Trypanosome diversity in small mammals in Uganda and the spread of Trypanosoma lewisi to native species

Abstract

Uganda's diverse small mammalian fauna thrives due to its rich habitat diversity, which hosts a wide range of blood parasites, including trypanosomes, particularly the subgenus Herpetosoma typical for rodent hosts. We screened a total of 711 small mammals from various habitats for trypanosomes, with 253 microscopically examined blood smears and 458 tissue samples tested by nested PCR of the 18S rRNA gene. Of 51 rodent and 12 shrew species tested, microscopic screening reaches 7% overall prevalence (with four rodent species positive out of 15 and none of the shrew species out of four), while nested PCR indicated a prevalence of 13% (17 rodent and five shrew species positive out of 49 and 10, respectively). We identified 27 genotypes representing 11 trypanosome species, of which the majority (24 genotypes/9 species) belong to the Herpetosoma subgenus. Among these, we detected 15 new genotypes and two putative new species, labeled AF24 (found in Lophuromys woosnami) and AF25 (in Graphiurus murinus). Our finding of three new genotypes of the previously detected species AF01 belonging to the subgenus Ornithotrypanum in two Grammomys species and Oenomys hypoxanthus clearly indicates the consistent occurrence of this avian trypanosome in African small mammals. Additionally, in Aethomys hindei, we detected the putative new species of the subgenus Aneza. Within the T. lewisi subclade, we detected eleven genotypes, including six new; however, only the genotype AF05b from Mus and Rattus represents the invasive T. lewisi. Our study has improved our understanding of trypanosome diversity in African small mammals. The detection of T. lewisi in native small mammals expands the range of host species and highlighting the need for a broader approach to the epidemiology of T. lewisi.

Keywords: Aneza; Herpetosoma; Muridae; Ornithotrypanum; Soricidae.

Fig. 1

View into the study areas showing the main vegetation types in each survey location; note that bushed fallows are not indicated because they bordered most vegetation types as an ecotone between protected area and communities

Fig. 2

An 18S rRNA-based maximum likelihood phylogenetic reconstruction of all detected genotypes clustering into 11 phylogroups (putative species); already known genotypes are indicated by magenta, new genotypes are indicated by red (putative new species are in bold red); for details of the Trypanosoma lewisi subclade and the subgenera Ornithotrypanum and Squmatrypanum, see the individual subtrees (Supplementary figures S1, S2 and S3). Country ISO (International Organization of Standardization) alpha-3 codes and vertebrate host genera are indicated for all taxa/genotypes; asterisks mark branches with maximal statistical support (bootstrap values for maximum likelihood > 95, Bayesian posterior probabilities > 0.99); double-crossed branch is 50% of the original length; the scale bar denotes the number of substitutions per site

Fig. 3

Species accumulation curves illustrating the Trypanosoma (Herpetosoma) species richness in different habitats. The curves depict the accumulation of species richness as the sampling effort increases

Fig. 4

Host-trypanosome matrix plot illustrating the interactions between various host species and associated trypanosome genotypes detected in this study. The plot emphasizes the significant host specificity observed within most trypanosome phylogroups. The different shades in the cells of the web serve to highlight variations in the numbers of each genotype where lighter shades indicate lower values and darker shades represent higher values