Abstract

Many parasitic infections, including those of humans, are caused by complex lifecycle parasites (CLPs): parasites that sequentially infect different hosts over the course of their lifecycle. CLPs come from a wide range of taxonomic groups-from single-celled bacteria to multicellular flatworms-yet share many common features in their life histories. Theory tells us when CLPs should be favoured by selection, but more empirical studies are required in order to quantify the costs and benefits of having a complex lifecycle, especially in parasites that facultatively vary their lifecycle complexity. In this article, we identify ecological conditions that favour CLPs over their simple lifecycle counterparts and highlight how a complex lifecycle can alter transmission rate and trade-offs between growth and reproduction. We show that CLPs participate in dynamic host-parasite coevolution, as more mobile hosts can fuel CLP adaptation to less mobile hosts. Then, we argue that a more general understanding of the evolutionary ecology of CLPs is essential for the development of effective frameworks to manage the many diseases they cause. More research is needed identifying the genetics of infection mechanisms used by CLPs, particularly into the role of gene duplication and neofunctionalisation in lifecycle evolution. We propose that testing for signatures of selection in infection genes will reveal much about how and when complex lifecycles evolved, and will help quantify complex patterns of coevolution between CLPs and their various hosts. Finally, we emphasise four key areas where new research approaches will provide fertile opportunities to advance this field.

Highlights

  • Parasites vary in the complexity of their lifecycles. Some complete their lifecycle in a single host, while others require multiple successive hosts; some parasitic helminths must sequentially infect four obligate host species to complete their lifecycle (Cribb et al, 2003)

  • We suggest the following avenues of research will strengthen our understanding of both the causes and consequences of increased lifecycle complexity in parasites: (1) Conduct experimental evolution studies using parasites that can facultatively vary the complexity of their lifecycle and examine how increased lifecycle complexity impacts on parasite transmission rate and virulence

  • Increased lifecycle complexity likely evolved via upward incorporation (UI) if the neofunctionalised paralogue is associated with infection of the definitive host, whereas downward incorporation (DI) is more likely to have occurred if the neofunctionalised paralogue is associated with infection of the intermediate host (Box 1)

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Summary

SKJR Auld and MC Tinsley

Many parasitic infections, including those of humans, are caused by complex lifecycle parasites (CLPs): parasites that sequentially infect different hosts over the course of their lifecycle. We identify ecological conditions that favour CLPs over their simple lifecycle counterparts and highlight how a complex lifecycle can alter transmission rate and trade-offs between growth and reproduction. More research is needed identifying the genetics of infection mechanisms used by CLPs, into the role of gene duplication and neofunctionalisation in lifecycle evolution. We propose that testing for signatures of selection in infection genes will reveal much about how and when complex lifecycles evolved, and will help quantify complex patterns of coevolution between CLPs and their various hosts. Heredity (2015) 114, 125–132; doi:10.1038/hdy.2014.84; published online 17 September 2014

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