Persistent Gene Flow Suggests an Absence of Reproductive Isolation in an African Antelope Speciation Model

Xi Wang; Casper-Emil Tingskov Pedersen; Georgios Athanasiadis; Genís Garcia-Erill; Kristian Hanghøj; Laura D Bertola; Malthe Sebro Rasmussen; Mikkel Schubert; Xiaodong Liu; Zilong Li; Long Lin; Renzo F Balboa; Emil Jørsboe; Casia Nursyifa; Shanlin Liu; Vincent Muwanika; Charles Masembe; Lei Chen; Wen Wang; Ida Moltke; Hans R Siegismund; Anders Albrechtsen; Rasmus Heller

doi:10.1093/sysbio/syae037

Persistent Gene Flow Suggests an Absence of Reproductive Isolation in an African Antelope Speciation Model

Syst Biol. 2024 Aug 14:syae037. doi: 10.1093/sysbio/syae037. Online ahead of print.

Authors

Xi Wang¹, Casper-Emil Tingskov Pedersen², Georgios Athanasiadis^{1

3}, Genís Garcia-Erill¹, Kristian Hanghøj¹, Laura D Bertola¹, Malthe Sebro Rasmussen¹, Mikkel Schubert⁴, Xiaodong Liu¹, Zilong Li¹, Long Lin¹, Renzo F Balboa¹, Emil Jørsboe^{4

5

6}, Casia Nursyifa¹, Shanlin Liu⁷, Vincent Muwanika⁸, Charles Masembe⁹, Lei Chen¹⁰, Wen Wang¹⁰, Ida Moltke¹, Hans R Siegismund¹, Anders Albrechtsen¹, Rasmus Heller¹

Affiliations

¹ Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200 Copenhagen N, Denmark.
² COPSAC, Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, Denmark.
³ Department of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, 08028 Barcelona, Spain.
⁴ Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
⁵ Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, University of Oxford, Oxford, United Kingdom.
⁶ Nuffield Department of Population Health, University of Oxford, Oxford, United Kingdom.
⁷ Department of Entomology, College of Plant Protection, China Agricultural University, Beijing 100193, China.
⁸ Department of Environmental Management, Makerere University, PO Box 7062, Kampala, Uganda.
⁹ Department of Biology, Makerere University, PO Box 7062, Kampala, Uganda.
¹⁰ School of Ecology and Environment, Northwestern Polytechnical University, Xi'an 710072, China.

PMID: 39140829
DOI: 10.1093/sysbio/syae037

Abstract

African antelope diversity is a globally unique vestige of a much richer world-wide Pleistocene megafauna. Despite this, the evolutionary processes leading to the prolific radiation of African antelopes are not well understood. Here, we sequenced 145 whole genomes from both subspecies of the waterbuck (Kobus ellipsiprymnus), an African antelope believed to be in the process of speciation. We investigated genetic structure and population divergence and found evidence of a mid-Pleistocene separation on either side of the eastern Great Rift Valley, consistent with vicariance caused by a rain shadow along the so-called 'Kingdon's Line'. However, we also found pervasive evidence of both recent and widespread historical gene flow across the Rift Valley barrier. By inferring the genome-wide landscape of variation among subspecies, we found 14 genomic regions of elevated differentiation, including a locus that may be related to each subspecies' distinctive coat pigmentation pattern. We investigated these regions as candidate speciation islands. However, we observed no significant reduction in gene flow in these regions, nor any indications of selection against hybrids. Altogether, these results suggest a pattern whereby climatically driven vicariance is the most important process driving the African antelope radiation, and suggest that reproductive isolation may not set in until very late in the divergence process. This has a significant impact on taxonomic inference, as many taxa will be in a gray area of ambiguous systematic status, possibly explaining why it has been hard to achieve consensus regarding the species status of many African antelopes. Our analyses demonstrate how population genetics based on low-depth whole genome sequencing can provide new insights that can help resolve how far lineages have gone along the path to speciation.

Keywords: Admixture; Islands of differentiation; Speciation genomics; Waterbuck.