Parasite diversity and host evolution: A global analysis of carnivores

Background/Question/Methods Identifying the evolutionary mechanisms that generate and maintain parasite diversity in natural ecosystems is important for advancing the field of macroecology in which one of the primary goals is to fully understand drivers of biodiversity as well as to predict the future of biodiversity. Here, we draw attention to the link between host evolutionary history and parasite diversity. Host evolution affects opportunities for parasites to colonize and evolve within and be lost from host lineages over evolutionary time. In turn, parasites play important roles in shaping key aspects of host evolutionary history, including speciation. In this study, we investigate how important host evolutionary distinctiveness is, relative to other biological and environmental factors, in explaining parasite diversity in wildlife hosts, and why. For example, evolutionarily distinctive host lineages might harbor fewer parasite species because they have fewer opportunities for parasite sharing than hosts having extant close relatives, and/or because diverse parasite assemblages promote host diversification. Our data set includes 930 species of parasites reported to infect free-living carnivores. We applied several richness estimators to estimate parasite diversity among well-sampled carnivore species and compared the relative importance of a series of host factors using a machine-learning approach.

Results/Conclusions Species richness estimates indicate that the current published literature captures less than 50% of the true parasite diversity for most carnivores. As expected, parasite species richness declined with evolutionary distinctiveness of carnivore hosts (i.e. length of terminal ranches of the phylogeny) and increased with host species body mass and geographic range area. We did not find hosts from more diverse lineages to support a higher number of generalist parasites, thus rejected the hypothesis that the observed association between parasite diversity and host distinctiveness is generated by that closely related host species have higher frequencies of parasite sharing. However, we did find that stronger male-biased sexual dimorphism was displayed by host species harboring large parasite diversity, suggesting the negative association between parasite diversity and host evolutionary distinctiveness is due to parasites driving host diversification through host sexual selection. Collectively, this work provides strong support for host evolutionary history being an essential predictor of parasite diversity, and offers a simple model for predicting parasite diversity in understudied carnivore species. We also demonstrate here the utility of diversity estimators for global-scale parasite datasets from heterogeneous sources.