Clock gene polymorphism, migratory behaviour and geographic distribution: a comparative study of trans-Saharan migratory birds

• Published in: Molecular ecology 2016-12, Vol.25 (24), p.6077-6091
• Main Authors: Bazzi, Gaia, Cecere, Jacopo G., Caprioli, Manuela, Gatti, Emanuele, Gianfranceschi, Luca, Podofillini, Stefano, Possenti, Cristina D., Ambrosini, Roberto, Saino, Nicola, Spina, Fernando, Rubolini, Diego
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - genetics; Adcyap1; Africa, Northern; Alleles; Animal behavior; Animal Migration; Animals; Bird migration; Birds - genetics; Birds - physiology; breeding latitude; candidate genes; CLOCK Proteins - genetics; Gene Frequency; long-distance migration; Mediterranean Sea; phenology; phylogenetic path analysis; Phylogeny; Pituitary Adenylate Cyclase-Activating Polypeptide - genetics; Polymorphism; Population genetics; Seasons; Selection, Genetic
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/mec.13913

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.