Parasite life cycle evolution and the ecology of trophic interactions

• Applicant: Dr. Daniel Benesh
• Subject Area: Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions ; Evolution, Anthropology
• Term: from 2013 to 2017
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 240212824

• Final Report Year: 2017

Final Report Abstract

Some parasitic worms infect up to five different host species before reproducing. A life cycle with more hosts in it seems intuitively more difficult to complete. Parasites with such complex life cycles must also deal with immune attacks from multiple hosts. What then are the advantages of a long and complex life cycle? And how did parasite life cycles evolve in the first place? Parasitologists have described many life cycles over the last ~150 years, but there have been few attempts to synthesize this information in a way that can answer questions about life cycle evolution. I constructed a life cycle database for three groups of parasitic worms (thorny-headed worms, tapeworms, and roundworms). For 973 parasite species, I summarized the hosts infected at each life cycle stage. I also collected data on how long parasites spend in each host and how large they grow. The result is the most comprehensive data summary available for these parasites. Initial analyses indicate that parasites have longer life cycles (i.e. they infect more hosts in succession) when the first host is small and when the last host is a top predator. The advantage to starting a life cycle in a small host may be a higher transmission rate for the eggs or free larvae, because small animals are numerous and likely to mistake tiny parasite propagules for food. Top predators are usually big and long-lived, so one could expect parasites reproducing in these hosts to grow to a large and fecund size. The data do not strongly support this, though, so it is unclear what parasites gain by being transmitted all the way up the food chain into apex predators. I confirmed that complex life cycle parasites infect a wider and more diverse range of host species than those with simple one-host cycles, and there are patterns suggesting such generalism could be costly in terms of reduced parasite growth. Parasites may adopt strategies to mitigate the risks associated with long life cycles. For example, life cycle flexibility, where a parasite can complete its cycle with or without infecting certain hosts, is more common in species with longer life cycles. The database produced during the fellowship summarizes decades of research, identifies gaps in our current knowledge, and will allow testing new hypotheses about life cycle evolution, host specificity, parasite life-history strategies, and the roles of parasites in food webs.

Publications

• 2014. Lifetime inbreeding depression, purging, and mating system evolution in a simultaneous hermaphrodite tapeworm. Evolution 68 (6): 1762-1774
  Benesh, D.P., Weinreich, F., Kalbe, M., and Milinski, M.
  
• 2014. The trophic vacuum and the evolution of complex life cycles in trophically-transmitted helminths. Proceedings of the Royal Society B 281: 20141462
  Benesh, D.P., Chubb, J.C., and Parker, G.A.
  
• 2015. Does resource availability affect host manipulation? – an experimental test with Schistocephalus solidus. Parasitology Open 1: e3
  Hafer, N. and Benesh, D.P.
  
• 2016. Autonomy and integration in complex parasite life cycles. Parasitology 143: 1824-1846
  Benesh, D.P.
  
• 2016. Experimental parasite community ecology: intraspecific variation in a large tapeworm affects community assembly. Journal of Animal Ecology 85 (4): 1004–1013
  Benesh, D.P. and Kalbe, M.
  
• 2017. A life cycle database for parasitic acanthocephalans, cestodes, and nematodes. Ecology
  Benesh, D.P., Lafferty, K., Kuris, A