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Sexual dimorphism, i.e., differences in morphology, physiology, and behavior between conspecific males and females, is ubiquitous, extensive, and often species-specific, indicative of its rapidly evolving nature. Ever since Darwin first described a general theory of sexual selection to explain the extraordinary differences between males and females of the same species, biologists have proposed a variety of mechanisms ranging from runaway selection to good genes to sexual conflict. While a popular approach is studying the effects of sexual selection on different components of fitness, the results of these studies are generally difficult to interpret and are typically not generalizable across populations, let alone taxa. Recent advances in the “omics” field are transforming the way that we study patterns and processes involved in sexual selection. At the molecular level, sexual dimorphism is present in gene expression differences between the sexes, providing a powerful framework to study sexual selection. By studying genes that are sex-biased in expression, we will better understand the underlying genetic basis of traits that are sexually dimorphic. Alreadly, studies of sex-biased genes in model organisms, particularly Drosophila, have revealed that male-biased genes are among the most rapidly evolving functional classes of genes. However, while a number of intrinsic factors appear to correlate with evolutionary rate (e.g., gene expression level, codon bias), it is unclear whether any of these factors drive the rapid divergence of male-biased genes. Another important discovery is the prevalence of sex-biased gene expression. However, even with widespread sexual dimorphism at the phenotypic level, it remains unknown the extent to which sex-biased gene expression exists in humans and their primate relatives. In fact, studies of sexual dimorphism on a molecular level in primates have been very few, even though understanding this phenomenon in humans could further our knowledge of the nature of sex-biased phenotypes and diseases. In this thesis, I advance our knowledge of the genetic bases and mechanisms that shape sexual dimorphism. First, I review a classic framework that biologists have traditionally applied to define and partition fitness measures between males and females in the model system, Drosophila. Second, I apply a molecular framework to compare the relative roles of intrinsic factors on the evolutionary rate of rapidly evolving male-biased genes in Drosophila. Third, I review the current state of our knowledge of sexual dimorphism and sex-biased gene expression in humans. Fourth, I present a bioinformatics framework to identify the extent of sex-biased expression in primate tissue and to examine the selective forces involved in their evolution. Overall, I demonstrate the effectiveness of using a functional comparative genomics approach in studying the nature of sexual dimorphism at the molecular level across multiple taxa. / Biology

The variation of genome content and structure across the tree of life is astounding and can provide clues to understand the process of evolution. Overall, this helps us understand the history of life and how organisms have fundamentally changed and adapted to their environments. Gene duplication is an important mechanism for molecular evolution because it provides opportunity for functional novelty and molecular innovation. Gene duplication creates new functional gene copies with different selective pressures that allow them to take on new or specialized functions. Throughout this work, I explored the interplay between genetic changes, molecular phenotype, and the selection of duplicate gene copies. I particularly focused on the genetic opportunity, consequences, and selective pressures of the mechanisms for short-term and long-term duplicate copy retention. I modeled the stochastic processes of mutation and selection and their effect on duplicate gene copy retention. Specifically, I modeled the interplay between subfunctionalization and dosage balance and found that selection may cause genes that are sensitive to dosage balance effects to experience delayed subfunctionalization, but ultimately lead to higher levels of subfunctionalization. These findings suggest that subfunctionalization may not occur as a purely neutral process. Next, I used survival analysis methods to model patterns of duplicate gene retention in genomes experiencing consecutive whole genome duplication events. I modeled three hypotheses to explain patterns of duplicate gene retention including the Independence Hypothesis, the Gene Duplicability Hypothesis, and a novel Mutational Opportunity Hypothesis. Under the Gene Duplicability and Mutational Opportunity hypotheses, the expected patterns of duplicate gene retention after consecutive whole genome duplication events are greatly affected by the ages of the whole genome duplication events and the functional properties of the genomic content that influence opportunity and selection. Additionally, I describe how statistical model testing techniques can be applied to investigate which hypothesis is consistent with patterns of retention in real-world phylogenetic datasets. I used these described techniques to explore the hypotheses’ parameter space consistent with a modest dataset of fish and plant lineages. These results suggest that a gene duplicate’s retention after whole genome duplication events may be influenced by its functional properties. Key findings underscore the multifaceted nature of duplicate gene retention, influenced by a myriad of factors including genetic opportunity, selective pressures, and evolutionary context. By dissecting the underlying mechanisms driving duplicate gene retention, this dissertation advances our understanding of the evolutionary dynamics shaping genome evolution and functional diversity across diverse biological systems. / Biology

What selective forces and molecular mechanisms govern the integration of worker body size and morphology, brain architecture, and behavior in insect societies? Workers of the remarkably polyphenic and socially complex fungus-growing leafcutter ant Atta cephalotes exhibit a striking agricultural division of labor. The number of morphologically distinct and behaviorally differentiated worker groups, adaptive mosaic neural phenotypes, and brain transcriptomes have not been examined and the influences of socioecological challenges on behavioral performance, cognition, and brain evolution are unclear. We quantified worker morphological and behavioral variation to assess the number of worker size classes and characterized their social roles. We discriminated multiple worker size groups using a Gaussian mixture model: mid-sized workers (“medias”) had the most diverse task repertories and serve dominant roles in leaf harvesting, whereas workers of other size classes performed fewer, more specialized behaviors. We used variation among tasks in sensorimotor functions and task performance frequencies to create an estimate of sensory integration and processing demands across worker size groups. This metric predicted that medias require the greatest neural investment due to the high diversity of sensory inputs and motor functions associated with their task set. We quantified the volumes of key neuropils in brains of workers of different sizes and determined their allometries, finding that our estimate corresponded to proportional investment in the mushroom bodies, a brain compartment responsible for learning, memory, and sensory integration, and identifying allometric scaling patterns in other brain centers. Additionally, we measured whole-brain gene expression and identified significant differences in expression levels for numerous genes likely to underpin behavior. Differences were most pronounced between the smallest (fungal gardener “minims”) and largest (defensive “majors”), although not all expression differences were driven by worker size. Overrepresented gene functional categories included those related to sensory processing (enriched in genes upregulated in medias and minims) and metabolism (enriched in genes upregulated in majors). These results identify the nature of selective forces favoring differentiation along morphological, neuroanatomical, behavioral, and molecular axes among A. cephalotes workers and the impact of advanced division of labor on brain evolution. / 2023-03-01T00:00:00Z

2024 / Mnemiopsis leidyi, the sea walnut, is one of the most destructive invasive species in the world. The ctenophore has broad environmental tolerances, a high rate of zooplankton consumption, extensive regeneration capabilities, and extraordinary fecundity. While there is a substantial body of research on M. leidyi’s role as a predator of zooplankton and as prey to the ctenophore Beroe ovata, only a few studies have examined M. leidyi’s relationship with its parasite, the lined sea anemone, Edwardsiella lineata. Previous research has shown that E. lineata may be exerting top-down control on the ctenophore in areas where present along the Northwestern Atlantic; the parasite has not established a population in M. leidyi’s invasive range. While a handful of studies have examined the ecological relationship between host and parasite, all studies have taken place at the same site, Woods Hole, and some failed to report key parameters such as host size and parasite number. More detailed examinations of this relationship are necessary to understand the parasite’s potential for controlling host populations in both native and European waters and how this control may be affected under various abiotic conditions. In my dissertation I performed three studies exploring the ecological relationship between M. leidyi and E. lineata. First, I profiled the variation in infection frequency in populations in Massachusetts and Rhode Island and examined the relationship between host size, parasite load, and seasonality. My results show that in natural populations, infected ctenophores are larger than non-infected conspecifics. The pattern of infection was also highly variable across sites and time. Second, I tested the temperature and salinity tolerances of E. lineata larvae to determine if certain conditions, such as those found in the invasive range of M. leidyi are refuges for the host from parasitism. My data indicate that temperature and salinity conditions alone will not prevent E. lineata from establishing a population in Europe. However, developmental outcomes and survival are both reduced at lower salinities and higher temperatures. Finally, using a RAD-seq approach I profiled population connectivity between juvenile parasite and adult polyp populations of E. lineata in Massachusetts and Rhode Island. E. lineata populations were found to be panmictic like host M. leidyi, though some structuring appeared between parasite and polyp populations. While asexual reproduction was seen in polyp mats, none was found within hosts.These data help contribute to the wider body of research on the M. leidyi-E. lineata system and also provide data on sea anemone genetic structure, which is currently understudied. I suggest that future studies examine cues for asexual reproduction in both the parasite and host and profile infection frequency and genetic structure in populations further south. / 2027-02-10T00:00:00Z