CAREER: Host-Parasite Coevolutionary Dynamics: Testing key hypotheses in host mating system evolution

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Reproduction is the most essential biological process. It influences how DNA is inherited from one generation to the next. Organisms actually have many different ways of reproducing. It is unclear why the most common should involve genetic contributions from two parents (bi-parental reproduction) as opposed to one (uni-parental reproduction). One important consequence of bi-parental reproduction is that it produces more genetically variable offspring. Why this is an advantage, however, is unclear. One possibility is that genetically variable offspring are more likely to escape infection from parasites and diseases that have adapted to the parents' genetic make-up. Another is that the genetic variability is helpful more generally for adaptation to changing environments. This project uses the nematode worm Caenorhabditis elegans, which can reproduce either uni- or bi-parentally, along with its bacterial parasite, Serratia marcescens, to experimentally test these ideas. The project will also contribute to teaching and training students at many levels, providing opportunities for them to learn scientific methods in a hands-on fashion. It will integrate research with education in undergraduate teaching labs and will include developing and implementing new teaching laboratory classes. It will also train graduate students. Finally, it will include an outreach program that will bring hypothesis testing science to a neighborhood with many young children from underrepresented groups in science. The questions of both how and why bi-parental reproduction is maintained in nature largely remain a mystery in evolutionary biology. Currently, the Red Queen hypothesis (RQH) is the most well supported hypothesis regarding the evolution and maintenance of outcrossing. The central prediction of the RQH is that negative frequency-dependent selection, imposed by coevolving parasites, favors reproduction via outcrossing over self-fertilization in host populations. Although a rapidly growing number of studies demonstrate the ability of coevolving parasites to favor host outcrossing over host self-fertilization, the mode of selection imposed by coevolving parasites, and in general, the coevolutionary dynamics between outcrossing hosts and their respective parasites remain unclear. Here, the fundamental predictions of the RQH will be comprehensively tested in perhaps the only experimental system currently capable of permitting such a test. Specifically, the host, Caenorhabditis elegans, and parasite, Serratia marcescens, populations will be experimentally evolved to determine if coevolving parasites are necessary for the evolution and maintenance of outcrossing, or if only a dynamic changing environment is required. After which, the phenotypic and underlying genetic changes in the hosts and parasites, as well as the mode (or modes) of selection that result from antagonistic coevolution, will be determined through a combination of phenotypic assays, next-generation sequencing, functional genetic testing via transformation, and subsequent experimental evolution.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.