The evolutionary significance of genetic pleiotropy in species interactions

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Nearly all plants and animals rely on other species for food or to attract mates. These beneficial partnerships between species are known as mutualisms. Although mutualisms are necessary for survival and reproduction, they come at a cost: often, forming a mutualism leaves an individual defenseless against parasites and other infections. This research will investigate when and how parasites affect the function and evolution of mutualisms. The researchers will test these questions in legume plants (alfalfa, peas, and beans) that rely on mutualistic bacteria for a key nutrient, nitrogen. In a series of experiments using alfalfa and its relatives, the researchers will determine how parasites affect the evolution of plant genes used to form mutualisms, and test whether some mutualistic partnerships (i.e., plant-bacteria pairs) are less affected by parasites than others. This research is important because nearly all crop plants rely on fungi or bacteria for nutrients, so understanding when and how parasites jeopardize mutualisms like these is essential to protect these economically and ecologically significant partnerships. The broader impacts of this project include training junior scientists and two new programs to teach data analysis—an essential scientific skill—to undergraduate biology students.The overarching goal of this research is to test the central hypothesis that genetic pleiotropy—when the same gene influences multiple traits—is a widespread and evolutionarily significant feature of species interactions. This project will test this hypothesis in the model mutualism between legumes in the genus Medicago and nitrogen-fixing bacteria. Many plant genes involved in the bacterial mutualism are implicated in resistance to parasitic root-knot nematodes, creating a genetic tradeoff between the two interactions. This project has three objectives: (1) Test whether pleiotropy linking mutualism and parasitism constrains the evolution of genes underlying both interactions by comparing population genomic signatures of selection at pleiotropic genes to mutualism- and parasitism-specific genes. (2) Evaluate whether pleiotropy is context dependent by testing whether pleiotropic tradeoffs with parasitism persist across multiple strains of mutualistic bacteria, integrating population genomics and quantitative genetics. (3) Determine whether pleiotropy is evolutionarily conserved by comparing the genetic tradeoff between the bacterial mutualism and resistance to parasitic nematodes across six Medicago species.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.