Crop domestication facilitated rapid geographic expansion of a specialist pollinator, the squash bee Peponapis pruinosa

Authors: LOPEZ-URIBE, MARGARITA - North Carolina State University; Cane, James; MINCKLEY, ROBERT - University Of Rochester; DANFORTH, BRYAN - Cornell University

Submitted to: Proceedings of the Royal Society B
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/26/2016
Publication Date: 6/22/2016
Citation: Lopez-Uribe, M.M., Cane, J.H., Minckley, R.L., Danforth, B.N. 2016. Crop domestication facilitated rapid geographic expansion of a specialist pollinator, the squash bee Peponapis pruinosa. Proceedings of the Royal Society B. doi: 10.1098/rspb.2016.0443.

Interpretive Summary: Limited fossil evidence documents the spread of cultivated squashes out of Mexico and across today’s USA over the past 10,000 years. Comparable fossil evidence for the spread of their native specialist bee, Peponapis pruinosa, is wanting. It must have followed squash cultivation, inasmuch as its wild gourd host is absent from most of the continent. We used molecular data for insights into this bee’s accompanying Holocene range expansion (as far as southern Ontario and Idaho, and northern California). East of the Rockies, genetic diversity decreases with distance from the Southwest. Analyses indicate that the bee passed through the Midwest to colonize the eastern seaboard, probably over millennia. West of the Rockies, populations of the eastern Great Basin and California are genetically distinct and monotonous, indicating recent and strong genetic bottlenecks during northward colonizations. Those of the Great Basin likely followed homesteader gardens, which served as “stepping stones” for the bees. In California, both bee and its wild gourd likely arrived in the Central Valley by long-distance dispersal across the southern mountain passes. These scenarios are consistent with these squash bees’ depleted genetic diversity in the West.

Technical Abstract: Over the past 10,000 years, humans have facilitated rapid range expansions of animal, plants and microorganisms, often accompanying agriculture’s spread. Three squash species were early domesticates in the New World. Their spreading cultivation out of the Southwest across much of today’s USA has been followed by their native specialist pollinator. Molecular markers were used to characterize genetic divergence and similarities of this solitary bee, Peponapis pruinosa, an obligate pollen specialist (oligolege) for plants in the genus Cucurbita. We found that this bee’s genetic diversity decreases with geographic distance from its origin in the US Southwest. East of the Rocky Mountains, our data support a demographic scenario of an early (mid-Holecene), broad range expansion through the Midwest, starting from the range of its wild Cucurbita host in the warm deserts. Opportunities for western P. pruinosa to spread northward are much more recent. The route into California’s Central Valley required long-distance dispersal of both host and bee. Independently, P. pruinosa moved northward through the eastern Great Basin, likely following gardens of pioneer homesteads. Populations of P. pruinosa in these two regions are genetically differentiated but remarkably uniform, reflecting severe bottlenecks that these bees have tolerated in rapidly colonizing and then persisting across much of North America, supported solely by cultivated squashes.