Speciation is the process through which populations diverge and accumulate reproductive isolating mechanisms through a buildup of genetic differences. I am an evolutionary geneticist that is interested in studying the forces that generate and maintain genetic diversity within and between species. I explore the genetic basis of reproductive isolation through a combination of classical genetics, field collections, and population genomics approaches across groups of genetically tractable organisms that hybridize in natural conditions and in the lab. My research goal is to discover the molecular basis of traits that underlie reproductive isolation, and characterize patterns in how genomes diverge as speciation progresses. My research spans multiple hybridizing species complexes, with a focus on genetic sources of incompatibility, evolution of behavioral preference, and gene by environment interactions.
Genetic Sources of Incompatibility
Transposable Elements in Speciation
Transposable elements (TEs) are DNA sequences with the ability to move within genomes. TEs are ubiquitous throughout eukaryotic genomes and have been shown to alter regulatory networks, gene expression, and to rearrange genomes as a result of their transposition. I systematically compiled the evidence for TEs as potential causes of reproductive isolation across the tree of life. We found that TEs are often associated with hybrid defects that might reduce gene flow between species, however, the involvement of TEs in other barriers to gene flow apart from postzygotic isolation is poorly understood.
P-elements are one of the most studied TEs in Eukaryotes due to a suite of deleterious fitness effects when PE-carrying males mate with PE-absent females. Despite detrimental effects, PEs spread throughout worldwide populations of D. melanogaster and D. simulans within decades. I leveraged the recent invasion of PEs into D. simulans, to test how PE copy-number affects PE-induced phenotypes. I found that as copy-number of PEs throughout the genome increases, so do the deleterious effects that reduce fitness in the host.
D. simulans can hybridize with its sister species, unlike D. melanogaster, providing a unique window to explore the effect of PEs on hybrization between closely related species. I found that, compared PE-absent crosses, the presence of the PE in D. simulans parentals resulted in a significant drop in fecundity of F1 hybrid females. PE-mediated reproductive costs between species were significantly higher than the PE-associated costs within species. Overall we suggest mechanisms through which TEs can spread throughout populations rapidly, before the onset of significant deleterious consequences and that the presence of TEs can serve to strengthen reproductive isolation between sister species.
P-elements & Hybridization in Drosophila
Evolution of Behavior
Characterizing the traits that cause defects in hybrids illuminates how and when gene flow is expected to occur. Inviability and sterility are extreme examples of fitness reductions but are not the only type of defects in hybrids. Some traits specific to hybrids are more subtle but are important to determine their fitness. Cuticular hydrocarbons (CHCs) are are fatty acid-derived apolar lipids that accumulate on the body cuticle of insects, serving as protection against dessication and communication between individuals. We developed a novel method to characterize CHC profiles across two distinct monophyletic groups of hybridizing sister species. We find that in both species pairs, the sexual attractiveness of the F1 hybrids is reduced, due to intermediate CHC profiles, and that pure species discriminate strongly against them. This work highlights behavioral discrimination against hybrids as an important component of the persistence of species that can hybridize.
Specialization onto different host plants has been hypothesized to be a major driver of diversification in insects. We collect and test the first population-level of D. orena in 40 years from the island of Bioko, describing a novel case of host specialization on waterberries. Traits controlling olfaction have been shown to play a fundamental role in host preferences. By comparing signatures of positive selection on olfactory genes between D. orena and its sister species we show that odorant-binding and chemosensory have evidence of positive selection. Overall we show that a nonrandom subset of genes controlling olfaction-–those controlling odorant-binding and chemosensory proteins–-have an enriched signature of positive selection relative to the rest of the D. orena genome.
Plasticity: Gene by Environment Interactions
Spadefoots of the genus Spea normally produce alternative larval ecomorphs that utilize different dietary resources: ‘omnivores,’ which eat mostly detritus, and ‘carnivores,’ which are induced by, and specialize on, shrimp and other tadpoles. These ecomorphs phenotypically differ phenotypically alongside their dietary specialization. Carnivores (left) are larger than omnivores in body size and have proportionally larger jaw muscles, a more serrated keratinized beak and a shorter gut. We investigated whether sympatric populations that historically produce mostly carnivores (reduces competition with heterospecific) experience reduced plasticity in carnivore-candidate genes. Our data shows that sympatric populations have lost diet-induced gene expression plasticity, constitutively producing carnivore-like morphs.
Adaptation in Texas Wildflower Hybrids
Identifying and experimentally testing the effects of variation in key environmental variables on fitness provides vital insight into how selection maintains species barriers. Phlox drummondii shares a zone of sympatry with two sister species, P. roemeriana and P. cuspidata, yet has only evolved character displacement in coloration with the latter. We tested whether another form of reproductive isolation has reduced selection for character displacement in the P. drummondii and P. roemeriana sympatry zone. We used environmental niche modeling and experimental manipulation to determine whether the sister species are locally adapted and experience ecological reproductive isolation. We found that P. drummondii and P. cuspidata overlap greatly in their modeled niche space and have overlap in their phenotypic response to a dry-down experiment, while P. roemeriana has reduced niche overlap and a different trait response than its sister species. Our findings provide support for differential local adaptation of P. roemeriana acting as a reproductive isolating barrier, suggesting that overlap in niche optimum between P. drummondii and P. cuspidata increased selection for the evolution of character displacement within P. drummondii.