Clock Gene Variation Is Associated with Breeding Phenology and Maybe under Directional Selection in the Migratory Barn Swallow

Abstract

BackgroundIn diverse taxa, photoperiodic responses that cause seasonal physiological and behavioural shifts are controlled by genes, including the vertebrate Clock orthologues, that encode for circadian oscillator mechanisms. While the genetic network behind circadian rhythms is well described, relatively few reports exist of the phenological consequences of and selection on Clock genes in the wild. Here, we investigated variation in breeding phenology in relation to Clock genetic diversity in a long-distance migratory bird, the barn swallow (Hirundo rustica).Methodology/Principal FindingsIn a sample of 922 adult barn swallows from a single population breeding in Italy we found one very common (Q7) and three rare (Q5, Q6, Q8) length variants of a functionally significant polyglutamine repeat. Rare (2.9%) Q7/Q8 heterozygous females, but not males, bred significantly later than common (91.5%) Q7/Q7 females, consistent with the expectation that ‘long’ alleles cause late breeding, as observed in a resident population of another bird species. Because breeding date depends on arrival date from migration, present results suggest that the association between breeding date and Clock might be mediated by migration phenology. In addition, fecundity selection appears to be operating against Q7/Q8 because late migrating/breeding swallows have fewer clutches per season, and late breeding has additional negative selection effects via reduced offspring longevity. Genotype frequencies varied marginally non-significantly with age, as Q7/Q8 frequency showed a 4-fold reduction in old individuals. This result suggests negative viability selection against Q7/Q8, possibly mediated by costs of late breeding.Conclusions/SignificanceThis is the first study of migratory birds showing an association between breeding phenology and Clock genotype and suggesting that negative selection occurs on a phenologically deviant genotype. Low polymorphism at Clock may constrain microevolutionary phenological response to changing climate, and may thus contribute to the decline of barn swallow populations.

Annual rhythms that underlie phenology: biological time-keeping meets environmental change

“…An appealing candidate for phenological variation is the circadian gene clock (but see [74]). Recently, Liedvogel et al [75] and Caprioli et al [76] reported an association between polymorphism in clock and breeding phenology in birds.…”

Avian circadian organization: A chorus of clocks

“…However, these studies were conducted in free-living tits using radio frequency transponders under semi-natural conditions, not under DD or dimLL, so that these effects cannot distinguish circadian clock effects from light-induced effects or effects on homeostatic regulation of sleep. Other studies have focused on allelic differences in C-terminal polyglutamine repeats in the CLOCK protein in breeding and migratory patterns of barn swallows, Hirundo rustica , suggesting negative selection on “deviant” genotypes [27]. However, other studies in several different swallow species in the genus Tachycineta failed to show similar associations [42].…”

Circannual Transitions in Gene Expression

“…Variants in the circadian gene Clock have been implicated in the seasonal timing of breeding in barn swallows ( Hirundo rustica ) and are also predicted to be involved in migration (Caprioli et al, 2012). A microsatellite approach in European blackcaps ( Sylvia atricapilla ) found an association between migratory behavior and a microsatellite polymorphism within the 3′UTR of the ADCYAP1 gene locus (Mueller et al, 2011).…”