Biogeography of Leptospira in wild animal communities inhabiting the insular ecosystem of the western Indian Ocean islands and neighboring Africa

Abstract

Understanding the processes driving parasite assemblages is particularly important in the context of zoonotic infectious diseases. Leptospirosis is a widespread zoonotic bacterial infection caused by pathogenic species of the genus Leptospira. Despite a wide range of animal hosts, information is still lacking on the factors shaping Leptospira diversity in wild animal communities, especially in regions, such as tropical insular ecosystems, with high host species richness and complex biogeographical patterns. Using a large dataset (34 mammal species) and a multilocus approach at a regional scale, we analyzed the role of both host species diversity and geography in Leptospira genetic diversity in terrestrial small mammals (rodents, tenrecs, and shrews) and bats from 10 different islands/countries in the western Indian Ocean (WIO) and neighboring Africa. At least four Leptospira spp. (L. interrogans, L. borgpetersenii, L. kirschneri, and L. mayottensis) and several yet-unidentified genetic clades contributed to a remarkable regional Leptospira diversity, which was generally related to the local occurrence of the host species rather than the geography. In addition, the genetic structure patterns varied between Leptospira spp., suggesting different evolutionary histories in the region, which might reflect both in situ diversification of native mammals (for L. borgpetersenii) and the more recent introduction of non-native host species (for L. interrogans). Our data also suggested that host shifts occurred between bats and rodents, but further investigations are needed to determine how host ecology may influence these events.

Fig. 1. Diversity and geographic distribution of Leptospira in terrestrial small mammals and bats of the western Indian Ocean islands and neighboring Africa.

a Map of the sample locations. b Schematic representation of the Leptospira phylogenetic relationships based on the maximum-likelihood secY and rrs2 phylogenetic trees (details in Figures S1 and S2). Circle sizes are proportional to the number of samples included for each branch. Colors within the pie charts refer to the different countries as shown on the map. Samples denoted by an asterisk (*) refer to the sequences that could not be assigned to any clade

Fig. 2. Comparison of Leptospira haplotype diversity (± standard error, se) among the host groups and locations in the western Indian Ocean islands and neighboring Africa.

“tsm” refers to terrestrial small mammals. “MAU”=Mauritius, “RUN”=La Réunion, “MAY”=Mayotte, “SA” = South Africa, “TANZ” = Tanzania, “MADA” = Madagascar, “COM” = Union of the Comoros. Letters a–c above the bars refer to significantly different averages based upon a Tukey HSD test and “ns” = non-significant. Bars can have more than one letter to reflect the “overlap” between them

Fig. 3. Leptospira–host associations in the western Indian Ocean islands and neighboring Africa based on a Bayesian multilocus phylogenetic analysis.

The genetic clades identified in Fig. 1 are shown in the gray circle, and the major genetic groups within these clades (squares, numbers 1 to 12) are highlighted by dashed boxes. Animal silhouettes represent host groups. Sequences from the samples specific to this study are in black and coded with the sample ID, geographic location, and host species/genus. Colored circles at the tip of the branches correspond to the geographic locations as shown in Fig. 1. Reference samples are in gray and are coded as follow: Li = L. interrogans, Lk = L. kirschneri, and Lb = L. borgpetersenii (see Table S1 for details). Posterior probabilities higher than 80% are represented by white circles at the nodes. Clade C was not included (refer to Results section for more information)