Evolutionary biologists and philosophers of biology recently gathered at the KLI, an international centre for advanced studies in theoretical biology, to discuss the nature of causation in evolutionary biology. The workshop, organised by Tobias and Kevin Laland, aimed to clarify how the ongoing integration of development and evolution may influence the structure of evolutionary theory and the nature of evolutionary explanations.

The classic view on causation in evolutionary biology makes a clear distinction between proximate and ultimate causes. The former explains how biological organisms work, very much like the causal-mechanistic explanations we see in engineering or chemistry. Ultimate causes, on the other hand, are historical; they explain why organisms work in particular ways. Natural selection is an ultimate cause and, to many biologists, it is the only cause needed to explain the adaptive fit between organism and environment.

The proximate-ultimate distinction seems to follow, almost logically, from (what we may call) the genetic representation of evolution by natural selection. But biologists these days regularly invoke proximate causes in their evolutionary explanations – think ‘plasticity-first’ scenarios, extra-genetic inheritance, and niche construction, for example.

One view is that this is a categorical mistake; a confusion arising from an inability to understand the distinction between proximate and ultimate causes. Another view is that, as useful as the proximate-ultimate distinction may be, it is a consequence of the genetic representation of evolution by natural selection and not a fundamental fact about biological causation. Other ways to think about the causal relations between the fundamentals of evolution – variation, differential reproduction, and heredity – may result in an evolutionary theory with a different structure.

Participants at the 2017 KLI meeting on Cause and Process in Evolution

Workshop participants scrutinized the problem in a variety of ways – from biologically motivated reasons why organisms are more responsible for their own evolution than we typically grant, to conceptually motivated scepticism towards population thinking and the causal status of natural selection itself.

The result was an exceptionally vibrant workshop, with very many insights on the relationship between development and evolution, individuals and populations, and cause and effect. Many participants commented that it was one of the most intellectually stimulating meetings they had ever attended. There was, of course, no universal agreement on how evolutionary causation should be understood. But we are definitely several steps closer to provide a 21^st century account of the causes of evolution that is both biologically informed and conceptually coherent.

There will be a book published from the talks so that you can make up your own mind on the nature of causation in evolution – but for now, you may want to read these meeting reports by Massimo Pigliucci and Wim Hordijk.

If you are interested in this research program that supported this workshop, please visit our webpage and follow us on twitter.

This year marked the 6^th 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.

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.

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.

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.

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

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.

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!

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.