Timing of molt of barn swallows is delayed in a rare<i>Clock</i>genotype

Saino, Nicola; Romano, Maria; Caprioli, Manuela; Fasola, Mauro; Lardelli, Roberto; Micheloni, Pierfrancesco; Scandolara, Chiara; Rubolini, Diego; Gianfranceschi, L.

doi:10.7717/peerj.17

Cited by 30 publications

(36 citation statements)

References 64 publications

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“…In addition, Clock genotype was found to be associated with the phenology of moult at the tropics (Saino et al . ): in the barn swallow, winter moult close to the Equator was delayed in individuals with a rare long Clock allele. Hence, Clock may indeed control photoperiodic responses also in Equatorial areas.…”

Section: Discussionmentioning

confidence: 99%

Polymorphism at the Clock gene predicts phenology of long‐distance migration in birds

et al. 2015

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Dissecting phenotypic variance in life history traits into its genetic and environmental components is at the focus of evolutionary studies and of pivotal importance to identify the mechanisms and predict the consequences of human-driven environmental change. The timing of recurrent life history events (phenology) is under strong selection, but the study of the genes that control potential environmental canalization in phenological traits is at its infancy. Candidate genes for circadian behaviour entrained by photoperiod have been screened as potential controllers of phenological variation of breeding and moult in birds, with inconsistent results. Despite photoperiodic control of migration is well established, no study has reported on migration phenology in relation to polymorphism at candidate genes in birds. We analysed variation in spring migration dates within four trans-Saharan migratory species (Luscinia megarhynchos; Ficedula hypoleuca; Anthus trivialis; Saxicola rubetra) at a Mediterranean island in relation to Clock and Adcyap1 polymorphism. Individuals with larger number of glutamine residues in the poly-Q region of Clock gene migrated significantly later in one or, respectively, two species depending on sex and whether the within-individual mean length or the length of the longer Clock allele was considered. The results hinted at dominance of the longer Clock allele. No significant evidence for migration date to covary with Adcyap1 polymorphism emerged. This is the first evidence that migration phenology is associated with Clock in birds. This finding is important for evolutionary studies of migration and sheds light on the mechanisms that drive bird phenological changes and population trends in response to climate change.

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Section: Discussionmentioning

confidence: 99%

Polymorphism at the Clock gene predicts phenology of long‐distance migration in birds

et al. 2015

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“…; Saino et al. , ; Bazzi et al. ; Bourret and Garant ), with individuals bearing “shorter” alleles (i.e., with fewer glutamine residues) showing advanced timing, while individuals bearing “longer” alleles showed a delayed phenology.…”

Section: Introductionmentioning

confidence: 98%

“…Within populations, Clock polymorphism may affect an individual's response to photoperiod. Intrapopulation variation in Clock allele size predicted timing of key lifehistory events of birds, such as reproduction, molt, and migration (Liedvogel et al 2009;Caprioli et al 2012;Saino et al 2013Saino et al , 2015Bazzi et al 2015;Bourret and Garant 2015), with individuals bearing "shorter" alleles (i.e., with fewer glutamine residues) showing advanced timing, while individuals bearing "longer" alleles showed a delayed phenology. Yet, other studies failed to find any association between Clock genotype and timing of phenophases (Liedvogel and Sheldon 2010;Dor et al 2011;Chakarov et al 2013;Morbey et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Adcyap1 polymorphism covaries with breeding latitude in a Nearctic migratory songbird, the Wilson's warbler (Cardellina pusilla)

Bazzi

Galimberti

Hays

et al. 2016

Ecology and Evolution

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Understanding the genetic background of complex behavioral traits, showing multigenic control and extensive environmental effects, is a challenging task. Among such traits, migration is known to show a large additive genetic component. Yet, the identification of specific genes or gene regions explaining phenotypic variance in migratory behavior has received less attention. Migration ultimately depends on seasonal cycles, and polymorphism at phenological candidate genes may underlie variation in timing of migration or other aspects of migratory behavior. In this study of a Nearctic-Neotropical migratory songbird, the Wilson's warbler (Cardellina pusilla), we investigated the association between polymorphism at two phenological candidate genes, Clock and Adcyap1, and two aspects of the migratory phenotype, timing of spring migration through a stopover site and inferred latitude of the breeding destination. The breeding destination of migrating individuals was identified using feather deuterium ratio (d 2 H), which reliably reflects breeding latitude throughout the species' western breeding range. Ninety-eight percent of the individuals were homozygous at Clock, and the rare heterozygotes did not deviate from homozygous migration phenology. Adcyap1 was highly polymorphic, and allele size was not significantly associated with migration date. However, Adcyap1 allele size significantly positively predicted the inferred breeding latitude of males but not of females. Moreover, we found a strong positive association between inferred breeding latitude and Adcyap1 allele size in long-distance migrating birds from the northern sector of the breeding range (western Canada), while this was not the case in short-distance migrating birds from the southern sector of the breeding range (coastal California). Our findings support previous evidence for a role of Adcyap1 in shaping the avian migratory phenotype, while highlighting that patterns of phenological candidate gene-phenotype associations may be complex, significantly varying between geographically distinct populations and even between the sexes.

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“…We cannot exclude the possibility that our results were affected by the small sample size relative to previous studies focused on the same genes, where significant patterns emerged only after the identification of rare genotypes (e.g. Caprioli et al ., ; Saino et al ., ). However, we note that our sampling was properly designed to catch the largest variability in the laying date.…”

Section: Discussionmentioning

confidence: 97%

“…Johnsen et al, 2007). Within-population polymorphism at the Clock poly-Q region has been observed to predict the schedule of crucial annual events, such as reproduction, incubation, moult and migration (Liedvogel et al, 2009;Caprioli et al, 2012;Saino et al, 2013Saino et al, , 2015Bazzi et al, 2015), with individuals bearing more glutamine residues showing a delayed phenology compared to those which possess 'shorter' alleles. However, other studies have failed to find any significant association between Clock allele size and timing of phenophases (Liedvogel & Sheldon, 2010;Dor et al, 2011;Chakarov et al, 2013;Kuhn et al, 2013;Peterson et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Circadian genes polymorphism and breeding phenology in a resident bird, the yellow‐legged gull

et al. 2017

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In species living in seasonally variable environments, the ability to synchronize the timing of breeding with the peak of critical resources is under positive selection within populations. The temporal scheduling of animal annual cycle is controlled by endogenous rhythms, which are set by ‘circadian clock’ genes. Many studies have supported the hypothesis that length polymorphism in some ‘phenological genes’ is associated with differences in the photoperiodic responses among individuals and populations. However, evidence is inconsistent across species, genes and phenological traits. Among birds, there is a dearth of knowledge concerning the gene‐phenotype association in non‐migratory species. To contribute filling this gap, here we analyzed clutch initiation date of females of a species resident at temperate latitudes, the yellow‐legged gull (Larus michahellis), in relation to the length polymorphism at four loci previously associated with breeding and migration phenology in other species: Adcyap1 and Npas2 genes, as well as two regions of the Clock gene. Although polymorphism was observed at three loci, allele size of the candidate genes seems not to predict the timing of breeding in females. In addition, similar genotype frequencies of all the analyzed genes were observed in early compared to late breeding females. Our results therefore suggest that the associations between photoperiodic candidate genes and breeding phenotype are not general across species and might represent adaptations of individual populations to the local environment.

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Timing of molt of barn swallows is delayed in a rareClockgenotype

Cited by 30 publications

References 64 publications

Polymorphism at the Clock gene predicts phenology of long‐distance migration in birds

Polymorphism at the Clock gene predicts phenology of long‐distance migration in birds

Adcyap1 polymorphism covaries with breeding latitude in a Nearctic migratory songbird, the Wilson's warbler (Cardellina pusilla)

Circadian genes polymorphism and breeding phenology in a resident bird, the yellow‐legged gull

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