Relationship between Intrapopulation Processes and Reproductive Isolation

For sexually reproducing organisms, a large part of their fitness depends on how well they compete for and obtain mating opportunities. This “sexual selection” was recognized as a strong driver of evolution by Darwin, and has since been invoked to describe broad scale patterns of biodiversity. Only by studying the mechanistic and genetic links between sexual selection and reproductive isolation will biologists be able to determine the influence of this force on evolutionary processes generating biodiversity.

My research focuses on the genetics and evolution of sexual interactions, mating behavior and speciation, especially prezygotic reproductive isolation, leveraging the power of multiple empirical systems in conjunction with new statistical approaches and theory. A challenge for understanding the evolution of prezygotic reproductive isolation is that many different forces shape the complex behaviors involved in sexual interactions. Thus, it is paramount to understand how traits, and their underlying genes, respond to these various selective pressures.  My goal is to integrate understanding of behavioral phenotypes with the genes and molecular mechanisms underlying these traits.

speciation diagram
Sexual selection, adaptation, and drift operate throughout lineage diversification and speciation. A major challenge is to determine which forces contribute to the evolution of reproductive isolation

Postmating Prezyogitc Isolation

One common assumption in evolutionary biology is that sexual selection unilaterally drives the evolution of reproductive isolation. Given a shared genetic basis, however, selection for increased reproductive isolation could constrain or facilitate sexual selection, when closely related species co-occur. This shared genetic basis is foundational to many models of speciation but remained untested. We demonstrated that genes important for sperm competition also contribute to reproductive isolation in D. melanogaster (Castillo & Moyle 2014; Proc. Roy. Soc.). In this experiment, we used strains of D. melanogaster that lacked function of an important component of sperm competition and demonstrated these genes also impact the level of reproductive isolation, via conspecific sperm precedence, between D. melanogaster and D. simulans.

I subsequently tested the hypothesis that selection for increased reproductive isolation in sympatry (reinforcement) can affect sexual selection and sexual interactions within natural populations. Using the sister species D. pseudoobscura and D. persimilis, I found a pattern consistent with reinforcement where reproductive isolation via conspecific sperm precedence was stronger in sympatric populations compared to allopatric populations (Fig. 1). Using these same genotypes, I completed a within-population sperm competition experiment and found, unexpectedly, that reinforcement had constrained sexual selection in sympatric populations (Castillo & Moyle In Review).

Quartz %d

In parallel, I determined how sperm competition could maintain genetic differentiation between populations. I assayed sperm competition of simulated “migrant” individuals and found that sympatric males suffer a sperm competition disadvantage. I tested which genomic regions are differentiated by sequencing whole fly transcriptomes for both males and females of all genotypes to examine. I found that known accessory gland proteins with roles in sperm competition were highly differentiated between allopatric and sympatric populations.

I am developing this system as a model to study how complex traits respond to sexual selection and reproductive isolation. Females in this group have spermicidal reproductive tracts, which we can use to compare the physiology of female reproductive tracts and male sperm survival to understand the mechanistic basis of postcopulatory reinforcement.  This work will establish this system as an example of reproductive isolation mediated by cryptic female choice and heterospecific male-female compatibility.

Incipient speciation and the genetic basis of female choice

The evolution of reproductive isolation is necessary for diversification and we must understand which traits confer reproductive isolation at the earliest stages of divergence. I am using races of D. melanogaster that show partial reproductive isolation as a model to understand how female preference evolves. A strong candidate gene, desat2, has been previously identified in this system and is thought to contribute to female preference and pheromone differences between these races. Genes, like desat2, that affect multiple traits may facilitate rapid speciation by linking female preference with mating signals, such as pheromones. I am using genomic editing (CRISPR) and analysis of expression patterns to differentiate the effects of this gene on pheromone production, pheromone perception, and female choice. I have generated desat2 null mutations in specific wild-type backgrounds to analyze changes in pheromone production and sexual behaviors caused exclusively by desat2. I am also creating mutants that no longer produce female pheromones to manipulate pheromone content. Combined, these experiments will allow for a definitive test of whether pheromone production or pheromone perception, mediated by desat2, is responsible for female choice.

Experimental Evolution of Premating Isolation

The use of experimental evolution in model systems is a powerful method to uncover the underlying mechanisms controlling evolution, and to reveal historical processes that contribute to adaptation and speciation. When populations adapt to new environments, ecological divergence and/or behavioral divergence are often correlated with reproductive isolation. Experimental evolution is one of the few ways that trait divergence can actually be connected with the selective forces shaping these populations.

Using experimental evolution, I determined the relative contribution of ecological divergence and sexual selection to the evolution of premating isolation in Caenorhabditis remanei populations (Castillo et al. 2015; Evolution). I found that sexual selection led to the rapid evolution of assortative mating and copulation latency. One prevalent expectation is that segregating variation facilitates rapid evolution. Using the power of a model system in which an ancestral population can be retained and retested, I was able to provide evidence in support of this expectation by demonstrating significant genotypic variation between male x female genotype combinations for mating traits (Castillo & Delph 2016; Evolution).

Transposable Elements and Speciation

Using D. virilis and relatives I am trying to determine whether TEs can have any effect on reproductive isolation between species via dysgenesis (a phenomenon seen in intraspecies crosses) by completing controlled crosses where I know the identity of a specific TE that causes dysgenesis within species

TE expectation
One model describing the expectation that increased reproductive isolation will only be seen in interspecific crosses where one species has a unique TE (blue circles)

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