Host use dynamics in a heterogeneous fitness landscape generates oscillations and diversification

Authors: BRAGA, MARIANA - Stockholm University; ARAUJO, SABRINA - Universidade Federal Do Parana; AGOSTA, SALAVTORE - Virginia Commonwealth; BROOKS, DANIEL - Institute For Advanced Studies; Hoberg, Eric; NYLIN, SOREN - Stockholm University; JANZ, NIKLAS - Stockholm University; BOEGER, WALTER - Universidade Federal Do Parana

Submitted to: Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/18/2018
Publication Date: 7/18/2018
Citation: Braga, M.P., Araujo, S.B., Agosta, S., Brooks, D., Hoberg, E.P., Nylin, S., Janz, N., Boeger, W.A. 2018. Host use dynamics in a heterogeneous fitness landscape generates oscillations and diversification. Evolution. https://doi.org/10.1111/evo.13557.
DOI: https://doi.org/10.1111/evo.13557

Interpretive Summary: Pathogen evolution and the development of host associations across geography and time is central to understanding emergent diseases. We continue to lack a complete theoretical framework for understanding the relationship of these processes. Increasingly data for host-pathogen systems in the field are at odds with a long history of concepts that have dominated thinking about the nature of what we call the host-parasite interface. In contrast to cospeciation (association of host and pathogen by evolutionary descent) colonization of novel hosts is now thought to play an important role in parasite diversification. Little consensus, however, has been achieved about the macroevolutionary consequences of changes in host use. In our study we use a novel computer-based model system to explore the mechanistic basis for the origins of macroevolutionary patterns of parasite diversity. Here we describe an individual-based model in which (i) parasites undergo sexual reproduction limited by genetic proximity, (ii) hosts are uniformly distributed along a one-dimensional resource gradient, and (iii) host use is determined by the interaction between the phenotype of the parasite and a heterogeneous fitness landscape. We found two main effects of host use on the evolution of a parasite lineage. First, the colonization of a novel host allows parasites to explore new areas of the resource space, increasing phenotypic and genotypic variation. Second, hosts produce heterogeneity in the parasite fitness landscape, resulting in speciation. By isolating the effects of the number of hosts and the diversity of resources they encompass, we found that resource heterogeneity, rather than host range per se, is the main driver of parasite species richness. This result was validated with empirical data from nymphaline butterflies, and is broadly consistent with studies linking parasitology and insect-plant systems. Our studies provide a new and expanding view of the nature of host-pathogen evolution that is relevant to emerging infectious diseases across time broad temporal and spatial scales. Our insights will contribute to theoretical and practical issues in hosat-pathogen evolution and distribution and will be of particular interest to evolutionary biologists, entomologists, parasitologists and disease ecologists.

Technical Abstract: Colonization of novel hosts is thought to play an important role in parasite diversification, yet little consensus has been achieved about the macroevolutionary consequences of changes in host use. We offer a mechanistic basis for the origins of macroevolutionary patterns of parasite diversity by simulating lineages evolved in silico, where character states are an outcome of system dynamics. Here we describe an individual-based model in which (i) parasites undergo sexual reproduction limited by genetic proximity, (ii) hosts are uniformly distributed along a one-dimensional resource gradient, and (iii) host use is determined by the interaction between the phenotype of the parasite and a heterogeneous fitness landscape. We found two main effects of host use on the evolution of a parasite lineage. First, the colonization of a novel host allows parasites to explore new areas of the resource space, increasing phenotypic and genotypic variation. Second, hosts produce heterogeneity in the parasite fitness landscape, resulting in speciation. By isolating the effects of the number of hosts and the diversity of resources they encompass, we found that resource heterogeneity, rather than host range per se, is the main driver of parasite species richness. This result was validated with empirical data from nymphaline butterflies.