The expansion of agriculture has shaped the recent evolutionary history of a specialized squash pollinator

Significance

The conversion of natural to agricultural environments results in a dramatic modification of existing ecological conditions, and there are well-studied examples of crop pests that have rapidly evolved to fill novel agricultural niches. However, the degree to which agricultural intensification influences the evolution of wild insect pollinators is unknown, despite the importance of these mutualists to the global food supply and the persistence of plant populations. This study demonstrates that historical human agriculture in North America has had a profound impact on the recent evolutionary history of a wild, squash-specialized bee that is an essential pollinator of cucurbit crops. This provides a clear example of the role of agriculture as an evolutionary force acting on wild insect pollinators.

Abstract

The expansion of agriculture is responsible for the mass conversion of biologically diverse natural environments into managed agroecosystems dominated by a handful of genetically homogeneous crop species. Agricultural ecosystems typically have very different abiotic and ecological conditions from those they replaced and create potential niches for those species that are able to exploit the abundant resources offered by crop plants. While there are well-studied examples of crop pests that have adapted into novel agricultural niches, the impact of agricultural intensification on the evolution of crop mutualists such as pollinators is poorly understood. We combined genealogical inference from genomic data with archaeological records to demonstrate that the Holocene demographic history of a wild specialist pollinator of Cucurbita (pumpkins, squashes, and gourds) has been profoundly impacted by the history of agricultural expansion in North America. Populations of the squash bee Eucera pruinosa experienced rapid growth in areas where agriculture intensified within the past 1,000 y, suggesting that the cultivation of Cucurbita in North America has increased the amount of floral resources available to these bees. In addition, we found that roughly 20% of this bee species’ genome shows signatures of recent selective sweeps. These signatures are overwhelmingly concentrated in populations from eastern North America where squash bees were historically able to colonize novel environments due to human cultivation of Cucurbita pepo and now exclusively inhabit agricultural niches. These results suggest that the widespread cultivation of crops can prompt adaptation in wild pollinators through the distinct ecological conditions imposed by agricultural environments.