The comparative phylogeography of fruit bats of the tribe Scotonycterini (Chiroptera, Pteropodidae) reveals cryptic species diversity related to African Pleistocene forest refugia

Abstract

The hypothesis of Pleistocene forest refugia was tested using comparative phylogeography of Scotonycterini, a fruit bat tribe endemic to Africa containing four species: Scotonycteris zenkeri, Casinycteris argynnis, C. campomaanensis, and C. ophiodon. Patterns of genetic structure were assessed using 105 Scotonycterini (including material from three holotypes) collected at 37 localities, and DNA sequences from the mitochondrial cytochrome b gene (1140 nt) and 12 nuclear introns (9641 nt). Phylogenetic trees and molecular dating were inferred by Bayesian methods. Multilocus analyses were performed using supermatrix, SuperTRI, and *BEAST approaches. Mitochondrial analyses reveal strong phylogeographical structure in Scotonycteris, with four divergent haplogroups (4.9-8.7%), from Upper Guinea, Cameroon, western Equatorial Africa, and eastern Democratic Republic of the Congo (DRC). In C. argynnis, we identify two mtDNA haplogroups corresponding to western and eastern Equatorial Africa (1.4-2.1%). In C. ophiodon, the mtDNA haplotypes from Cameroon and Ivory Coast differ by only 1.3%. Nuclear analyses confirm the validity of the recently described C. campomaanensis and indicate that western and eastern populations of C. argynnis are not fully isolated. All mtDNA clusters detected in Scotonycteris are found to be monophyletic based on the nuclear dataset, except in eastern DRC. In the nuclear tree, the clade from western Equatorial Africa is closely related to individuals from eastern DRC, whereas in the mitochondrial tree it appears to be the sister-group of the Cameroon clade. Migrate-n analyses support gene flow from western Equatorial Africa to eastern DRC. Molecular dating indicates that Pleistocene forest refugia have played an important role in shaping the evolution of Scotonycterini, with two phases of allopatric speciation at approximately 2.7 and 1.6 Mya, resulting from isolation in three main forest areas corresponding to Upper Guinea, Cameroon, and Equatorial Africa. Two cryptic species and two subspecies are described herein in the genus Scotonycteris. Female philopatry and male biased dispersal are supported for the smallest taxa, i.e., the three species of Scotonycteris and C. argynnis. The Congo, Ntem, and Sanaga rivers are identified as biogeographic barriers to the dispersal of Scotonycteris during interglacial periods. A greater capacity for long-distance dispersal is inferred for the largest species, C. ophiodon.

Multilocus phylogeny of the Crocidura poensis species complex (Mammalia, Eulipotyphla): Influences of the palaeoclimate on its diversification and evolution

“…The increased aridity and/or extreme environmental variability at this period could have favoured the diversification within the C. poensis species complex through a vicariance event. It is interesting to note that at more or less the same time period diversification events between West Africa and Central‐East Africa were also recorded in several other forest‐adapted small mammals (Hassanin et al., ; Nicolas et al., , ) and birds (Fuchs & Bowie, ; Fuchs, Fjeldså, & Bowie, ; Huntley & Voelker, ).…”

Comparative phylogeography of bamboo bats of the genus Tylonycteris (Chiroptera, Vespertilionidae) in Southeast Asia

“…Similarly, the nuclear distances between the two Indochinese clades of T. robustula were between 0.41 and 0.56%, which is more than twice those calculated between Indochinese individuals of T. pachypus (0-0.2%; Appendix 5) and in the range of interspecific distances found in other groups of Laurasiatheria, such as fruit bats of the tribes Myonycterini (Nesi et al 2013) and Scotonycterini (Hassanin et al 2015), or cattle and buffalo of the tribe Bovini . Although none of the nuclear markers could be sequenced for Sumatran and Bornean Tylonycteris, their high mtDNA divergence from Indochinese populations (> 5.7 % in both COI and Cytb sequences; Appendix 5) suggests they might represent distinct lineages based on nuclear markers as well.…”

“…Indeed, bat species with philopatric females generally display high geographic structure when relationships are examined with maternally inherited markers, such as the mitochondrial DNA. This pattern can disappear with biparentally inherited markers when adult males are able to disperse over long distances, allowing gene flow between otherwise isolated populations (Castella et al 2001;Hassanin et al 2015;Hulva et al 2010;Pereira et al 2009;Rivers et al 2005). Behavioral and population genetic studies in southern China have shown that T. pachypus bats are philopatric to their natal area and that philopatry is especially pronounced in females (Hua et al 2011(Hua et al , 2013.…”

Evolutionary Scenarios Associated with thePteronotus parnelliiCryptic Species-Complex (Chiroptera: Mormoopidae)

“…Thus, despite recent efforts to address the issue, not only in the Neotropics (Clare, 2011; Clare et al, 2011; Pavan et al, 2011; Larsen et al, 2012;Hernández-Dávila et al, 2012; Pavan et al, 2013; Velazco and Patterson, 2013; Parlos et al, 2014) but also in several other regions of the world (Mayer and von Helversen, 2001;Ibáñez et al, 2006;Furman et al, 2010;Raghuram et al, 2014; Bogdanowicz et al, 2015; Dammhahn et al, 2015;and Hassanin et al, 2015), cryptic species complexes have become a top priority for a number of international agendas.…”