Dispersal in a Parasitic Worm and Its Two Hosts: Consequence for Local Adaptation

Abstract

Characterizing host and parasite population genetic structure and estimating gene flow among populations is essential for understanding coevolutionary interactions between hosts and parasites. We examined the population genetic structure of the trematode Schistosoma mansoni and its two host species (the definitive host Rattus rattus and the intermediate host Biomphalaria glabrata) using microsatellite markers. Parasites were sampled from rats. The study was conducted in five sites of the Guadeloupe Island, Lesser Antilles. Mollusks display a pattern of isolation by distance whereas such a pattern is not found neither in schistosomes nor in rats. The comparison of the distribution of genetic variability in S. mansoni and its two host species strongly suggests that migration of parasites is principally determined by that of the vertebrate host in the marshy focus of Guadeloupe. However, the comparison between genetic differentiation values in schistosomes and rats suggests that the efficacy of the schistosome rat-mediated dispersal between transmission sites is lower than expected given the prevalence, parasitic load and migration rate of rats among sites. This could notably suggest that rat migration rate could be negatively correlated to the age or the infection status of individuals. Models made about the evolution of local adaptation in function of the dispersal rates of hosts and parasites suggest that rats and mollusks should be locally adapted to their parasites.

Understanding the ecology and evolution of host–parasite interactions across scales

“…In other cases, no relationship has been found between the genetic structure of host populations and that of their parasites (Mulvey et al 1991). Among the reasons for such asymmetries and variation among systems are that the genetic structure of host and parasite populations depends on life histories of the organisms (reviewed in Barrett et al 2008), including whether the parasite has a complex life cycle (Prugnolle et al 2005) or a broad or narrow host range (Johnson et al 2002).…”

Low genetic diversity in a snail intermediate host (Biomphalaria pfeifferi Krass, 1848) and schistosomiasis transmission in the Senegal River Basin

“…Low genetic diversity in the intermediate host may have afforded rapid development of an extremely compatible snail-schistosome system, explaining the exceptionally high transmission rates of S. mansoni in this region. However, simultaneous characterization of host and parasite population genetic structure from natural populations is essential to understand co-evolutionary trajectories (Prugnolle et al 2005). Ultimately, co-evolution, and hence transmission, will be tempered by the protagonists' relative gene flow from beyond the SRB (Gandon et al 1996;Gow et al 2004).…”

Invasion genetics of the introduced black rat (Rattus rattus) in Senegal, West Africa

“…Genomic DNA was extracted from toe or spleen tissue samples with the QIAGEN DNeasy Tissue Kit or Gentra Puregene DNA Purification Kit, according to the manufacturer's instructions. We genotyped 17 microsatellite loci, seven of which were originally developed for the brown rat (Rattus norvegicus) and had already been used in studies of black rat populations (D5Rat83, D7Rat13, D10Rat20, D11Mgh5, D11Rat56, D16Rat81 and D18Rat75; Prugnolle et al 2005). The other 10 microsatellite loci were developed by Loiseau et al (2008), specifically for the black rat (Rr14, Rr17, Rr21, Rr22, Rr54, Rr67, Rr68, Rr93, Rr107 and Rr114).…”

“…The spread of rats has had substantial economic and human health consequences, including the spread of haemorrhagic fever viruses (Mills & Childs 1998), plague (Tollenaere et al 2010a), rickettsiosis (Azad et al 1997), trypanosomiasis (Dobigny et al 2011) and schistosomiasis (Prugnolle et al 2005). However, despite the considerable impact of invasive rat populations on various aspects (biodiversity, the economy and health), little is known about the evolutionary history and dynamics of these populations, as the available data were obtained in highly focal (Abdelkrim et al 2005(Abdelkrim et al , 2009(Abdelkrim et al , 2010Prugnolle et al 2005;Gilabert et al 2007) and historical biogeographic studies (Matisoo-Smith & Robins 2009;Tollenaere et al 2010b;Aplin et al 2011;Lack et al 2012). In particular, no study has yet specifically addressed the issues of the history of the invasion process, the geographic pathway of the invasion and the origin and genetic composition of the invading populations.…”