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.

Figure 1

Growth–reproduction trade-off for SLPs and CLPs. Solid blue or solid orange circles represent two different clonal genotypes; circles that are both blue and orange represent the sexual progeny resulting from mating events between the blue and orange genotypes. (a) Within-host competition subjects simple parasites to the growth–reproduction trade-off: asexual reproduction leads to a few large parasites, whereas sexual reproduction leads to more small parasites. (b) CLPs can escape this trade-off: both growth and reproduction can, to a greater extent, evolve independently (see light grey arrows). A full color version of this figure is available at the Heredity journal online

Figure 2

The evolutionary consequences of definitive host migration for a CLP metapopulation. Migration rates often vary among the different hosts of a CLP. The migration rate of a CLP is expected to be most similar to that of its most mobile host—in this case the definitive host (Jarne and Théron, 2001). Immigration of mobile hosts into a population can supply novel parasite genotypes, promoting parasite LA to the less-mobile host (Gandon et al., 1996; Gandon and Michalakis, 2002).

Figure 3

Scenario for the evolution of host-specific infection mechanisms with increasing parasite lifecycle complexity. (a) The ancestral state: a parasite with a single infection mechanism (M1) for infecting different host types. (b) Gene duplication creates paralogues of the ancestral infection mechanism: a precursor for distinct infection mechanisms. (c) Varying selective pressures from intermediate and definitive hosts lead to neofunctionalisation in one of the paralogues (M2) and the evolution distinct infection mechanisms.