Iconic savanna antelopes face genetic problems due to fences and roads

The blue wildebeest is a keystone species in savanna ecosystems and is renowned for its spectacular migrations. 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.
Iconic savanna antelopes face genetic problems due to fences and roads
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Migration is a widespread phenomenon observed in all major branches of the animal kingdom. Animal migration has fascinated humans for millennia. Our earliest evidence of recognizing  animal migration dates back to the Stone Age. Some petroglyphs, depicting animals moving across the African savannah, are as old as 20,000 years. Today, one of the most iconic examples of large-scale animal movement can be found in Tanzania’s Serengeti and Kenya’s Masai Mara, where 1.3 million blue wildebeest (Connochaetes taurinus) thunder across the African savanna, cross rivers en masse and are picked off by lions, hyenas, and crocodiles. This so-called ‘Great Migration’ attracts hundreds of thousands of tourists each year. More importantly, it also plays a key role in sustaining local ecosystems. Indeed, the migrations of blue wildebeest make them a keystone species for savanna ecosystems, as their grazing keeps vegetation healthy, transports and distributes nutrients, while they themselves serve as prey for predators and carrion for scavengers.

Unfortunately, epic annual migrations of blue wildebeest have become a rarer sight in Africa due to disruption in their historic migratory routes. In some areas, roads, fences, farms, and urban sprawl have fractured the migratory routes of wildebeest herds and prevented them from roaming far and wide in search of resources such as fresh grass and water. Despite multiple records of local population crashes in blue wildebeest due to anthropogenic disturbances, there is still a lack of understanding regarding how forced changes in migration regime impact population genetic patterns of a highly migratory species like the blue wildebeest.

 In our recent study including 144 wildebeest genomes, we investigated the evolutionary history of the blue wildebeest, and their sister species, the black wildebeest (Connochaetes gnou) and assessed the impact of recent anthropogenic habitat fragmentation on their genetic health.

 Unexpected ancient introgression from black wildebeest to southern populations of blue wildebeest

Compared to the widely distributed blue wildebeest, the black wildebeest is less well known and endemic to the southern part of Africa. As the two species can interbreed when they come into contact, there are widespread concerns about genetic swamping of the black wildebeest by the much more abundant blue wildebeest. Unexpectedly, our results of PCA and ADMIXTURE analysis revealed no clear signals of recent admixture between the two species. Even more surprisingly, based on multiple lines of evidence, we identified a late Pleistocene introgression of black wildebeest into the southern populations of blue wildebeest populations, hence in the opposite direction than the suspected genetic swamping of black wildebeest by blue wildebeest.

Gene flow is commonly detected in closely related species or population pairs. However, determining the direction of gene flow remains a challenging task, as gene flow in opposite directions can generate similar patterns, e.g., reduced divergence between the pair. Our finding of ancient gene flow from the black wildebeest into the blue wildebeest relied on the recent advances in implementation of the f-statistics, i.e., findGraphs in the ADMIXTOOLS2 package and the extension of the related D-statistic, i.e., D frequency spectrum (DFS).

 Contrasting population genetic patterns between migratory and non-migratory populations

As our study sampled the genomes of many blue wildebeest from virtually their entire range, we have been able to make a general genetic comparison of migratory versus non-migratory populations of the blue wildebeest. It is evident that populations which no longer migrate, but have historically done so, are simply less genetically healthy than those that continue to migrate. Wildebeest that can no longer migrate have lower genetic diversity, are less genetically connected and are more inbred. These population genetic patterns will very likely lead to lower survival, reduced fertility, and other negative effects on fitness in populations that have been prevented from migrating.

Comparison between adjacent migratory and non-migratory populations in eastern (left) and southern Africa (right).

 The results demonstrate that the genetic decline of non-migratory populations is reflected in several of the parameters by which genetic health is measured in nature conservation. Not just for wildebeest, migration is a key life-history strategy or foraging behavior of many animal species, enabling them to maintain higher population sizes in spatiotemporally variable environments. They might survive in resident, non-migratory populations, but their population sizes simply shrink when they cannot migrate.

 Planned road and rail corridors, expanding settlements and fences threaten the last population

Most transitions from a migratory population into a non-migratory and less genetically healthy one in wildebeest did not appear to occur a long time ago. Unlike today, many wildebeest populations made great migrations as recently as one hundred and fifty years ago. However, by forty years ago, only two large intact wildebeest migrations remained in Africa: the famed Great Migration of the Serengeti-Masai Mara and one in the Kalahari Desert of southern Africa. However, in Botswana, a country in southern Africa, fencing to protect cattle from coming into contact with migratory wild animals was put up in recent times. Botswana's Kalahari population declined from roughly 260,000 in the 1970’s to fewer than 15,000 in the late 1980’s. So today,   the only remaining large population is that of the Serengeti-Masai Mara. But the Serengeti-Mara migration is also threatened by plans for roads and rail corridors through the area and land use developments pressing on its edges.

Putting things into perspective

Taken together, our work sheds light on how two major evolutionary forces—hybridization and migration, drive the distribution of genetic variation in wildebeest. More broadly, the study shows us that wild animal species, for whom migration is an essential part of their biology, struggle to survive in an increasingly human-dominated world, unless special attention is paid to preserving their old and natural migratory routes and the sufficiently large habitats they connect. As such, we hope that people will be more cautious about continuing to disrupt these migratory routes and ranges. This concern is not just with regards to wildebeest, but also for other migratory species in Africa and elsewhere.

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Evolutionary Biology
Life Sciences > Biological Sciences > Evolutionary Biology
Population Genetics
Life Sciences > Biological Sciences > Genetics and Genomics > Population Genetics
Conservation Biology
Life Sciences > Biological Sciences > Ecology > Conservation Biology
Animal Migration
Life Sciences > Biological Sciences > Ecology > Animal Migration

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