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.

Timing avian long-distance migration: from internal clock mechanisms to global flights

“…These studies give important leads to identifying the physiological organization of the timing of migration and the interactive roles of different physiological systems. Other studies have looked at genetic differentiation of populations that differed in migratory phenotype, such as the timing or direction of their journeys 27,169,170 . Several studies indicate evolutionary changes that are associated with the timing of migration 25,171 .…”

“…Several studies indicate evolutionary changes that are associated with the timing of migration 25,171 . It is now entirely feasible to combine tracking data with molecular information, such as differences in candidate genes that based on mechanistic studies in chronobiology are predicted to influence migratory timing, even if suspected links currently are still often tenuous 170 . A concurrent challenge, however, for efficient data-mining of bird tracking information, is development of sound theoretical frameworks within migration biology (e.g., 58,67,172 , and what the potential consequences of mismatches across annual cycle stages exist (but see, 75,79 for examples in birds, and 174,175 for examples in mammals).…”

The genetics and epigenetics of animal migration and orientation: birds, butterflies and beyond

“…In birds, migratory timing appears to be controlled in concert with timing of reproduction and moult by a circannual clock in both wild populations and caged birds (Gwinner, 2003;Visser et al, 2010). Correlative studies using a candidate gene approach identified the Clock gene as a possible candidate for migratory timing (Peterson et al, 2013;Bazzi et al, 2015Bazzi et al, , 2016Saino et al, 2017;Contina et al, 2018). The otherwise highly conserved Clock gene shows length variation at a poly-glutamine repeat, and shorter alleles have been associated with earlier arrival times at the breeding grounds in barn swallows (Bazzi et al, 2015).…”

Annual chronotypes functionally link life histories and life cycles in birds

“…Such a short circannual period is consistent with gonadal recrudescence starting in late autumn in house sparrows, perhaps an adaptation to high territorial competition in a sedentary bird (Hegner & Wingfield, ). In contrast, precise timing will be particularly important for long‐distance migrants, and especially extreme “long‐jump” migrants, of which Arctic‐breeding shorebirds are a typical example (Åkesson et al., ; Bazzi et al., ; Conklin, Senner, Battley, & Piersma, ; Helm, Gwinner, & Trost, ; Piersma, ). For these species, environmental cues at departure from equatorial or temperate wintering sites are uninformative of the phenological conditions at remote Arctic breeding grounds (Piersma et al., ; Winkler, Jørgensen, et al., ).…”