Genetics of Migration

11 Mar 2024, 15:00 → 14 Mar 2024, 12:55 Europe/Berlin

Lecture Hall (Max Planck Institute for Evolutionary Biology)

A symposium on the genetics of migration – integrating developments in behavioural genomics, evolutionary biology, bioinformatics and animal movement ecology to advance research in this field.

Confirmed keynote speakers are:

• Teresa Pegan, University of Michigan
  Comparative analysis of a species assemblage reveals effects of migratory strategy on population genetic patterns in North American boreal birds
• Jane Reid, Norwegian University of Science and Technology, Trondheim
  Keynote: Quantitative genetic approaches to predicting micro-evolutionary dynamics of migration in the wild
• Kazuhiro Wada, Hokkaido University, Sapporo
  Unraveling the neural and genetic basis of species-specific song learning: A comparative single-cell transcriptomic analysis in songbirds
• Kristina Brauburger, Lund University
  The Australian Bogong moth - an emerging model system to investigate highly directed long-distance migration
• Koosje Lamers, University of Groningen
  Migratory connectivity of pied flycatchers unravelled in a common garden experiment
• Gillian Durieux, Max Planck Institute of Evolutionary Biology
  The neurogenomics of avian migration
• Daria Shipilina, Uppsala University
  Genomics of butterfly migration: insights from the painted lady butterfly (Vanessa cardui)

Scientific Organisation: Miriam Liedvogel

 

 

Monday, 11 March

15:00 → 15:15 Welcome

Speaker: Miriam Liedvogel (Institute of Avian research)

15:15 → 16:00 Keynote: Kristina Brauburger

15:15 The Australian Bogong moth - an emerging model system to investigate highly directed long-distance migration

The Bogong moth is an iconic Australian insect species of significant cultural and ecological relevance and also a remarkable nocturnal migrator. Each spring freshly emerged Bogong moths escape the deadly high temperatures in their breeding grounds in southern Queensland and north-western New South Wales by embarking on a 1000 km journey to locate specific, cool, ridge-top caves in the Australian Alps where they spend the next months in a resting state called aestivation. After summer, the same individuals will return to their breeding grounds to mate, lay eggs and die. The next generation emerging in spring will then continue the migratory cycle. This yearly migration of naïve Bogong moths is an excellent phenomenon to tackle fundamental questions of nocturnal long-distance migration, which our group studies from behavioral, neurobiological and genetic angles.

Our behavioral work has revealed that Bogong moths use a combination of the Earth’s magnetic field, landmarks and the starry sky to orient during their migration. To illuminate how these cues are detected and translated into steering commands, we analyzed the sensory periphery (compound eyes and ocelli) and known navigational brain-centers. This included electrophysiological recordings from neurons processing starry sky cues, transcriptional profiling of brains, antenna and eyes comparing migratory and aestivating states, as well as identification and, ongoing, localization of light sensors, (opsins) and putative magneto-sensors (cryptochromes). The anatomical ground plan of the Bogong moth brain surprisingly lacks obvious specializations compared to non-migratory lepidopterans, prompting ongoing studies of neural circuits at synaptic resolution.

To investigate the genetic foundations of the Bogong moth’s migrations, we exploit two features of their life history. First, the moths need to pinpoint a limited set of caves, year after year, converging from widely spread breeding grounds. This results in flight directions that differ by up to 120º for moths starting their migration at the extremes of their breeding range. Each moth only migrates once, suggesting that the specific migratory heading is inherited. Second, the entire migratory journey is performed by a single generation of moths, providing a simpler system compared to the multigenerational migration of other well-studied insect migrants, like the Monarch butterfly or the oriental armyworm. To use these advantages, we sequenced and annotated a high-quality reference genome of the Bogong moth and carried out whole-genome resequencing across the geographic range of their breeding grounds and summer caves. While still preliminary, the data indicate that Bogong moths likely form a single panmictic population with low migratory connectivity. This apparent contradiction with an inherited migratory heading is the backdrop for further investigation into possible epigenetic determinates of migratory direction. The one-generation migratory system of the moths should enable us to raise and study migrants even in the lab. The establishment of a breeding facility as well as a CRISPR/Cas9 workflow on another moth species in Lund paves the way to exploit the Bogong moth as an ideal model to study the molecular and physiological mechanisms of compass sensing, as well as the genetic underpinnings of nocturnal long-distance insect migration.

Speaker: Kristina Brauburger (Lund University)

16:00 → 16:30 Flash Talks

16:30 → 18:15 Poster Session: Session 1

18:15 → 19:15 Finger Food Dinner

19:15 → 20:15 Poster Session: Session 2

Tuesday, 12 March

09:30 → 10:15 Keynote: Koosje Lamers

09:30 Migratory connectivity of pied flycatchers unravelled in a common garden experiment

Migrant birds have species- and population-specific routes linking their distant breeding and wintering grounds. They often show migratory connectivity: birds are not only more similarly timed as others from the same breeding population, but also winter closer together. Yet, it is unknown what determines these shared wintering sites, whilst they are vital to understand migrants’ adaptive capacity. Here, we present a unique tracking study in pied flycatchers (Ficedula hypoleuca), where we not only investigate natural wintering site variation across the breeding range, but also test its causality using an ambitious common garden experiment. Over the course of a five-year experiment, we translocated pied flycatcher females and eggs from the Netherlands to Sweden, hereby creating a free-living population of birds of Dutch, half-Dutch, and Swedish descent in our Swedish study population. By comparing the migratory journeys and destinations of birds from this natural experiment and the common garden experiment, we provide experimental evidence on whether genes and/or natal environment drive between-population variation in migratory timing and wintering sites.

Speaker: Koosje Lamers (University of Groningen)

10:15 → 10:55 Talks: Session 1

10:15 Causes and consequences of non-random gene flow in lake-stream stickleback

Marius Roesti, Nicole Nesvadba, Thor Veen, Keila Stark, Jeffrey Groh, Daniel Bolnick, Yoel Stuart, Catherine L. Peichel

Adaptive population divergence is commonly ascribed to selection favoring different individuals in different habitats. In this case, random migration between habitats, and hence gene flow between populations, should counteract adaptive divergence. Yet, population divergence could also occur from different individuals selecting different habitats. In case of such individual habitat selection, gene flow between habitats may be non-random and could help maintain or even promote population divergence. In this project, we evaluate this overall idea by testing for the causes and consequences of habitat selection using a pair of directly adjacent but phenotypically distinct populations of lake and stream threespine stickleback. Using a mark-transplant-recapture experiment with wild-caught stickleback, we first show that habitat selection is phenotype-dependent. To test for a genetic basis of this habitat selection and to find traits and genomic regions associated with this habitat selection, we then gave laboratory-raised purebred stickleback (from lake-lake and stream-stream crosses) and lake-stream F2 hybrids the choice between the same natural lake and stream habitats. Purebred stickleback showed increased preference for the native habitat of their parents, indicating a genetic basis to habitat selection. In this talk, I will also present first results from phenotypic and genetic analyses of the 800 lake-stream F2 hybrids that either selected the lake or stream habitat. Furthermore, I will present results from a subsequent fitness enclosure experiment in which we asked whether the selection of a certain habitat by an individual is associated with increased fitness in that habitat.

Speaker: Marius Roesti

10:35 Ancestral winter quarters shape and constrain the evolution of long-distance migration

Staffan Bensch
Migration propensity in birds is evolutionary labile, with many examples of within-species migratoriness increasing or decreasing on the time scale of modern ornithology. In contrast, shifts in migration routes to more nearby wintering grounds seem to be a much slower process, resulting in what has been called “suboptimal migration routes”. We examined the evolutionary history of how some species of Palearctic migratory landbirds have expanded their wintering ranges to include both tropical Africa and Asia, a process that has involved major shifts of migration routes. We found that species with longer migration distances are less likely to colonise wintering grounds in both Africa and Asia. Instead, species with resident populations in the Palearctic have evolved wintering in both Africa and Asia more frequently. While it seems paradoxical that species most capable of extreme migrations are least likely to establish new wintering grounds, these findings indicate that drastic modifications to the genetic migration program are evolutionary difficult. Our analyses imply that major changes of wintering areas occur over long time scales, with the extent migration routes of many species traceable back at least to the last ice age. I will discuss the genetic and evolutionary implications of this apparent inertia, and how it can be understood in the light of few but prominent examples of fast changes of migration directions observed in ecological time.

Speaker: Staffan Bensch (Lund University)

10:55 → 11:30 Coffee Break

11:30 → 12:15 Keynote: Gillian Durieux

11:30 The neurogenomics of avian migration

The avian migratory phenotype is both spectacular and complex, encompassing a range of morphological, physiological, and behavioural traits such as pre-migratory fat storage, circannual rhythms, and sensory mechanisms for navigation. Many of these traits have a strong genetic basis, however the identity of the molecular mechanisms that underpin the migratory phenotype is still unknown. To address this, we contrast Eurasian blackcaps (Sylvia atricapilla) during and out of the migratory season to gain insight into (i) the changes in gene expression associated with the migratory phenotype, and link this to (ii) how these expression changes are regulated. For this we combine RNA-seq with open chromatin profiling (ATAC-seq) in the same bird, focusing on brain areas likely related to migration; the hypothalamus, the hippocampus and cluster N, a region that plays a role in processing magnetic compass information. I will present unpublished results that correlate the gene expression profiling with characterisation of activity at cis-regulatory sequences in each brain region. This study provides a novel insight into how the complex phenotype of migration is regulated in a wild passerine and constitutes a powerful approach to identify important candidate genes and genomic regulatory elements that underlie avian migratory behaviour.

Speaker: Gillian Durieux (Doctoral Researcher)

12:15 → 13:00 Talks: Session 2

12:20 Molecular regulation of population-specific migratory behaviour in songbirds at single cell resolution

Avian migration is an ecologically and evolutionarily important behaviour. Classic breeding experiments show that the difference in migratory propensity between migrant and resident populations has genetic bases. More recent population genomic studies indicate that differential selection on gene regulation instead of protein variants may be responsible for this heritable behavioural variation. However, the molecular regulation and its cell type-specificity underlying this behavioural variation between populations are still unknown. To address differential molecular regulation between populations with different propensity to migrate at the single cell level, I perform single nucleus Assay for Transposase-Accessible Chromatin sequencing (snATAC-seq) to study chromatin accessibility in blackcaps (Sylvia atricapilla) from a short distance migratory and one resident population during migratory and a control condition outside the migratory season. I specifically focus on the hypothalamus, which is a brain structure with conserved anatomy, cell types and functions regulating adaptive physiology and behaviour relevant for seasonal migration. I will present preliminary results of three analyses: (1) motif enrichment - asking what cis-regulatory elements in what cell types are differentially accessible between populations and seasons; (2) differential transcription factor footprinting - addressing what transcription factors are differentially bound to cis-elements between populations and seasons; and (3) characterisation of cis-co-accessibility networks describing sets of co-regulated cis elements. This study highlights the relevance of heterogeneity on the single-cell level and interaction of multiple regulatory elements in studying molecular mechanisms of behavioural variation.

Speaker: Jun Ishigohoka (MPI for Evolutionary Biology)

12:40 One or two quails? Migration and fenotype diversity leaded by a big chromosomal inversion

How multitrait phenotypic polymorphisms that are geographically structured can be mantained in a highly mobile and panmictic species is difficult to explain. However, that is what we observe in the common quail (Coturnix coturnix), a small migratory galliform that moves widely during the breeding season following ephemeral habitats, in search of sequential matings and with successive clutches at different locations while migrating. We used population genomics and cytogenetics to explore the basis of this polymorphism and discovered that it is induced by a large inversion in the genome of the common quail, which extends 115 Mbp in length and encompasses about 12% of the genome. Quails with the inversion are larger, have darker throat coloration and rounder wings (what is related to poorer flight efficiency). Stable isotope analyses confirmed that birds carrying the inversion migrate shorter distances or do not migrate. These quails are geographically restricted despite the high mobility of the species, to the Macaronesian islands, Morocco and Southern Iberian Peninsula. Moreover, we found no evidence of pre- or post-zygotic isolation, indicating the two forms interbreed while the differences are mantained and that the polymorphism remains locally restricted because of the effect of the chromosomal inversion over their migratory behavior.

Speaker: Ines Sanchez-Donoso (Doñana Biological Station (CSIC-EBD) )

13:00 → 14:00 Lunch Break

14:00 → 16:30 Discussion: Going beyond SNPs

16:30 → 17:15 Coffee Break

17:15 → 18:00 Keynote: Kazuhiro Wada

17:15 Unraveling the neural and genetic basis of species-specific song learning: A comparative single-cell transcriptomic analysis in songbirds

Species-specific behaviors evolve through changes in gene expression among species and the resulting effects on physiological and anatomical alterations in associated neural circuits. However, the neural and genetic mechanisms underlying species-specific learned behaviors remain unclear. Songbirds acquire species-specific songs through vocal learning by a neural circuit known as the song system, which is highly conserved across songbird species. To elucidate the species differences in gene expression at the cellular level in the song system, we conducted the single-cell transcriptional analysis focusing on two vocal motor nuclei (HVC and RA) in four species —zebra finch: Taeniopygia guttata, owl finch: T. bichenovii, cherry finch: Aidemosyne modesta, and Bengalese finch: Lonchura striata var. Domestica. Each possesses unique song features in syllable acoustics and sequences. Our interspecies transcriptomic comparison across multiple neural and non-neural cell types revealed significantly greater species-specific gene expression differences in glutamatergic excitatory projecting neurons than in other cell types within the vocal motor nuclei across all tested species. The species-differentially expressed genes in these neurons were predominantly enriched in ion channels and neurotransmitter/modulator receptors and were significantly located on the Z sexual chromosome. This suggests that specific genomic alterations modify the excitatory properties in neural circuits, underlying the species-specific learned behaviors. Furthermore, we observed that these species-specific transcriptional signatures were already presented at the initial stage of song learning. We are currently investigating the potential relationship between these transcriptional signatures and the learned song phenotypes.

Speaker: Kazuhiro Wada

18:00 → 19:00 Dinner

19:00 → 20:15 Poster Session: Session 3

Wednesday, 13 March

09:30 → 10:15 Keynote: Jane Reid

09:30 Quantitative genetic approaches to predicting micro-evolutionary dynamics of migration in the wild

Understanding and predicting micro-evolutionary dynamics of seasonal migration in the face of rapid environmental changes requires quantifying the relative magnitudes of genetic and environmental effects underlying facultative expression of migration, and of migratory plasticity. Foundational work in migration genetics invoked the quantitative genetic paradigm, envisaging that overall genetic variation stems from numerous small-effect variants, to dissect phenotypic variation in migration in birds, fish and insects. This approach has potential to estimate key effects, and also to generate important conceptual insights into emerging phenotypic variation. Yet, despite recent revolutions in quantitative genetics methodologies, there has still been remarkably little effort to estimate key quantitative genetic effects on migration, or predict resulting system dynamics, in wild populations in nature. I summarise recent quantitative genetic dissections of expression of seasonal migration versus residence in partially migratory European shags (Gulosus aristotelis). State of the art ‘animal models’ fitted to year-round ring-resighting data revealed non-zero additive genetic variance in liability to migrate in adults and juveniles. Such variances were small relative to the magnitudes of permanent and temporary environmental variances. However, substantial gene-by-environment interactions emerged at the phenotypic level, implying that environmental variation can expose otherwise cryptic genetic variation to selection. Yet, peak expression of additive genetic variance was partially temporally decoupled from episodes of strong selection, limiting micro-evolutionary responses. This work illustrates how quantitative genetics approaches can now be employed to generate major new insights into the micro-evolutionary dynamics of migration in the wild.

Speaker: Jane M. Reid (Norwegian University of Science and Technology, NTNU)

10:15 → 10:55 Talks: Session 3

10:15 Unfolding Wings: Understanding the development of migration patterns and flight skills in a long-distance migrant

How the migratory behaviour of birds develops over their lifetime is a longstanding question with important implications for predicting the adaptive capacity of migrants in a changing world. However, our inability to follow the movements of individuals from early life has limited our understanding of the ontogeny of migration. My research examines the development of migratory behaviour in long-distance migrants at two spatio-temporal scales. First, we study large-scale changes in route choice and selection over long periods of time, investigating the factors that influence shifts in migratory pathways and the implications for species survival and adaptation. Secondly, we examine small-scale improvements in flight behaviour, focusing on the intricate adjustments birds make to optimise flight efficiency, navigate effectively and adapt to challenging environmental conditions. Our research combines innovative tracking technology with advanced data analysis to provide a comprehensive understanding of bird migration patterns. The results provide valuable insights into bird behaviour, potentially informing conservation strategies and enhancing our understanding of this remarkable natural phenomenon.

Speaker: Andrea Flack (Max Planck Institute of Animal Behavior )

10:35 Stonechat migratory divide in Asia – an unconventional avian model for the study of genetic migration

Tianhao Zhao, Yuri Anisimov, Wieland Heim, Guoming Zhang, Wenjia Chen, Zongzhuang Liu, Xiaolu Jiao, Depin Li, Magnus Hellström, Staffan Bensch, Gang Song, Fumin Lei, Miriam Liedvogel, Kristen Ruegg, Bregje Wertheim, Barbara Helm
The global distribution of geographical barriers is often associated with differentiation of global avian flyways. Selection pressure from the presence of geographical barriers contributed to the formation of various migration patterns, including migratory divides in many avian species. In several model species, using migratory divides has facilitated exploration on how genes control migration. Nevertheless, the differential genomic signals associated with migratory differences do not yet conclusively indicate a convergent background. More studies are thus needed to harness the diversity of genetic mechanisms using further species, as well other geographical distributions than the Euro-African flyway and Americas Flyway. The Qinghai-Tibet Plateau (QTP), a significant highland barrier for avian migrants in Asia, has resulted in a Siberian migratory divide in many species, but hitherto received little attention in research on genetic migration. Our individual tracking study has confirmed the existence of a migratory divide close to Baikal region in Russia between Siberian (Saxicola maurus) and Amur stonechats (S. stejnegeri): Siberian stonechats employ a western detour around the QTP, whereas the Amur stonechats employ an eastern detour. We also detected autumn intermediate routes employed by potential hybrids, which directly crossed the plateau. Our additional discovery that Tibetan stonechats (S. m. przewalski) breeding on the QTP use an exclusively highland migration route, demonstrates that stonechats may have a strong capability of highland adaptation. We then explored the genomic variation in association with the phenotypical variations in these closely related taxa from a population genetics perspective, expecting to establish a new model system for genetic migration study. We wish that our study can contribute more potential insights for cross-flyway phylogenetic analyses, and perhaps finally resolve the mystery how genes control the migratory route choices of songbirds.

Speakers: Barbara Helm (Swiss Ornithological Institute ) , Tianhao Zhao (University of Groningen)

10:55 → 11:30 Coffee Break

11:30 → 12:15 Keynote: Teresa Pegan

11:30 Comparative analysis of a species assemblage reveals effects of migratory strategy on population genetic patterns in North American boreal birds

Seasonal migration is both a movement behavior and a substantial investment of time and energy into overwinter survival. Migration therefore potentially affects the evolutionarily consequential processes of dispersal (movements between breeding sites) and life history allocation (the trade-off between survival and reproduction). I examined evolutionary consequences of seasonal migration by comparing population genetic patterns in an assemblage of 34 North American boreal bird species. These species are an excellent comparison system for assessing effects variation in migratory strategy at the species level because they are co-distributed on their boreal breeding grounds, yet they show a wide range of migratory strategies ranging from residency to long-distance migration to South America. I generated population genomic datasets from across the boreal region for each of the 34 species using low-coverage whole genome sequencing. Using these data, I found that non-migratory species tend to show stronger structure than migratory species, which suggests that non-migrants experience greater dispersal limitation than migrants. However, genetic structure was unrelated to migration distance, and some of the longest-migrating species displayed as much structure as non-migrants. In these species, migratory site fidelity produces similar effects on spatial genetic patterns as dispersal limitation. I also used mitochondrial coding sequences from this dataset to demonstrate that seasonal migration distance correlates with molecular evolutionary rates. Across many lineages, animals on the “slow” end of the slow-fast life history continuum (which have high survival and low annual fecundity) tend to show slow molecular evolutionary rates, perhaps due to long generation time or reduced mutation. Long-distance migrants in the boreal region display slower life history than short-distance migrants because they sacrifice time on the breeding grounds in favor of long journeys to warm climates, which favor overwinter survival. I found that long-distance migrants have correspondingly slower molecular evolution in their mitochondria than short-distance migrants. In other words, the effects of migration on life history extend to the evolutionary rate of the genome. Overall, my comparative analyses reveal that the interplay between migration and genetics operates in both directions. At the same time that specific genes shape the migratory behavior of individuals, the ecological trade-offs inherent to migration can also feedback to shape genome-wide patterns of evolution in populations.

Speaker: Teresa Pegan (University of Michigan)

12:15 → 13:00 Talks: Session 4

12:15 The genetic basis of partial migration in blackbirds

Matthias H. Weissensteiner, Kira Delmore, Juan Sebastian Lugo Ramos, Gregoire Arnaud, Julio Blas, Bruno Faivre, Paolo Franchini, Ivan Pokrovsky, Martin Wikelski, Jesko Partecke, Miriam Liedvogel

Partial migration describes the phenomenon of one population of a species containing both migratory and sedentary individuals and it has been suggested that this type of behavior is genetically determined. Here we investigated partial migration and its genetic underpinnings in the European blackbird, a ubiquitous and well-known songbird. While populations in Spain and France are fully sedentary with no migratory movement occurring, individuals of Northern European and Russian populations are obligate migrants. To study the genetic basis of this behavior, we generated whole-genome sequencing data for 30 individuals of a population in South-Western Germany, where both migrants and resident birds occur and interbreed. In addition, we also sequenced a total of 30 individuals from Spain, France, and Russia. Analysis of genetic differentiation (FST) based on single-nucleotide polymorphisms (SNPs) between migrants and residents in the German population yielded a very low overall degree of differentiation, further supported by the absence of within-population structure in the principal component analysis of SNP genotypes. To directly investigate any association between the migratory phenotype and individuals’ genotypes, we ran linear mixed models on the entire genome. After correcting for multiple testing, we found only a single SNP to be significantly associated with the migratory phenotype. While this result is a promising first step towards revealing the genetic basis of partial migration in blackbirds, it represents only an association, and further experiments and analyses are needed to corroborate the conclusion.

Speaker: Matthias Weissensteiner (Institute of Avian Research)

12:35 Adaptation of Spanish robins (Erithacus rubecula) to habitats with different seasonality

Corinna Langebrake, Javier Pérez-Tris, Juan Carlos Illera, Georg Manthey, Miriam Liedvogel

Bird migration evolved as an adaptation to seasonally changing habitats. Migratory behaviour can vary within the same species in case of partial migratory behaviour, i.e. one population (or individual) is migratory and another one is resident. Species that exhibit a wide variety of migratory phenotypes provide valuable systems to understand the evolutionary drivers behind different phenotypes and how populations adapt to habitats with distinct seasonality. The European robin (Erithacus rubecula) expresses migratory behaviour in central and northern areas of the species distribution range, whereas populations in the South are predominantly resident, providing a suitable system to investigate these questions. We use high coverage whole genome re-sequencing data of 63 Iberian robins to investigate how migration behaviour affects population structure and demography, and how it affects the selection landscape in the genome. Iberian robins cluster in two populations, which coincide with migratory phenotype and geography and are characterised by distinct demographic histories. Our results suggest that the southern resident population is derived from an ancestral migratory population. Unexpectedly, tests for differential selection revealed extensive positive selection pressure acting across all chromosomes in the resident population, while selective sweeps are largely absent from migrants. We speculate that this might be an analytical artefact due to mismatching timescales between what population genomics methods can detect and the scale on which migration behaviour likely evolved in the robin. We suggest that future studies on the genomics of migration should more focally investigate different time scales to capture the full evolutionary history of migratory traits.

Speaker: Corinna Langebrake (Institute of Avian Research "Vogelwarte Helgoland" )

13:00 → 14:00 Lunch Break

14:00 → 16:30 Workshop: Comparative Approaches

16:30 → 17:15 Coffee Break

17:15 → 18:00 Poster Session: Session 4

18:00 → 19:00 Dinner

19:00 → 20:15 Poster Session: Session 5

Thursday, 14 March

09:30 → 10:30 Talks: Session 5

09:30 Male migrants live fast and die young

Toby Doyle & Karl Wotton

Migration is a widely observed phenomenon with long-distance movements supported by morphological, physiological and behavioural traits, of which the genetic bases of are poorly understood. While these traits vary with season, they can also vary between sexes due to different life-history requirements. Recently we have unpacked the genetic components underpinning migration in the marmalade hoverfly (Diptera: Syrphidae) by detecting differential gene expression between female summer and female migratory forms. However, male hoverflies also migrate, but sex ratios change during their journeys from roughly equal in northern Europe to >90% female in southern Europe, suggesting males are poorer long-distance migrants. To elucidate the mechanisms underpinning this sex difference we carried out morphological, physiological and transcriptomic characterisation of actively migrating male and females caught as they traversed a high mountain pass in the Pyrenees. Our results demonstrate that males and females show similar physiological adaptations to migration such as hyperphagia and resistance to starvation and cold tolerance, but display significantly different morphological features including larger thorax size and higher wing aspect ratios and wing loading in males. Premimilary results also suggest that females are up to twice the age of male migrants while analysis of differentially expressed genes suggest that males are metabolically very active but fail to maintain energy balance or the health of body tissues as seen in female migrants. Our study suggests that males are dying en route with females joined by more local males throughout their long migration, and these males 'live fast and die young' by spending their resources to mate on migration.

Speakers: Karl Wotton (University of Exeter ) , Toby Doyle (University of Exeter )

09:50 Enhanced flight performance following repeated bouts of flight and recovery in an insect migrant

Oliver Poole, Karl Wotton

The regulation of muscle tissue is crucial for migration as it directly impacts the efficiency and success of long-distance movement. Migratory birds increase muscle mass prior to migration with subsequent muscle catabolism thought to be important for maintaining optimal power to weight ratios as fuel is used up and as an endogenous source of water and Kreb cycle intermediates. Furthermore, genes associated with repair pathways are also modulated to allow the repair and replenishment of stores during stopover rests when food is available. Migrant insects face many of the same challenges as birds, yet little is known about the seasonal regulation of their flight muscles. Here we survey transcriptomic data to demonstrate wide-spread differences in the expression of muscle transcripts between migrant and non-migrant hoverflies (Diptera: Syrphidae) and between male and female migrants with divergent migratory behaviours. Additionally, we test the ability of these migrants to maintain and recover from multiple bouts of long-distance flight: hoverflies caught actively migrating through a high mountain pass were subject to four 12-hour flights on a flight-mill with a single day of recovery between each flight. Surprisingly, our initial analysis shows a significant increase in total flight distance and speed along with other flight parameters with each flight bout. Future studies aim to characterise the structural and molecular signatures of flight muscle function that contribute to the enhanced flight performance in this model system.

Speaker: Oliver Poole (University of Exeter)

10:10 Risks to migrants in agroecosystems: increased sensitivity to pesticides linked to down-regulation of a key detoxification gene.

Jaimie Barnes, Karl Wotton, Chris Bass

Animal migrations worldwide are changing in response to human activities and migratory insects have been subject to the same drastic declines seen in many resident species. Long-distance movement can expose migrants to a diverse range of habitats, and migratory demands may reduce the function of physiological processes not directly linked to migration, with consequences for susceptibility and mortality. This may be particularly true for insect migrants that frequent agroecosystems, thereby increasing their exposure to agrochemicals such as pesticides. While several studies have now addressed the effects of pesticides on non-target bee species, the consequences of these chemicals on non-target migrants remains undetermined. Here we utilise the marmalade hoverfly (Episyrphus balteatus), an important pollinator, biological control agent of aphids, long-distance migrant, and one of the most abundant insect species found within agroecosystems. Active migrants were collected from the Bujarelo Pass in the Pyrenees mountains as they flew south in the Autumn. We compared their survival following exposure to different doses of the neonicotinoid Imidacloprid to individuals reared in the lab under summer and Autumn conditions. We found migrant hoverflies were significantly more vulnerable to Imidacloprid than lab reared hoverflies, while male migrants showed increased sensitivity over female migrants. Analysis of transcriptomic data from migrant vs. non-migrant and male vs. female migrant comparisons identified the Cyp6 family of cytochrome p450s as likely key players. We identify down-regulation of Cyp6g1 (a protein known to metabolise Imidacloprid in D. melanogaster) in migrating females compared to summer females but at higher levels when comparing female to male migrants. Interestingly, a second member of this family, Cyp6g2, was also differentially expressed and has been proposed to play a role in the production of juvenile hormone, a factor strongly implemented in the oogenesis flight syndrome. Our results strongly implicate Cyp6g1 as responsible for determining the sensitivity of migrants to Imidacloprid and future work is focused on the functional characterisation of this pathway and sublethal exposure effects that could be critical in determining the success of long-distance migration.

Speaker: Jaimie Barnes (University of Exeter)

10:30 → 11:15 Keynote: Daria Shipilina

10:30 Genomics of butterfly migration: insights from the painted lady butterfly (Vanessa cardui)

Butterfly migration is an enchanting yet complex natural phenomenon. However, to date, detailed knowledge about its genetic basis is limited to a few model organisms. The painted lady butterfly, Vanessa cardui, stands out for its remarkably long-distance migrations and virtually cosmopolitan distribution and has become an emerging model species for research on migratory behavior. Here we focused on two aspects of migration in the painted lady. Using stable isotopes, we identified two distinct migratory phenotypes - short-distance migrants flying from temperate Europe to the Mediterranean, and long-distance migrants crossing the Sahara to reach West Africa (> 4,000 km). We found no significant genetic differentiation between these groups, indicating that individual differences in migration distance reflects a plastic response to environmental conditions. To get insight into the genetic basis of the response to environmental cues, we quantified gene expression and chromatin accessibility differences between experimental cohorts exposed to different conditions associated with migration-reproduction trade-offs. Our results revealed significant changes in gene expression and regulatory element activity of pathways predominantly associated with metabolism, immunity and reproduction. We identified ecdysone esterase, juvenile hormone, ARC1 and Geminin as key candidates involved in the trade-off between migration and reproduction. Our results provide novel insights into the genomic underpinnings of migratory behavior in butterflies and how long-distance migration can affect population structure in insects in general.

Speaker: Daria Shipilina (Uppsala University)

11:15 → 12:35 Talks: Session 6

11:15 Conserved genetic diversity and preliminary support for behavioural changes after a rapid range expansion of a long-distance migrant (Acrocephalus scirpaceus)

Bergman, N., Lehikoinen, P., Kluen, E., Procházka, P., Stokke, B., Lo Cascio Sætre C., Eroukhmanoff, F., Thorogood, R., Rönkä, K.
Many species are currently undergoing range shifts to track their environmental niche with climate change. However, colonizing new areas can also cause changes in the shifting population. Repeated founder events are expected to erode genetic variation and reduce adaptive potential, possibly slowing or even halting the expansion. This is especially known to affect species with limited dispersal and gene flow, but it is less clear whether highly mobile species are experiencing similar bottlenecks during range shifts. Additionally, selection or spatial sorting for expansion-facilitating traits can lead to behavioural differences between range edge and range core populations. Here, we investigated the origin, and genetic and phenotypic effects of a recent, northward range expansion of the common reed warbler (Acrocephalus scirpaceus). Evidence from historical observations, ringing data from the leading range edge, and genomic RAD-seq data covering the European breeding range all support a southwestern expansion origin. Nucleotide diversity was conserved along the expansion axis, suggesting that with high enough dispersal capability even philopatric species can escape the genetic costs of rapid range expansions, retaining adaptive potential in newly colonized areas. One possible process that could facilitate sufficient gene flow despite philopatry would be the evolutionary change in levels of philopatry and dispersal during the expansion. These traits often correlate with other behavioural traits such as exploration or aggression, and I will present preliminary results from a range-wide behavioural experiment looking at these more closely.

Speaker: Nora Bergman (University of Helsinki )

11:35 Sensing a long day at adult stage is cruical for Cnaphalocrocis medinalis to decide to migrate

Chao-min Xu, Meng-yu Hu, Yu-meng Wang, Gao Hu*

Migration is a behavioral strategy that allows insects to respond to seasonal changes in resources and the environment. Insect migration is regulated by external environmental factors such as nutrient conditions, temperature and humidity, photoperiod, and population density, as well as by intrinsic factors. Photoperiod, an important feature of seasonal changes, is a vital environmental cue affecting insect migration. But how the photoperiod affects insect migration remains vague. We investigated the effect of photoperiod on the willingness of insect migration and the critical stage for sensing the environmental cues with Cnaphalocrocis medinalis on laboratory-simulated conditions. We found that the peak of emergence occurs during the 5th to 6th hour of darkness at different photoperiods. The 2nd day female adults hardly took off under short day (11L:13D & 12L:12D), whereas the take-off ratio reached near 40% under long day (13L:11D & 14L:10D). Only sensing long day in the early stages of adult, was the proportion of take-off higher than sensing short day regardless of the photoperiod prior to emergence. Suggesting, long day is an important cue for C. medinalis to decide to migrate. We showed that sense a long day at 2nd days after emergence was crucial for C. medinalis to decide to migrate. Pupal stage and 1st day of adult were not sensitive to long light. Further research found that the take-off ratio increased after experiencing a long light period (14 hours), independent of the dark period. These findings advance our understanding of the regulatory mechanism of insect seasonal migration.

Speaker: Chao-min Xu (Nanjing Agricultural University)

11:55 How flexible is the migration strategy in Alpine swifts?

Christoph M. Meier, Guilia Masoero, Gwenaël Jacob, Hakan Karaardıç, Raül Aymí, Strahil G. Peev, Pierre Bize

How readily birds can adapt their migration strategy to a changing environment is a longstanding inquiry in ornithology. It is firmly established that crucial behaviours, such as migration direction and departure date, are genetically hardwired. However, certain aspects, like the utilization of landmarks, may be acquired and influenced by individual experiences. In this study, we present a comprehensive dataset comprising over 100 repeatedly tracked Alpine swifts, revealing a consistent migration strategy among individuals across multiple years. Through a comparative analysis of the tracks of closely related individuals, we provide initial evidence shedding light on the aspects of the journey with the strongest heritability. Our findings contribute to the understanding of how Alpine swifts may modify their migration strategy in response to the warming global climate.

Speaker: Christoph Meier (Swiss ornithological institute)

12:15 Could deep learning and population genomics unravel the mystery of songbird vagrancy?

Joe Wynn, Robert Rollins, Jochen Dierschke, Staffan Bensch, Darren Irwin and Miriam Liedvogel

Vagrancy - the tendency of (migratory) animals to leave their known range - is an essential yet poorly understood component of migratory route evolution. Vagrant birds are, by definition, extremely uncommon, and hence conventional tracking technologies are not practical since vagrant individuals can only be identified post hoc. Genomic comparison of already-established birds to the source population could, however, offer a surprisingly cheap alternative. Here, we used a ~1300bp mitochondrial DNA fragment to trace the origins of vagrant greenish warblers (Phylloscopus trochiloides) caught in Western Europe. These birds are typically found in Asia and Eastern Europe, but using a deep-learning algorithm we compared the genomes of vagrants to samples collected across the normal breeding range to infer the geographic and evolutionary origins of these pioneering individuals. More generally we discuss the generalisability of this method, and place our findings within a broader evolutionary context.

Speaker: Joe Wynn (Institute for Avian Research )

12:35 → 12:55 Closing & Conclusion

Speaker: Miriam Liedvogel (Institute for Avian Research)