Dispersal out of Wallacea spurs diversification of Pteropus flying foxes, the world's largest bats (Mammalia: Chiroptera)

Abstract

Aim: Islands provide opportunities for isolation and speciation. Many landmasses in the Indo-Australian Archipelago (IAA) are oceanic islands, and founder-event speciation is expected to be the predominant form of speciation of volant taxa on these islands. We studied the biogeographic history of flying foxes, a group with many endemic species and a predilection for islands, to test this hypothesis and infer the biogeographic origin of the group.

Location: Australasia, Indo-Australian Archipelago, Madagascar, Pacific Islands.

Taxon: Pteropus (Pteropodidae).

Methods: To infer the biogeographic history of Pteropus, we sequenced up to 6169 bp of genetic data from 10 markers and reconstructed a multilocus species tree of 34 currently recognized Pteropus species and subspecies with 3 Acerodon outgroups using BEAST and subsequently estimated ancestral areas using models implemented in BioGeoBEARS.

Results: Species-level resolution was occasionally low because of slow rates of molecular evolution and/or recent divergences. Older divergences, however, were more strongly supported and allow the evolutionary history of the group to be inferred. The genus diverged in Wallacea from its common ancestor with Acerodon; founder-event speciation out of Wallacea was a common inference. Pteropus species in Micronesia and the western Indian Ocean were also inferred to result from founder-event speciation.

Main conclusions: Dispersal between regions of the IAA and the islands found therein fostered diversification of Pteropus throughout the IAA and beyond. Dispersal in Pteropus is far higher than in most other volant taxa studied to date, highlighting the importance of inter-island movement in the biogeographic history of this large clade of large bats.

Keywords: BioGeoBEARS; Indo-Pacific; Pteropodidae; Southeast Asia; dispersal; founder-event speciation; island biogeography; peripatric speciation.

Figure 1.. Map of biogeographic areas and specimens used in this study:

Wallacea (A), New Guinea + Australia + South Pacific (B), Sundaland + South Asia (C), the Philippines (D), Micronesia (E), and Wester Indian Ocean (F). Collection localities of fresh tissue samples obtained for this study are represented by black dots; museum loans are shown with white dots. The Japanese Ryukyu and Bonin islands were included as part of Micronesia due to their proximity and shared geologic history. Wallace’s Line (red) and Lydekker’s Line (blue) are indicated on the map to separate the Sunda Shelf, Wallacea, and the Sahul Shelf.

Figure 2.. Multilocus species tree of nuclear markers of Pteropus from BEAST 2.5.2 (ESS > 200).

Numbers above branches indicate Bayesian posterior probabilities. A dated species tree with 95% CI node bars is included as Appendix S3 along with the species tree estimated using both nuclear and mitochondrial markers. Inset photo © Godfrey Jakosalem and used with permission.

Figure 3.. Ancestral area estimations from DEC+j model implemented in BioGeoBEARS.

Ancestral area estimations at nodes represent areas before an inferred instantaneous speciation event; colored boxes at the tips indicate the current distribution of extant species. Species groups based on Almeida et al. (2014) were modified based on our results and indicated to the right. This tree was calibrated with secondary calibrations from a cytb molecular phylogeny from Almeida et al. (2014).