Introgression and disruption of migration routes have shaped the genetic integrity of wildebeest populations

Authors: LIU, XIAODONG - University Of Copenhagen; LIN, LONG - University Of Copenhagen; SINDING, MIKKEL-HOLGER - University Of Copenhagen; BERTOLA, LAURA - University Of Copenhagen; HANGHOJ, KRISTIAN - University Of Copenhagen; QUINN, LIAM - University Of Copenhagen; GARCIA-ERILL, GENIS - University Of Copenhagen; RASMUSSEN, MALTHE - University Of Copenhagen; SCHUBERT, MIKKEL - University Of Copenhagen; PECNEROVA, PATRICIA - University Of Copenhagen; BALBOA, RENZO - University Of Copenhagen; LI, ZILONG - University Of Copenhagen; Heaton, Michael - Mike; Smith, Timothy - Tim; PINTO, RUI - The University Of Porto; WANG, XI - University Of Copenhagen; KUJA, JOSIAH - University Of Copenhagen; BRUNICHE-OLSEN, ANNA - University Of Copenhagen; MEISNER, JONAS - University Of Copenhagen; SANTANDER, CINDY - University Of Copenhagen; OGUTU, JOSEPH - University Of Hohenheim; MASEMBE, CHARLES - Makerere University; DA FONSECA, RUTE - The University Of Porto; MUWANIKA, VINCENT - Makerere University; SIEGISMUND, HANS - University Of Copenhagen; ALBRECHTSEN, ANDERS - University Of Copenhagen; MOLTKE, IDA - University Of Copenhagen; HELLER, RASMUS - University Of Copenhagen

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/11/2024
Publication Date: 4/12/2024
Citation: Liu, X., Lin, L., Sinding, M.S., Bertola, L.D., Hanghoj, K., Quinn, L., Garcia-Erill, G., Rasmussen, M.S., Schubert, M., Pecnerova, P., Balboa, R.F., Li, Z., Heaton, M.P., Smith, T.P.L., Pinto, R., Wang, X., Kuja, J., Bruniche-Olsen, A., Meisner, J., Santander, C.G., Ogutu, J.O., Masembe, C., da Fonseca, R.R., Muwanika, V., Siegismund, H.R., Albrechtsen, A., Moltke, I., Heller, R. 2024. Introgression and disruption of migration routes have shaped the genetic integrity of wildebeest populations. Nature Communications. 15. Article 2921. https://doi.org/10.1038/s41467-024-47015-y.
DOI: https://doi.org/10.1038/s41467-024-47015-y

Interpretive Summary: The blue wildebeest is a remarkable animal found in savanna ecosystems across southern to eastern Africa. It is famous for its impressive migrations and large population numbers. On the other hand, the black wildebeest is native to southern Africa and faced near extinction in the past. Today it is at risk of losing its genetic uniqueness due to interbreeding with the blue wildebeest. Despite the significance of wildebeests in the ecosystem, we still don't fully understand how their migration patterns have affected their genetics and overall distribution. To address this, scientists studied the DNA of 121 blue wildebeests and 22 black wildebeests from different regions. They discovered distinct genetic differences that align with the visually identified subspecies. Surprisingly, there was no recent interbreeding between the two species. Instead, they found evidence of black wildebeest genes introgressing into southern populations of blue wildebeests during the late Pleistocene era. Although blue wildebeests are abundant, their genetic diversity was unexpectedly low. Interestingly, both species had similar levels of genetic diversity despite their different histories. Additionally, migrating blue wildebeest populations showed a combination of freely mixing genes over long distances, higher genetic diversity, and low levels of inbreeding. This contrasts with populations that had disrupted migrations, which exhibited reduced genetic diversity. These findings shed light on the evolutionary history of wildebeests and provide concrete genetic proof of the negative impact of human activities on the genetic health of highly migratory animals that play a crucial role in their ecosystems.

Technical Abstract: The blue wildebeest (Connochaetes taurinus) is a keystone species in savanna ecosystems from southern to eastern Africa, and is well known for its spectacular migrations and locally extreme abundance. In contrast, the black wildebeest (C. gnou) is endemic to southern Africa, barely escaped extinction in the 1900s and is feared to be in danger of genetic swamping from the blue wildebeest. Despite the ecological importance of the wildebeest, there is a lack of understanding of how its unique migratory ecology has affected its gene flow, genetic structure and phylogeography. Here, we analyze whole genomes from 121 blue and 22 black wildebeest across the genus’ range.We find discrete genetic structure consistent with the morphologically defined subspecies. Unexpectedly, our analyses reveal no signs of recent interspecific admixture, but rather a late Pleistocene introgression of black wildebeest into the southern blue wildebeest populations. Finally, we find that migratory blue wildebeest populations exhibit a combination of long-range panmixia, higher genetic diversity and lower inbreeding levels compared to neighboring populations whose migration has recently been disrupted. These findings provide crucial insights into the evolutionary history of the wildebeest, and tangible genetic evidence for the negative effects of anthropogenic activities on highly migratory ungulates.