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Male lizards often display multiple pigment-based and structural colour signals which may reflect various quality traits (e.g. performance, parasitism), with testosterone (T) often mediating these relationships. Furthermore, environmental conditions can explain colour signal variation by affecting processes such as signal efficacy, thermoregulation and camouflage. The relationships between colour signals, male quality traits and environmental factors have often been analysed in isolation, but simultaneous analyses are rare. Thus, the response of multiple colour signals to variation in all these factors in an integrative analysis remains to be investigated.

Here, we investigated how multiple colour signals relate to their information content, examined the role of T as a potential mediator of these relationships and how environmental factors explain colour signal variation.

We performed an integrative study to examine the covariation between three colour signals (melanin-based black, carotenoid-based yellow–orange and structural UV), physiological performance, parasitism, T levels and environmental factors (microclimate, forest cover) in male common lizards Zootoca vivipara from 13 populations.

We found that the three colour signals conveyed information on different aspects of male condition, supporting a multiple message hypothesis. T influenced only parasitism, suggesting that T does not directly mediate the relationships between colour signals and their information content. Moreover, colour signals became more saturated in forested habitats, suggesting an adaptation to degraded light conditions, and became generally brighter in mesic conditions, in contradiction with the thermal melanism hypothesis.

We show that distinct individual quality traits and environmental factors simultaneously explain variations of multiple colour signals with different production modes. Our study therefore highlights the complexity of colour signal evolution, involving various sets of selective pressures acting at the same time, but in different ways depending on colour production mechanism.