Antagonism between parasites within snail hosts impacts the transmission of human schistosomiasis

Abstract

Human disease agents exist within complex environments that have underappreciated effects on transmission, especially for parasites with multi-host life cycles. We examined the impact of multiple host and parasite species on transmission of the human parasite Schistosoma mansoni in Kenya. We show S. mansoni is impacted by cattle and wild vertebrates because of their role in supporting trematode parasites, the larvae of which have antagonistic interactions with S. mansoni in their shared Biomphalaria vector snails. We discovered the abundant cattle trematode, Calicophoron sukari, fails to develop in Biomphalaria pfeifferi unless S. mansoni larvae are present in the same snail. Further development of S. mansoni is subsequently prevented by C. sukari’s presence. Modeling indicated that removal of C. sukari would increase S. mansoni-infected snails by two-fold. Predictable exploitation of aquatic habitats by humans and their cattle enable C. sukari to exploit S. mansoni, thereby limiting transmission of this human pathogen.

Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley

“…Alternatively, complex intramolluscan mechanisms may inhibit the occurrence of this co-infection, such as the antagonism/relationship that has been observed between S. mansoni and S. haematobium with Calicophoron spp. trematode parasites [80,81], or the induced immunoregulation and adaptive immunity of the snail during multiple schistosome infection challenges [82][83][84][85], including those of the same Schistosoma species. The role that hybridisation plays in relation to these coinfections adds an extra element of complexity, with S. haematobium group hybrids being observed to co-infect with both S. bovis [30] and S. haematobium, signifying the expanded range of compatibility between schistosome hybrids and their intermediate snail hosts warranting further investigation.…”

Genomic and transcriptional analysis of genes containing fibrinogen and IgSF domains in the schistosome vector Biomphalaria glabrata, with emphasis on the differential responses of snails susceptible or resistant to Schistosoma mansoni

“…It will be of particular interest to learn if certain FREP genotypes might vary in time relative to extant infectivity genes in S . mansoni in accordance with matching alleles models of compatibility [ 104 – 106 ] or whether a different, more generalized anti-trematode strategy, possibly based on FREPs as well, also exists in snail populations experiencing heavy burdens of parasitism from a variety of trematode species [ 107 ].…”

The weird eusociality of polyembryonic parasites

“…In theory, when parasite niches overlap, the fitness benefits of aggressive interference (and thus soldier morphs) should positively correlate with host characteristics that increase susceptibility (or exposure [ 13 ]) to parasite co-infections. We will learn more about the selective conditions favouring soldier castes with further understanding of parasite competitive ecology, which, serendipitously, is also a potentially useful avenue of research for medically relevant parasitology [ 80 , 81 ].…”