African bush pigs exhibit porous species boundaries and appeared in Madagascar concurrently with human arrival

Authors: BALBOA, RENZO - University Of Copenhagen; BERTOLA, LAURA - University Of Copenhagen; BRUNICHE-OLSEN, ANNA - University Of Copenhagen; RASMUSSEN, MALTHE SEBRO - University Of Copenhagen; LIU, XIAODONG - University Of Copenhagen; BESNARD, GUILLAUME - University Of Toulouse; SALMONA, JORDI - University Of Toulouse; SANTANDER, CINDY - University Of Copenhagen; HE, SHIXU - University Of Copenhagen; ZINNER, DIETMAR - Leibniz Institute; Heaton, Michael - Mike; Smith, Timothy - Tim; MOLTKE, IDA - University Of Copenhagen; ALBRECHTSEN, ANDERS - University Of Copenhagen; HELLER, RASMUS - University Of Copenhagen

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/30/2023
Publication Date: 1/3/2024
Citation: Balboa, R.F., Bertola, L., Bruniche-Olsen, A., Rasmussen, M., Liu, X., Besnard, G., Salmona, J., Santander, C.G., He, S., Zinner, D., Heaton, M.P., Smith, T.P., Moltke, I., Albrechtsen, A., Heller, R. et al. 2024. African bush pigs exhibit porous species boundaries and appeared in Madagascar concurrently with human arrival. Nature Communications. 15. Article 172. https://doi.org/10.1038/s41467-023-44105-1.
DOI: https://doi.org/10.1038/s41467-023-44105-1

Interpretive Summary: The evolutionary history of African pigs is unresolved in several aspects, including the controversial timeline of their divergence, which stems from molecular estimates that predate fossil records by millions of years, and the unresolved role of gene flow between lineages. Bushpigs and red river hogs are recognized as separate species due to morphological distinctions, a perceived lack of interbreeding at contact, and putatively old divergence times. However, historically, they were considered to be belonging to the same species. The presence of Malagasy bushpigs as the sole large terrestrial mammal shared with the African mainland raises intriguing questions about their origin and arrival in Madagascar. Here, we analyzed whole genomes from 67 African pigs and discovered a genetic continuum between the two species, evidence of historical gene flow, and estimated a recent divergence time of less than 500,000 years. Our study challenges key arguments for splitting Potamochoerus into two species and suggests that their speciation might be incomplete. Our findings also indicate that Malagasy bushpigs diverged from southern African populations and underwent a limited bottleneck 1,000-5,000 years ago, concurrent with human arrival in Madagascar. These results shed new light on the evolutionary history of an iconic and widespread African genus and provide insight into the longstanding biogeographic puzzle surrounding the bushpig’s presence in Madagascar.

Technical Abstract: Several African mammals exhibit a phylogeographic pattern where closely related taxa are split between West/Central and East/Southern Africa, but their evolutionary relationships and histories remain controversial. Bushpigs (Potamochoerus larvatus) and red river hogs (P. porcus) are recognised as separate species due to morphological distinctions, a perceived lack of interbreeding at contact, and putatively old divergence times, but historically, they were considered conspecific. Moreover, the presence of Malagasy bushpigs as the sole large terrestrial mammal shared with the African mainland raises intriguing questions about its origin and arrival in Madagascar. Analyses of 67 whole genomes revealed a genetic continuum between the two species, with putative signatures of historical gene flow, variable FST values, and a recent divergence time (<500,000 years). Thus, our study challenges key arguments for splitting Potamochoerus into two species and suggests their speciation might be incomplete. Our findings also indicate that Malagasy bushpigs diverged from southern African populations and underwent a limited bottleneck 1,000-5,000 years ago, concurrent with human arrival in Madagascar. These results shed new light on the evolutionary history of an iconic and widespread African genus and provide insight into the longstanding biogeographic puzzle surrounding the bushpig’s presence in Madagascar.