The role of hybridization and introgression as mechanisms of diversification and adaptation has been well documented in plants but are only starting to gain equivalent appreciation in animals. Despite increased evidence of patterns of variation consistent with hybridization in animals, rarely do we understand how those patterns come about and when hybridization will shape the evolution of organisms and their genomes. Therefore, a major challenge for evolutionary biologists is to connect causes of hybridization with their consequences for diversification and adaptation.

Our research addresses this challenge using the European Wall lizard (Podarcis muralis). Wall lizards, are a genetically diverse species of lacertid lizard common to southern Europe. The two main lineages of the wall lizard, which diverged approximately 3 mya, have come back into secondary contact both through natural range expansion and through human mediated processes. Importantly, as well as having diverged genetically these lineages also show striking phenotypic divergence, specifically in several key traits related to sexual selection (e.g., colouration, body size, performance). We have shown that this divergence results in strong differences in male competitive ability between lineages, with Italian males being competitively dominant over French males, resulting in increased access to females of both their own and the other lineage and thus uni-directional hybridisation. Females appear relatively unperturbed to this as we do not find any evidence of female choice nor do we find any negative fitness costs associated with hybrid matings. The consequences is strong asymmetric introgression of sexually selected characters from one lineage to another across all zones of secondary contact. Indeed, in our natural hybrid zone in Northern Italy, Italian phenotypic traits have introgressed approximately 250 km into the French lineage.

This work has identified a number of significant questions that we are currently addressing. Specifically, we are employing state-of-the art genomic techniques and sampling across additional (independent) zones of secondary contact to examine the consistency of introgression at both a genomic and phenotypic level. We also have a new PhD project examining the environmental mediators of patterns of introgression. Interestingly, although introgression occurs rapidly along the coast, there are limits to the spread of Italian genes at higher altitudes. This may be the result of topographical constraints on gene flow or it might be the result of selection against the Italian phenotype at higher altitudes. These all provide exciting opportunities for future research.

This work is carried out in collaboration with Tobias Uller (Lund, Sweden), Nathalie Feiner (Lund, Sweden), Marco Zuffi (Pisa, Italy), Roberto Sacchi (Pavia, Italy), Fabien Aubret (CNRS, France), Pau Carazo (Valencia, Spain), Guillem Perez i de Lanuza (Porto, Portugal), Danielle Salvi (Rome, Italy) and many others.

If you want to know more:

Minano, M.R., While, G.M., Yang, W., Burridge, C. P., Sacchi, R., Zuffi, M., Scali, S., Salvi, D. and Uller, T. (2021) Climate shapes geographic variation and introgressive spread of colour ornamentation in common wall lizards. American Naturalist.

Yang, Y., Feiner, N., Pinho, C., While, G. M., Kaliontzopoulou, A., Harris, D. J., Salvi, D. and Uller, T. (2021) Extensive introgression and mosaic genomes of Mediterranean endemic lizards. Nature Communications. 12:2762.

Yang, W., Feiner, N., Laakkonen, H., Sacchi, R., Zuffi, M. A. L., Scali, S., While, G. M. and Uller, T. (2020) Spatial variation in gene flow across a hybrid zone reveals causes of asymmetric introgression and reproductive isolation in wall lizards. Evolution. 74: 1289-1300.

Andrade, P., Pinho, C., Pérez i de Lanuza, G., Afonso, S., Brejcha, J., Rubin, C-J., Wallerman, O., Pereira, P., Sabatino, S., Bellati, A., Pellitteri-Rosa, D., Bosakova, Z., Bunikis, I., Carretero, M. A., Feiner, N., Marsik, P., Paupério, F., Salvi, D., Soler, L., While, G. M., Uller, T., Font, E., Andersson, L. and Carneiro, M. (2019) Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard. Proceedings of the National Academy of Sciences, USA. 116: 5633-5642.

Yang, W., While, G.M., Laakkonen, H., Sacchi, R., Zuffi, M., Scali, S., Salvi, D. and Uller, T. (2018) Genomic evidence for asymmetric introgression by sexual selection in the common wall lizard. Molecular Ecology. 27:4213–4224.

MacGregor, H.E.A., While, G. M., Barret, J., Perez l de Lanuza, G., Carazo, P., Michaelides, S., and Uller T. (2017) Character divergence and the role of sexual selection upon secondary contact in Wall lizards. Functional Ecology, 31, 742-752.

While, G, M., Michaelides, S., Heathcote, R.J.P., MacGregor, H.E.A., Zajac, N., Beninde, J., Carazo, P., Perez I de Lanuza, G., Sacchi, R., Zuffi, M., Horvathova, T., Fresnillo, B., Schulte, U., Veith, M., Hochkirch, A. and Uller, T. (2015) Sexual selection drives asymmetric introgression in wall lizards. Ecology Letters, 18, 1366-1375.