ABSTRACT

Harmful mutations can negatively affect gene, protein, and organism function. In the extreme, the accumulation of harmful mutations can lead to population extinction. The genetic information in mitochondria - the main source of energy production in most complex organisms - is usually passed intact from parents to offspring. Thus, the mitochondria should be especially prone to the buildup of harmful mutations. However, mitochondria have maintained their function for more than one billion years; how and why is an important question in evolutionary biology. This research uses a model snail system to address these questions. It takes advantage of the fact that some lineages of snails pass both their nuclear and mitochondrial genomes on to their offspring without any genetic shuffling; a process that accelerates the accumulation of mutations in these snails. By contrast, there is shuffling of genetic material between parents and offspring in other lineages of the same snail species. This project will compare different lineages of snails, some with genetic shuffling and some without. In doing so, this research will explore how harmful mutations are cleared from populations. Reducing the impact of harmful mutations is important for keeping organisms healthy. In turn, healthy organisms can guard against population extinction. It is possible that harmful mutations in the mitochondria are compensated for by mutations in nuclear genes. This hypothesis will also be tested by this research. Because functional mitochondria are important to the health of many organisms, the research will be relevant to the biomedical and agricultural communities. The research will also train a new generation of scientists and broaden participation in biology. The broader impacts include collaborations with high school students and museums. The project will also extend an award-winning partnership with the National Center for Science Education to new audiences.

The research combines genetic and functional methods to test for signatures of mitochondrial-nuclear coevolution in the New Zealand freshwater snail Potamopyrgus antipodarum. In this snail system, some lineages are sexual and others are asexual. Crucially for this study, the asexual lineages of P. antipodarum have higher mitochondrial substitution rates than the sexual lineages. This contrast in mitochondrial substitution rates permits the study's two objectives. Objective 1 will test the hypothesis that higher mitochondrial substitution rates in asexual versus sexual lineages drive stronger mitochondrial-nuclear molecular coevolutionary dynamics. One prediction of these coevolutionary dynamics is that substitution rates for proteins encoded by the nuclear genome that are then targeted to the mitochondria will be higher than the substitution rates in control nuclear gene sets. Objective 2 will test for functional effects of mitonuclear interactions on mitochondrial respiration and snail metabolic rate. Since temperature can impact snail metabolic rates, the second objective will include four different temperature treatments. Results of this research will contribute to our understanding of the mitochondrial-nuclear interactions that define eukaryotes. Furthermore, they are of broad relevance to genome evolution, speciation, and the functional and evolutionary consequences of reproductive mode variation.

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.

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