Understanding the relative contributions of historical and anthropogenic factors to declines in genetic diversity is important for informing conservation action. Using genome-wide DNA of fresh and historic specimens, including that of two species widely thought to be extinct, we investigated fluctuations in genetic diversity and present the first complete phylogenomic tree for all nine species of the threatened shorebird genus Numenius, known as whimbrels and curlews. Most species faced sharp declines in effective population size, a proxy for genetic diversity, soon after the Last Glacial Maximum (around 20,000 years ago). These declines occurred prior to the Anthropocene and in spite of an increase in the breeding area predicted by environmental niche modeling, suggesting that they were not caused by climatic or recent anthropogenic factors. Crucially, these genetic diversity declines coincide with mass extinctions of mammalian megafauna in the Northern Hemisphere. Among other factors, the demise of ecosystem-engineering megafauna which maintained open habitats may have been detrimental for grassland and tundra-breeding Numenius shorebirds. Our work suggests that the impact of historical factors such as megafaunal extinction may have had wider repercussions on present-day population dynamics of open habitat biota than previously appreciated.
Keywords: Numenius; Target enrichment; curlews; ecology; evolutionary biology; whimbrels.
About 20,000 years ago, the Earth was a much colder world roamed by giant mastodons, gigantic elks, woolly mammoths and sabre-tooth tigers. Yet these imposing creatures were living on borrowed time: by the start of the Holocene, around 10,000 years later, many animals over 45kg had vanished across the Northern Hemisphere, closing the book on what is known as the Quaternary extinction event. As large grazers disappeared, the landscape likely changed too. Where open tundra and grasslands may have once dominated, woodlands and shrubs probably took over, creating ripple effects for surviving species. These extinction events took place in a changing world, with glaciers starting to retreat about 20,000 years ago and human populations colonizing an increasing share of this planet’s land area. In fact, since the end of this last glacial maximum, ecosystems have been reshaped by a succession and a combination of climatic, historical and human-driven forces. This makes it difficult for scientists to disentangle the relative contribution of these factors on the lives of animals. Tan et al. decided to explore this question by reconstructing how effective population sizes changed over the past 20,000 years for nine species of curlews and whimbrels. These shorebirds, which together comprise the genus Numenius, breed slowly and nest in open environments such as moorlands or tundra. Many are currently under threat. Fluctuations in the numbers of breeding individuals affect the genetic diversity of a species, and these events leave tell-tale genetic signatures that can be uncovered through DNA analyses. Tan et al. had enough fresh and museum samples to infer these changes for five Numenius species, revealing that genetic diversity brutally dropped soon after the last glacial period ended. At the time, humans were yet to make significant changes on their environment and a warming world should have supported population growth. Tan et al. suggest that, instead, this sharp decline is linked to the late Quaternary extinctions of large mammals: with the demise of grazing animals which could keep woodlands at bay, the shorebirds lost their open nesting grounds. This event has left its mark in the genome of existing species, with these birds still exhibiting a low level of genetic diversity that may put them at further risk for extinction.
© 2023, Tan et al.