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.

Length polymorphisms at two candidate genes explain variation of migratory behaviors in blackpoll warblers (Setophaga striata)

“…The results of our individual‐level analyses demonstrate the value of studies that reveal individual migratory phenotypes, for example, by using light‐level geolocators (McKinnon & Love, ). The combination of geolocator data with candidate gene analysis has been an important advancement in the study of migration (Bazzi et al, ; Contina et al, ; Saino et al, ). For example, in the study of barn swallows, individual‐level analyses revealed that rare Clock genotypes can have a significant impact on migratory phenology (Bazzi et al, ) and that degree of DNA methylation at the Clock gene can explain individual variation in migratory behavior (Saino et al, ).…”

“…The combination of geolocator data with candidate gene analysis has been an important advancement in the study of migration (Bazzi et al, ; Contina et al, ; Saino et al, ). For example, in the study of barn swallows, individual‐level analyses revealed that rare Clock genotypes can have a significant impact on migratory phenology (Bazzi et al, ) and that degree of DNA methylation at the Clock gene can explain individual variation in migratory behavior (Saino et al, ). Both of these insights would likely have been missed with analysis of population‐level genetic and migratory variation.…”

Timing as a sexually selected trait: the right mate at the right moment

“…For instance, in mammals the SCN plays a far more dominant role in both daily and seasonal processes than in birds (see molecular mechanisms above, figure 1), and thus selection on processes that affect the functioning of the SCN may have a larger impact on circadian phenotypes in mammals compared with birds. By contrast, sexual selection would be expected to act on between-individual variation in one sex in the timing of signal expression (see sexual selection section above), which may be more likely generated by clock-controlled genes (ccgs; see molecular mechanisms above) that mediate the clock output and/or modulate gene functioning, perhaps even in a tissue-specific manner [48]. The latter may also involve tissue-specific DNA methylation [49], which can have sexspecific phenotypic effects (see below).…”

“…Furthermore, the Clock genotype shows a weak relationship with individual variation in breeding time in blue tits, though only in females (and not in males, [113]). In barn swallows (Hirundo rustica), Clock gene diversity as well as clock gene methylation is linked with individual variation in breeding time [48,114]. Understanding whether clock genes and/or their methylation causally underlie these relationships that can be sex-dependent, and are present in some species but not others [115], clearly requires further work.…”

Two sides of a coin: ecological and chronobiological perspectives of timing in the wild

“…Another example are candidate genes for timing, identified by chronobiologists, whose sequences, expression patterns or epigenetic modification can be compared in wild animals that differ in timing (e.g. [16,210]). With these methods, animals in the wild can be characterized for their clock, and chronotype, plasticity and fitness can be assessed, rstb.royalsocietypublishing.org Phil.…”