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Unravelling the mechanisms underlying the evolution of ultraviolet signals

Periodic Reporting for period 1 - UVSIGNAL (Unravelling the mechanisms underlying the evolution of ultraviolet signals)

Reporting period: 2018-04-01 to 2020-03-31

Animals signals constitute the backbone of animal social interactions and their study has greatly advanced our understanding of animal evolution, ecology, and ecology. To become evolutionarily (ESS) stable strategies, signals must confer net fitness benefits to both senders and receivers and this condition can be achieved only if signals are honest, at least to some degree. To ensure that signals are honest in the face of deception, various mechanisms have been described, and perhaps one of the most widely known is costly signalling theory. It posits that a cost is associated with signal expression and prevents low quality individuals to signal high quality. These costs can take several forms, such as physiological costs associated with signal production/maintenance, predation costs as signalling may attract predators/parasites, or social costs that conspecifics impose on dishonest individuals, thus maintaining signal honesty. Colour signals frequently reflect individual quality traits and can be either pigment-based, structural, or both. Research on chromatic signals has long focused on pigment-based colours and as a result we now have a good understanding of the maintenance mechanisms underlying the honesty of some these signals. However, how structurally produced colour signals, such as ultraviolet (UV) signals, became ESS still is an open question because the mechanisms enforcing their honesty remain elusive. The over-arching aim of this project was to investigate these mechanisms and costs to improve our understanding of the evolution of colour signals. More specifically, this project aimed to investigate the costs associated with UV signal expression in male common lizards (Zootoca vivipara) using a combination of field studies and experimental approaches. Male common lizards are ideal study models because they have a UV patch on their throat that reflect their quality as mate and rival. Animal coloration and communication have always be a source of inspiration and awe for many people across space and time, including scientists, naturalists, or artists of all kind. To protect and preserve this diversity, one needs first to understand how it came to be, and this project has contributed in this sense.
In June 2018, we sampled 13 wild populations of common lizard in the Cevennes National Park (South-Central France) to explore the relationships between colour signals, morphology, performance, parasitism, testosterone, and ecogeographical variables. We found that UV signals were good indicators of male quality (i.e. sprint speed) and their expression increased to compensate degraded light conditions, as expected from theoretical background.

In August 2018, we manipulated the testosterone levels of subadult common lizards during two weeks to see whether or not it affected their coloration, including UV, their performance and morphology. We then measure these same lizards once a month during 10 months as they reached sexual maturity to detect any long-term effects of our testosterone treatments. These results will allow us to detect whether signal honesty can be mediated by testosterone early in the ontogeny and affect signalling level at sexual maturity.

Then, we performed a similar experiment but this time in adult lizards to understand the potential role of testosterone in UV signalling in the short term. We did this experiment on males from two lizard species, the common lizard (Zootoca vivipara) and the common wall lizard (Podarcis muralis). This experiment took place in spring 2019. We manipulated testosterone levels during two weeks and measured the lizards’ performance, morphology, coloration, metabolism, and immunocompetence before and after treatments. These results, along with the ones from the previous paragraph, will tell us whether testosterone mediate physiological costs associated with the expression of UV signals in these lizards.

In spring 2019, we performed a behavioural experiment aiming at identifying the potential social costs associated with UV signals during male agonistic contests. We found that social costs indeed participate to enforce UV signal honesty in common lizard. This study has been published as an open access preprint on the public repository Zenodo and is currently under review for publication in a peer-reviewed scientific journal.

In spring 2019, we started an experiment to investigate whether or not predation costs were associated with UV signals. To do so, hundreds of common lizards (males, females, and subadults) were placed in 25 outdoor enclosures reproducing semi-natural conditions. Half of these enclosures were covered with antipredation nets while the other half was vulnerable to bird predation. We measured the coloration and morphology of all lizards and recaptured them in spring 2020 to test whether or not predation occurred and whether it targeted individuals based on their coloration.

We assembled a large data set from many years of study on common lizard coloration that took place at the CEREEP-Ecotron, the experimental station where most of this project took place. This data set will allow us to test whether UV signals are heritable by analysing whether sons have UV signals more similar to their father and brothers than to other male lizards, controlling by lizards age. Knowing this will pave the way to future research aiming to identify the genetic markers responsible for UV coloration in this species.

Finally, in spring 2019, we released in ten large outdoor enclosures reproducing semi-natural conditions adult males and females and let them compete and reproduce as naturally as possible. We took their coloration, performance and morphological measurements and recaptured the gravid females to performed paternity tests. The Covid-19 crisis interrupted the paternity analyses but they will be resumed as soon as possible. This study will improve our understanding of the role of UV signals during the reproductive season, especially with a measure of reproductive success.
For now, the most significant result we obtained is the evidence that social costs participate to enforce UV signal honesty. This had never been shown in lizards, and only suggested in other animals. This is a breakthrough because until now, the mechanisms and costs maintaining the honesty of structurally produced colour signals (as opposed to pigment-based colour signals) were unknown. This result opens the door to future research aiming at quantifying these costs, and at testing whether or not they exist in other taxa so that we can have an idea of how generalised are these results. In addition, our remaining results are in line with the theoretical background and consolidate our knowledge of the role and evolution of UV signals in this species. The expected results that are to come are also promising. If negative, they will participate to improve the state of the art by discarding hypotheses, and if positive they will provide new insights that will significantly improved the way we comprehend the evolution of structurally produced colour signals, and animal communication at large.
Male Common Lizard (Zootoca vivipara)