Eurasian blackcaps (Sylvia atricapilla) that migrate north in autumn are recovered significantly closer to the sites predicted by an exact 180-degree reversal of their population's traditional southward migratory direction than chance would allow, suggesting that migratory direction varies bi-axially and that such variation fuels rapid wintering-range expansion. What remains unresolved is the underlying encoding and inheritance: whether the reversed direction is heritable, whether direction is stored as an axis together with a pole preference (an architecture suggested by the pole/equator symmetry of the avian magnetic inclination compass), and what genetic architecture — polygenic and/or epistatic interactions between loci — produces axis reversal. The question matters practically because genome-wide association studies of migratory direction can produce erroneous locus associations if the axial structure of the trait is ignored. Later work has advanced adjacent strands — two-locus epistatic control of direction at a willow warbler migratory divide, a structural variant associated with blackcap direction, epigenetic divergence across orientation phenotypes, and confirmation that large-scale reverse misorientation occurs in vagrant yellow-browed warblers — but the encoding mechanism of bi-axial orientation itself remains untested.

Background

Many songbirds migrate at night, alone, along population-specific routes to population-specific wintering quarters, and this behaviour has a strong genetic component: in classic cross-breeding experiments, hybrid blackcaps from a migratory divide (a boundary between populations migrating in different directions) oriented intermediate between their parents' south-eastern and south-western directions, and selective breeding compressed migratory restlessness and direction within a few generations. Under a clock-and-compass model, a young bird inherits an endogenous direction and time programme rather than a route map; its first autumn trajectory is therefore a direct read-out of inherited information, measurable either in orientation cages (funnel-shaped arenas that record the nocturnal hops of caged migrants as a bearing) or from ringing recoveries and geolocators (light-level tracking devices). The avian magnetic compass is an inclination compass: it distinguishes poleward from equatorward, not north from south, and is therefore directionally symmetric along a north-south axis (Wiltschko & Wiltschko 1972); the same two-fold symmetry holds for star-compass information. Temporary reverse (opposite-direction) migration has long been recorded in autumn, e.g. in Scandinavian passerines, and diametrically opposed 'reverse' trajectories have been proposed to be surprisingly common. Against this background, Wynn, Fandos, Delmore, Van Doren, Fransson and Liedvogel (preprint 2022; published as Journal of Avian Biology 2025:e03196) analysed European ringing recoveries and geolocator tracks of blackcaps whose wintering sites lie north of their breeding sites. Using randomisation tests whose null model preserved real recovery sites and distances, they found that these northward autumn migrants lay significantly closer to the locations predicted by reversing each bird's population-specific southward bearing than chance allows (in the peer-reviewed version, randomisation tests on the angular deflection between observed and axis-reversal-predicted trajectories gave p < 0.001 for the mean and p = 0.027 for the median; the 2022 preprint had reported p < 0.0001 for both the mean and the median observed-versus-expected distances), consistent with bi-axial orientation — variation along an axis rather than around a single preferred direction — facilitating the recent, rapid northerly expansion of the blackcap's wintering range. The authors explicitly rule out, or leave unsupported, the main alternatives: additive inheritance of an intermediate direction cannot generate divergent trajectories in sympatry; a wholesale reversal of the annual cycle (as in hemisphere-switching cliff swallows) would reverse breeding phenology too, which blackcaps do not show; and purely environmental explanations (wind drift, ringing-effort bias) are addressed by the null model but cannot be fully excluded from correlative data alone, and the authors likewise note that the data do not rule out a change in migratory destination underpinned by learnt information. They therefore propose that direction is genetically encoded in two steps — an axis of direction plus a preference for one pole of that axis — so that a single change (of pole preference) yields a precise 180-degree reversal, and they note that such an architecture would most plausibly arise through epistasis (interaction between genes at different loci, e.g. axis genes and preference genes), which is rarely documented in animal behaviour. Finally, they stress as an implication of their hypothesis that any genome-wide association study (GWAS) of migratory direction — now feasible with biologging plus sequencing, as in blackcap and willow warbler genomics — must be parameterized around the true encoding, since ignoring the axial structure of the trait would lead to erroneous association or disassociation of loci with directional traits; as an illustrative consequence of axial encoding, if direction is stored as an axis plus preference, birds migrating south-west would be expected to be genetically more similar at direction loci to birds migrating north-east than to birds migrating due south. The two-step encoding hypothesis awaits direct testing — by direct experiment or pedigree analysis — to establish whether the axis-plus-pole-preference architecture underlies the observed bi-axial variation.

Problem Statement

Determine the mechanism by which migratory direction is encoded and inherited in the Eurasian blackcap such that bi-axial — precisely axis-reversed (180-degree) — orientation variants arise at unexpectedly high frequency. The overarching objective, as posed by Wynn et al. (Journal of Avian Biology 2025:e03196), has three jointly supporting components: (i) establish whether the reversed (northward autumn) migratory direction is heritable rather than environmentally induced; (ii) discriminate between the candidate mechanisms — execution of the inherited spring migratory trajectory in autumn (a phenology reversal, weakened by the absence of reversed breeding phenology in blackcaps) and the encoding of direction as an axis of migration together with a separate preference for one pole of that axis, an architecture made plausible by the pole/equator symmetry of the avian magnetic inclination compass; and (iii) identify the genetic architecture, including possible polygenic and/or epistatic interactions between loci controlling the axis and loci controlling the pole preference, that produces bi-axiality. The source paper frames the parameterization of genetic association studies as a motivating implication rather than a required deliverable: understanding how migratory direction is encoded is crucial when characterizing its genetic basis, because association analyses that ignore the true encoding may fail to capture variance in migratory direction correctly and hence lead to erroneous association or disassociation of loci with directional traits. The encoding question for the blackcap system is resolved either by establishing the inheritance mode and genomic basis of axis reversal, or by direct evidence that the observed bi-axial pattern arises without a separate heritable axis-plus-pole-preference direction-encoding architecture — whether an environmental (wind-drift), ringing-effort or sampling-bias, or learnt-information explanation of the ringing and geolocator data (alternatives the source paper acknowledges it cannot fully exclude from correlative data alone), or a heritable phenological reversal (execution of the inherited spring migratory trajectory in autumn).

References

  1. Wynn, J., Fandos, G., Delmore, K., Van Doren, B. M., Fransson, T., & Liedvogel, M. (2025). Could bi-axial orientation explain range expansion in a migratory songbird? Journal of Avian Biology, 2025:e03196. DOI: 10.1111/jav.03196. https://doi.org/10.1111/jav.03196 (peer-reviewed version of the 2022 preprint; published online 2024-07-09)
  2. Wynn, J., Fandos, G., Delmore, K., Van Doren, B. M., Fransson, T., & Liedvogel, M. (2022). Bi-axial orientation could explain range expansion in a migratory songbird. bioRxiv preprint. DOI: 10.1101/2022.05.04.490589. https://doi.org/10.1101/2022.05.04.490589
  3. Helbig, A. J. (1991). Inheritance of migratory direction in a bird species: a cross-breeding experiment with SE- and SW-migrating blackcaps (Sylvia atricapilla). Behavioral Ecology and Sociobiology, 28:9-12. DOI: 10.1007/BF00172133. https://doi.org/10.1007/BF00172133
  4. Berthold, P., Helbig, A. J., Mohr, G., & Querner, U. (1992). Rapid microevolution of migratory behaviour in a wild bird species. Nature, 360:668-670. DOI: 10.1038/360668a0. https://doi.org/10.1038/360668a0
  5. Pulido, F., Berthold, P., Mohr, G., & Querner, U. (2001). Heritability of the timing of autumn migration in a natural bird population. Proceedings of the Royal Society of London B, 268:953-959. DOI: 10.1098/rspb.2001.1602. https://doi.org/10.1098/rspb.2001.1602
  6. Bearhop, S., Fiedler, W., Furness, R. W., Votier, S. C., Waldron, S., Newton, J., Bowen, G. J., Berthold, P., & Farnsworth, K. (2005). Assortative mating as a mechanism for rapid evolution of a migratory divide. Science, 310:502-504. DOI: 10.1126/science.1115661. https://doi.org/10.1126/science.1115661
  7. Wiltschko, W., & Wiltschko, R. (1972). Magnetic compass of European robins. Science, 176:62-64. DOI: 10.1126/science.176.4030.62. https://doi.org/10.1126/science.176.4030.62
  8. Åkesson, S., Karlsson, L., Walinder, G., & Alerstam, T. (1996). Bimodal orientation and the occurrence of temporary reverse bird migration during autumn in south Scandinavia. Behavioral Ecology and Sociobiology, 38:293-302. DOI: 10.1007/s002650050245. https://doi.org/10.1007/s002650050245
  9. Areta, J. I., Salvador, S. A., Gandoy, F. A., Bridge, E. S., Gorleri, F. C., Pegan, T. M., Gulson-Castillo, E. R., Hobson, K. A., & Winkler, D. W. (2021). Rapid adjustments of migration and life history in hemisphere-switching cliff swallows. Current Biology, 31:2914-2919. DOI: 10.1016/j.cub.2021.04.019. https://doi.org/10.1016/j.cub.2021.04.019
  10. Delmore, K., Illera, J. C., Pérez-Tris, J., Segelbacher, G., Lugo Ramos, J. S., Durieux, G., Ishigohoka, J., & Liedvogel, M. (2020). The evolutionary history and genomics of European blackcap migration. eLife, 9:e54462. DOI: 10.7554/eLife.54462. https://doi.org/10.7554/eLife.54462
  11. Wynn, J., Padget, O., Mouritsen, H., Morford, J., Jaggers, P., & Guilford, T. (2022). Magnetic stop signs signal a European songbird's arrival at the breeding site after migration. Science, 375:446-449. DOI: 10.1126/science.abj4210. https://doi.org/10.1126/science.abj4210
  12. Sokolovskis, K., Lundberg, M., Åkesson, S., Willemoes, M., Zhao, T., Caballero-Lopez, V., & Bensch, S. (2023). Migration direction in a songbird explained by two loci. Nature Communications, 14:165. DOI: 10.1038/s41467-023-35788-7. https://doi.org/10.1038/s41467-023-35788-7
  13. Delmore, K. E., Van Doren, B. M., Ullrich, K., Curk, T., van der Jeugd, H. P., & Liedvogel, M. (2023). Structural genomic variation and migratory behavior in a wild songbird. Evolution Letters, 7:401-412. DOI: 10.1093/evlett/qrad040. https://doi.org/10.1093/evlett/qrad040
  14. Wynn, J., Leberecht, B., Liedvogel, M., Burnus, L., Chetverikova, R., Döge, S., Karwinkel, T., Kobylkov, D., Xu, J., & Mouritsen, H. (2023). Naive songbirds show seasonally appropriate spring orientation in the laboratory despite having never completed first migration. Biology Letters, 19:20220478. DOI: 10.1098/rsbl.2022.0478. https://doi.org/10.1098/rsbl.2022.0478
  15. Wynn, J., & Liedvogel, M. (2023). Lost: on what level should we aim to understand animal navigation? Journal of Experimental Biology, 226. DOI: 10.1242/jeb.245441. https://doi.org/10.1242/jeb.245441
  16. Zolotareva, A., Utvenko, G., Romanova, N., Pakhomov, A., & Chernetsov, N. (2021). Ontogeny of the star compass in birds: pied flycatchers (Ficedula hypoleuca) can establish the star compass in spring. Journal of Experimental Biology, 224. DOI: 10.1242/jeb.237875. https://doi.org/10.1242/jeb.237875
  17. Wynn, J., Broniszewska, M., Edney, A., Garrido Garduno, T., Moford, J., Polakowski, M., Rollins, R. E., Salmon, P., Vedder, O., & Liedvogel, M. (2026). Rapid and divergent changes in the continental-scale organisation of a short-lived songbird's migratory strategy. bioRxiv preprint. DOI: 10.64898/2026.06.16.732301. https://doi.org/10.64898/2026.06.16.732301
  18. Wynn, J., Dierschke, J., Dufour, P., Langebrake, G., Rollins, R. E., Schmaljohann, H., Salmon, P., Irestedt, M., Künzel, S., Bossu, C. M., Ruegg, K., Schnelle, A., Zhao, T., Sin, Y. C. K., Bairlein, F., Burnus, L., Hosner, P. A., Heim, W., de Jong, A., Karwinkel, T., Laine, V., Michalik, A., Neumann, M. A., Päckert, M., Renner, S. C., Ünsold, M., Winker, K., & Liedvogel, M. (2026). The road to nowhere: geolocation-by-genotype traces large-scale yellow-browed warbler vagrancy to central Siberia. bioRxiv preprint. DOI: 10.64898/2026.06.15.731303. https://doi.org/10.64898/2026.06.15.731303
  19. Adeniji, O., Justen, H., Sepers, B., Pepper, A., & Delmore, K. (2026). Epigenetic signatures of migratory orientation in a songbird hybrid zone. Philosophical Transactions of the Royal Society B, 381:2025.0021. DOI: 10.1098/rstb.2025.0021. https://doi.org/10.1098/rstb.2025.0021