Life Cycles Shape Parasite Evolution: Comparative Population Genetics of Salmon Trematodes

Abstract

Abstract. Little is known about what controls effective sizes and migration rates among parasite populations. Such data are important given the medical, veterinary, and economic (e.g., fisheries) impacts of many parasites. The autogenic-allogenic hypothesis, which describes ecological patterns of parasite distribution, provided the foundation on which we studied the effects of life cycles on the distribution of genetic variation within and among parasite populations. The hypothesis states that parasites cycling only in freshwater hosts (autogenic life cycle) will be more limited in their dispersal ability among aquatic habitats than parasites cycling through freshwater and terrestrial hosts (allogenic life cycle). By extending this hypothesis to the level of intraspecific genetic variation, we examined the effects of host dispersal on parasite gene flow. Our a priori prediction was that for a given geographic range, autogenic parasites would have lower gene flow among subpopulations. We compared intraspecific mitochondrial DNA variation for three described species of trematodes that infect salmonid fishes. As predicted, autogenic species had much more highly structured populations and much lower gene flow among subpopulations than an allogenic species sampled from the same locations. In addition, a cryptic species was identified for one of the autogenic trematodes. These results show how variation in life cycles can shape parasite evolution by predisposing them to vastly different genetic structures. Thus, we propose that knowledge of parasite life cycles will help predict important evolutionary processes such as speciation, coevolution, and the spread of drug resistance.

Spatial covariation of local abundance among different parasite species: the effect of shared hosts

“…In such cases, the mobile host is usually the definitive host, and is commonly a bird. The inclusion of a mobile host in the life cycle is thought to be responsible for profound differences between autogenic and allogenic parasites in terms of local infection levels (Kennedy et al 1986;Esch et al 1988), population genetic structure (Criscione and Blouin 2004;Blasco-Costa and Poulin 2013), and geographic distribution (Thieltges et al 2011). The use of mobile versus waterbound definitive hosts may also uncouple patterns of spatial variation in local densities between autogenic and allogenic parasites that otherwise have shared intermediate hosts in their life cycles.…”

Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas)

“…Pérez-Tris and Bensch (2005) found a positive relationship between dispersal distance of the blackcap, Sylvia atricapilla, and the local transmission of Haemoproteus and Plasmodium. Other studies have also shown that host movement increases parasite range with the parasites of sheep (Blouin et al 1995), cattle (Blouin et al 1995), and salmon (Criscione and Blouin 2004). Waldenström et al (2002) also found multiple avian haemosporidian lineages in both the wintering and breeding ground of European migrants, showing that the combination of bird migration and competent vectors can spread these parasites.…”

Integrating fish and parasite data as a holistic solution for identifying the elusive stock structure of Pacific sardines (Sardinops sagax)

“…Cryptic species arise when genetic variation between closely related species is less conserved than morphological characteristics (Jousson et al 2000). With the increasing availability of parasite DNA sequences, cryptic species have been discovered among several parasite taxa (Criscione and Blouin 2004;Vilas et al 2005), and have altered our understanding of the geographic ranges of some platyhelminthes (Jousson et al 2000). Mattiucci et al (2004) used allozyme differences to demonstrate that seven genetically distinct species existed among morphologically similar individuals of Anisakis species collected from European hake (Merluccius merluccius).…”

“…For instance, Criscione and Blouin (2004) suggested that parasites with allogenic life cycles (definitive host a mammal or bird) had more gene flow between distant populations than parasites with autogenic life cycles (definitive host a fish). This was expected, since geographic barriers are less likely to influence the movement of birds or mammals than fish.…”