a major challenge. The majority of these traits are phenotypically plastic and different parts of the genome can be involved in shaping the trait under different environmental conditions. These variable genotype-phenotype associations could be one explanation for the limited success of genome-wide association studies in such traits. We here use avian seasonal timing of breeding, a trait that is highly plastic in response to spring temperature, to explore effects of such genotype-by-environment interactions in genome-wide association studies. We genotyped 2045 great tit females for 384081 single nucleotide polymorphisms (SNPs) and recorded their egg-laying dates in the wild. When testing for associations between SNPs and egg-laying dates, no SNP reached genome-wide significance. We then explored whether SNP effects were modified by annual spring temperature by formally testing for an interaction between SNP effect and temperature. The models including the SNP∗temperature interaction performed consistently better although no SNP reached genome-wide significance. Our results suggest that the effects of genes shaping seasonal timing depended on annual spring temperature. Such environment-dependent effects are expected for any phenotypically plastic trait. Taking these effects into account will thus improve the success of detecting genes involved in phenotypically plastic traits, thereby leading to a better understanding of their evolutionary potential.
Highlights
Environmental change, as, e.g., global warming, will inevitably lead to novel selection pressures, especially in phenological traits, as, for example, timing of breeding, migration or hibernation (Gienapp et al, 2014), and in the long run only adaptive microevolution (‘evolutionary rescue’) will enable population persistence (Bürger and Lynch, 1995; Visser, 2008; Gienapp et al, 2013; Gonzalez et al, 2013)
When we tested whether single nucleotide polymorphisms (SNPs) effects differed between cold, intermediate and warm springs, without fitting heterogeneous residuals, two SNPs reached genome-wide significance and one SNP was close to genome-wide significance (Supplementary Table S2)
Three SNPs that were among the 10 most significant SNPs were located within the thyroglobulin (TG) gene, the heparan sulfate-glucosamine 3-sulfotransferase 5 (HS3ST5) gene and the teneurin transmembrane protein 4 (TENM4) gene, respectively (Table 2)
Summary
Environmental change, as, e.g., global warming, will inevitably lead to novel selection pressures, especially in phenological traits, as, for example, timing of breeding, migration or hibernation (Gienapp et al, 2014), and in the long run only adaptive microevolution (‘evolutionary rescue’) will enable population persistence (Bürger and Lynch, 1995; Visser, 2008; Gienapp et al, 2013; Gonzalez et al, 2013). Understanding the genetics of traits that are affected by environmental change is important, as this will allow us to assess the adaptive potential of these traits. Heritability is, not necessarily constant across environments (Pigliucci, 2001, 2005; Nussey et al, 2007; Husby et al, 2011), which complicates predictions about evolutionary adaptation. This is especially true when environmental conditions will shift beyond the currently observed range due to climate change. In the end a better understanding of the genomics of the traits under selection will help us to predict whether they will be able to adapt fast enough to novel environmental conditions
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