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Highlights from ESEB 2017

This year’s European Society for Evolutionary Biology meeting was held in Groningen. ESEB is always a great opportunity to see old friends, learn new things, and – somewhat jealously! – see the progress on the most famous study systems in evolutionary biology, such as cichlids, Heliconius butterflies, and bird beaks. And progress there was. Among the most memorable were further evidence from the Seehausen group – presented by Joana Meier and others – that hybridization has played a creative role in fish evolution in both African and European lakes, and a tour-de force of Heliconius evolutionary genomics in a plenary by Chris Jiggins (there is a book, not only for butterfly lovers!). Hybridization was hot at the meeting so it was a shame that Yang was unable to join this year. Wallies were represented, however, by a nice talk on the ventral colour polymorphism by Pedro Andrade. Chances are they will make a big splash next year in Montpellier!

To be fair, ESEB has never been a hotspot for development and this year was no different. Manhattan plots abound, but there was generally little process-oriented research to allow us to connect genotype and phenotype. Exceptions included an excellent plenary by Renee Duckworth, where she demonstrated how to integrate proximate and ultimate causation to understand why organisms change over time or, in this case, why they may not do so. Another exceptional talk was delivered by Alex Badyaev, expanding on his recent papers on the evolution of carotenoid colouration in birds. Describing evolution as transitions between external and internal control in regulatory networks, this work demonstrated the potential for taking a comparative network approach to study innovation and diversification from a developmental perspective.

Other welcome islands in the sea of genomics of adaptation include Andreas Wagner’s plenary on innovation and modularity, or a talk by Christoph Thies from Richard Watson’s group who presented some refreshing ideas on evolutionary transitions in individuality and demonstrated how to capture this process formally. Plasticity and evolution was represented here and there, including an update on the spadefoot toad story by Ivan Gomez-Mestre.

Judging from the ESEB talks, evolutionary biologists are very interested in extra-genetic inheritance. Most talks – including a pretty well-attended symposium keynote by Tobias – revealed this interest to largely be about adaptive function, but with some nice links to life history and ageing (many thanks to Foteini Spagopolou and the other organisers). With a better integration between development and evolution we may look forward to more work on how inheritance systems actually originate and evolve. Chances are Daphnia will deliver some of the pieces of the puzzle and Reinder’s poster – showing preliminary data that quantify the extent of extra-genetic inheritance – was indeed well attended.

The poster sessions were actually one of the meeting’s highlight. Taking place in what resembled an aircraft hangar, it was cool and spacious. And there was wine. Nathalie – presenting her work on the evolution of embryonic gene expression in wall lizards adapting to cool climate – was super busy explaining her findings to other attendees. The whole meeting was full on – I did not even manage to talk to many of the people I know well!

It is always nice to visit Groningen, a place where many of the most creative researchers in evolutionary biology took their first steps as MSc students. With 1600 attendees, these meetings are really too big to take on, but the organising committee – headed by Leo Beukeboom and Simon Verhulst – did a great job pulling it all together. We are already looking forward to see what Turku and Prague can come up with in the years to come!

 

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Friends shape the distribution of genetic variation

Small encounters can have large impacts. This counts for animals as well. Particular for social animals – such as great tits – encounters with others affect how they move around and where they eventually settle. And this influences with whom they mate and how successful they are in life. In a new paper published in Molecular Ecology, Reinder Radersma and colleagues from Oxford and Sheffield show that the social environment has a large impact on the movement of great tits – a bird species roaming around Wytham Woods and many other Eurasian forests. These movements affect the distribution of genotypes, which is crucial for how the population can evolve. After all, the distribution of genotypes across an area shapes the genetic combinations that arise and thus, the opportunity for local adaptation.

A particular difficulty when investigating how movements are affected by social interactions is that it is very hard to separate social effects from other factors which vary in space. For instance, when food is not equally distributed – as is often the case – animals might aggregate in food-rich areas. It may look like individuals choose to interact, because many individuals are at the same location. However, it is simply the food, not the company, that is the attraction.

 

Reinder and his colleagues used techniques recently developed for spatial statistics and extended its use to analyze social networks to separate the effects of spatial variables and social interactions on tit movement.

They show that the movement of individuals and therefore the distribution of genotypes is strongly affected by the preference to move around with the same individuals, in other words, hanging out with “friends”. In addition, the birds do not befriend simply individuals that live in close proximity, because neighbors have similar genotypes. Instead, they pick friends that are genetically different from themselves. As a result, the genetic structure of the population is affected by both social and spatial effects.

 

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Why do lizards smell?

Many male lizards produce secretions that they rub on the ground of their territories. The function of these secretions remains contentious, in particular whether or not they serve as indicators of male fighting ability or suitability as a mate. A new paper, published in Evolution, suggests that sexual selection on chemical composition is, in fact, quite weak.

Headed by recent PhD graduate Hannah MacGregor, and in collaboration with Geoff While and Patrizia d’Ettorre, we analysed the chemical composition of secretions from male lizards from France and Italy. The results confirmed previous work showing that chemical profiles can correlate with male secondary sexual characters. However, the correlations were generally weak and inconsistent across the season and between populations. More importantly, there was little evidence that a male’s chemicals make him have more offspring.

That sexual selection on the femoral secretions is weak was further supported by the overall neutral pattern of introgression of chemical profiles in the hybrid zone between the highly sexually selected form (the ‘Tuscan’ lizards) and the ancestral phenotype (details on this hybrid zone can be found here). Nevertheless, three candidate compounds were candidates for asymmetric introgression via direct selection or genetic linkage with visual or behavioural characters.

On the whole, these results are bad news for the hypothesis that chemical communication is sexually selected in wall lizards. Instead, femoral secretions probably function as signature mixtures; that is, they help lizards to keep track of who’s who and to resolve territorial disputes. Yet, every now and then, a particular compound may become consistently selected – perhaps due to genetic linkage – and evolve a more signal-like function. May we speculate that this process can be facilitated by introgressive hybridization?

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New philosophy of biology paper

Ever wondered why there is such intense disagreement over the evolutionary significance of development, non-genetic forms of inheritance, and niche construction? If so, you may be helped by a recent analysis by Tobias and Heikki Helanterä. The paper, accepted in the premier philosophy of science journal British Journal for the Philosophy of Science, uses niche construction as a case study to demonstrate how the way we think of causality in biological systems shape the structure of evolutionary explanations.

Richard Lewontin famously described evolution by natural selection in terms of three principles: variation, differential fitness and inheritance. Organisms fulfil these principles and so they evolve, diversify and adapt. But this does not tell us how the principles are causally related, nor how they should best be construed.

The classic instantiation of Lewontin’s principle describes evolution in genetic terms. This version is what we are taught at school. What we are not often taught, however, is that the genetic instantiation imposes a large degree of autonomy on the biological processes that produce variation, differential fitness, and heredity. Variable rates of survival determine what features will occur in the next generation. But selection does not affect the process of inheritance; inheritance is merely the passing on of whatever genes were selected. The variation that fuels evolution is similarly autonomous. Mutations occur randomly with respect to their consequences for development and fitness, and the acquisition of new variants does not change how variation is transmitted down generations. The result is an ordered set of causally autonomous processes; each step determines (partly) the inputs for the next step, but not how those inputs will be processed.

nicheconstruction

 

The autonomy of variation, differential fitness and inheritance is deeply entrenched in contemporary evolutionary biology. But it is a convenient heuristic and not a logical necessity, and it may or may not accurately capture biological reality. Many biologists suspect that it does not and that, in the real world, causes of variation, fitness, and heredity are intertwined. Tobias and Heikki show that such alternative instantiations of the principles of evolution by natural selection can affect the structure of evolutionary theory. And this, in turn, can make it perfectly valid to consider both natural selection and niche construction part of an evolutionary explanation for why organisms are well suited to their environments.

Failing to appreciate how different instantiations of Lewontin’s principles affect causal explanation in evolution is a major source of communication failure surrounding not only niche construction, but also developmental plasticity, extra-genetic inheritance and other phenomena.

Tobias and Heikki also suggests another reason people do not seem to understand each other: the views held by scientists on how science works. Many scientists expect their deep-held views, such as the core of the genetic instantiation of evolution by natural selection, to be falsified by data before they consider alternatives. Other scientists put less emphasis on anomalies and evaluate conceptual frameworks primarily on their ability to stimulate useful research. These different perspectives on scientific progress cut across disciplines but are rarely made explicit in scientific debates.

Nevertheless, philosophy of science is important to understand what the contention actually is about. If one considers niche construction theory an attempt to formulate an alternative research programme, it should be evaluated on the basis of its ability to stimulate new questions and predict patterns and phenomena that would otherwise appear surprising; not on the basis of whether or not it falsifies the genetic perspective. On the other hand, those arguing for more substantial conceptual change must strive towards showing that their framework leads to a different, theoretically and empirically progressive, research programme. Maybe the need for scientific pluralism is a good topic to bring up at your next coffee break?

 

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Cause and Process at the KLI

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

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 21st 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.

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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.

populations_greenness

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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