Cytonuclear incompatibility contributes to incipient speciation

Barnard-Kubow, Karen, Biology - Graduate School of Arts and Sciences, University of Virginia
Galloway, Laura, Department of Biology, University of Virginia

Understanding how new species form is one of the central goals of evolutionary biology. While historically studies have focused on the role of nuclear genetic incompatibilities in speciation, cytonuclear incompatibilities have been proposed to be among the first genetic incompatibilities to arise, influencing the early stages of the speciation process. However, due to the lack of studies characterizing reproductive isolation at the intraspecific level, little is known regarding the role of cytonuclear incompatibilities at these early stages. The effect of cytonuclear incompatibility could be mitigated though biparental plastid inheritance, by increasing the likelihood of individuals inheriting a compatible chloroplast. Alternatively, accelerated plastid evolution could speed up the co-evolution of the plastid and nuclear genomes, increasing the propensity for cytonuclear incompatibility when crossing between populations. This dissertation uses Campanulastrum americanum as a system to study how biparental plastid inheritance and accelerated plastid evolution may impact the evolutionary dynamics of cytonuclear incompatibilities and their contribution to incipient speciation. Analysis of chloroplast and nuclear markers distinguished four geographically structured, genetically divergent lineages in C. americanum. Crossing studies found substantial reductions in germination and survival when crossing between these lineages. There was also evidence for cytonuclear incompatibility underlying reproductive isolation in survival, supporting the idea that cytonuclear incompatibilities arise early in the speciation process. However, reproductive isolation between divergent lineages appeared to be reduced in the Appalachians where these lineages are likely in secondary contact. In addition, analysis of plastid inheritance patterns found that C. americanum has biparental plastid inheritance, which in genetically-divergent crosses mitigates the impact of cytonuclear incompatibility on reproductive isolation, potentially slowing the speciation process. In contrast, analysis of plastid sequence divergence and polymorphism in C. americanum found evidence for increased nucleotide substitution rates acting at the among and within species level, suggesting that accelerated plastid evolution may facilitate the development of cytonuclear incompatibility in this species. Altogether, cytonuclear incompatibility appears to be contributing to incipient speciation in C. americanum, but the dynamics of this contribution are being influenced, often in opposing ways, by a variety of mechanisms, including gene flow, biparental plastid inheritance and accelerated plastid evolution.

PHD (Doctor of Philosophy)
evolution, speciation, cytonuclear incompatibility, reproductive isolation
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