Evidence brief: Genetic structure of Rattus rattus populations in an endemic plague focus in Madagascar: Implications for rodent surveillance and management

Abstract

Plague remains a major public health concern in Madagascar. In the Central Highlands, where the disease is still endemic, the black rat (Rattus rattus) is the main reservoir of the causative agent Yersinia pestis. Understanding its population dynamics and structure is therefore crucial to inform control strategies, as dispersal may greatly limit the effectiveness of local interventions during outbreaks. In this context, our study investigates the genetic structure of R. rattus populations at a fine geographical scale and across two different years.

Sampling was conducted in six villages of the Azobenzene district, both inside houses and in habitat outside villages. A total of 480 individuals, captured in March – May 2019 and 2020, were genotyped at 18 microsatellite loci. Our results showed that genetic diversity levels were relatively similar among villages and years. However, subpopulations living outside villages displayed significantly higher genetic diversity and lower genetic differentiation levels than those from inside houses, indicating larger effective population sizes outside villages in the cultivated habitats. These findings suggest more restricted movement among rat subpopulations from the houses, and greater connectivity among subpopulations living outside villages. However, overall genetic differentiation was rather low, suggesting extensive dispersal of rats at the scale of the district, facilitating rapid recolonization after local control efforts.

Because of the recolonization problem, an integrated approach combining flea control inside houses together with measures to reduce human-rodent contact would thus appear more appropriate than rodent control only to limit plague transmission.

Introduction

Plague, though often perceived as a disease of the past, continues to pose serious public health challenges in certain regions of the world, particularly in Africa [1]. This zoonosis, caused by the bacterium Yersinia pestis, persists in natural foci. It affects a large variety of mammals, including rodents that act as reservoirs, while their fleas are vectors [2,3]. Because the pathogen circulates among many wild reservoir populations [4], plague cannot be eradicated [1]. Human outbreaks typically occur within or near these natural foci, and their occurrence is partly related to the spatio-temporal dynamics of the reservoirs and vectors, and notably of commensal rodents and their fleas living in close contact with humans [5–7]. Understanding these dynamics is therefore critical for improving surveillance and anticipating epidemic outbreaks on the one hand, and for implementing early effective control strategies on the other hand [8].

Madagascar is one of the major plague foci, with up to 80% of human plague cases reported worldwide annually [9]. The disease was introduced on the island over a century ago via maritime transports [10], and it rapidly moved to and became endemic in the Central Highlands, typically at elevation above 800 m [11]. In rural areas of the highlands, the black rat (Rattus rattus) is the main reservoir of Y. pestis, and occurs in villages and their surrounding environments [11]. Habitats inside houses and outside villages constitute distinct ecological contexts for rat populations, characterized by contrasting demographic dynamics: reproduction is continuous and relatively stable inside houses, whereas marked seasonal fluctuations occur outdoors [12]. The habitats are also associated with distinct flea assemblages [6,13]: Xenopsylla cheopis, a cosmopolitan flea, is found inside houses, whereas Synopsyllus fonquerniei, an endemic species, is mainly found outdoors. Rats sampled outdoors exhibit higher plague seroprevalence than those captured inside houses, suggesting potential differences in the transmission dynamics of Y. pestis [14].