Phylogeography of the introduced species Rattus rattus in the western Indian Ocean, with special emphasis on the colonization history of Madagascar

Abstract

Aim To describe the phylogeographic patterns of the black rat, Rattus rattus, from islands in the western Indian Ocean where the species has been introduced (Madagascar and the neighbouring islands of Réunion, Mayotte and Grande Comore), in comparison with the postulated source area (India).Location Western Indian Ocean: India, Arabian Peninsula, East Africa and the islands of Madagascar, Réunion, Grande Comore and Mayotte.Methods Mitochondrial DNA (cytochrome b, tRNA and D-loop, 1762 bp) was sequenced for 71 individuals from 11 countries in the western Indian Ocean. A partial D-loop (419 bp) was also sequenced for eight populations from Madagascar (97 individuals), which were analysed in addition to six previously published populations from southern Madagascar. ResultsHaplotypes from India and the Arabian Peninsula occupied a basal position in the phylogenetic tree, whereas those from islands were distributed in different monophyletic clusters: Madagascar grouped with Mayotte, while Réunion and Grand Comore were present in two other separate groups. The only exception was one individual from Madagascar (out of 190) carrying a haplotype that clustered with those from Réunion and South Africa. 'Isolation with migration' simulations favoured a model with no recurrent migration between Oman and Madagascar. Mismatch distribution analyses dated the expansion of Malagasy populations on a time-scale compatible with human colonization history. Higher haplotype diversity and older expansion times were found on the east coast of Madagascar compared with the central highlands.Main conclusions Phylogeographic patterns supported the hypothesis of human-mediated colonization of R. rattus from source populations in either the native area (India) or anciently colonized regions (the Arabian Peninsula) to islands of the western Indian Ocean. Despite their proximity, each island has a distinct colonization history. Independent colonization events may have occurred simultaneously in Madagascar and Grande Comore, whereas Mayotte would have been colonized from Madagascar. Réunion was colonized independently, presumably from Europe. Malagasy populations may have originated from a single successful colonization event, followed by rapid expansion, first in coastal zones and then in the central highlands. The congruence of the observed phylogeographic pattern with human colonization events and pathways supports the potential relevance of the black rat in tracing human history.

Discovery of hantavirus circulating among Rattus rattus in French Mayotte island, Indian Ocean

“…This analysis showed that MAYOV clusters within the Thailand hantavirus clade closer to the isolates circulating in the Indian Ocean, South-East Asia (Hugot et al, 2006;Plyusnina et al, 2009;Johansson et al, 2010) and Madagascar (Reynes et al, 2014), rather than the Murinae-associated hantaviruses circulating in continental Africa (Klempa et al, 2006(Klempa et al, , 2012Witkowski et al, 2014). The data suggested that both MAYOV and Anjozorobe virus, the closest variant within the Thailand hantavirus clade, may have resulted from a westward expansion of an ancestral South-East Asian hantavirus introduced with R. rattus (Cheke & Hume, 2008;Tollenaere et al, 2010). Pairwise sequence identities between their coding regions, calculated with the BLASTN tool available online at http://blast.ncbi.nlm.nih.gov/Blast.cgi, were 91/99 % (nucleotide/amino acid identity) for the S segment, 90-91/ 97-98 % (nucleotide/amino acid identity) for the M segment (for ATD49 and AT261 Anjozorobe virus strains, respectively) and 90/99 % (nucleotide/amino acid identity) for the L segment.…”

Similarities in Leptospira Serogroup and Species Distribution in Animals and Humans in the Indian Ocean Island of Mayotte

“…36,37 Tollenaere and others 38 showed that Mayotte presents (at least) three genetic variants of R. rattus that are very similar to Malagasy R. rattus genotypes but different from those of East Africa. Moreover, some Leptospira strains reported in Mayotte have previously been described in East Africa 3,39,40 : This may be indicative of a two-step colonization pattern: Mayotte was first colonized by the East African R. rattus carrying East-African leptospiral strains, but significant migrations from Madagascar occurred later.…”

“…The Malagasy black rats could have driven out earlier East African occupants. 38 Consequently, Leptospira species first arrived with the East African R. rattus, and then may have infected introduced Malagasy black rats. The actual strains circulating in Mayotte might result from a genetic selection pressure, a selection by the hosts, and possibly DNA recombination events.…”

Where did the rats of Big South Cape Island come from?

“…Haplotype 1 has a world-wide distribution, including Antilles, Britain, Europe, French Polynesia, Guadeloupe, Mediterranean Basin, New Guinea, New Zealand, Polynesia, West Africa, and the USA (Robins et al 2007;Nilsson et al 2010;Tollenaere et al 2010;Colangelo et al 2015). It is common in New Zealand, but we did not find it on Stewart Island.…”

“…Our analysis is possible due to the availability of rat samples from the island which are both contemporary (just prior to the eradication; Harper & Rutherford 2016) and historical (just after the invasion; Te Papa Museum specimens). Analysis of the hypervariable region of mitochondrial DNA, known as the D-loop, allows a broad-scale assessment of population differences, and matches recent approaches used in studies of the ship rats of Madagascar (Hingston et al 2005;Tollenaere et al 2010). By comparing the D-loop signature of rats from Big South Cape Island with that of rats from surrounding locations, which have previously been hypothesised as potential sources for the invasion (Table 1), we attempt to resolve the question, "where did the rats on Big South Cape Island come from?"…”