Abstract

Cercarial emission of schistosomes is a determinant in the transmission to the definitive host and constitutes a good marker to identify which definitive host is responsible for transmission, mainly in introgressive hybridization situations. Our goal was to test the hypothesis that micro-mammals play a role in Schistosoma haematobium, S. bovis, and/or S. haematobium x S. bovis transmission. Small mammal sampling was conducted in seven semi-lacustrine villages of southern Benin. Among the 62 animals trapped, 50 individuals were investigated for Schistosoma adults and eggs: 37 Rattus rattus, 3 Rattus norvegicus, 9 Mastomys natalensis, and 1 Crocidura olivieri. Schistosoma adults were found in four R. rattus and two M. natalensis, with a local prevalence reaching 80% and 50%, respectively. Two cercarial chronotypes were found from Bulinus globosus experimentally infected with miracidia extracted from naturally infected M. natalensis: a late diurnal and nocturnal chronotype, and an early diurnal, late diurnal, and nocturnal chronotype. The cytochrome C oxidase subunit I mtDNA gene of the collected schistosomes (adults, miracidia, and cercariae) belonged to the S. bovis clade. Eleven internal transcribed spacer rDNA profiles were found; four belonged to S. bovis and seven to S. haematobium x S. bovis. These molecular results together with the observed multi-peak chronotypes add M. natalensis as a new host implicated in S. haematobium x S. bovis transmission. We discuss the origin of the new chronotypes which have become more complex with the appearance of several peaks in a 24-h day. We also discuss how the new populations of offspring may optimize intra-host ecological niche, host spectrum, and transmission time period.

Highlights

  • Schistosomiasis is an acute and chronic disease caused by flatworms of the genus Schistosoma and estimates have shown that at least 229 million people required preventive treatment in 2018 (WHO 2020)

  • The cercariae of Schistosoma bovis Sonsino, 1876 are shed during the early morning when cattle go to watering (Mouahid and Théron 1986; Mouahid et al 1987, 1991); the cercariae of Schistosoma haematobium (Bilharz, 1852) Weinland, 1858 and S. mansoni Sambon, 1907 are shed around mid-day when humans go to water for bathing, washing, or fishing (Mouahid et al 1991, 2012); the cercariae of S. rodhaini Brumpt 1931 and of some chronotypes of S. mansoni and of S. japonicum Katsurada 1904 are shed during the early night, when nocturnal rodents actively use water (Théron 1989; Mouahid et al 2012; Su et al 2013)

  • From the 24 sequences of schistosomes extracted from children stool, we found 8 haplotypes (KU1_Hs_Hap6; KU3_Hs_Hap7; KU4_Hs_Hap8; KU13_Hs_Hap9; KU10_Hs_Hap11, KS5_Hs_Hap13, KS10_Hs_Hap14), among which five were shared with some haplotypes found in the urine, and one haplotype (K14M1_Mn_Hap1) shared with the schistosome haplotypes found in M. natalensis

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Summary

Introduction

Schistosomiasis is an acute and chronic disease caused by flatworms of the genus Schistosoma and estimates have shown that at least 229 million people required preventive treatment in 2018 (WHO 2020). The cercariae of Schistosoma bovis Sonsino, 1876 are shed during the early morning when cattle go to watering (Mouahid and Théron 1986; Mouahid et al 1987, 1991); the cercariae of Schistosoma haematobium (Bilharz, 1852) Weinland, 1858 and S. mansoni Sambon, 1907 are shed around mid-day when humans go to water for bathing, washing, or fishing (Mouahid et al 1991, 2012); the cercariae of S. rodhaini Brumpt 1931 and of some chronotypes of S. mansoni and of S. japonicum Katsurada 1904 are shed during the early night, when nocturnal rodents actively use water (Théron 1989; Mouahid et al 2012; Su et al 2013) This makes cercarial pattern a good marker for identifying which definitive host is responsible for Schistosoma transmission, mainly in the introgressive hybridization situations between different species of schistosomes that have increasingly been described in the literature over the last decade (Boissier et al 2019)

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