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Indiana Yang and the origin of the Tuscans!

This year marked the 6th in our quest for the evolutionary origin and introgressive spread of a sexually selected syndrome in wall lizards. It marked a return to central Italy to fill in the remaining gaps in the map tracing the origins of this phenotype. What has been revealed so far is an intricate history of isolation, evolution, and conquest through interbreeding.

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Phenotypes of the sampled populations in Italy vary from “Tuscan” (green) to ancestral (brown)

Here is the background to the Italian drama. The ancestral phenotype of the wall lizards is characterised by brown coloration and relatively small body size. This phenotype persists across the wall lizard’s current distribution, from western Spain throughout most of southern Europe and into the eastern Greek islands. However, in the not-so-distant past a population of wall lizards somewhere on the west coast of Italy evolved a suite of highly exaggerated characters – larger heads, bulkier bodies, green-and-black colour, aggressive behaviour, to name just some features. The green-and-black lizards – we call them Tuscans, but they are formally described as P. muralis nigriventris – later came into contact with their closest relatives, and then with a much older lineage evolving in western Europe. Both of these retain the usual brown wall lizard phenotype. Since then the whole suite of characters has spread via introgressive hybridization to cover most of the lowland areas from south of Rome to Genoa in the West, Bologna and Modena in the North, and the Appennines in the East.

 

Tobias and Yang

Catching lizards

The first aim of our research has been to reveal when and where this all happened. This detective work has so far taken in 100+ wall lizard populations in Italy. Like any good detective story, our suspect for the location of the origin of the Tuscan phenotype has been a moving target, constantly changing as more phenotypic and genetic sampling has ruled out potential hypotheses and given rise to others. This year saw the final pieces of the puzzle come together and, thanks to Yang’s and Hanna’s efforts in the lab, we expect to release a detailed evolutionary history in due time.

The second aim is to nail down who is guilty. We know one part of the answer: sexual selection. The exaggerated characters give males an advantage in competition with other males. Male-male competition thus promoted the evolution of the green-black phenotype during their time in geographic isolation. Sexual selection is also what has made the suite of characters introgress as the lizards came into contact with lizards of different genetic lineages. What remains to be understood are the ecological conditions that made sexual selection take off and persist to drive the characters to fixation.

 

Mara

Happy PhD student

None of the introgressive spread would be possible, however, unless genomic and developmental organisation allowed the transfer of a whole suite of characters between lineages. Despite that the characters are quantitative, their spread is associated with limited overall genetic exchange. Thus, evolution of this suite of characters is shaped by, and probably shapes, genomic and developmental modularity. We suspect that an ancestral developmental organisation may contribute to the repeated evolution of similar phenotypes across wall lizard species. This is exciting because theoretical studies (Jones et al. 2014, Watson et al. 2014) suggest that evolution of development under correlational selection can make even random mutation produce phenotypes that are non-random with respect to fitness. One of our main long-term goals is therefore to use the wall lizards to study how the evolution of development shapes the capacity for continued evolution, or evolvability.

A second long-term goal is to understand what, if anything, will make the introgression stop? Our phenotypic sampling has revealed a potential kryptonite to the Tuscan phenotype – high altitude. The introgressive spread of the Tuscan phenotype is restricted in the mountains and in some cases cease altogether, resulting in the persistence of the brown backed morph at the highest altitudes. There are several potential explanations for this, including geographic barriers or selection. This year we added to new detectives to the team, Mara and Théo, whose projects are designed to address this question.

 

So the wall lizard story continues. As one chapter draws to a close new research questions have emerged allowing us to continue our spring forays to the land of pizza, pasta and lucertole. Now with the genome at our hands, the opportunities to explore these questions at both a phenotypic and genomic level have never been greater. Let us know if you’d like to join us.

Théo, Valentina, Mara, Yang

Hard fieldwork this April

 

For the published work to date, please see the following papers

While, G.M., Michaelides, S., Heathcote, R.J.P., MacGregor, H.E.A., Zajac, N., Beninde, J., Carazo, P., Pérez i de Lanuza, G., Sacchi, R., Zuffi, M.A.L., Horváthová, T., Fresnillo, B., Schulte, U., Veith, M., Hochkirch A. & Uller, T. 2015. Sexual selection drives asymmetric introgression in wall lizards. Ecology Letters 18:1366-1375

Heathcote, R., MacGregor, H., Sciberras, J., While, G.M., D’Ettorre, P. & Uller, T. 2016. Male behaviour drives assortative reproduction during the initial stage of secondary contact in lizards. Journal of Evolutionary Biology 29:1003-1015

MacGregor, H.E.A., While, G.M., Barrett, J., Perez I de Lanuza, G., Carazo, P., Michaelides, S. & Uller, T. Experimental contact zones reveal causes and targets of sexual selection in hybridizing lizards. Functional Ecology 31:742–752

MacGregor, H.A.M., While, G.M. & Uller, T. Comparison of reproductive investment in native and non-native populations of common wall lizards reveals sex differences in adaptive potential. Oikos, in press

While, G.M. & Uller, T. Female reproductive investment in response to male phenotype in wall lizards and its implications for introgression. Biological Journal of the Linnean Society, in press

 

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What’s new in lizard social evolution?

A series of recent papers show how good places to live shapes family life in Egernia lizards. Our research – headed by Geoff and his students Ben and Tom – have revealed that the distribution of crevice sites influence group size, polygyny, and the opportunity for sexual selection. This affects the offspring too, because the distribution of adults determine the costs and benefits of dispersal. What about males? They do not like when females mate outside of the pair bond. This can disrupt family living since it is the aggression between fathers and offspring, and between siblings, that make the youngsters pack their bags and move. You can read the details here, here, and here.

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New group members!

We are very happy to welcome Mara Ruiz Miñano and Théo Ducos to the group. Mara is a new PhD student at the University of Tasmania, supervised by Geoff and Tobias. Mara will join our research project on the causes and consequences of hybridization in wall lizards. This means she will split her time between Lund and Tasmania, with a fair bit in between catching lizards in Italy. Théo will also be working on wall lizards for his MSc project, which continues our collaboration with Patrizia D’Ettorre at the University of Paris 13. Looks like it could be a fun field season!

 

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This View of Life

Tobias is interviewed by David Sloan Wilson on This View of Life. The piece can also be read on our EES blog, together with recent posts by Massimo Pigliucci, Kim Sterelny, Armin Moczek and others.

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Alfredo Rago joins us as postdoc!

alfredo_ragoAs pointed out by Scott Gilbert, the environment is a “normal agent of development”. But how do organisms evolve to integrate features of the environment into their development? And how does that affect their ability to evolve further? These are some of the questions that Alfredo will address in his research, which is a close collaboration with computer scientist Richard Watson at the University of Southampton. We are very excited to have Alfredo here on what promises to be an outstanding project!

Alfredo brings strong opinions about coffee and much more to the group. Except for the coffee we think he’ll be fine. Just consider that he is from Rome, the epicentre of green-and-black wall lizards, and did his PhD at the University of Birmingham with John Colbourne, one of the founders of the Daphnia Genomics Consortium. Not to mention that he began his science career as an Msc student with Tobias at Oxford, unravelling what makes some frogs such good invaders. Welcome, Alfredo!

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Are jumping genes driving the radiation of Anolis lizards?

A new study by Nathalie Feiner brings a fresh perspective on the famous adaptive radiation of Anolis lizards. The paper, published this week in the Proceedings of the Royal Society of London B, reveals that speciation events are accompanied by accumulation of DNA sequences that can copy and paste themselves within the genome. Such transposable elements (TEs), popularly referred to as jumping genes, have long been suspected to contribute to evolutionary diversification. Good evidence for this intriguing idea has been hard to come by, however.

There are two main hypothesis for how TEs can contribute to adaptive radiation. Firstly, TE activity may promote speciation by causing genomic incompatibility between incipient species. Secondly, TEs may facilitate adaptation by rewiring gene regulatory networks such that new variants become available for selection.

To test these hypotheses, Nathalie compared the DNA sequences of Hox gene clusters of thirty lizard species. The results revealed that there was a burst of TE activity in the lineage leading to extant Anolis. It did not stop there – TEs have continued to accumulate during speciation events, leading to the pattern that Anolis lizards whose evolutionary history is characterized by many speciation events also accumulated many TEs. This finding nicely supports the hypothesis that TE proliferation may contribute to reproductive isolation.

 

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Could TE activity also have caused the morphological differences that characterize Anolis ecotypes? Well, there is no evidence for this as yet, but this hypothesis is much more difficult to test since we need to learn more about developmental genetics to know where to look. Nevertheless, Nathalie’s study is an exciting first step towards unravelling the genomics of adaptive radiation of these wonderful lizards!

 

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