title: Clock gene polymorphism, migratory behaviour and geographic distribution: a comparative study of trans-Saharan migratory birds.
abstract: Migratory behaviour is controlled by endogenous circannual rhythms that are synchronized by external cues, such as photoperiod. Investigations on the genetic basis of circannual rhythmicity in vertebrates have highlighted that variation at candidate 'circadian clock' genes may play a major role in regulating photoperiodic responses and timing of life cycle events, such as reproduction and migration. In this comparative study of 23 trans-Saharan migratory bird species, we investigated the relationships between species-level genetic variation at two candidate genes, Clock and Adcyap1, and species' traits related to migration and geographic distribution, including timing of spring migration across the Mediterranean Sea, migration distance and breeding latitude. Consistently with previous evidence showing latitudinal clines in 'circadian clock' genotype frequencies, Clock allele size increased with breeding latitude across species. However, early- and late-migrating species had similar Clock allele size. Species migrating over longer distances, showing delayed spring migration and smaller phenotypic variance in spring migration timing, had significantly reduced Clock (but not Adcyap1) gene diversity. Phylogenetic confirmatory path analysis suggested that migration date and distance were the most important variables directly affecting Clock gene diversity. Hence, our study supports the hypothesis that Clock allele size increases poleward as a consequence of adaptation to the photoperiodic regime of the breeding areas. Moreover, we show that long-distance migration is associated with lower Clock diversity, coherently with strong stabilizing selection acting on timing of life cycle events in long-distance migratory species, likely resulting from the time constraints imposed by late spring migration.
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, via Celoria 26, I-20133, Milan, Italy.
authors.forename: Gaia
authors.initials: G
authors.lastname: Bazzi
authors.affiliation: ISPRA - Istituto Superiore per la Protezione e la Ricerca Ambientale, via Cà Fornacetta 9, I-40064, Ozzano dell'Emilia (BO), Italy.
authors.forename: Jacopo G
authors.initials: JG
authors.lastname: Cecere
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, via Celoria 26, I-20133, Milan, Italy.
authors.forename: Manuela
authors.initials: M
authors.lastname: Caprioli
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, via Celoria 26, I-20133, Milan, Italy.
authors.forename: Emanuele
authors.initials: E
authors.lastname: Gatti
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, via Celoria 26, I-20133, Milan, Italy.
authors.forename: Luca
authors.initials: L
authors.lastname: Gianfranceschi
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, via Celoria 26, I-20133, Milan, Italy.
authors.forename: Stefano
authors.initials: S
authors.lastname: Podofillini
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, via Celoria 26, I-20133, Milan, Italy.
authors.forename: Cristina D
authors.initials: CD
authors.lastname: Possenti
authors.affiliation: Dipartimento di Scienze dell'Ambiente e della Terra (DISAT), Università degli Studi di Milano Bicocca, Piazza della Scienza 1, I-20126, Milan, Italy.
authors.forename: Roberto
authors.initials: R
authors.lastname: Ambrosini
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, via Celoria 26, I-20133, Milan, Italy.
authors.forename: Nicola
authors.initials: N
authors.lastname: Saino
authors.affiliation: ISPRA - Istituto Superiore per la Protezione e la Ricerca Ambientale, via Cà Fornacetta 9, I-40064, Ozzano dell'Emilia (BO), Italy.
authors.forename: Fernando
authors.initials: F
authors.lastname: Spina
authors.affiliation: Dipartimento di Bioscienze, Università degli Studi di Milano, via Celoria 26, I-20133, Milan, Italy.
authors.forename: Diego
authors.initials: D
authors.lastname: Rubolini
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics; D000352:Africa, Northern; D000483:Alleles; D025041:Animal Migration; D000818:Animals; D001717:Birds / Q000235:genetics* / Q000502:physiology; D056926:CLOCK Proteins / Q000235:genetics*; D005787:Gene Frequency; D008522:Mediterranean Sea; D010802:Phylogeny; D051219:Pituitary Adenylate Cyclase-Activating Polypeptide / Q000235:genetics; D012621:Seasons; D012641:Selection, Genetic
chemical_list: D051219:Pituitary Adenylate Cyclase-Activating Polypeptide; D056926:CLOCK Proteins
keywords: 
  Adcyap1
  ; breeding latitude; candidate genes; long-distance migration; phenology; phylogenetic path analysis