Different underlying mechanisms drive associations between multiple parasites and the same sexual signal

Associations between parasite loads and sexual signal expression have long been the focus of research. However, our understanding of how sexual selection operates in the context of multiple parasite infections within the same host is still quite limited. We examined the expression of plumage coloration, which is sexually selected in North American barn swallows, Hirundo rustica erythrogaster, and tail streamer length, which is sexually selected in other barn swallow subspecies, in the context of eight different parasite infections. We found that two parasites, nest mites and Plasmodium, were associated with colour expression, but in opposite directions. Attractive males were less likely to have mites in their nests, but more likely to be infected with Plasmodium. We found that different underlying mechanisms were generating the links between these different parasites and the same colour signal. Males that invested more in colour expression were less likely to survive when infected with Plasmodium, suggesting a physiological mechanism linking colour to Plasmodium infections. However, we found no clear cost to males when examining nest mites, which primarily infect offspring. Instead, using experimental mite manipulations, we provide evidence for a behavioural mechanism, where territorial behaviour and male–male competition likely drive the association between colour expression and nest mite infections. We did not find associations between parasites and streamer length in this subspecies, suggesting that the links between divergent sexual signals and parasites may be quite flexible. These results suggest that the evolution of a single sexual signal can be shaped by several, even opposing, links with different parasite infections. •We examined associations between plumage colour and parasite loads in barn swallows.•Darker males had fewer nest mites but greater likelihood of Plasmodium infection.•Colour investment decreased survival when males were infected with Plasmodium.•Territorial behaviour likely drives colour expression–nest mite association.•Sexual signal evolution can be shaped by different links with multiple parasites.