Monoculture is good if you are a squash bee

The industrialization of agriculture has left a massive footprint on our planet’s natural ecosystems, leading to major losses of biodiversity (1). Agricultural lands now cover nearly 50% of the Earth’s surface (2), and common agricultural practices typically result in vast amounts of land dedicated to the production of a small number of species grown in monoculture (3). While the industrialization of agriculture has had a negative effect on most lifeforms (1), some species were able to adapt and thrive in highly modified agri-environments. Crop pests, for example, have an amazing capacity to quickly adapt to the anthropogenic pressures associated with agriculture (4). However, it is unclear whether agriculture can drive the evolution of plant mutualists, such as pollinators. In this issue, Pope et al. (5) exploit the close relationship between the squash and its specialist pollinator to study how the expansion of agriculture in North America can affect the evolution of an obligate crop mutualist.

Bees are important pollinators of a large number of flowering plants, including the vast majority of cultivated crops (6), but it is not entirely obvious how the evolutionary genetics of bees was influenced by the rise and intensification of agriculture. Many bees are diet generalists that consume pollen and nectar from a variety of plant taxa, which complicates our understanding of how bee populations respond to expansions of specific crops. Specialist bees (7) on the other hand are restricted to foraging on a specific group of plants, making them ideal candidates for understanding the impacts of agriculture on bee evolution.

The North American squash bee, Eucera pruinosa (Fig. 1), is a specialist that collects pollen only from plants of the genus Cucurbita (8). Cucurbits include agriculturally important crops like pumpkins, squash, and zucchini. The squash bee’s native host is Cucurbita foetidissima, wild buffalo gourd, which is found in Mexico and the southwestern United States (9). However, the squash bee is also able to utilize the pollen of the many varieties of cultivated cucurbits, Cucurbita pepo, which were domesticated in central Mexico approximately 10,000 years ago (10). The industrialization of agriculture led to the expansion of the domesticated squash, and the squash bee, into eastern North America, where the squash bee exclusively relies on pollen from cultivated cucurbits to provision its larvae (11). This narrow mutualism provides ideal conditions for understanding how squash agriculture has shaped the evolutionary history and population genetics of its specialist pollinator.

Fig. 1.

A male squash bee, covered in pollen, on a zucchini blossom. In this issue, Pope et al. show that the rise of squash agriculture has shaped the evolution of squash bees over the past thousand years. Photo by Amro Zayed.

Pope et al. (5) first genotyped a large number of squash bees throughout their current range in North America and found that the bees clustered into five major lineages, mostly restricted to southern and western North America. The authors then sequenced the genomes of several haploid males from each of these lineages to reconstruct the squash bee’s evolutionary history. The authors developed and applied a novel method to simultaneously estimate effective population size, migration rate, and divergence times of the five squash bee lineages. This analysis indicated that all contemporary squash bee lineages originated and diversified between 50,000 and 100,000 years ago, prior to the development of human agriculture in North America (12).

Pope et al. (5) then set out to understand how the domestication and expansion of cultivated cucurbits influenced the squash bee’s population genetics. The authors used species distribution models and climate projections and found that wild gourd was mostly restricted to Mexico and the southwestern United States at the end of the last glacial maximum before spreading into the central United States after the glaciers receded. Data from archaeological sites suggested that domesticated cucurbits were widespread in eastern North America as early as 7,000 years ago. Demographic modeling indicated that all North American squash bee populations experienced a substantive increase in effective population size—approximately an order of magnitude higher—over the past 1,000 y; a period that coincided with agricultural intensification in pre-Columbian North America (5). This period also saw increased levels of gene flow between squash bee populations. Diet specialization has been predicted to limit the effective population size and migration rate of specialist bees (13), and the results of Pope et al. provide a clear example of how artificial supplementation of floral resources—driven by agriculture in this case—can have a positive influence on the effective population size and rates of gene flow of specialist pollinators.

Pope et al. exploit the close relationship between squash and its specialist pollinator to study how the expansion of agriculture in North America can affect the evolution of an obligate crop mutualist.

Finally, Pope et al. (5) searched for signatures of recent adaptive evolution in squash bees. They first developed a model to forecast the expected effects of background selection on the squash bee genome to account for the enhanced ability of natural selection to remove deleterious mutations, and linked neutral mutations, as squash bee population sizes expanded over the past 1,000 y. Pope et al. (5) then searched for genomic regions with signs of adaptive evolution that could not be explained by their models of background selection alone. They found the strongest signatures of recent adaptive evolution in the northeastern population of squash bees, which exclusively relies on cultivated cucurbits for pollen. Approximately 20% of the northeastern squash bee population’s genome has highly reduced genetic diversity, as would be expected from directional selection fixing beneficial mutations—and nearby neutral mutations—that allow squash bees to adapt to the conditions of newly formed agri-environments. The relatively large size of these selective sweeps makes identifying the specific genes driving adaptation difficult, but these regions appear to be enriched for genes associated with olfaction, perhaps allowing the squash bee to quickly find new cultivated populations of its host. The authors also found evidence of adaptive evolution at a key detoxification gene, which is interesting in light of recent evidence of heritable variation in tolerance to some pesticides in another bee species (14).

Pope et al. (5) have shed new light on the multidirectional impacts of agricultural expansion and its influence on the evolution of a specialist pollinator, but to what extent can agriculture influence the evolution of generalist pollinators? While agriculture can increase the density of flowering plants and availability of floral resources in a given space, it also exposes pollinators to a slew of harmful agrochemicals (15–17) and promotes interactions between wild and managed bees that can lead to the spillover of pests and pathogens (18). A recent population genomic study of an at-risk bumblebee hints at this. The yellow-banded bumblebee, Bombus terricola, has had a massive reduction in effective population size over a similar timeframe as the industrialization of agriculture in North America (19). In addition, populations of B. terricola near agricultural areas have genomic signatures associated with exposure to novel honey-bee derived pathogens as well as pesticides that are highly toxic to bees (20). It is possible that the artificial availability of floral resources from crops may not offset the negative effects of agriculture on generalist pollinators (e.g., habitat loss and fragmentation and exposure to agrochemicals). While additional research is needed to understand the fitness trade-offs that generalist bees experience in agricultural landscapes, Pope et al. (5) provide a powerful example of how agriculture can influence the evolution of an obligate plant mutualist.