Genetic characterization of schistosome species from cattle in Côte d'Ivoire

Abstract

Background: Schistosomiasis is a water-based parasitic disease that affects humans, livestock and wild animals. While considerable resources are dedicated to the surveillance, disease mapping, control and elimination of human schistosomiasis, this is not the case for livestock schistosomiasis. Indeed, there are important data and knowledge gaps concerning the species present, population genetic diversity, infection prevalence, morbidity and economic impact. This study aimed to identify circulating schistosome species in cattle across Côte d'Ivoire and to investigate their population diversity and structuring.

Methods: Overall, 400 adult schistosomes were collected from slaughtered cattle at six sites across Côte d'Ivoire. Additionally, 114 miracidia were collected from live cattle at one site: Ferkessédougou, in the northern part of Côte d'Ivoire. DNA from all specimens was extracted and the cox1 and ITS1/2 regions amplified and analysed to confirm species. The genetic diversity and structuring of the schistosome populations were investigated using 12 microsatellite markers.

Results: All adult schistosomes and miracidia presented Schistosoma bovis mitochondrial cox1 profile. Nuclear ITS1/2 data were obtained from 101 adult schistosomes and four miracidia, all of which presented an S. bovis profile. Genetic diversity indices revealed a deficiency of heterozygotes and signals of inbreeding across all sites, while structure analyses displayed little geographic structuring and differentiation. Cattle in Côte d'Ivoire thus appear to be mono-species infected with S. bovis. Hybrids of Schistosoma haematobium × S. bovis have not been identified in this study. Cattle schistosomes appear to be panmictic across the country.

Conclusions: Our results contribute to a deeper understanding of schistosome populations in Ivorian cattle and emphasize a One Health approach of joint human and animal surveillance and prevention and control programmes for schistosomiasis.

Keywords: Schistosoma bovis; Schistosoma curassoni; Cattle; Côte d’Ivoire; Genetic diversity; Genetic structuring; Microsatellites; One Health; Schistosomiasis.

Fig. 1

Map of Côte d’Ivoire. Orange circles indicate abattoir sites sampled for adult schistosomes from slaughtered cattle. In Ferkessédougou (green triangle), both slaughtered cattle from abattoirs and live cattle on farms were sampled for adult schistosomes and miracidia, respectively

Fig. 2

Plot of structure analysis of schistosomes from cattle across Côte d‘Ivoire. Each column represents one schistosome with the colours indicating the relative contribution of the three genetic clusters (K = 3) to the parasite’s genome

Fig. 3

Scatterplot of the first two components of discriminant analysis of principal components (DAPC) of populations of schistosomes from cattle, based on geography. Dots are individuals, circles inertia ellipses. Forty principal components were retained, representing 84.3% of the total variation in allele frequencies. Ab, Abengourou; Ag, Agboville; Du, Duekoué; Fk, Ferkessédougou; Og, Ouangolodougou; Sk, Sikensi

Fig. 4

STRUCTURE analysis of male and female schistosomes obtained from slaughtered cattle across Côte d’Ivoire (K = 4) (see Additional file 1: Fig. S4)

Fig. 5

Boxplots of diversity measures from randomly drawn schistosomes across all cattle hosts (between, “B”) and within three individual cattle hosts (within, “W1”, “W2”, “W3”) in Ferkessédougou. **Significant pairwise difference at P < 0.01; ***significant pairwise difference at P < 0.001. See Additional file 1: Table S2 for detailed statistical values

Fig. 6

Structure analysis of miracidia from live cattle and adult schistosomes from slaughtered cattle in Ferkessédougou, Côte d’Ivoire, in 2018 and 2019 (K = 3)

Fig. 7

Structure analysis of miracidia and adult schistosomes from within live and slaughtered cattle, respectively, in Ferkessédougou, Côte d’Ivoire, in 2018 and 2019 (K = 2). Individual codes are as in Table 5

Fig. 8

Scatterplot of the first two components of discriminant analysis of principal components (DAPC) of schistosomes from within slaughtered and live cattle hosts. Dots are individuals, circles inertia ellipses. Forty principal components were retained, representing 86.7% of the total variation in allele frequencies. Individual codes are as in Table 5