Migration phenology and breeding success are predicted by methylation of a photoperiodic gene in the barn swallow

Abstract

Individuals often considerably differ in the timing of their life-cycle events, with major consequences for individual fitness, and, ultimately, for population dynamics. Phenological variation can arise from genetic effects but also from epigenetic modifications in DNA expression and translation. Here, we tested if CpG methylation at the poly-Q and 5'-UTR loci of the photoperiodic Clock gene predicted migration and breeding phenology of long-distance migratory barn swallows (Hirundo rustica) that were tracked year-round using light-level geolocators. Increasing methylation at Clock poly-Q was associated with earlier spring departure from the African wintering area, arrival date at the European breeding site, and breeding date. Higher methylation levels also predicted increased breeding success. Thus, we showed for the first time in any species that CpG methylation at a candidate gene may affect phenology and breeding performance. Methylation at Clock may be a candidate mechanism mediating phenological responses of migratory birds to ongoing climate change.

Figure 1

Phenological variation in departure date from the wintering area (a), arrival date at the breeding site (b), and breeding date (c) of male (full symbols) and female (open symbols) barn swallows in relation to methylation at the poly-Q locus. Linear regression lines for males (dashed) and females (continuous) are shown. Dates are expressed as Julian day (1 = 1 January). See Table 1 for sample sizes.

Figure 2. Seasonal breeding success of male (full symbols) and female (open symbols) barn swallows in relation to methylation at the poly-Q locus.

Linear regression lines for males (dashed) and females (continuous) are shown. See Table 2 for sample sizes.

Figure 3. Path diagram of the direct or the indirect effect of methylation at the poly-Q mediated by spring migration phenological variables and breeding date on breeding success for females and males.

Black numbers: path coefficients (i.e. the standard partial regression coefficient that estimates the strength of the relationship between each putative causative variable and the corresponding effect). Red numbers: products of the chains of path coefficients along all the paths connecting methylation at Clock poly-Q and seasonal breeding success; the sum of these products is used to compute the compound correlation between methylation at Clock poly-Q and seasonal breeding success (see Results). Blue numbers: simple correlation coefficients between pairs of variables. Underlining of correlation coefficients indicates statistical significance (P < 0.05). See Tables 1 and 2 for sample sizes.