Evolutionary history of the grey-faced Sengi, Rhynchocyon udzungwensis, from Tanzania: a molecular and species distribution modelling approach

Abstract

Rhynchocyon udzungwensis is a recently described and poorly understood sengi (giant elephant-shrew) endemic to two small montane forests in Southern Tanzania, and surrounded in lower forests by R. cirnei reichardi. In this study, we investigate the molecular genetic relationship between R. udzungwensis and R. c. reichardi, and the possible role that shifting species distributions in response to climate fluctuations may have played in shaping their evolutionary history. Rhynchocyon udzungwensis and R. c. reichardi individuals were sampled from five localities for genetic analyses. Three mitochondrial and two nuclear loci were used to construct species trees for delimitation and to determine whether introgression was detectable either from ancient or ongoing hybridization. All species-tree results show R. udzungwensis and R. c. reichardi as distinct lineages, though mtDNA shows evidence of introgression in some populations. Nuclear loci of each species were monophyletic, implying introgression is exclusively historical. Because we found evidence of introgression, we used distribution data and species distribution modelling for present, glacial, and interglacial climate cycles to predict how shifting species distributions may have facilitated hybridization in some populations. Though interpretations are affected by the limited range of these species, a likely scenario is that the mtDNA introgression found in eastern mid-elevation populations was facilitated by low numbers of R. udzungwensis that expanded into lowland heavily occupied R. c. reichardi areas during interglacial climate cycles. These results imply that relationships within the genus Rhynchocyon may be confounded by porous species boundaries and introgression, even if species are not currently sympatric.

Figure 1. Map of the north-eastern portion of the Udzungwa Mountains, south-central Tanzania with sampling localities.

Distribution records of the grey-faced sengi, Rhynchocyon udzungwensis, shown as white dots. The occurrence of the checkered sengi, R. cirnei reichardi, shown as black triangles. The western portion of the distribution of R. udzungwensis is in Ndundulu/Luhomero forest, and the eastern portion is in Mwanihana forest. Rhynchocyon c. reichardi’s distribution extends into the Magombera forest on the eastern plain. The five sampling sites for molecular analysis of the two species are also shown. The background layer is a topographic map (dark is lower elevation). The inset shows the location of the Udzungwa Mountains in Tanzania (left) and of the mapped area within the Udzungwa Mountains (right). Insert reprinted from under a CC BY license, with permission from A. Marshall, original copyright 2005.

Figure 2. Gene Trees and Haplotype networks.

Bayesian Gene trees of two nuclear loci (top: ENAM and vWF) and concatenated mtDNA (bottom left: ND2, D-loop region, and the ribosomal gene 12S) constructed in MrBayes. Posterior probabilities displayed for major nodes. Branch lengths proportional to genetic distance. (Bottom Right) Haplotype network of concatenated mtDNA. Each node represents one base pair change.

Figure 3. Highest probability species tree selected by all three methods (*BEAST, BPP, and BEST).

Posterior probabilities shown for each node. Both species are monophyletic for all species tree reconstructions. Branch lengths proportional to genetic distance.

Figure 4. Bayesian concordance analysis in BUCKy: Population Tree (top), Primary concordance tree (bottom).

Posterior mean concordance factors at major nodes are displayed above branches. Branches with concordance factors below 0.2 are not shown except in major nodes. The population tree shows monophyly for the two species, while the primary concordance tree shows admixture between the species and poorly supported relationships implying some level of admixture.

Figure 5. Species Distribution Models during current climate scenario (left) and wetter Last Interglacial (right; LIG).

Current sampling points used in model construction are shown. The limited distribution of R. udzungwensis is entirely contained within the suitable area for R. c. reichardi at both time points. During the LIG, the ranges for both species were predicted to occur at lower elevations in the eastern areas of the Udzungwa Mountains foothills. During this time, R. udzungwensis shifted its entire distribution eastward resulting in a loss occupancy in the western Ndundulu/Luhomero forest, a reduced range in the Mwanihana forest, and a relatively extensive distribution east of Mwanihana in the Kilombero Valley including the Magombera forest (see Fig. 1 for place names).