title: Clock gene variation is associated with breeding phenology and maybe under directional selection in the migratory barn swallow.
abstract: BACKGROUND
  In 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).
  
  
  RESULTS
  In a sample of 922 adult barn swallows from a single population breeding in Italy we found one very common (Q(7)) and three rare (Q(5), Q(6), Q(8)) length variants of a functionally significant polyglutamine repeat. Rare (2.9%) Q(7)/Q(8) heterozygous females, but not males, bred significantly later than common (91.5%) Q(7)/Q(7) 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 Q(7)/Q(8) 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 Q(7)/Q(8) frequency showed a 4-fold reduction in old individuals. This result suggests negative viability selection against Q(7)/Q(8), possibly mediated by costs of late breeding.
  
  
  CONCLUSIONS
  This 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.
authors.affiliation: Dipartimento di Biologia, Università degli Studi di Milano, Milano, Italy.
authors.forename: Manuela
authors.initials: M
authors.lastname: Caprioli
authors.forename: Roberto
authors.initials: R
authors.lastname: Ambrosini
authors.forename: Giuseppe
authors.initials: G
authors.lastname: Boncoraglio
authors.forename: Emanuele
authors.initials: E
authors.lastname: Gatti
authors.forename: Andrea
authors.initials: A
authors.lastname: Romano
authors.forename: Maria
authors.initials: M
authors.lastname: Romano
authors.forename: Diego
authors.initials: D
authors.lastname: Rubolini
authors.forename: Luca
authors.initials: L
authors.lastname: Gianfranceschi
authors.forename: Nicola
authors.initials: N
authors.lastname: Saino
mesh_terms: D025041:Animal Migration / Q000502:physiology*; D000818:Animals; D057906:Circadian Clocks / Q000235:genetics / Q000502:physiology*; D005260:Female; D005787:Gene Frequency; D053263:Gene Regulatory Networks; D014644:Genetic Variation; D005838:Genotype; D006579:Heterozygote; D007558:Italy; D008297:Male; D012098:Reproduction / Q000502:physiology*; D012621:Seasons; D046388:Swallows / Q000235:genetics / Q000502:physiology*