Pan African phylogeography and palaeodistribution of rousettine fruit bats: Ecogeographic correlation with Pleistocene climate vegetation cycles

Abstract

Aim The impact of Pleistocene climatic oscillations on tropical biomes is associated with changes in the extent of forest cover. Fruit bats have played a role in woodland dynamics via pollination and seed dispersal. We hypothesized that phylogeographic patterns of Rousettus on continental Africa and adjacent islands should show a signature of pluvial‐drought cycles, involving demographic expansions and contractions. Location Afrotropical, Malagasy and Saharo‐Arabian biogeographic realms. Taxon Genus Rousettus (Pteropodidae). Methods Phylogeographic and population genetic approaches using mitochondrial and microsatellite data were integrated with species distribution modelling of currently suitable habitats and those of the Last Glacial Maximum using climate simulations. Results Phylogenetic reconstruction yielded an Asian outgroup followed by pectinate branching of the Indian Ocean taxa and Rousettus aegyptiacus. While nuclear microsatellites were homogeneous across the African mainland, two mitochondrial haplogroups were found. Haplogroup I is widespread in regions with extensive tree cover, including tropical rain forests, and has close relationships to isolated lineages in the Middle East and islands in the Gulf of Guinea. Haplogroup II is sister to the rest of the R. aegyptiacus radiation and is found in eastern and southern Africa and the Sudanian savanna in habitats with semi‐open land cover. Main Conclusion Palaeodistributional modelling ascertained that the Indian Ocean islands provided more extensive areas of suitable habitat in the past relative to conditions today, suggesting stepping stone connectivity between Asia and Africa during Pleistocene interpluvial sea‐level lowstands. Inverse pluvial‐drought demography was detected in lineages ancestral to recent haplogroups, providing evidence of past forest refugia and complex ecogeographic scenarios of haplogroup origins involving allopatry and parapatry connected with the eastern Afromontane biodiversity hotspot, and subsequent admixture of nuclear gene pools. The Middle Eastern lineage probably originated during pluvial green Sahara periods, possibly in co‐evolution with ancestors of tree crop species domesticated later during the Neolithic revolution. The keystone role of rousettine bats for forest regeneration and their ability to pioneer dry and distant habitats emphasize their role in conservation biology and restoration ecology.

The first complete mitochondrial genome data of Geoffroy's rousette, Rousettus amplexicaudatus originating from Malaysia

“…Their flexibility to adapting in mesic and dry habitats, ability for long-distance dispersal and remarkably precise lingual echolocation support the species wide-range distribution and colonization (Happold & Happold 2013 ; Stribna et al. 2019 ; Hassanin et al. 2020 ).…”

“…are reported to be more adaptive to certain biogeographic barriers. Their flexibility to adapting in mesic and dry habitats, ability for long-distance dispersal and remarkably precise lingual echolocation support the species wide-range distribution and colonization (Happold & Happold 2013;Stribna et al 2019;Hassanin et al 2020). Therefore, further taxonomical and mitogenome comparative studies are essential to resolve the evolutionary relationships of this widely distributed Rousettus genus especially within Southeast Asia region.…”

“…Rousettus spp. are selected as the best candidate amongst the Pteropodidae family to study evolutionary relationships as it is the only genus that has the capability of long-distance dispersal and has showed remarkable ecological flexibility in characteristics such as a well-developed echolocation system (Almeida et al 2016;Stribna et al 2019;Hassanin et al 2020). However, lack of genomic data of Asian Rousettus sp.…”

Molecular dating for phylogenies containing a mix of populations and species by using Bayesian and RelTime approaches

“…Although it may seem biologically improbable, such type of phylogenies is often reported in the literature (e.g. Benítez‐Benítez, Escudero, Rodríguez‐Sánchez, Martín‐Bravo, & Jiménez‐Mejías, 2018; Betkas et al., 2019; Lim & Lee, 2018; Stribna et al., 2019) and one of the reasons for getting such phylogenies is small effective population sizes and/or high levels of purifying selection on the analysed locus. We will use the nomenclature ILS and no‐ILS to refer to the MSC branching process and mixture branching process, respectively (Figure 1).…”

The ecology of Nipah virus in Bangladesh: a nexus of land use change and opportunistic feeding behavior in bats

“…The range of henipaviruses including Hendra [19], Cedar [20], and others [21][22][23] extends throughout the geographic range of pteropodid bats to Australia, Indian Ocean islands, and sub-Saharan Africa [24]. These data, combined with limited evidence of pathology in henipavirus-infected bats [25,26], suggest that henipaviruses have had a long association with their bat reservoirs that spans the dispersal of pteropodid bats out of Southeast Asia to other regions [27][28][29][30][31].…”