Introgressive hybridization of human and rodent schistosome parasites in western Kenya

Abstract

Hybridization and introgression can have important consequences for the evolution, ecology and epidemiology of pathogenic organisms. We examined the dynamics of hybridization between a trematode parasite of humans, Schistosoma mansoni, and its sister species, S. rodhaini, a rodent parasite, in a natural hybrid zone in western Kenya. Using microsatellite markers, rDNA and mtDNA, we showed that hybrids between the two species occur in nature, are fertile and produce viable offspring through backcrosses with S. mansoni. Averaged across collection sites, individuals of hybrid ancestry comprised 7.2% of all schistosomes collected, which is a large proportion given that one of the parental species, S. rodhaini, comprised only 9.1% of the specimens. No F1 individuals were collected and all hybrids represented backcrosses with S. mansoni that were of the first or successive generations. The direction of introgression appears highly asymmetric, causing unidirectional gene flow from the rodent parasite, S. rodhaini, to the human parasite, S. mansoni. Hybrid occurrence was seasonal and most hybrids were collected during the month of September over a 2-year period, a time when S. rodhaini was also abundant. We also examined the sex ratios and phenotypic differences between the hybrids and parental species, including the number of infective stages produced in the snail host and the time of day the infective stages emerge. No statistical differences were found in any of these characteristics, and most of the hybrids showed an emergence pattern similar to that of S. mansoni. One individual, however, showed a bimodal emergence pattern that was characteristic of both parental species. In conclusion, these species maintain their identity despite hybridization, although introgression may cause important alterations of the biology and epidemiology of schistosomiasis in this region.

Modelling the Effects of Mass Drug Administration on the Molecular Epidemiology of Schistosomes

“…Schistosomes are known to hybridize frequently (Steinauer et al, 2010), and reports from Senegal have identified hybridisation between S. haematobium/ S. mansoni (Huyse et al, 2013), S. haematobium /S. curassoni and S. haematobium / S. bovis and between S. mansoni / S. rodhaini in western Kenya (Steinauer et al, 2008). The implications of these events for MDA programs have yet to be established, but hybridisation may have implications for disease morbidity and drug tolerance and therefore represent a public health concern.…”

Out of Animals and Back Again: Schistosomiasis as a Zoonosis in Africa

“…rodentum. More recent analyses have shown using molecular tools that there is gene flow between the parasites found in rodents and in man, suggesting that the form observed in rodents subtly changes its morphology in response to different host environments (Steinauer et al, 2008b); this work was done on rodent populations in Western Kenya, where several other reports of S. mansoni in rodents from recent years have originated (Hanelt et al, 2010, Steinauer et al, 2008a. Rodents have also been found infected with S. mansoni throughout the rest of Africa, with more reports from Kenya (Kawashima et al, 1978, Nelson et al, 1962, South Africa (Pitchford and Visser, 1962), Senegal (Duplantier and Sène, 2000), Sudan (Karoum and Amin, 1985) and Egypt (Arafa andMassoud, 1990, Mansour, 1973).…”

DNA Barcoding of Schistosome Cercariae Reveals a Novel Sub-Lineage within Schistosoma rodhaini From Ngamba Island Chimpanzee Sanctuary, Lake Victoria

“…Schistosoma rodhaini is commonly considered primarily an infection of rodents and insectivores (Hanelt et al, 2010). The species has a very patchy distribution in East Africa, where it co-occurs alongside the more widely spread S. mansoni; in areas of overlap, S. mansoni has been observed to be much more abundant, suggesting ecological dominance (Steinauer, Hanelt et al, 2008). This is perhaps due to the greater susceptibility of human hosts to S. mansoni compared with small mammals and S. rodhaini, which, for the latter, tend to have lower infection intensities (Steinauer, Mwangi et al, 2008;Hanelt et al, 2010).…”

“…The species has a very patchy distribution in East Africa, where it co-occurs alongside the more widely spread S. mansoni; in areas of overlap, S. mansoni has been observed to be much more abundant, suggesting ecological dominance (Steinauer, Hanelt et al, 2008). This is perhaps due to the greater susceptibility of human hosts to S. mansoni compared with small mammals and S. rodhaini, which, for the latter, tend to have lower infection intensities (Steinauer, Mwangi et al, 2008;Hanelt et al, 2010). Intriguingly, at a single site in the Lake Victoria basin, genetic introgression between S. mansoni and S. rodhaini has been observed (Steinauer, Hanelt et al, 2008); several snails collected from this region near Kisumu in Kenya were co-infected with both species of schistosome (Steinauer, Mwangi et al, 2008).…”

“…This is perhaps due to the greater susceptibility of human hosts to S. mansoni compared with small mammals and S. rodhaini, which, for the latter, tend to have lower infection intensities (Steinauer, Mwangi et al, 2008;Hanelt et al, 2010). Intriguingly, at a single site in the Lake Victoria basin, genetic introgression between S. mansoni and S. rodhaini has been observed (Steinauer, Hanelt et al, 2008); several snails collected from this region near Kisumu in Kenya were co-infected with both species of schistosome (Steinauer, Mwangi et al, 2008). Elsewhere in Lake Victoria, a hybrid S. mansoni 3 S. rodhaini adult worm was recovered from a trapped rat on Ukerewe Island in Tanzania (Morgan, DeJong, Lwambo et al, 2003), which emphasizes the potential for interaction between these schistosomes given their close evolutionary relationship.…”