Embracing colonizations: A new paradigm for species association dynamics

Authors: NYLIN, SOREN - Stockholm University; AGOSTA, SALVATORE - Virginia Commonwealth University; BENSCH, STEFFAN - Lund University; BOEGER, WALTER - Federal University Of Parana Polytechnic Center; BRAGA, MARIANA - Stockholm University; BROOKS, DANIEL - Stellenbosch University; FORISTER, MATTHEW - University Of Nevada; HAMBACK, PETER - Stockholm University; Hoberg, Eric; NYMAN, TOMMI - University Of Eastern Finland; SCHAPERS, ALEXANDER - Stockholm University; STIGALL, ALYCIA - Ohio University

Submitted to: Trends in Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/4/2017
Publication Date: 1/1/2018
Citation: Nylin, S., Agosta, S., Bensch, S., Boeger, W.A., Braga, M., Brooks, D.R., Forister, M.L., Hamback, P.A., Hoberg, E.P., Nyman, T., Schapers, A., Stigall, A. 2018. Embracing colonizations: A new paradigm for species association dynamics. Trends in Ecology and Evolution. 33(1):4-14. https://doi.org/10.1016/j.tree.2017.10.005
DOI: https://doi.org/10.1016/j.tree.2017.10.005

Interpretive Summary: Paradigms, or our our world views, are critical in providing the foundations for understanding patterns and processes in the natural world. Paradigms codify traditions and bodies of knowledge and should encompass considerable explanatory power. Considering parasitology, the discipline has been substantially hindered by a flawed view of the nature of associations or linkages between host and parasite species. A currently prevalent idea about host-parasite association embraces simplicity rather than complexity and has direct implications for addressing the expanding crisis for emerging infectious diseases. We explore the development of a new way of viewing the host-parasite interface, and necessary junction between parasitology and insect-plant evolution and ecology. Parasite-host and insect-plant research have very divergent traditions despite the fact that many phytophagous (plant-eating) insects live parasitically on their host plants. In parasitology it is a traditional assumption that parasites are typically highly specialized. These assumptions about specialization have contributed to the idea that evolution between parasites and hosts primarily occurs through association by descent in which evolution and speciation of the parasite is dependent the host in which it occurs. Cospeciation between parasites and hosts has remained a frequently expressed and basic model despite considerable evidence to the contrary. Insect-plant theory has been more concerned with host shifts than with cospeciation, and more with hierarchies among hosts than with extreme specialization. We suggest that the divergent assumptions in the respective fields have hidden a fundamental similarity with an important role for potential as well as actual hosts, and hence for host colonizations in structuring species assemblages and faunas. A common research program is proposed which better prepares us for the challenges from introduced species and global change. Broader discussion linking the parasitology and plant-insect communities is critically important in our regime of accelerating environmental change. Common approaches are necessary that emphasize fundamental processes as a path to understand how complex biological systems respond to disruption and perturbation. Our current discussion should be of importance to a broad community of evolutionary biologists, and disease ecologists across the federal and academic sectors.

Technical Abstract: Parasite-host and insect-plant research have very divergent traditions despite the fact that many phytophagous insects live parasitically on their host plants. In parasitology it is a traditional assumption that parasites are typically highly specialized. Cospeciation between parasites and hosts is a frequently expressed null model. Insect-plant theory has been more concerned with host shifts than with cospeciation, and more with hierarchies among hosts than with extreme specialization. We suggest that the divergent assumptions in the respective fields have hidden a fundamental similarity with an important role for potential as well as actual hosts, and hence for host colonizations via ecological fitting. A common research program is proposed which better prepares us for the challenges from introduced species and global change.