Collaborative Research: Rapid and Pervasive Mitochondrial Heteroplasmy with Recombination in a Remerging Ectoparasite

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Mitochondria are parts of cells that have their own DNA, as well as a fundamental role in metabolism. They are essential for animal life. With advances in DNA sequencing it has recently been shown that some individuals may possess multiple, distinct lineages of mitochondria in their cells. This suggests that the presence of multiple types of mitochondria, a condition known as heteroplasmy, may be an integral part of the evolution of many species. This finding is very surprising, because mitochondria, almost always are inherited from the mother only, and in humans, heteroplasmy has been linked to severe genetic disease. From an evolutionary perspective, the presence of more than one type of mitochondria in an individual may have an important function in generating genetic diversity. It is likely that the presence of multiple types of mitochondria presents opportunities to exchange genes between different mitochondrial lineages. Despite growing recognition of the potential significance of heteroplasmy, this aspect of animal evolution remains poorly understood. This project aims to address key questions relating to how heteroplasmy is generated, how long it can be maintained, and whether genes are exchanged between mitochondrial lineages. The bed bug will be used as a model species for these studies because it exhibits unusually high levels of heteroplasmy. Experiments to resolve these questions have the potential to fundamentally change how we look at genetic inheritance of mitochondrial DNA in animals. The project will include training of undergraduate and post-doctoral scholars, the establishment of a collaborative network of researchers and pest control operators, and public outreach in both Oklahoma and North Carolina. Furthermore, given that the bed bug is a significant public health concern, establishing it as a model system will continue to bring them to public attention, reinforcing awareness of the species.While uniparental inheritance appears to predominate in the animal kingdom, the growing evidence of heteroplasmy through paternal leakage and compelling recent evidence of mtDNA recombination, underscores that while we have developed a great understanding of mitochondrial function and evolution, our understanding of mitochondrial inheritance is far from complete. The bed bug, Cimex lectularius, is an ectoparasite that has seen an unprecedented resurgence in recent years. Studies have revealed that it exhibits high levels of mtDNA heteroplasmy, which is both pervasive and rapidly generated. Furthermore, mtDNA recombination appears common. Given the suitability and tractability of this species as a model system, this study will: (1) Address how intra- and inter-population genetic characteristics correlate with rates of heteroplasmy; (2) Investigate the degree to which mitogenomic divergence and mitonuclear interactions affect the rate of paternal leakage; (3) Empirically and theoretically examine heteroplasmy decay in a species where it is common and pervasive and for which genetic drift vs. selection may be evaluated; and (4) Take a complete mitogenomic approach to investigate recombination and the presence of recombination hotspots. Due to the high rate of leakage and recombination seen in the bed bug in concert with recent advances in DNA sequencing technology and analytical methods, this system offers a unique opportunity to address this hotly debated and evolutionarily consequential question.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.