Historical biogeography, systematics, and integrative taxonomy of the non-Ethiopian speckled pelage brush-furred rats (Lophuromys flavopunctatus group)

Zhong-Zheng Chen,Leonid A. Lavrenchenko,Xue-Long Jiang,Josef Bryja,Simon Musila,Julian Kerbis Peterhans,Noé U. de la Sancha,Erik Verheyen,Benjamin Dudu Akaibe,Kenneth Otieno Onditi,Frederik Van de Perre,Terrence C. Demos

doi:10.1186/s12862-021-01813-w

Abstract

BackgroundThe speckled-pelage brush-furred rats (Lophuromys flavopunctatus group) have been difficult to define given conflicting genetic, morphological, and distributional records that combine to obscure meaningful accounts of its taxonomic diversity and evolution. In this study, we inferred the systematics, phylogeography, and evolutionary history of the L. flavopunctatus group using maximum likelihood and Bayesian phylogenetic inference, divergence times, historical biogeographic reconstruction, and morphometric discriminant tests. We compiled comprehensive datasets of three loci (two mitochondrial [mtDNA] and one nuclear) and two morphometric datasets (linear and geometric) from across the known range of the genus Lophuromys.ResultsThe mtDNA phylogeny supported the division of the genus Lophuromys into three primary groups with nearly equidistant pairwise differentiation: one group corresponding to the subgenus Kivumys (Kivumys group) and two groups corresponding to the subgenus Lophuromys (L. sikapusi group and L. flavopunctatus group). The L. flavopunctatus group comprised the speckled-pelage brush-furred Lophuromys endemic to Ethiopia (Ethiopian L. flavopunctatus members [ETHFLAVO]) and the non-Ethiopian ones (non-Ethiopian L. flavopunctatus members [NONETHFLAVO]) in deeply nested relationships. There were distinctly geographically structured mtDNA clades among the NONETHFLAVO, which were incongruous with the nuclear tree where several clades were unresolved. The morphometric datasets did not systematically assign samples to meaningful taxonomic units or agree with the mtDNA clades. The divergence dating and ancestral range reconstructions showed the NONETHFLAVO colonized the current ranges over two independent dispersal events out of Ethiopia in the early Pleistocene.ConclusionThe phylogenetic associations and divergence times of the L. flavopunctatus group support the hypothesis that paleoclimatic impacts and ecosystem refugia during the Pleistocene impacted the evolutionary radiation of these rodents. The overlap in craniodental variation between distinct mtDNA clades among the NONETHFLAVO suggests unraveling underlying ecomorphological drivers is key to reconciling taxonomically informative morphological characters. The genus Lophuromys requires a taxonomic reassessment based on extensive genomic evidence to elucidate the patterns and impacts of genetic isolation at clade contact zones.

Highlights

The speckled-pelage brush-furred rats (Lophuromys flavopunctatus group) have been difficult to define given conflicting genetic, morphological, and distributional records that combine to obscure meaningful accounts of its taxonomic diversity and evolution
The genus Lophuromys bifurcated into two main groups that corresponded to the current subgeneric divisions—Lophuromys and Kivumys (Fig. 1, Additional file 1: Fig. S1)
The major clades in the Kivumys group and L. sikapusi group corresponded to currently recognized species except for a single clade in the sikapusi group (L. sp.1 in Fig. 1 and Additional file 1: Fig. S1) and were assigned names based on the corresponding identifications in literature

Summary

Introduction

The speckled-pelage brush-furred rats (Lophuromys flavopunctatus group) have been difficult to define given conflicting genetic, morphological, and distributional records that combine to obscure meaningful accounts of its taxonomic diversity and evolution. New developments in integrative morphologic, phylogeographic, genetic, and ecological analysis have increasingly complemented traditional reliance on morphological evidence to resolve taxonomic limits [2]. This ‘integrative systematics’ approach is most effective when delimiting cryptic species [3]. Between the two speckledpelage groups—L. flavopunctatus group and L. aquilus group—species are classified based on morphological affinities It is not clear how morphology (external body features, pelage color, craniodental characters) explicitly delimits species in the literature [6, 12]. There is a need to clearly define whether and how pelage coloration and morphological affinities relate to phylogenetic relationships in the genus Lophuromys. We use ‘Ethiopian L. flavopunctatus members [ETHFLAVO]’ to refer to the Lophuromys taxa endemic to the Ethiopian Highlands, the ‘non-Ethiopian L. flavopunctatus members [NONETHFLAVO]’ to refer to the remaining Lophuromys taxa not belonging to the L. sikapusi group or the Kivumys group, while the ‘L. flavopunctatus group’ is used to combine ETHFLAVO and NONETHFLAVO

Methods

Results

Discussion

Conclusion