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

Renzo F. Balboa, Laura D. Bertola, Anna Brüniche-Olsen, Malthe Sebro Rasmussen, Xiaodong Liu, Guillaume Besnard, Jordi Salmona, Cindy G. Santander, Shixu He, Dietmar Zinner, Miguel Pedrono, Vincent Muwanika, Charles Masembe, Mikkel Schubert, Josiah Kuja, Liam Quinn, Genís Garcia-Erill, Frederik Filip Stæger, Rianja Rakotoarivony, Margarida HenriqueLong Lin, Xi Wang, Michael P. Heaton, Timothy P.L. Smith, Kristian Hanghøj, Mikkel Holger S. Sinding, Anagaw Atickem, Lounès Chikhi, Christian Roos, Philippe Gaubert, Hans R. Siegismund, Ida Moltke*, Anders Albrechtsen, Rasmus Heller

*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

4 Citationer (Scopus)
36 Downloads (Pure)

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 F ST 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 1000-5000 years ago, concurrent with human arrival in Madagascar. These results shed light on the evolutionary history of an iconic and widespread African mammal and provide insight into the longstanding biogeographic puzzle surrounding the bushpig’s presence in Madagascar.

OriginalsprogEngelsk
Artikelnummer172
TidsskriftNature Communications
Vol/bind15
Udgave nummer1
Antal sider15
ISSN2041-1723
DOI
StatusUdgivet - 2024

Bibliografisk note

Funding Information:
We thank Amal Al-Chaer for her invaluable help with DNA extractions. We are also grateful to Peter Arctander, who organised sample collections between the 1980s and 1990s and to David Moyer for contributing Tanzanian bushpig samples, collected between 1995 and 1997 and subsequently stored in the collection at the University of Copenhagen. We would also like to acknowledge our collaborators from African wildlife management authorities for granting express permission to use samples within this study. We thank Komlan Afiademanyo (Université de Lomé, Togo), Flobert Njikou (Université de Yaoundé I, Cameroon), Alain Didier Missoup (Université de Douala), Gabriel Ngua (ANDEGE, Equatorial Guinea), and Jonas Muhindo and Idriss Ayaya (CIFOR, Democratic Republic of Congo) for collecting red river hog samples in West and Central Africa. We are also grateful to Jonathan Kingdon for providing express permission for the use of his illustrations within this manuscript. RFB, XL, and IM are supported by a Villum Young Investigator grant (VIL19114) awarded to IM. A. Albrechtsen, RFB, LL, and ZL are funded by the Novo Nordisk Foundation (NNF20OC0061343). ABO is supported by a Carlsberg Foundation Reintegration Fellowship (CF19-0427). MSS is supported by a Carlsberg Foundation Reintegration Fellowship (CF20-0355). MSR and A. Albrechtsen are supported by the Independent Research Fund Denmark (8021-00360B). GGE and RH are supported by a Danmarks Frie Forskningsfond Sapere Aude research grant (DFF8049-00098B), and RH is further supported by a Carlsberg Young Researcher grant (CF21-0497). A. Atickem is supported with a Rufford Small Grants for Nature Conservation (1118-C). GB, JS, LC, and PG are members of the EDB laboratory, which is supported by the Laboratoire d’Excellence (LABEX) CEBA (ANR-10-LABX-2501) and LABEX TULIP (ANR-10-LABX-0041), both managed by the Agence Nationale de la Recherche in France. PG received additional support from Fundação para a Ciência e a Tecnologia through the project BUSHRISK (IC&DT 02/SAICT/2017-032130).

Funding Information:
We thank Amal Al-Chaer for her invaluable help with DNA extractions. We are also grateful to Peter Arctander, who organised sample collections between the 1980s and 1990s and to David Moyer for contributing Tanzanian bushpig samples, collected between 1995 and 1997 and subsequently stored in the collection at the University of Copenhagen. We would also like to acknowledge our collaborators from African wildlife management authorities for granting express permission to use samples within this study. We thank Komlan Afiademanyo (Université de Lomé, Togo), Flobert Njikou (Université de Yaoundé I, Cameroon), Alain Didier Missoup (Université de Douala), Gabriel Ngua (ANDEGE, Equatorial Guinea), and Jonas Muhindo and Idriss Ayaya (CIFOR, Democratic Republic of Congo) for collecting red river hog samples in West and Central Africa. We are also grateful to Jonathan Kingdon for providing express permission for the use of his illustrations within this manuscript. RFB, XL, and IM are supported by a Villum Young Investigator grant (VIL19114) awarded to IM. A. Albrechtsen, RFB, LL, and ZL are funded by the Novo Nordisk Foundation (NNF20OC0061343). ABO is supported by a Carlsberg Foundation Reintegration Fellowship (CF19-0427). MSS is supported by a Carlsberg Foundation Reintegration Fellowship (CF20-0355). MSR and A. Albrechtsen are supported by the Independent Research Fund Denmark (8021-00360B). GGE and RH are supported by a Danmarks Frie Forskningsfond Sapere Aude research grant (DFF8049-00098B), and RH is further supported by a Carlsberg Young Researcher grant (CF21-0497). A. Atickem is supported with a Rufford Small Grants for Nature Conservation (1118-C). GB, JS, LC, and PG are members of the EDB laboratory, which is supported by the Laboratoire d’Excellence (LABEX) CEBA (ANR-10-LABX-2501) and LABEX TULIP (ANR-10-LABX-0041), both managed by the Agence Nationale de la Recherche in France. PG received additional support from Fundação para a Ciência e a Tecnologia through the project BUSHRISK (IC&DT 02/SAICT/2017-032130).

Publisher Copyright:
© 2024, The Author(s).

Citationsformater