Plant Virus Impacts on Yield and Plant-Pollinator Interactions Are Phylogenetically Modulated Independently of Domestication in Cucurbita spp.

Abstract

Plant defenses are conserved among closely related species, but domestication can alter host genotypes through artificial selection with potential losses in host defenses. Therefore, both domestication and host phylogenetic structure may influence plant virus infection outcomes. Here, we examined the association of phylogeny and domestication with the fitness of infected plants. We inoculated three pairs of domesticated and wild/noncultivated squash (Cucurbita spp.) with a combination of two viruses commonly found to coinfect cucurbits, zucchini yellow mosaic virus and squash mosaic virus, and recorded fitness traits related to flowers, pollination, fruit, and seed viability in the field over 2 separate years. In an additional field experiment, we recorded the relative abundance of both viruses via RT-qPCR. We found a gradient of susceptibility across the six tested lineages, and phylogenetic structure, but not domestication, contributed to differences in infection outcomes and impacts on several fitness traits, including fruit number, fruit weight, and germination. Plant virus infection also impacted the quantity and quality of floral rewards and visitation rates of specialist bee pollinators. There were no detectable differences in viral load between the six host taxa for either virus individually or the ratio of zucchini yellow mosaic virus to squash mosaic virus. Our results highlight the importance of phylogenetic structure in predicting host susceptibility to disease across wild and domesticated plants and the ability of several hosts to maintain fitness in the field despite infection. Broader consequences of plant pathogens for beneficial insects, such as pollinators, should also be considered in future research.