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

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.     

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

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 (δ²H), 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.     

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

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.     

Time trees and clock genes: a systematic review and comparative analysis of contemporary avian migration genetics

Timing is a crucial aspect for survival and reproduction in seasonal environments leading to carefully scheduled annual programs of migration in many species. But what are the exact mechanisms through which birds (class: Aves) can keep track of time, anticipate seasonal changes, and adapt their behaviour? One proposed mechanism regulating annual behaviour is the circadian clock, controlled by a highly conserved set of genes, collectively called ‘clock genes’ which are well established in controlling the daily rhythmicity of physiology and behaviour. Due to diverse migration patterns observed within and among species, in a seemingly endogenously programmed manner, the field of migration genetics has sought and tested several candidate genes within the clock circuitry that may underlie the observed differences in breeding and migration behaviour. Among others, length polymorphisms within genes such as Clock and Adcyap1 have been hypothesised to play a putative role, although association and fitness studies in various species have yielded mixed results. To contextualise the existing body of data, here we conducted a systematic review of all published studies relating polymorphisms in clock genes to seasonality in a phylogenetically and taxonomically informed manner. This was complemented by a standardised comparative re-analysis of candidate gene polymorphisms of 76 bird species, of which 58 are migrants and 18 are residents, along with population genetics analyses for 40 species with available allele data. We tested genetic diversity estimates, used Mantel tests for spatial genetic analyses, and evaluated relationships between candidate gene allele length and population averages for geographic range (breeding- and non-breeding latitude), migration distance, timing of migration, taxonomic relationships, and divergence times. Our combined analysis provided evidence (i) of a putative association between Clock gene variation and autumn migration as well as a putative association between Adcyap1 gene variation and spring migration in migratory species; (ii) that these candidate genes are not diagnostic markers to distinguish migratory from sedentary birds; and (iii) of correlated variability in both genes with divergence time, potentially reflecting ancestrally inherited genotypes rather than contemporary changes driven by selection. These findings highlight a tentative association between these candidate genes and migration attributes as well as genetic constraints on evolutionary adaptation.     

Interactions between a Candidate Gene for Migration (ADCYAP1), Morphology and Sex Predict Spring Arrival in Blackcap Populations

Avian research has begun to reveal associations between candidate genes and migratory behaviors of captive birds, yet few studies utilize genotypic, morphometric, and phenological data from wild individuals. Previous studies have identified an association between ADCYAP1 polymorphism and autumn migratory behavior (restlessness, or zugunruhe), but little is known about the relationship between ADCYAP1 and spring migratory behavior. The timing of spring migration and arrival to the breeding ground are phenological traits which could be particularly favorable for establishing territories and acquiring mates, thus important to fitness and reproductive success. Here, we investigated how individual genotypic ADCYAP1 variation and phenotypic variation (wing length and shape) of blackcaps (Sylvia atricapilla) affect spring arrival date across nine natural populations in Europe. We hypothesized that longer alleles should be associated with earlier spring arrival dates and expected the effect on arrival date to be stronger for males as they arrive earlier. However, we found that longer wings were associated with earlier spring arrival to the breeding grounds for females, but not for males. Another female-specific effect indicated an interaction between ADCYAP1 allele size and wing pointedness on the response of spring arrival: greater allele size had a positive effect on spring arrival date for females with rounder wings, while a negative effect was apparent for females with more pointed wings. Also, female heterozygotes with pointed wing tips arrived significantly earlier than both homozygotes with pointed wings and heterozygotes with round wings. Stable isotope ratios (δ ² H) of a subset of blackcaps captured in Freiburg in 2011 allowed us also to assign individuals to their main overwintering areas in northwest (NW) and southwest (SW) Europe. NW males arrived significantly earlier to the Freiburg breeding site than both SW males and females in 2011. NW females had more pointed wing tips compared to SW females, but no difference in ADCYAP1 allele size was found between the different migration routes.     

Light‐level geolocation reveals wintering distribution,migration routes,and primary stopover locations of an endangered long‐distance migratory songbird

The importance of understanding the geographic distribution of the full annual cycle of migratory birds has been increasingly highlighted over the past several decades. However, the difficulty of tracking small birds between breeding and wintering areas has hindered progress in this area. To learn more about Kirtland's warbler Setophaga kirtlandii movement patterns throughout the annual cycle, we deployed archival light‐level geolocators across their breeding range in Michigan. We recovered devices from 27 males and analyzed light‐level data within a Bayesian framework. We found that most males wintered in the central Bahamas and exhibited a loop migration pattern. In both fall and spring, departure date was the strongest predictor of arrival date, but in spring, stopover duration and migration distance were also important. Though stopover strategies varied, males spent the majority of their spring migration at stopover sites, several of which were located just before or after large ecological barriers. We argue that loop migration is likely a response to seasonal variation in prevailing winds. By documenting a tight link between spring departure and arrival dates, we provide a plausible mechanism for previously documented carry‐over effects of winter rainfall on reproductive success in this species. The migratory periods remain the least understood periods for all birds, but by describing Kirtland's warbler migration routes and timing, and identifying locations of stopover sites, we have begun the process of better understanding the dynamics of their full annual cycle. Moreover, we have provided managers with valuable information on which to base future conservation and research priorities.     

Circannual variation in blood parasitism in a sub‐Saharan migrant passerine bird,the garden warbler

Knowing the natural dynamics of pathogens in migratory birds is important, for example, to understand the factors that influence the transport of pathogens to and their transmission in new geographical areas, whereas the transmission of other pathogens might be restricted to a specific area. We studied haemosporidian blood parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon in a migratory bird, the garden warbler Sylvia borin. Birds were sampled in spring, summer and early autumn at breeding grounds in Sweden, on migration at Capri, Italy and on arrival and departure from wintering staging areas in West Africa: mapping recoveries of garden warblers ringed in Fennoscandia and Capri showed that these sites are most probably on the migratory flyway of garden warblers breeding at Kvismaren. Overall, haemosporidian prevalence was 39%, involving 24 different parasite lineages. Prevalence varied significantly over the migratory cycle, with relatively high prevalence of blood parasites in the population on breeding grounds and at the onset of autumn migration, followed by marked declines in prevalence during migration both on spring and autumn passage. Importantly, we found that when examining circannual variation in the different lineages, significantly different prevalence profiles emerged both between and within genera. Our results suggest that differences in prevalence profiles are the result of either different parasite transmission strategies or coevolution between the host and the various parasite lineages. When separating parasites into common vs. rare lineages, we found that two peaks in the prevalence of rare parasites occur; on arrival at Swedish breeding grounds, and after the wintering period in Africa. Our results stress the importance of appropriate taxonomic resolution when examining host‐parasite interactions, as variation in prevalence both between and within parasite genera can show markedly different patterns.     

Crosswise migration by Yellow Warblers,Nearctic‐Neotropical passerine migrants

Yellow Warblers (Setophaga petechia) are abundant breeding birds in North America, but their migratory and non‐breeding biology remain poorly understood. Studies where genetic and isotopic techniques were used identified parallel migration systems and longitudinal segregation among eastern‐ and western‐breeding populations of Yellow Warblers in North America, but these techniques have low spatial resolution. During the 2015 breeding season, we tagged male Yellow Warblers breeding in Maine (N = 10) and Wisconsin (N = 10) with light‐level geolocators to elucidate fine‐scale migratory connectivity within the eastern haplotype of this species and determine fall migration timing, routes, and wintering locations. We recovered seven of 20 geolocators (35%), including four in Maine and three in Wisconsin. The mean duration of fall migration was 49 d with departure from breeding areas in late August and early September and arrival in wintering areas in mid‐October. Most individuals crossed the Gulf of Mexico to Central America before completing the final eastward leg of their migration to northern South America. Yellow Warblers breeding in Maine wintered in north‐central Colombia, west of those breeding in Wisconsin that wintered in Venezuela and the border region between Brazil, Colombia, and Venezuela. Our results provide an example of crosswise migration, where the more easterly breeding population wintered farther west than the more westerly breeding population (and vice versa), a seldom‐documented phenomenon in birds. Our results confirm earlier work demonstrating that the eastern haplotype of northern Yellow Warblers winters in northern South America, and provide novel information about migratory strategies, timing, and wintering locations of birds from two different populations.     

Central European Greylag Geese Anser anser show a shortening of migration distance and earlier spring arrival over 60 years

Global climate change can cause pronounced changes in species? migratory behaviour. Numerous recent studies have demonstrated climate‐driven changes in migration distance and spring arrival date in waterbirds, but detailed studies based on long‐term records of individual recapture or re‐sighting events are scarce. Using re‐sighting data from 430 marked individuals spanning a 60‐year period (winters 1956/1957 to 2015/2016), we assessed patterns in migration distance and spring arrival date, wintering‐site fidelity and survival in the increasing central European breeding population of Greylag Geese Anser anser. We demonstrate a long‐term decrease in migration distance, changes in the wintering range caused by winter partial short‐stopping, and the earlier arrival of geese on their breeding grounds. Greylag Geese marked on central Europe moulting grounds have not been recorded wintering in Spain since 1986 or in Tunisia and Algeria since 2004. The migration distance and spring arrival of geese indicated an effect of temperature at the breeding site and values of the NAO index. Greylag Geese migrate shorter distances and arrive earlier in milder winters. We suggest that shifts in the migratory behaviour of Central European Greylag Geese are individual temperature‐dependent decisions to take advantage of wintering grounds becoming more favourable closer to their breeding grounds, allowing birds to acquire breeding territories earlier.     

Distribution of genetic variation underlying adult migration timing in steelhead of the Columbia River basin

Fish migrations are energetically costly, especially when moving between freshwater and saltwater, but are a viable strategy for Pacific salmon and trout (Oncorhynchus spp.) due to the advantageous resources available at various life stages. Anadromous steelhead (O. mykiss) migrate vast distances and exhibit variation for adult migration phenotypes that have a genetic basis at candidate genes known as greb1L and rock1. We examined the distribution of genetic variation at 13 candidate markers spanning greb1L, intergenic, and rock1 regions versus 226 neutral markers for 113 populations (n = 9,471) of steelhead from inland and coastal lineages in the Columbia River. Patterns of population structure with neutral markers reflected genetic similarity by geographic region as demonstrated in previous studies, but candidate markers clustered populations by genetic variation associated with adult migration timing. Mature alleles for late migration had the highest frequency overall in steelhead populations throughout the Columbia River, with only 9 of 113 populations that had a higher frequency of premature alleles for early migration. While a single haplotype block was evident for the coastal lineage, we identified multiple haplotype blocks for the inland lineage. The inland lineage had one haplotype block that corresponded to candidate markers within the greb1L gene and immediately upstream in the intergenic region, and the second block only contained candidate markers from the intergenic region. Haplotype frequencies had similar patterns of geographic distribution as single markers, but there were distinct differences in frequency between the two haplotype blocks for the inland lineage. This may represent multiple recombination events that differed between lineages where phenotypic differences exist between freshwater entry versus arrival timing as indicated by Micheletti et al. (2018a). Redundancy analyses were used to model environmental effects on allelic frequencies of candidate markers, and significant variables were migration distance, temperature, isothermality, and annual precipitation. This study improves our understanding of the spatial distribution of genetic variation underlying adult migration timing in steelhead as well as associated environmental factors and has direct conservation and management implications.     

Potential for an Arctic‐breeding migratory bird to adjust spring migration phenology to Arctic amplification

Arctic amplification, the accelerated climate warming in the polar regions, is causing a more rapid advancement of the onset of spring in the Arctic than in temperate regions. Consequently, the arrival of many migratory birds in the Arctic is thought to become increasingly mismatched with the onset of local spring, consequently reducing individual fitness and potentially even population levels. We used a dynamic state variable model to study whether Arctic long‐distance migrants can advance their migratory schedules under climate warming scenarios which include Arctic amplification, and whether such an advancement is constrained by fuel accumulation or the ability to anticipate climatic changes. Our model predicts that barnacle geese Branta leucopsis suffer from considerably reduced reproductive success with increasing Arctic amplification through mistimed arrival, when they cannot anticipate a more rapid progress of Arctic spring from their wintering grounds. When geese are able to anticipate a more rapid progress of Arctic spring, they are predicted to advance their spring arrival under Arctic amplification up to 44 days without any reproductive costs in terms of optimal condition or timing of breeding. Negative effects of mistimed arrival on reproduction are predicted to be somewhat mitigated by increasing summer length under warming in the Arctic, as late arriving geese can still breed successfully. We conclude that adaptation to Arctic amplification may rather be constrained by the (un)predictability of changes in the Arctic spring than by the time available for fuel accumulation. Social migrants like geese tend to have a high behavioural plasticity regarding stopover site choice and migration schedule, giving them the potential to adapt to future climate changes on their flyway.     

Longer wings for faster springs – wing length relates to spring phenology in a long‐distance migrant across its range

In migratory birds, morphological adaptations for efficient migratory flight often oppose morphological adaptations for efficient behavior during resident periods. This includes adaptations in wing shape for either flying long distances or foraging in the vegetation and in climate‐driven variation of body size. In addition, the timing of migratory flights and particularly the timely arrival at local breeding sites is crucial because fitness prospects depend on site‐specific phenology. Thus, adaptations for efficient long‐distance flights might be also related to conditions at destination areas. For an obligatory long‐distance migrant, the common nightingale, we verified that wing length as the aerodynamically important trait, but not structural body size increased from the western to the eastern parts of the species range. In contrast with expectation from aerodynamic theory, however, wing length did not increase with increasing migration distances. Instead, wing length was associated with the phenology at breeding destinations, namely the speed of local spring green‐up. We argue that longer wings are beneficial for adjusting migration speed to local conditions for birds breeding in habitats with fast spring green‐up and thus short optimal arrival periods. We suggest that the speed of spring green‐up at breeding sites is a fundamental variable determining the timing of migration that fine tune phenotypes in migrants across their range.     

Population-specific adjustment of the annual cycle in a super-swift trans-Saharan migrant

For migratory birds optimal timing of the onset of reproduction is vital, especially when suitable conditions for reproduction occur only for a short while during the year. With increasing latitude the suitable period becomes shorter and we expect the organization of annual cycle to be more synchronized to the local conditions across individuals of same population. This should result in low variation of arrival and departure date in breeding sites at higher latitudes. We quantify the temporal and geographical variation in pre- and post-breeding migration between individuals from four different populations of alpine swifts Tachymarptis melba along a latitudinal gradient. We tracked 215 individuals in three years with geolocators. The two western and two eastern populations showed separate migratory flyways and places of residence in Africa. Length of stay at the breeding sites was negatively correlated with latitude and differed by more than a month between populations. Duration of migration was similarly short in all populations (median 6.2 days in autumn and 8.7 days in spring). However, variation in timing of migration was unrelated to latitude and individuals everywhere arrived in the same asynchrony at the breeding site.     

Candidate gene–environment interactions and their relationships with timing of breeding in a wild bird population

Monitoring and predicting evolutionary changes underlying current environmental modifications are complex challenges. Recent approaches to achieve these objectives include assessing the genetic variation and effects of candidate genes on traits indicating adaptive potential. In birds, for example, short tandem repeat polymorphism at four candidate genes (CLOCK, NPAS2, ADCYAP1, and CREB1) has been linked to variation in phenological traits such as laying date and timing of migration. However, our understanding of their importance as evolutionary predictors is still limited, mainly because the extent of genotype–environment interactions (GxE) related to these genes has yet to be assessed. Here, we studied a population of Tree swallow (Tachycineta bicolor) over 4 years in southern Québec (Canada) to assess the relationships between those four candidate genes and two phenological traits related to reproduction (laying date and incubation duration) and also determine the importance of GxE in this system. Our results showed that NPAS2 female genotypes were nonrandomly distributed across the study system and formed a longitudinal cline with longer genotypes located to the east. We observed relationships between length polymorphism at all candidate genes and laying date and/or incubation duration, and most of these relationships were affected by environmental variables (breeding density, latitude, or temperature). In particular, the positive relationships detected between laying date and both CLOCK and NPAS2 female genotypes were variable depending on breeding density. Our results suggest that all four candidate genes potentially affect timing of breeding in birds and that GxE are more prevalent and important than previously reported in this context.     

Does wintering north or south of the Sahara correlate with timing and breeding performance in black‐tailed godwits?

Migrating long distances requires time and energy, and may interact with an individual's performance during breeding. These seasonal interactions in migratory animals are best described in populations with disjunct nonbreeding distributions. The black‐tailed godwit (Limosa limosa limosa), which breeds in agricultural grasslands in Western Europe, has such a disjunct nonbreeding distribution: The majority spend the nonbreeding season in West Africa, while a growing number winters north of the Sahara on the Iberian Peninsula. To test whether crossing the Sahara has an effect on breeding season phenology and reproductive parameters, we examined differences in the timing of arrival, breeding habitat quality, lay date, egg volume, and daily nest survival among godwits (154 females and 157 males), individually marked in a breeding area in the Netherlands for which wintering destination was known on the basis of resightings. We also examined whether individual repeatability in arrival date differed between birds wintering north or south of the Sahara. Contrary to expectation, godwits wintering south of the Sahara arrived two days earlier and initiated their clutch six days earlier than godwits wintering north of the Sahara. Arrival date was equally repeatable for both groups, and egg volume larger in birds wintering north of the Sahara. Despite these differences, we found no association between wintering location and the quality of breeding habitat or nest survival. This suggests that the crossing of an important ecological barrier and doubling of the migration distance, twice a year, do not have clear negative reproductive consequences for some long‐distance migrants.     

Large-scale variation in the temporal patterns of the frass fall of defoliating caterpillars in oak woodlands in Britain: implications for nesting woodland birds

Capsule Frass fall was later and of longer duration in woods to the north and west of Britain compared with those in the southeast.

Aims Defoliating caterpillars are a major food resource for woodland breeding birds and our aims were to quantify large-scale patterns in the timing and duration of the spring peak in abundance of these caterpillars in oak woodlands in Britain.

Methods We deployed traps to collect caterpillar frass at regular intervals through spring in 19 oak woods distributed through England, Wales and Scotland. Models of the temporal patterns of the rate of frass fall were used to explore relationships with geographic variables and average local temperature.

Results The date of peak frass fall in 2010 ranged from 20 May to 18 June and was significantly related to altitude, latitude and local April–May temperature. The duration of the peak ranged from 20 to 53 days and was correlated with the date of the peak and April–May temperature. Limited data from 2008 and 2009 indicated considerable between-year variation in the date of the peak, which was consistent with the relationship with local temperature found in 2010.

Conclusions The date of peak frass fall was later and the duration of the peak longer in the north and west of Britain compared with the southeast which will have considerable implications for nesting woodland birds such as Pied Flycatchers. The date of the peak was well modelled by local April–May temperature offering the prospect of good predictive models. However, the duration of the peak was less well modelled by local temperature and may be determined by other factors.     

Connecting the dots: Stopover strategies of an intercontinental migratory songbird in the context of the annual cycle

The phases of the annual cycle for migratory species are inextricably linked. Yet, less than five percent of ecological studies examine seasonal interactions. In this study, we utilized stable hydrogen isotopes to geographically link individual black‐and‐white warblers (Mniotilta varia) captured during spring migration with breeding destinations to understand a migrant's stopover strategy in the context of other phases of the annual cycle. We found that stopover strategy is not only a function of a bird's current energetic state, but also the distance remaining to breeding destination and a bird's time‐schedule, which has previously been linked to habitat conditions experienced in the preceding phase of the annual cycle. Birds in close proximity to their breeding destination accumulate additional energy reserves prior to arrival on the breeding grounds, as reflected by higher migratory condition upon arrival, higher refueling rates measured via blood plasma metabolites, and longer stopover durations compared to birds migrating to breeding destinations farther from the stopover site. However, late birds near their breeding destination were more likely to depart on the day of arrival (i.e., transients), and among birds that stopped over at the site, the average duration of stopover was almost half the time of early conspecifics, suggesting late birds are trying to catch‐up with the overall time‐schedule of migration for optimal arrival time on the breeding grounds. In contrast, birds with long distances remaining to breeding destinations were more likely to depart on the day of arrival and primarily used stopover to rest before quickly resuming migration, adopting similar strategies regardless of a bird's time‐schedule. Our study demonstrates that migrants adjust their en route strategies in relation to their time‐schedule and distance remaining to their breeding destination, highlighting that strategies of migration should be examined in the context of other phases of the annual cycle.     

Low variability and absence of phenotypic correlates of Clock gene variation in a great tit Parus major population

Studies of a range of taxa, including birds, have revealed latitudinal clines in allele length at the conserved Clock locus, a gene with known influences on behaviour and physiology. Such clines might reflect adaptation to seasonal variation, a suggestion supported by a recent within‐population analysis of blue tits Cyanistes caeruleus, which found associations between Clock genotype and timing of breeding in females. To test the generality of this pattern, we sequenced the polymorphic poly‐Q locus of the Clock gene in 521 female great tits Parus major, which were selected based on possession of extreme breeding phenotypes. In total, we identified five alleles with one allele accounting for 96% of allelic diversity in the sample set. Overall variability at the poly‐Q locus was very low, and the spatial distribution of Clock alleles across Wytham was highly homogenous. Our data further provide no evidence for a connection between Clock genotype and reproductive timing phenotype in female great tits; further, we found no effect of Clock genotype on reproductive success. Hence, these results are in contrast to the pattern found for the sympatric blue tit population inhabiting the same woodlands, suggesting that phenotypic effects of Clock are not general in passerine birds.     

Local parasite lineage sharing in temperate grassland birds provides clues about potential origins of Galapagos avian Plasmodium

Oceanic archipelagos are vulnerable to natural introduction of parasites via migratory birds. Our aim was to characterize the geographic origins of two Plasmodium parasite lineages detected in the Galapagos Islands and in North American breeding bobolinks (Dolichonyx oryzivorus) that regularly stop in Galapagos during migration to their South American overwintering sites. We used samples from a grassland breeding bird assemblage in Nebraska, United States, and parasite DNA sequences from the Galapagos Islands, Ecuador, to compare to global data in a DNA sequence registry. Homologous DNA sequences from parasites detected in bobolinks and more sedentary birds (e.g., brown‐headed cowbirds Molothrus ater, and other co‐occurring bird species resident on the North American breeding grounds) were compared to those recovered in previous studies from global sites. One parasite lineage that matched between Galapagos birds and the migratory bobolink, Plasmodium lineage B, was the most common lineage detected in the global MalAvi database, matching 49 sequences from unique host/site combinations, 41 of which were of South American origin. We did not detect lineage B in brown‐headed cowbirds. The other Galapagos‐bobolink match, Plasmodium lineage C, was identical to two other sequences from birds sampled in California. We detected a close variant of lineage C in brown‐headed cowbirds. Taken together, this pattern suggests that bobolinks became infected with lineage B on the South American end of their migratory range, and with lineage C on the North American breeding grounds. Overall, we detected more parasite lineages in bobolinks than in cowbirds. Galapagos Plasmodium had similar host breadth compared to the non‐Galapagos haemosporidian lineages detected in bobolinks, brown‐headed cowbirds, and other grassland species. This study highlights the utility of global haemosporidian data in the context of migratory bird–parasite connectivity. It is possible that migratory bobolinks bring parasites to the Galapagos and that these parasites originate from different biogeographic regions representing both their breeding and overwintering sites.     

Intronic variation at the CHD1‐Z gene in Black‐tailed Godwits Limosa limosa limosa: correlations with fitness components revisited

Recently, Schroeder et al. (2010, Ibis 152: 368–377) suggested that intronic variation in the CHD1‐Z gene of Black‐tailed Godwits breeding in southwest Friesland, The Netherlands, correlated with fitness components. Here we re‐examine this surprising result using an expanded dataset (2088 birds sampled from 2004 to 2010 vs. 284 birds from 2004 to 2007). We find that the presence of the Z* allele (9% of the birds) is not associated with breeding habitat type, egg size, adult survival, adult body mass or adult body condition. The results presented here, when used in synergy with the previously reported results by Schroeder et al., suggest that there might be a tendency towards female adults with the Z* allele laying earlier clutches than adult females without the Z* allele. The occurrence of the Z* allele was also associated with a higher chick body mass and return rate. Chicks with the Z* allele that had hatched early in the breeding season were heavier at birth than chicks without the Z* allele and chicks with the Z* allele that had hatched late. Collectively, the results suggest that variation in the CHD1‐Z gene may indeed have arisen as a byproduct of selection acting on females during the egg fase and on chicks during the rearing stages of the reproductive cycle.