Diversity, distribution, and evolutionary history of the most studied African rodents, multimammate mice of the genus<i>Mastomys</i>: An overview after a quarter of century of using DNA sequencing

Abstract

Despite the importance of rodents as agricultural pests and reservoirs of zoonoses, the taxonomy and evolutionary history of many groups is still not sufficiently understood. The genus Mastomys (multimammate mice or rats) comprises abundant and intensively studied rodents, widespread across sub-Saharan Africa. Here, we used an extensive dataset of mitochondrial DNA markers comprising of nearly 2700 individual sequences from 30 African countries to update the information about the geographical distribution of their genetic diversity. In the next step, we sequenced complete mitogenomes, six nuclear markers, and produced anchored phylogenomic data (355 loci) and, for the first time, sufficiently resolved phylogenetic relationships among all extant Mastomys species and reconstructed their evolutionary history. The results suggest eight species of Mastomys occupying various non-forested environments. Some species are very widespread (Mastomys natalensis, Mastomys kollmannspergeri, and Mastomys erythroleucus; for the latter we provide first records from Tanzania, thus significantly extending its distribution), while others have their distribution restricted to particular geographical areas (Mastomys coucha in South African region, Mastomys awashensis in Ethiopia, and Mastomys angolensis in Angola and southern DRC) or to particular habitat, that is, wetlands in western (Mastomys huberti) or southwestern (Mastomys shortridgei) Africa. The first split separating M. angolensis (with five pairs of mammae only) from remaining multimammate taxa occurred in mid-Pliocene, but the most intensive radiation occurred in mid-Pleistocene and was likely driven by the intensification of climate oscillations. The resolved phylogeny of Mastomys will facilitate their further use as model taxa, for example, in understanding proximate mechanisms of evolution of the multimammate phenotype. Malgré l'importance des rongeurs comme ravageurs agricoles et réservoirs de zoonoses, la taxonomie et l'histoire évolutive de nombreux groupes restent largement méconnues. Le genre Mastomys (souris ou rats à mamelles multiples) comprend des rongeurs abondants et intensément étudiés, répandus dans toute l'Afrique subsaharienne. Ici, nous avons utilisé un important jeu de données comprenant près de 2700 séquences d'ADN mitochondrial provenant de 30 pays pour mettre à jour les informations sur la répartition géographique de leur diversité génétique. Nous avons également séquencé des mitogénomes complets, ainsi que six marqueurs nucléaires et produit des données phylogénomiques (355 loci). Cela nous a permis, pour la première fois, de résoudre les relations phylogénétiques entre toutes les espèces actuelles du genre, et de reconstruire son histoire évolutive. Les résultats suggèrent l’existence de huit espèces de Mastomys occupant divers environnements non boisés. Certaines espèces sont très répandues (Mastomys natalensis, Mastomys kollmannspergeri, Mastomys erythroleucus ; pour cette dernière nous montrons qu’elle est présente en Tanzanie, étendant ainsi considérablement son aire de distribution), tandis que d'autres ont une distribution restreinte à des zones géographiques particulières (Mastomys coucha dans la région sud-africaine, Mastomys awashensis en Éthiopie, Mastomys angolensis en Angola et sud de la RDC) ou à un habitat particulier (zones humides de l'ouest de l'Afrique pour Mastomys huberti ou du sud-ouest pour Mastomys shortridgei). La première scission séparant Mastomys angolensis (avec cinq paires de mamelles seulement) des autres Mastomys s'est produite au milieu du Pliocène, mais la radiation la plus importante s'est produite au milieu du Pléistocène et était probablement due à l'intensification des oscillations climatiques à cette période. La phylogénie résolue obtenue pour le genre Mastomys facilitera sont utilisation comme taxon modèle, par exemple pour comprendre les mécanismes proximaux conduisant à l'évolution du phénotype multimammelles. Figure S1. Maximum likelihood tree of 1169 CYTB haplotypes. Figure S2. Bayesian species tree of Mastomys based on 355 anchored phylogenomic loci. Table S1. Description of the data set, including information about data sources, GenBank accession numbers, inclusion of sequences in particular analyses, and sampling information of the individuals. Table S2. Primers used for Sanger sequencing. Table S3. Details of PCR protocols. Data S1. Complete CYTB alignment. Data S2. Alignment of CYTB haplotypes for ML tree inference in RAxML. Data S3. CYTB haplotypes used for haplotype network analyses. Data S4. Codon-position partitioning of CYTB in RAxML format. Data S5. Subset of 60 CYTB sequences for ML tree inference in RAxML. Data S6. Subset of 60 CYTB sequences for Bayesian tree inference in MrBayes (including a block of MrBayes commands). Data S7. Initial partitioning of mtDNA, subjected to model selection in IQ-TREE. Data S8. Final partitioning of mtDNA with some partitions merged by IQ-TREE. Data S9. mtDNA alignment for ML tree inference in IQ-TREE. Data S10. mtDNA alignment for Bayesian tree inference in MrBayes (including a block of MrBayes commands). Data S11. Initial partitioning of alignment of six nuclear loci for model selection in IQ-TREE. Data S12. Final partitioning of alignment of six nuclear loci with some partitions merged by IQ-TREE. Data S13. Alignment of six nuclear loci for ML tree inference in IQ-TREE. Data S14. Input file for Bayesian species tree inference in StarBEAST2. Data S15. Control file for Bayesian species tree inference in BP&P, based on 355 anchored phylogenomic loci. Data S16. Sequence file for Bayesian species tree inference in BP&P. Data S17. Mapping file for Bayesian species tree inference in BP&P (classification of individuals to species). Data S18. Input file for divergence dating analysis in StarBEAST2, based on 56 anchored phylogenomic loci. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.

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