Genetic variation of the most abundant forest‐dwelling rodents in Central Africa (Praomys jacksoni complex): Evidence for Pleistocene refugia in both montane and lowland forests

Abstract

Aim We investigate the Plio‐Pleistocene evolutionary history of one of the most abundant rodents in Afrotropical forests. Specifically, we ask how their diversification was influenced by climate change, topography and major rivers. Location Tropical Africa: Lower Guinea (including Cameroon volcanic line; CVL), Congolia, Albertine Rift (AR), Kenyan highlands (KH). Taxon Murine rodents of the Praomys jacksoni complex. Methods We used 849 genotyped individuals to describe the overall diversity and spatial genetic structure across a majority of their known distribution area. The combination of one mitochondrial and three nuclear markers was used to infer dated phylogenies using Bayesian and maximum likelihood approaches. Genetic structure was further assessed by multispecies coalescent species delimitation. Current and past distributions of particular taxa were predicted using environmental niche modelling. Results The complex is composed of five major genetic clades (proposed species). Two of them are restricted to specific habitat types (either montane forests of AR or wetlands in lowland forests along the Congo River), three others have wide geographic distributions and lower levels of ecological specialization. The earliest divergence is dated to the Plio‐Pleistocene boundary and is in accordance with the separation of AR forests and Guineo‐Congolian forests. Further diversification of the complex is associated with Pleistocene climate changes. Relatively stable refugia of suitable climatic conditions were identified in lowland Congolia (for two species currently distributed only in lowland forests) as well as in montane forests of CVL, AR, KH (playing the role of reservoirs of diversity). Large rivers, especially the Congo River, are important barriers to gene flow for most taxa, but probably were not the primary cause of differentiation. Main conclusions The evolutionary history of the complex was primarily affected by Pleistocene climate changes and diversification in forest refugia. There is little support for ecological parapatric speciation or the riverine barrier hypothesis.

Rodent species composition, relative abundance, and habitat association in the Mabira Central Forest Reserve, Uganda

“…H. stella appears to be a forest dweller, while others are more plastic in habitat use, such as L. stanleyi. The current findings are in agreement with earlier studies (Stanley & Foley 2008, Monadjem et al 2015, Mizerovská et al 2019. Basuta & Kasenene (1987) pointed out that some rodent species, such as P. jacksoni, are habitat specific and are mainly associated with closed forest habitats.…”

“…P. jacksoni occurs in a variety of forested habitats including primary and secondary forest (Monadjem et al 2015). The current findings concur with previous studies carried out in Uganda and Tanzania (Stanley & Foley 2008, Happold et al 2013, Mizerovská et al 2019).…”

Tectonics, climate and the diversification of the tropical African terrestrial flora and fauna

“…The exceptional and unique biodiversity of the ancient Eastern Arc Mountains of Tanzania and Kenya (Burgess et al ., 2007) was suggested to be driven by long‐term persistence of montane forests together with recurrent connections and disconnections between montane isolates since the Oligocene–Miocene (Lovett, 1993; Lovett et al ., 2005; Fjeldså & Bowie, 2008; Voelker et al ., 2010; Loader et al ., 2014). This mechanism was inferred for several clades such as songbirds (Passeriformes) (Bowie et al ., 2004; Fjeldså & Bowie, 2008; Voelker et al ., 2010; Fjeldså, Bowie, & Rahbek, 2012), rodents (Mizerovská et al ., 2019; Nicolas et al ., 2020), forest‐restricted chameleons (Tolley et al ., 2011; Ceccarelli et al ., 2014), brevicipitid frogs (Loader et al ., 2014), various insect groups such as Orthoptera (Voje et al ., 2009; Hemp et al ., 2010) and weevils (Grebennikov, 2017), and plants (Dimitrov et al ., 2012). Evidence suggests that most montane sister species in the Eastern Arc Mountains are allopatric but located on different montane areas, refuting in situ speciation (Hemp et al ., 2010; Voelker et al ., 2010; Missoup et al ., 2012; Ceccarelli et al ., 2014; Taylor et al ., 2014).…”

“…Rivers were not found to be important barriers within certain frog species complexes [ Hyperolius (Bell et al ., 2017); Chiromantis rufescens (Leaché et al ., 2019)] or in the common pangolin Manis tricuspis (Gaubert et al ., 2018). By contrast, rivers were shown to be intra‐species barriers in several other animal groups including insects (Simard et al ., 2009), mammals (Nicolas et al ., 2011; Guschanski et al ., 2013; Jacquet et al ., 2014; Huntley et al ., 2019; Mizerovská et al ., 2019), reptiles (Leaché & Fujita, 2010) and certain bird clades (Huntley et al ., 2018, 2019).…”

Late Quaternary habitat suitability models for chimpanzees (Pan troglodytes) since the Last Interglacial (120,000 BP)

“…Although initially these refugia were identified using species distributional patterns for birds and plants, an increasing number of recent studies have utilized molecular data to infer the geographical location of intraspecific diversity (i.e lineages or populations within species) across the Afrotropics. These studies have demonstrated contemporary phylogeographic patterns that suggest broadly concordant historical refugia in mammals (Bohoussou et al, 2015;Bryja, Mikula, Patzen, et al, 2014;Bryja, Mikula, Šumbera, et al, 2014;Bryja et al, 2017;Gaubert et al, 2016;Mizerovská et al, 2019;Nicolas et al, 2011), including other primates, (Anthony et al, 2014;Clifford et al, 2004;Gonder et al, 2011;Pozzi, 2016;Telfer et al, 2003), amphibians (Charles et al, 2018Leaché et al, 2019;Portik et al, 2017), and plants (Faye et al, 2016;Hardy et al, 2013;Piñeiro, Dauby, Kaymak, & Hardy, 2017;Piñeiro et al, 2019), albeit with some differences between species due to different ecological characteristics and idiosyncratic responses to climatic changes (Lowe, Harris, Dormontt, & Dawson, 2010).…”