Mastomys natalensis (Smith, 1834) as a natural host for Schistosoma haematobium (Bilharz, 1852) Weinland, 1858 x Schistosoma bovis Sonsino, 1876 introgressive hybrids

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.

Keywords: Cercarial chronobiology; Mastomys natalensis; Rattus rattus; Schistosoma haematobium x Schistosoma bovis; Schistosome transmission.

Fig. 1

Geographical positions of the villages where samples were collected. a Position of the area in South Benin; b zoom view and position of the seven villages (white circles)

Fig. 2

Adult paired worms in the mesenteric veins of Mastomys natalensis

Fig. 3

Cercarial emission patterns from infected snails, each exposed to 1 miracidium of Schistosoma from Mastomys natalensis. a Late diurnal and nocturnal pattern for Bulinus globosus (Bg1); b early and late diurnal and nocturnal pattern for B. globosus (Bg2)

Fig. 4

Maximum likelihood tree topology built with 14 haplotypes COI mtDNA (884 bp) showing that the schistosomes recovered from either rodents or schoolchildren (in black) belong to the S. bovis clade. The scale shows the number of nucleotide substitutions per site. Comparison was made with GenBank sequences (in red) obtained by Savassi et al. (2020) and sequences (in blue) obtained from various other references. Haplotype code/COI mtDNA accession nos.: K14M1_Mn_Hap1/MW022134; V20M1_Rr_Hap2/ MW022135; V20M2_Rr_Hap3/ MW022136; V20M3_Rr_Hap4/ MW022137; V132M1_Rr_Hap5/ MW022138; KU1_Hs_Hap6/MW022139; KU3_Hs_Hap7/MW022140; KU4_Hs_Hap8/MW022141; KU13_Hs_Hap9/MW022142; KU5_Hs_Hap10/MW022143; KU10_Hs_Hap11/MW022144; KU11_Hs_Hap12/MW022145; KS5_Hs_Hap13/MW022146; KS10_Hs_Hap14/MW022147

Fig. 5

The study of schistosomiasis transmission at Kessounou (Benin), based on the present paper and on Savassi et al. (2020) data, showed five distinct cercarial emission patterns. Three populations of cercariae are clearly present: in yellow those which emerge early in the morning, corresponding to S. bovis profile, in blue those which emerge in the afternoon, corresponding to S. haematobium profile, and in pink those that emerge at nightfall, corresponding to the involvement of Mastomys natalensis (nocturnal rodent), in the transmission. The bovis profile (a) and haematobium profile (b) appear alone (one peak per day) or each associated with the nocturnal profile (two peaks per day) (c, d). The three populations can be associated with three peaks per day (e)