The life cycles of parasitic worms, from macroevolutionary patterns to the genetics of adaptation

• Applicant: Dr. Daniel Benesh
• Subject Area: Evolution, Anthropology
• Term: from 2018 to 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 408202975

• Final Report Year: 2023

Final Report Abstract

Many parasitic worms (helminths) infect multiple hosts in succession before reproducing. As the number of successive hosts increases, so do the chances of not being transmitted to the next host. Moreover, such parasites must adapt to different host physiologies, immune systems, and often thermal regimes. Why do complex life cycles (CLC) evolve in parasitic worms, and how do helminths adapt to infecting multiple hosts in a CLC? To address these questions, we employed two approaches: (i) cross-species comparative analyses, and (ii) experiments measuring parasite gene expression. Comparative analyses with a comprehensive life-cycle database indicated that parasites with longer life cycles (i.e. more successive hosts) infected smaller first hosts and larger final hosts. Incorporating smaller first hosts likely enhances transmission because we found that small first hosts normally eat things the size of parasite propagules. In larger final hosts, parasites have more space and energy to grow, so they reach larger and more fecund reproductive sizes. The inability to maximize transmission and growth with a single host likely explains the ubiquity of CLCs in helminths. The costs of CLCs also seem overstated. The species-level generalism inherent to CLCs (i.e. infecting successive hosts) does not impair overall parasite growth, and the risk from multiple transmission steps is partly mitigated by increasing establishment rates with life cycle progression (i.e. infection rates are higher in the second than the first host). Comparative analyses also demonstrated that the traits of parasites at different life stages – like body size, host generalism, or thermal sensitivity of larval vs adult parasites – can evolve independently. This is consistent with a lack of genetic pleiotropy across life stages. To further assess such decoupling, we measured gene expression throughout the CLCs of two unrelated parasitic species: the nematode Camallanus lacustris and the tapeworm Schistocephalus solidus. Transcriptomic analyses revealed distinct shifts in gene expression, such that stages from different hosts expressed different genes, even when they performed similar functions, like growth. Our analysis also identified genes with similar annotations but different patterns of expression in functionally similar stages from different hosts; these genes may be instrumental to decoupling. In conclusion, macroevolutionary comparative analyses suggested that the benefits of CLCs outweigh the costs, whereas both macroevolutionary and microevolutionary (transcriptomics) approaches indicated that parasite life stages are decoupled and able to adapt independently to the challenges of infecting and exploiting successive hosts in a CLC.

Publications

• Examining the role of parasites in limiting unidirectional gene flow between lake and river sticklebacks. Journal of Animal Ecology, 88(12), 1986-1997.
  Erin, Noémie I.; Benesh, Daniel P.; Henrich, Tina; Samonte, Irene E.; Jakobsen, Per J. & Kalbe, Martin
  
• Tapeworm manipulation of copepod behaviour: parasite genotype has a larger effect than host genotype. Biology Letters, 15(9), 20190495.
  Benesh, Daniel P.
  
• Ungulate Helminth Transmission and Two Evolutionary Puzzles. Trends in Parasitology, 36(1), 64-79.
  Chubb, James C.; Benesh, Daniel & Parker, Geoff A.
  
• Comparative analysis of helminth infectivity: growth in intermediate hosts increases establishment rates in the next host. Proceedings of the Royal Society B: Biological Sciences, 288.
  Froelick, Spencer; Gramolini, Laura & Benesh, Daniel P.
  
• Life‐cycle complexity in helminths: What are the benefits?. Evolution, 75(8), 1936-1952.
  Benesh, Daniel P.; Parker, Geoff & Chubb, James C.
  
• Trade-Offs with Growth Limit Host Range in Complex Life-Cycle Helminths. The American Naturalist, 197(2), E40-E54.
  Benesh, Daniel P.; Parker, Geoff A.; Chubb, James C. & Lafferty, Kevin D.
  
• Adaptive division of growth and development between hosts in helminths with two‐host life cycles. Evolution, 76(9), 1971-1985.
  Benesh, Daniel P.; Chubb, James C. & Parker, Geoff A.
  
• Complex life-cycles in trophically transmitted helminths: Do the benefits of increased growth and transmission outweigh generalism and complexity costs?. Current Research in Parasitology & Vector-Borne Diseases, 2, 100085.
  Benesh, Daniel P.; Chubb, James C.; Lafferty, Kevin D. & Parker, Geoff A.
  
• The effects of phylogeny, habitat and host characteristics on the thermal sensitivity of helminth development. Proceedings of the Royal Society B: Biological Sciences, 289.
  Phillips, Jessica Ann; Vargas, Soto Juan S.; Pawar, Samraat; Koprivnikar, Janet; Benesh, Daniel P. & Molnár, Péter K.
  
• Selection on an extreme-yet-conserved larval life-history strategy in a tapeworm. Evolution, 77(5), 1188-1202.
  Benesh, Daniel P.