The phylogeny of the African wood mice (Muridae, Hylomyscus) based on complete mitochondrial genomes and five nuclear genes reveals their evolutionary history and undescribed diversity

Highlights

• Mitochondrial genomes and nuclear genes are used to infer the evolutionary history of the genus Hylomyscus.

• The six species groups defined on morphological grounds are monophyletic.

• There are a high number of cryptic species.

• Diversification after the end of the Miocene tightly linked to the history of the African forest.

Abstract

Wood mice of the genus Hylomyscus, are small-sized rodents widely distributed in lowland and montane rainforests in tropical Africa, where they can be locally abundant. Recent morphological and molecular studies have increased the number of recognized species from 8 to 18 during the last 15 years. We used complete mitochondrial genomes and five nuclear genes to infer the number of candidate species within this genus and depict its evolutionary history. In terms of gene sampling and geographical and taxonomic coverage, this is the most comprehensive review of the genus Hylomyscus to date. The six species groups (aeta, alleni, anselli, baeri, denniae and parvus) defined on morphological grounds are monophyletic. Species delimitation analyses highlight undescribed diversity within this genus: perhaps up to 10 taxa need description or elevation from synonymy, pending review of type specimens. Our divergence dating and biogeographical analyses show that diversification of the genus occurred after the end of the Miocene and is closely linked to the history of the African forest. The formation of the Rift Valley combined with the declining global temperatures during the Late Miocene caused the fragmentation of the forests and explains the first split between the denniae group and remaining lineages. Subsequently, periods of increased climatic instability during Plio-Pleistocene probably resulted in elevated diversification in both lowland and montane forest taxa.

Introduction

Wood mice of the genus Hylomyscus Thomas, 1926, are small-sized rodents belonging to the family Muridae (Wilson et al., 2017). They are distributed in lowland and montane rainforests in tropical Africa, where they can be locally abundant (Happold, 2013, Nicolas and Colyn, 2003, Rosevear, 1969). Morphological and molecular data support the monophyly of the genus (Lecompte et al., 2008, Lecompte et al., 2002a, Lecompte et al., 2002b, Nicolas et al., 2006, Nicolas et al., 2012) and its placement within the Praomyini tribe, with the genus Heimyscus as its nearest relative (Aghova et al., 2018, Lecompte et al., 2008, Schenk et al., 2013, Steppan and Schenk, 2017). Based on external and craniodental morphology, Hylomyscus species were separated into six species groups: aeta, alleni, anselli, baeri, denniae and parvus (Carleton et al., 2006). Within these groups, individual species are morphologically similar and, as a result, the taxonomic status of many populations remains a subject of debate (Carleton et al., 2015, Robbins et al., 1980, Rosevear, 1969, Rosevear, 1966). From just eight species recognized by Musser and Carleton (2005), recent morphological, morphometric and molecular studies have increased the number of recognized species to 18 (Carleton et al., 2015, Carleton et al., 2006, Carleton and Stanley, 2005, Nicolas et al., 2010, Nicolas et al., 2006, Nicolas et al., 2008b, Wilson et al., 2017), and more species surely await description (Nicolas et al., 2006, Nicolas et al., 2012, Olteanu et al., 2013).

The baeri group is composed of a single West African lowland species, H. baeri. The aeta group contains two species (Wilson et al., 2017): H. aeta (found both in lowland and montane forests of Central Africa) and H. grandis (endemic to montane forest of Mt Oku in Cameroon). The taxonomy of H. aeta is still unclear and it may represent a species complex: strong phylogeographic structure was observed within this species and at least one cryptic species has been reported, but not yet described within it (Kennis, 2012, Nicolas et al., 2006.

Nicolas et al., 2012, Olteanu et al., 2013). The parvus group is currently considered to contain only one lowland species from Central Africa (Wilson et al., 2017), but molecular studies suggest the presence of several cryptic species within it, not yet formally described (Nicolas et al., 2006, Nicolas et al., 2012, Olteanu et al., 2013). The alleni group is widely distributed in West and Central Africa lowland forest and includes six to seven nominal species (Monadjem et al., 2015, Wilson et al., 2017): H. alleni, H. stella, H. walterverheyeni, H. simus, H. pamfi, H. carillus and H. kaimosae. In most revisions of the genus H. kaimosae is considered as a synonym of H. stella, but in the last revision Wilson et al. (2017) considered it as a species based on the molecular data of Nicolas et al., 2006, Nicolas et al., 2012. However, the specimens named kaimosae in the study of Nicolas et al., 2006, Nicolas et al., 2012 were misidentified and corresponds to H. arcimontensis. The alleni group has a complicated taxonomic history because the holotype of alleni is a juvenile specimen with immature dentition and imprecise geographical origin, which compromises the utility of the species description and has lead several authors to consider this species as essentially unidentifiable (Rosevear, 1969). At least two cryptic species have been reported, but not yet described, within the alleni group, and H. simus probably represents a complex of species (Nicolas et al., 2006, Nicolas et al., 2012, Olteanu et al., 2013). The denniae group is composed of three East African allopatric montane forest specialists: H. denniae (Ruwenzori Mts), H. endorobae (Kenyan Highlands) and H. vulcanorum (central and southern Albertine Rift). Lastly, the anselli group is composed of four allopatric montane forest species: H. anselli (Zambia), H. arcimontensis (Tanzania, Malawi), H. heinrichorum (Angola) and H. kerbispeterhansi (Kenya). Four new species are being described within this group (Kerbis Peterhans et al., in press).

No phylogenetic study of the genus including all currently recognized species is available. Such a study would allow us to test the robustness of each species group delimited by morphology, and to better assess the total number of Hylomyscus species. This is important not only for general knowledge of systematics, taxonomy and the distribution of biodiversity, but also for ecological and virological studies. Hylomyscus is often among the most abundant members of the rodent communities in tropical African forest (Denys et al., 2009, Duplantier, 1989, Kennis, 2012, Nicolas and Colyn, 2003, Olayemi and Akinpelu, 2008) and it is known to carry several hantaviruses (Klempa et al., 2006, Sudi et al., 2018, Tesikova et al., 2017) and arenaviruses (Coulibaly-N'Golo et al., 2011, Olayemi et al., 2016), i.e. virus groups potentially harmful also to humans. Because it contains both lowland and montane forest specialists, the genus is widely distributed in tropical Africa, and an improved knowledge of its evolutionary history is key for our understanding of the dynamics of African rainforests.

In this study we analyze the most comprehensive genetic dataset of the genus Hylomyscus to date including both complete mitogenomes and five nuclear genes. This allows us to 1) clarify its systematics and taxonomy, and 2) investigate the evolutionary history of the genus, particularly the factors shaping its genetic diversity and geographical distribution.