Co-Radiation of Leptospira and Tenrecidae (Afrotheria) on Madagascar

Abstract

Leptospirosis is a bacterial zoonosis caused by pathogenic Leptospira that are maintained in the kidney lumen of infected animals acting as reservoirs and contaminating the environment via infected urine. The investigation of leptospirosis through a One Health framework has been stimulated by notable genetic diversity of pathogenic Leptospira combined with a high infection prevalence in certain animal reservoirs. Studies of Madagascar's native mammal fauna have revealed a diversity of Leptospira with high levels of host-specificity. Native rodents, tenrecids, and bats shelter several distinct lineages and species of Leptospira, some of which have also been detected in acute human cases. Specifically, L. mayottensis, first discovered in humans on Mayotte, an island neighboring Madagascar, was subsequently identified in a few species of tenrecids on the latter island, which comprise an endemic family of small mammals. Distinct L. mayottensis lineages were identified in shrew tenrecs (Microgale cowani and Nesogale dobsoni) on Madagascar, and later in an introduced population of spiny tenrecs (Tenrec ecaudatus) on Mayotte. These findings suggest that L. mayottensis (i) has co-radiated with tenrecids on Madagascar, and (ii) has recently emerged in human populations on Mayotte following the introduction of T. ecaudatus from Madagascar. Hitherto, L. mayottensis has not been detected in spiny tenrecs on Madagascar. In the present study, we broaden the investigation of Malagasy tenrecids and test the emergence of L. mayottensis in humans as a result of the introduction of T. ecaudatus on Mayotte. We screened by PCR 55 tenrecid samples from Madagascar, including kidney tissues from 24 individual T. ecaudatus. We describe the presence of L. mayottensis in Malagasy T. ecaudatus in agreement with the aforementioned hypothesis, as well as in M. thomasi, a tenrecid species that has not been explored thus far for Leptospira carriage.

Keywords: Leptospira mayottensis; Madagascar; Mayotte; leptospirosis; microbial endemism; tenrecids.

Figure 1

Geographical context and Bayesian phylogenetic tree of Leptospira species from Mayotte (blue) and Madagascar (green) based on secY gene (482 bp). Sequences in black correspond to Leptospira species used as ingroups and outgroup (L. biflexa). The accession number is indicated for each sequence. The analysis was conducted under the HKY + I + G substitution model. Black circles at the nodes indicate posterior probabilities superior or equal to 0.90. The red stars indicate new sequences generated in the present study and were obtained from two regions on Madagascar: Anjozorobe and Makira (Commune Antsirabe-Sahatany). The map was realized using worldHires function in mapdata package [27] under the R software version 4.1.1.