Emilie Lecompte

Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily.

BackgroundWithin the subfamily Murinae, African murines represent 25% of species biodiversity, making this group ideal for detailed studies of the patterns and timing of diversification of the African endemic fauna and its relationships with Asia. Here we report the results of phylogenetic analyses of the endemic African murines through a broad sampling of murine diversity from all their distribution area, based on the mitochondrial cytochrome b gene and the two nuclear gene fragments (IRBP exon 1 and GHR).ResultsA combined analysis of one mitochondrial and two nuclear gene sequences consistently identified and robustly supported ten primary lineages within Murinae. We propose to formalize a new tribal arrangement within the Murinae that reflects this phylogeny. The diverse African murine assemblage includes members of five of the ten tribes and clearly derives from multiple faunal exchanges between Africa and Eurasia. Molecular dating analyses using a relaxed Bayesian molecular clock put the first colonization of Africa around 11 Mya, which is consistent with the fossil record. The main period of African murine diversification occurred later following disruption of the migration route between Africa and Asia about 7–9 Mya. A second period of interchange, dating to around 5–6.5 Mya, saw the arrival in Africa of Mus (leading to the speciose endemic Nannomys), and explains the appearance of several distinctive African lineages in the late Miocene and Pliocene fossil record of Eurasia.ConclusionOur molecular survey of Murinae, which includes the most complete sampling so far of African taxa, indicates that there were at least four separate radiations within the African region, as well as several phases of dispersal between Asia and Africa during the last 12 My. We also reconstruct the phylogenetic structure of the Murinae, and propose a new classification at tribal level for this traditionally problematic group.

Novel Hantavirus Sequences in Shrew, Guinea

To the Editor: Hantaviruses, family Bunyaviridae, have been known as causative agents of hemorrhagic fever with renal syndrome in Asia and Europe (1,2) and hantavirus cardiopulmonary syndrome in the Americas (3). Hantaviruses are spread by aerosolized rodent excreta and are strongly associated with their natural hosts, rodents of the family Muridae. Based on phylogenetic analyses, hantaviruses have been divided into 3 major groups that resemble 3 subfamilies of their natural hosts (Figure, panel A). Figure Maximum likelihood phylogenetic analysis of hantaviruses showing the phylogenetic placement of Tan826 (Tanganya virus, indicated by arrow) based on partial L segment nucleotide (A) and amino acid (B) sequences and partial S segment amino acid sequences ... Recently, we found the first indigenous African hantavirus, Sangassou virus (SANGV), in an African wood mouse (Hylomyscus simus) collected in Guinea (5). Thottapalayam virus (TPMV), isolated from an Asian house shrew (Suncus murinus) in India (6), is the only known hantavirus to be hosted by a shrew instead of a rodent (7,8). We report the recovery of hantavirus RNA of a novel sequence from a shrew, collected in Guinea, West Africa. During a study of rodentborne hemorrhagic fever viruses performed in Guinea in 2002–2004, 32 shrews of the genus Crocidura were collected and screened for hantavirus RNA by reverse transcription–PCR (5). An RNA sample designated Tan826 produced a PCR product of the expected size. The animal host was a male Crocidura theresae collected in the grassland savannah around the village Tanganya (10°00′02″N, 10°58′22″W) in January 2004. Species identification, following the taxonomic nomenclature (9), was performed on the basis of morpho-anatomical characteristics and was supported by molecular analyses. Partial L segment sequence of 412 nt was determined by cloning and sequencing of the obtained PCR product. Nucleotide sequence comparisons between Tan826 and other representatives of the genus Hantavirus showed very low sequence identity values, ranging from 67.7% (Andes virus) to 72.3% (Puumala virus). Corresponding sequences of deduced viral RNA polymerase (137 aa) showed only slightly higher similarity values of 69.3% (Tula virus) to 76.6% (SANGV). In a maximum likelihood phylogenetic tree (Figure, panel A), Tan826 did not unambiguously cluster with any of the major groups (i.e., Murinae-, Arvicolinae-, Sigmodontinae-associated viruses) and showed equal relatedness to all 3 groups. This exceptional position of the Tan826 sequence within the tree is consistent with its detection in a shrew instead of a rodent host. Because the sequence is only distantly related to other hantaviruses, sequences from additional members of the Bunyaviridae family were analyzed. Despite use of a suboptimal dataset of very divergent and short sequences, the phylogenetic placement of Tan862 within the genus Hantavirus could be clearly demonstrated (Figure, panel B). Furthermore, a partial S segment sequence (442 nt, 147 aa of the putative nucleoprotein) was determined to compare Tan826 directly with the shrew-associated TPMV (for which only an S segment sequence was available in GenBank). Rather unexpectedly, the Tan826 sequence showed the lowest similarity to TPMV: 47.5% on nt level and 39.4% on aa level. The identity values to other Hantavirus members were also extremely low, 52.2% (Sin Nombre virus) to 62.1% (SANGV) on nt level and 50.6% (Andes virus) to 56.7% (Hantaan, Dobrava virus) on aa level. Corresponding aa sequences were then used for phylogenetic analysis to reduce problems derived from higher sequence diversities. In the resulting evolutionary tree, Tan826 and TPMV did not join any of the 3 major groups but also did not cluster together (Figure, panel C). Our attempts to obtain more sequence data were hampered by the unique nature of the Tan826 virus sequence, which makes it difficult to design additional effective PCR primers, as well as by the limited amount of available biological material from the shrew. Nevertheless, the sequence and phylogenetic analyses of the 2 partial sequences strongly indicate that they represent a novel hantavirus. The amino acid sequences are highly divergent (≈25%–50%) from those of other hantaviruses and in phylogenetic trees; the Tan826 virus sequence appeared approximately equally related to those of all other hantaviruses. We propose to name the putative new species Tanganya virus (TGNV), after the locality where it was detected. Detecting the virus in 1 of 32 Crocidura shrews, 15 of them C. theresae, is not sufficient to define C. theresae as a reservoir animal of this novel virus. However, the unique position of TGNV in evolutionary trees supports the idea that a shrew instead of a rodent is the natural host of TGNV. Therefore, it is rather surprising that TGNV did not form a monophyletic group with TPMV. Before this observation becomes either a challenge or support for the hantavirus–host coevolution concept, more extensive sequence data (for comprehensive phylogenetic analysis) and epizootiologic studies (to confirm the natural hosts of both viruses) are necessary. TGNV represents, after the recently described SANGV (5), a second hantavirus from Africa. Its low sequence similarity to other hantaviruses should make this virus serologically distinct from other hantaviruses, as shown for TPMV (10). Therefore, human infections by TGNV might be missed when using antibody detection assays based on antigens from conventional hantaviruses.

Mastomys natalensis and Lassa fever, West Africa.

PCR screening of 1,482 murid rodents from 13 genera caught in 18 different localities of Guinea, West Africa, showed Lassa virus infection only in molecularly typed Mastomys natalensis. Distribution of this rodent and relative abundance compared with M. erythroleucus correlates geographically with Lassa virus seroprevalence in humans.

Cytochrome b-based phylogeny of the Praomys group (Rodentia, Murinae): a new African radiation?

Complete cytochrome b gene sequences allows, for the first time, establishing a nearly complete phylogeny among the Praomys group sensu lato. The genera Praomys, Mastomys and Stenocephalemys appear paraphyletic. Myomys is polyphyletic and this genus name probably needs to be restricted to its type species, M. verreauxii. The genera Zelotomys and Colomys appear as sister groups. Mastomys pernanus and Malacomys verschureni nest within the Praomys group, but their generic assignation must be further clarified. The genus Heimyscus appears closest to Praomys than to Hylomyscus. The different lineages probably result from an adaptive radiation at the end of the Miocene.

Comparative phylogeography of two sibling species of forest‐dwelling rodent (Praomys rostratus and P. tullbergi) in West Africa: different reactions to past forest fragmentation

Two sibling species of the rodent genus Praomys occur in West African forests: P. tullbergi and P. rostratus. By sampling across their geographical ranges (459 individuals from 77 localities), we test the hypothesis that climatic oscillations during the Quaternary made an impact on the observed pattern of cytochrome b sequence variation. We show that, although these two species have parapatric geographical distributions, their phylogeographical histories are dissimilar, which could be related to their distinct ecological requirements. Since the arid phases of the Pleistocene were characterized by isolated forest patches, and intervening wetter periods by forest expansion, these changes in forest cover may be the common mechanism responsible for the observed phylogeographical patterns in both of these species. For example, in both species, most clades had either allopatric or parapatric geographical distributions; however, genetic diversity was much lower in P. tullbergi than in P. rostratus. The genetic pattern of P. tullbergi fits the refuge hypothesis, indicating that a very small number of populations survived in distinct forest blocks during the arid phases, then expanded again with forest recovery. In contrast, a number of populations of P. rostratus appear to have survived during the dry periods in more fragmented forest habitats, with varying levels of gene flow between these patches depending on climatic conditions and forest extent. In addition, historical variations of the West African hydrographic network could also have contributed to the pattern of genetic differentiation observed in both species.

Reproductive characteristics of Mastomys natalensis and Lassa virus prevalence in Guinea, West Africa.

We recently reported increased prevalence of Lassa virus (LASV) infection in Mastomys natalensis during the rainy season in Guinea, West Africa. Here, the association of LASV prevalence with fecundity, fertility, and the age structure of the rodent population was analyzed using data from the previous study. The animals reproduced throughout the year, but highest fecundity was observed during the rainy season. Accordingly, the rodent population was aged at the beginning and young at the end of the rainy season. Lassa virus infection was observed in all age groups, including the very young, which is compatible with vertical transmission. However, since the prevalence of infection showed a trend with increasing age in the younger age groups, horizontal transmission by yet unknown mechanisms may also play a role in LASV transmission. Multivariate analysis did not show an association of LASV prevalence with any demographic variable studied. Rodent behavior influencing virus transmissibility and contaminated environment may therefore be responsible for spatial and seasonal variations in LASV prevalence in M. natalensis.

The impact of human conflict on the genetics of Mastomys natalensis and Lassa virus in West Africa.

Environmental changes have been shown to play an important role in the emergence of new human diseases of zoonotic origin. The contribution of social factors to their spread, especially conflicts followed by mass movement of populations, has not been extensively investigated. Here we reveal the effects of civil war on the phylogeography of a zoonotic emerging infectious disease by concomitantly studying the population structure, evolution and demography of Lassa virus and its natural reservoir, the rodent Mastomys natalensis, in Guinea, West Africa. Analysis of nucleoprotein gene sequences enabled us to reconstruct the evolutionary history of Lassa virus, which appeared 750 to 900 years ago in Nigeria and only recently spread across western Africa (170 years ago). Bayesian demographic inferences revealed that both the host and the virus populations have gone recently through severe genetic bottlenecks. The timing of these events matches civil war-related mass movements of refugees and accompanying environmental degradation. Forest and habitat destruction and human predation of the natural reservoir are likely explanations for the sharp decline observed in the rodent populations, the consequent virus population decline, and the coincident increased incidence of Lassa fever in these regions. Interestingly, we were also able to detect a similar pattern in Nigeria coinciding with the Biafra war. Our findings show that anthropogenic factors may profoundly impact the population genetics of a virus and its reservoir within the context of an emerging infectious disease.

Community ecology of the terrestrial small mammals of Zakouma National Park, Chad

The terrestrial small mammal community of the Zakouma National Park (Chad) was assessed by live trapping in various habitats during the dry season. Nearly 3000 trap-nights yielded 505 captures of nine rodent and two shrew species, making up a representative small mammal community for the Sudanian savanna biotic zone. Murine rodents of the genusMastomys dominated, withM. erythroleucus andM. cf.kollmannspergeri occuring at similar abundances. The former was widespread and especially abundant in habitats with high tree cover. The latter was more localized, predominantly in annually flooded habitats characterized by a clay-rich soil, often withAcacia seyal as the main vegetation. Population structure differed between the two species, suggesting distinct reproductive strategies possibly linked with habitat preferences: theM. erythroleucus population comprised mainly young, immature individuals, whereasM. cf.kollmannspergeri was represented by older individuals, a significant fraction of which had already reproduced.Taterillus congicus andTatera kempi (gerbilline rodents), together withLemniscomys zebra, were mainly found in more open habitats with sand-rich soils.Arvicanthis niloticus, Acomys cf.johannis, Mus mattheyi andXerus erythropus were the other rodents captured, whereas shrews were represented byCrocidura fulvastra andSuncus sp.

Community Analysis of Muridae (Mammalia, Rodentia) Diversity in Guinea: A Special Emphasis on Mastomys Species and Lassa Fever Distributions

The Murid rodent diversity has been sampled following the 9th Meridian in the east of Guinea from the forest region to Sudanian savannas of southern Mali. This represents the first small mammals survey in North Guinea. Murid diversity patterns have been researched using correspondence analysis and faunal comparisons. A difference between southern forest communities and northern ones is observed. Mastomys natalensis is found only in houses in southern Guinea while in the north it is found in all sampled habitats. M. erythroleucus is absent from the forest zone, but found from the ecotone forest-savanna to the north, and it seems that this species never enter houses. Implications for Lassa fever transmission are discussed.