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How genetic constraint and selection drive colour diversification? Reconstructing the evolutionary history of sexual dichromatism in island endemic lizards

Periodic Reporting for period 1 - EvoColour (How genetic constraint and selection drive colour diversification? Reconstructing the evolutionary history of sexual dichromatism in island endemic lizards)

Période du rapport: 2022-09-01 au 2024-08-31

Animal colouration is a remarkable illustration of nature’s capacity for “endless forms most beautiful”. Yet, the drivers of this diversity remain largely unexplained. In particular, we have a limited understanding of the origin of novel colour variants and if and how genetic architecture biases adaptive change. These problems evoke an unresolved debate between Charles Darwin and Alfred Russel Wallace. Darwin considered sex differences in colouration – sexual dichromatism – to evolve gradually as a result of sexual selection for bright colours in males. Colours often signal dominance, fighting ability or other aspects of male quality. Wallace on the other hand pointed out that females often are colourful, too, and that bright colouration therefore is likely to appear in both sexes at first, only to occasionally disappear in females under natural selection for crypsis to reduce predation.

We have used the remarkable phenotypic diversification of the Balearic wall lizards (Podarcis pityusensis and P. lilfordi) to shed light on the Darwin-Wallace debate, as well as to provide unprecedented information on the origin and diversification of colour ornaments in general.

The overall aim of EvoColour is to advance our understanding of the origin and evolution of colour diversity –how it is shaped by genetic constraints and sexual and natural selection. We aimed to:
a) Establish the evolutionary history of Balearic wall lizards
b) Reconstruct evolutionary transitions in male and female colouration
c) Establish associations between evolutionary change and indicators of sexual and natural selection
d) Raise awareness about the diversity and biological importance of Balearic wall lizards

To conclude

Balearic wall lizards exhibit a higher degree of sexual dichromatism than previously anticipated, particularly in P. pityusensis. In this project, we have visited approximately 60 populations belonging to the two species under study. We have sampled all existing populations of P. pityusensis and a representative sample of P. lilfordi. We have collected unprecedented morphometric, colour, and genetic data for both species, expanding the scope of sampled populations beyond the original design. Additionally, we have reconstructed the evolutionary history of the Balearic wall lizards and mapped the evolutionary transitions in male and female coloration for all body regions. We are now in the final stages of analysis, where we have tested key indicators of natural and sexual selection. Furthermore, we have undertaken initiatives aimed at enhancing stakeholders and the public understanding of the ecological and evolutionary significance of the Balearic lizard.
In this project, we have optimized an analytical methodology for color measurement that we are confident will be highly valuable not only for future color studies in lizards but also for other organisms. This method enables the extraction of highly detailed information from different body regions of the animal, taking into account their specific characteristics. Additionally, we developed a field protocol whose success has inspired its implementation in parallel projects within Prof. Tobias Uller's research group. For Podarcis pityusensis, we gathered field data from all existing populations, providing the Balearic government with crucial information on presence, absence, and potential densities—some populations had not been surveyed in nearly a decade. Furthermore, we confirmed the absence of lizards on islands where they had been historically recorded. This finding is particularly significant as the species is currently endangered due to the introduction of exotic snakes accidentally brought from the mainland. For P. lilfordi, we obtained a representative sample of the species. In both species, we collected morphometric, colorimetric, and genetic data at an unprecedented scale, which has allowed us to map the evolutionary history of sexual dichromatism in the Balearic wall lizards.
This work represents an unprecedented effort in both sampling and analysis in the study of colour evolution in the Balearic wall lizards. In just two years, we have gathered data from all P. pityusensis populations and a substantial representative sample of P. lilfordi. We have sequenced the entire genome of individuals from each population (i.e. each island), marking a groundbreaking achievement in lizard evolutionary studies. This has contributed to map the evolutionary trajectories of both species together (and their colour characteristics) at an unparalleled level. While the methodology developed in this study for measuring lizard coloration builds on previous protocols, it has been adapted to follow a novel and tailored approach to optimise color analysis in lizards. Additionally, the species studied here hold cultural significance in the islands. Given the endangered status of both species, the sampling of their populations and the resulting data provided to the Balearic government will undoubtedly support more continuous and accurate monitoring efforts in the coming years. Overall, we believe that the results of our study will be highly valuable not only for the specific goals of our project but also for future research in evolution, ecology, morphometrics, and conservation.
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