Migratory behavior and its genetic basis in willow warblers Phylloscopus trochilus

Right before northern hemisphere’s summer shifts to autumn small insect-eatingbirds start lengthy journeys to tropical regions. It is well established that temporarylack food and annual changes in weather are the ultimate reasons for this behavior.On a proximal level however, the process is poorly understood. Yet crosscontinental bird migration is a widespread phenomenon that has evolved severaltimes independently. Different species execute specific migration routes withremarkable precision, over narrow species-specific time windows. Even moreremarkable is that songbirds migrate alone thus relying only on internal cues. Routesand exact winter locations can vary substantially even between populations of onespecies. Crossbreeding experiments have proved that migration direction and timingare highly heritable. However, we are still clueless on which exact genes encodeinformation necessary for migration. I studied the willow warbler Phylloscopustrochilus, a common songbird that breeds across the whole of northern Eurasia andspends the non-breeding period exclusively in tropical Africa. The far east Siberiansubspecies P.t. yakutensis winters in south-east Africa and begin the journey byflying NW. Northern and Eastern European willow warblers P.t. acredula aremigrating towards southern Africa and start the migration by heading SSE. WesternEuropean and southern Scandinavian populations P.t. trochilus head towards WestAfrica and initiate fall migration by flying SSW. European trochilus and acredulaare nearly identical genetically except for two inversion polymorphisms onchromosomes 1 and 5, and presence or absence of a large repeat block (MARB-a).Far east Siberian yakutensis are genetically almost inseparable from Scandinavianacredula, except for a set of nearly fixed differences on a small region onchromosome 6. I deployed small tracking devices to record migratory routes ofwillow warblers from breeding sites in Sweden and eastern Russia andsupplemented the tracking results with molecular methods to search for genesassociated with the migratory behaviors

Migration direction in a songbird explained by two loci

Migratory routes and remote wintering quarters in birds are often species and even population specific. It has been known for decades that songbirds mainly migrate solitarily, and that the migration direction is genetically controlled. Yet, the underlying genetic mechanisms remain unknown. To investigate the genetic basis of migration direction, we track genotyped willow warblers Phylloscopus trochilus from a migratory divide in Sweden, where South-West migrating, and South-East migrating subspecies form a hybrid swarm. We find evidence that migration direction follows a dominant inheritance pattern with epistatic interaction between two loci explaining 74% of variation. Consequently, most hybrids migrate similarly to one of the parental subspecies, and therefore do not suffer from the cost of following an inferior, intermediate route. This has significant implications for understanding the selection processes that maintain narrow migratory divides

Genetics of bird migration : Study on East Siberian willow warblers (Phylloscopus trochilus)

Seasonal long-distance bird migration between wintering and breeding grounds is oneof the most remarkable phenomena in the history of life on earth. Migration strategies androutes vary greatly. Some birds migrate in social groups whilst others migrate alone at night,some cross few hundreds of km whilst others cover thousands of km. Avian migration has beenstudied extensively nevertheless numerous important questions remain unanswered. This studyaims to contribute to the understanding of the genetic basis of the innate migratory program ofa common songbird.From results of classical crossbreeding and orientation experiments with captiveblackcaps (Sylvia atricapilla) we can be sure that songbird migration directions as well asdurations are traits that are being inherited genetically and most likely have a multi-locusgenetic architecture. The chosen model species for my project is the willow warbler(Phylloscopus trochilus), one of the most common leaf warblers in the Palearctic. The willowwarbler has a continuous breeding distribution from the coast of the Atlantic to the coast ofPacific. They overwinter in sub-Saharan Africa. Three subspecies have been recognized: P. t.trochilus (breeding in central/western Europe and migrating SSW to western Africa), P. t.acredula (breeding in northern and eastern Europe, migrating SSE to east and south Africa)and P. t. yakutensis (breeding east of Ural Mountains, presumably migrating to SouthernAfrica). Morphological differences across the willow warbler subspecies are subtle and it has been previously shown that genome wide FST is close to zero. The low level of neutral back-ground divergence offers a good system for studying the genetics of passerine migration. This report contributes with novel data on phenotypes and genotypes of the subspecies yakutensisstudied at Chaun river delta, at the very eastern range limit of the species. As a proxy for thewintering location of yakutensis I used C and N stable isotope signatures from winter grownfeathers and inferred wintering range to be in Southern Africa. I genotyped 36 yakutensis fromChaun on four nuclear markers, of which three are located on the only divergent regions thatdiffers between the migratory phenotypes in Europe + CLOCK gene (a candidate for timing ofmigration). Analyzes revealed that yakutensis, despite strong differences in migration direction,distance, timing and wintering ground location cannot be separated from acredula genetically

Striking difference in response to expanding brood parasites by birds in western and eastern Beringia

Two species of obligate brood-parasitic Cuculus cuckoos are expanding their ranges in Beringia. Both now breed on the Asian side, close to the Bering Strait, and are found in Alaska during the breeding season. From May to July 2017, we used painted 3D-printed model eggs of two cuckoo host-races breeding in northeastern Siberia to test behavioral responses of native songbirds on both sides of the Bering Strait, with particular attention to species that are known cuckoo hosts in their Siberian range. Each host nest was tested after the second egg was laid and, if possible, again 4 days later with a model of a different type. Although our Siberian study site was also outside the known breeding ranges of the cuckoos, we found that Siberian birds had strong anti-parasite responses, with 14 of 22 models rejected. In contrast, birds in Alaska had virtually no detectable anti-parasite behaviors, with only one of 96 models rejected; the rejecters were Red-throated Pipits (Anthus cervinus). Such differences suggest that the cuckoos might successfully parasitize naïve hosts and become established in North America whether or not their historic host species are widely available

Diurnal migration patterns in willow warblers differ between the western and eastern flyways

It is a long-standing view that the main mechanism maintaining narrow migratory divides in passerines is the selection against intermediate and suboptimal migratory direction, but empirical proof of this is still lacking. We present novel results from a willow warbler migratory divide in central Sweden from where birds take the typical SW and SE as well as intermediate routes to winter quarters in Africa. We hypothesized that individuals that take the intermediate route are forced to migrate in daytime more often when crossing wide ecological barriers than birds that follow the typical western or eastern flyways. Analyses of geolocator tracks of willow warblers breeding across the entire Sweden, including the migratory divide, provided no support for our hypothesis. Instead, birds that migrated along the western flyway were the most likely to undertake full day flights. The probability of migrating for a full day when crossing major barriers declined linearly from west to east. We speculate that this difference is possibly caused by more challenging conditions in the western part of the Sahara Desert, such as the lack of suitable day-time roost sites. However, it may equally likely be that willow warblers benefit from migrating in daytime if favorable tailwinds offer assistance.</p

Geolocator tagging of east Siberian Bluethroats

The Bluethroat subspecies Cyanecula svecica svecia occurs throughout the northern Palearctic. European C. s. svecia has been shown to follow a route west of the Himalaya to winter quarters in southern Asia. Out of 30 Bluethroats tagged with geolocators in eastern Siberia, we obtained one track suggesting that it migrated east of the Himalaya to a wintering area located in Myanmar. The different routes of western and eastern C. s. svecia implicate the presence of a migratory divide in Siberia, either formed in situ during the post-glacial colonization process or resulting from a secondary contact between different refuge populations

Phenotypic and genetic characterization of the East Siberian Willow Warbler (Phylloscopus trochilus yakutensis Ticehurst, 1935) in relation to the European subspecies

Long-distance migrants with transcontinental breeding ranges are of particular interest for the study of local adaptation and geographic differentiation in birds. We compared phenotypes and genotypes between Far East Siberian Willow Warblers Phylloscopus trochilus yakutensis Ticehurst, 1935 with the European subspecies P. t. trochilus Linnaeus, 1758 and P. t. acredula Linnaeus, 1758. We found significant differences in mean body size and plumage colour, but intra-population variation overlapped extensively between the European and Siberian populations. We used stable isotope composition in winter-grown flight feathers as a proxy for wintering sites and found differences between all three subspecies, indicating different wintering grounds. Out of four nuclear loci analyzed (three of which are known to be substantially divergent between the European subspecies), none allowed to seperate East Siberian yakutensis from North Scandinavian acredula. Hence, neither phenotypic traits nor the currently available genetic resources provide diagnostic criteria for confidently assigning individual Willow Warblers to a particular subspecies. Despite extensive overlap in phenotypes and genotypes, we propose that the subspecies names can still be used as biogeographical references to the three Willow Warbler populations that differ in migration strategies. We propose to use yakutensis for Willow Warblers breeding east of the Ural Mountains that presumably initiate autumn migration towards the southwest or west, in contrast to the genetically most similar acredula that start autumn migration towards the southeast or south. Future field studies are needed to elucidate whether the longitudinal variation in phenotype is a cline, or whether a clear contact zone between these subspecies can be identified

Shrub-dwelling species are joining the Arctic passerine bird community in the Chaun Delta (Western Chukotka, Russia)

Avian communities play a pivotal role in Arctic ecosystems and birds have become the key model taxa for climate change research. Due to funding priorities, Arctic passerines have been studied less intensively than waterfowl and shorebirds. In our study, we aim to partly fill this gap and look at the change in passerine community species composition in the Chaun River Delta in Northeast Siberia (68.81° N, 170.62° E) between 1970–1980 and 2002–2019. We restricted our comparison to 16 tundra-dwelling species associated with grass and shrub tundra habitats. During the first period, 12 passerine species were reported and by the end of the last period, 14 species. Our observations show that four species of shrub-dwelling passerines, the Dusky Warbler (Phylloscopus fuscatus), two species of Turdus thrushes, and the Siberian Rubythroat (Calliope calliope), have joined the local community. Additionally, one Turdus thrush species increased in numbers. The only passerine species that used to be common in the 70’s and rare in the 2000s is the Lapland Bunting (Calcarius lapponicus). Yellow-breasted Bunting (Emberiza aureola, vagrant in 70’s) and Siberian Chiffchaff (Phylloscopus tristis, rare breeder in 70’s) have not been recorded during the most recent period. At the same time, there was no observed change in abundance for eight species of songbirds. The results of supervised satellite image classification did not detect any local-scale increase of shrub cover in our study site. However, a broad-scale assessment of vegetation change using NDVI suggests substantial greening or ‘shrubification’ across the region. We speculate that it promotes region-wide increases and range expansion of some shrub-dwelling species, recorded in our study

Autumn migration direction of juvenile willow warblers (Phylloscopus t. trochilus and P. t. acredula) and their hybrids assessed by qPCR SNP genotyping

Backgrounds: Geographic regions, where two closely related taxa with different migration routes come into contact, are known as migratory divides. Hybrids originating from migratory divides are hypothesized to migrate intermediately relative to the parental populations. Few studies have tested this hypothesis in wild birds, and only in hybrids that have completed the migration back to the breeding grounds. Here, we make use of the well-established migration routes of willow warblers (Phylloscopus trochilus), for which the subspecies trochilus and acredula have migration-associated genetic markers on chromosomes 1 and 5. The genetic approach enabled us to analyze the geographic distribution of juveniles during their first autumn migration, predicting that hybrids should be more frequent in the central flyway over Italy than along the typical SW routes of trochilus and SE routes of acredula. Methods: Blood and feather samples were collected from wintering birds in Africa (n = 69), and from juveniles during autumn migration in Portugal (n = 33), Italy (n = 38) and Bulgaria (n = 32). Genotyping was carried out by qPCR SNP assays, on one SNP each on chromosome 1 (SNP 65) and chromosome 5 (SNP 285). Both these SNPs have alternative alleles that are highly fixed (> 97%) in each of the subspecies. Results: The observed combined genotypes of the two SNPs were associated with the known migration routes and wintering distributions of trochilus and acredula, respectively. We found hybrids (HH) among the juveniles in Italy (5/38) and in Portugal (2/33). The proportion of hybrids in Italy was significantly higher than expected from a background rate of hybrid genotypes (1.5%) in allopatric populations of the subspecies. Conclusions: Our genetic approach to assign individuals to subspecies and hybrids allowed us to investigate migration direction in juvenile birds on their first migration, which should better reflect the innate migratory direction than studies restricted to successful migrants. The excess of hybrids in Italy, suggests that they employ an intermediate route relative to the parental populations. Our qPCR SNP genotyping method is efficient for processing large sample sizes, and will therefore be useful in migration research of species with known population genetic structure

Additional file 4 of Diurnal migration patterns in willow warblers differ between the western and eastern flyways

Additional file4: Maps (.pdf) depicting locations where all the recorded FDFs took place. Black dots show closest reliable locations before and after the FDF event. The width of the red polygon shows the limits of standard deviation in longitude during the exact day when FDF took plac