A longstanding question in evolutionary biology is what factors contribute to the astounding levels of observed and estimated species diversity on this planet. Intimately tied to this question is both how new species form and how species remain distinct. The biological species concept links this process to the establishment of reproductive barriers. Under this framework, the process of speciation involves the acquisition of barriers that keep two populations from successfully reproducing, ultimately limiting gene flow between them.
One such barrier is hybrid incompatibility, which occurs when hybrids between two species are inviable, sterile, or simply less fit than the parental populations. Hybrid incompatibility is a particularly interesting reproductive barrier because, unlike others, it is irreversible once complete. Bateson, Dobzhansky, and Muller first showed how genetic incompatibilities could form between two populations such that hybrids between them would be less fit. Genes underlying genetic and sexual conflict are well-suited for generating these incompatibilities, as their selective interests are already in direct conflict with other genes in the genome.
My research interests focus on exploring how elements that generate genetic conflict generate hybrid incompatibility and potentially contribute to speciation. I do this by integrating population genetic theory and computer simulations that model long-term evolutionary processes with large-scale datasets containing whole-genome and -transcriptome information for populations exhibiting hybrid incompatibilities that may be due to genetic conflict.
Transposable Elements as Drivers of Speciation
Transposable elements (TEs) are mobile repetitive DNA sequences that actively increase their copy number and propagate themselves within genomes. TEs likely invade naive populations via horizontal transfer or hybridization, where the TE moves into the germline of the recipient population and then spreads through the genome as well as the population via vertical transmission. TE abundance varies greatly between species, and the proportion of the genome occupied by TEs ranges from ~10% in Arabidopsis to ~85% in maize.
Differences in TE content are known to contribute to reproductive isolation. The uncoupling of TEs from the molecular machinery that epigenetically silences their proliferation in hybrids is a potential cause of hybrid incompatibility. While the role of TEs in driving speciation is well-characterized, comparatively little attention has been given to how the interaction between repetitive DNA and their repressor systems may generate or sustain hybrid incompatibilities in an epigenetic paradigm somewhat analogous to traditional Dobzhanksy-Muller incompatibilities.
I am currently exploring how regulation of TE transposition impacts the mean copy number of a TE family within a population and whether compromising that regulation in hybrids is capable of driving and sustaining hybrid incompatibilities between populations. I am using both a theoretical approach, by constructing models and computer simulations that explore how biological differences between TE families and different mechanisms for transposition regulation contribute to mean TE copy number and host population size over time, and an experimental approach, by investigating a particularly strange form of hybrid incompatibility between domestic maize and teosinte which is thought to be due to TE proliferation.*
Mitochondrial-Nuclear Conflict and Hybrid Incompatibility
Eukaryotic genomes are partitioned between the nucleus, which stores autosomes and sex chromosomes, and cytoplasmic DNA, such as organellar or symbiont genomes. These distinct genetic elements are differentially transmitted. Unlike autosomes that spend equal amounts of time in males and females, sex chromosomes spend either ⅔ of their time in the homogametic sex (i.e., X or Z chromosome) or all of their time in the heterogametic sex (i.e., the Y or W chromosome). The mitochondrial genome, while present in both sexes, is almost universally exclusively maternally inherited.
This transmission asymmetry can lead to genetic conflict. Notably, exclusive maternal transmission of the mitochondrial allows male-harming, female-neutral/advantageous mutations to persist or even increase in frequency within the population. This results in selective pressure for nuclear compensators that counteract or reverse this reduction to male fitness. The chromosomal location of nuclear compensators likely influences the evolution and fixation of these variants determining how effectively they restore male fitness.
I am interested in how transmission asymmetries of autosomal, sex chromosome-linked, and mitochondrial genes may both cause and resolve sexual conflicts. We have developed theoretical models and computer simulations to how sexually antagonistic mitochondrial variants Invade populations and how resolution of this conflict differentially evolves depending on the chromosomal location of nuclear compensators. We have also leveraged a collection of nearly isogenic Drosophila melanogaster lines that vary only in either their mitochondrial haplotype or Y chromosome haplotype to identify genes that exhibit differential expression in males for genes involved with male fertility, metabolism, and immunity confirming theoretical expectations that mitochondrial and Y chromosomal genes interact to impact male phenotypes.