The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms

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.

Major host transitions are modulated through transcriptome-wide reprograming events inSchistocephalus solidus, a threespine stickleback parasite

“…Parasites with multiple hosts commonly undergo dramatic phenotypic transformations and endure 50 major environmental shifts over the course of their life cycle (Wilbur 1980;Poulin 2011), yet 51 very little is known about how these are orchestrated at the molecular and physiological levels, or 52 how conserved they are across species (Auld & Tinsley 2014). Among the key insights yet to be 53 gained is a detailed understanding of the metabolic and developmental regulation of parasites 54 associated with infection, survival and development in each host.…”

Interpreting immunological indices: The importance of taking parasite community into account. An example in blackbirdsTurdus merula

“…Owen, Nelson & Clayton 2010), intracellular parasites such as protozoan stimulate T-helper 1 (Th1) and Th17 immune responses, while extracellular parasites such as helminths mainly induce Th2 immune response (Moreau & Chauvin 2010;Hayward 2013;Moreno et al 2013). Immune responses may also vary according to the tissue or organ where parasites are localised, as well as to the life stage and life cycle of the infecting parasite (Roulin et al 2003;Moreau & Chauvin 2010;Auld & Tinsley 2015). Different predictions regarding the relationships between immune indices and parasite abundance may therefore arise, depending on the parasite species considered.…”

Beach environmental DNA fills gaps in photographic biomonitoring to track spatiotemporal community turnover across 82 phyla

“…The marsh was denser in Chromadorea (roundworms), Trematoda (flukes, parasites of mollusks and vertebrates), and Gastropoda (snails and slugs). The richness of complex lifecycle parasites in the marsh suggest high presence of mobile species and genotypic diversity, such is exemplified by high trematode density where snails and migrating birds are present (Hechinger and Lafferty, 2005; Auld and Tinsley, 2015). The marsh area has rich migrating bird diversity, tracked through eBIRD (GBIF.org; see original polygon DOI download for the embayment).…”