Exploring the Role of Transposable Elements in Reproductive Isolation

Understanding the phenotypic and molecular mechanisms that contribute to genetic diversity between and within species is fundamental in studying the evolution of species. In particular, identifying the interspecific differences that lead to the reduction or even cessation of gene flow between nascent species is one of the main goals of speciation genetic research. Genetic novelty is often implicated in the origin of new molecular functions and in some cases, new phenotypes. As a result, the mechanisms that produce genetic changes are integral in understanding the evolution of species as well as speciation itself. Here, I explore the reproductive consequences of novel mobile genetic elements across the D. simulans complex and its influence on hybridization between Drosophila species along distinct points in the speciation continuum. A precise quantification of the frequency of P-elements (PEs), and transposable elements in general, across different species is still in its infancy. Even though the phenomenon of hybrid dysgenesis has been rigorously characterized in D. melanogaster, the discovery of PEs in other Drosophila species allows us to understand how these elements behave in different genetic backgrounds and the role PEs, and TEs generally, play in affecting gene flow between closely related species. My work suggests that the invasion of TEs in a genome should not be quantified as the singular phenotype of hybrid dysgenesis, but rather multiple distinct effects that vary in intensity based off PE copy-number. I also explore the how PEs affect gene flow between naturally hybridizing species, the first such case in understanding PEs and reproductive isolation between species. This work suggests that 1) the deleterious effects of PEs within a species is dependent on copy-number and 2) PEs lead to a reduction in hybrid fitness within a species-complex, increasing reproductive isolation and potentially facilitating the speciation process.Doctor of Philosoph

Patterns of Population Structure and Introgression Among Recently Differentiated \u3ci\u3eDrosophila melanogaster\u3c/i\u3e Populations

Despite a century of genetic analysis, the evolutionary processes that have generated the patterns of exceptional genetic and phenotypic variation in the model organism Drosophila melanogaster remains poorly understood. In particular, how genetic variation is partitioned within its putative ancestral range in Southern Africa remains unresolved. Here, we study patterns of population genetic structure, admixture, and the spatial structuring of candidate incompatibility alleles across a global sample, including 223 new accessions, predominantly from remote regions in Southern Africa. We identify nine major ancestries, six that primarily occur in Africa and one that has not been previously described. We find evidence for both contemporary and historical admixture between ancestries, with admixture rates varying both within and between continents. For example, while previous work has highlighted an admixture zone between broadly defined African and European ancestries in the Caribbean and southeastern USA, we identify West African ancestry as the most likely African contributor. Moreover, loci showing the strongest signal of introgression between West Africa and the Caribbean/southeastern USA include several genes relating to neurological development and male courtship behavior, in line with previous work showing shared mating behaviors between these regions. Finally, while we hypothesized that potential incompatibility loci may contribute to population genetic structure across the range of D. melanogaster; these loci are, on average, not highly differentiated between ancestries. This work contributes to our understanding of the evolutionary history of a key model system, and provides insight into the partitioning of diversity across its range

The Role of Transposable Elements in Speciation

Understanding the phenotypic and molecular mechanisms that contribute to genetic diversity between and within species is fundamental in studying the evolution of species. In particular, identifying the interspecific differences that lead to the reduction or even cessation of gene flow between nascent species is one of the main goals of speciation genetic research. 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. However, no systematic effort has evaluated the role of TEs in speciation. We compiled the evidence for TEs as potential causes of reproductive isolation across a diversity of taxa. We find that TEs are often associated with hybrid defects that might preclude the fusion between species, but that the involvement of TEs in other barriers to gene flow different from postzygotic isolation is still relatively unknown. Finally, we list a series of guides and research avenues to disentangle the effects of TEs on the origin of new species

Data from: Genetic accommodation in the wild: evolution of gene expression plasticity during character displacement

Ecological character displacement is considered crucial in promoting diversification, yet relatively little is known of its underlying mechanisms. We examined whether evolutionary shifts in gene expression plasticity (‘genetic accommodation’) mediate character displacement in spadefoot toads. Where Spea bombifrons and S. multiplicata occur separately in allopatry (the ancestral condition), each produces alternative, diet-induced, larval ecomorphs: omnivores, which eat detritus, and carnivores, which specialize on shrimp. By contrast, where these two species occur together in sympatry (the derived condition), selection to minimize competition for detritus has caused S. bombifrons to become nearly fixed for producing only carnivores, suggesting that character displacement might have arisen through an extreme form of genetic accommodation (‘genetic assimilation’) in which plasticity is lost. Here, we asked if we could infer a signature of this process in regulatory changes of specific genes. In particular, we investigated whether genes that are normally expressed more highly in one morph (‘biased’ genes) have evolved reduced plasticity in expression levels among S. bombifrons from sympatry compared to S. bombifrons from allopatry. We reared individuals from sympatry vs. allopatry on detritus vs. shrimp and measured the reaction norms of nine biased genes. Although different genes displayed different patterns of gene regulatory evolution, the combined gene expression profiles revealed that sympatric individuals had indeed lost the diet-induced gene expression plasticity present in allopatric individuals. Our data therefore provide one of the few examples from natural populations in which genetic accommodation/assimilation can be traced to regulatory changes of specific genes. Such genetic accommodation might mediate character displacement in many systems

Levis et al. data

Levis et al. dat

Data from: A nonrandom subset of olfactory genes is associated with host preference in the fruit fly Drosophila orena

Specialization onto different host plants has been hypothesized to be a major driver of diversification in insects, and traits controlling olfaction have been shown to play a fundamental role in host preferences. A diverse set of olfactory genes control olfactory traits in insects, and it remains unclear whether specialization onto different hosts is likely to involve a nonrandom subset of these genes. Here, we test the role of olfactory genes in a novel case of specialization in Drosophila orena. We report the first population-level sample of D. orena on the West African island of Bioko, since its initial collection in Cameroon in 1975, and use field experiments and behavioral assays to show that D. orena has evolved a strong preference for waterberry (Syzygium staudtii). We then 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. By comparing signatures of positive selection on olfactory genes between D. orena and its sister species, D. erecta we show that odorant-binding and chemosensory have evidence of positive selection in both species; however, overlap in the specific genes with evidence of selection in these two classes is not greater than expected by chance. Finally, we use quantitative complementation tests to confirm a role for seven olfactory loci in D. orena’s preference for waterberry fruit. Together, our results suggest that D. orena and D. erecta have specialized onto different host plants through convergent evolution at the level of olfactory gene family, but not at specific olfactory genes

Pure species discriminate against hybrids in the Drosophila melanogaster species subgroup

Introgression, the exchange of alleles between species, is a common event in nature. This transfer of alleles between species must happen through fertile hybrids. Characterizing the traits that cause defects in hybrids illuminate 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. In this report, we study whether F1 hybrids between two species pairs of Drosophila are as attractive as the parental species. We find that in both species pairs, the sexual attractiveness of the F1 hybrids is reduced and that pure species discriminate strongly against them. We also find that the cuticular hydrocarbon (CHC) profile of the females hybrids is intermediate between the parental species. Perfuming experiments show that modifying the CHC profile of the female hybrids to resemble pure species improves their chances of mating. Our results show that behavioral discrimination against hybrids might be an important component of the persistence of species that can hybridize

Rapid and predictable evolution of admixed populations between two Drosophila species pairs

The consequences of hybridization are varied, ranging from the origin of new lineages, introgression of some genes between species, to the extinction of one of the hybridizing species. We generated replicate admixed populations between two pairs of sister species of Drosophila: D. simulans and D. mauritiana; and D. yakuba and D. santomea. Each pair consisted of a continental species and an island endemic. The admixed populations were maintained by random mating in discrete generations for over 20 generations. We assessed morphological, behavioral, and fitness-related traits from each replicate population periodically, and sequenced genomic DNA from the populations at generation 20. For both pairs of species, species-specific traits and their genomes regressed to those of the continental species. A few alleles from the island species persisted, but they tended to be proportionally rare among all sites in the genome and were rarely fixed within the populations. This paucity of alleles from the island species was particularly pronounced on the X-chromosome. These results indicate that nearly all foreign genes were quickly eliminated after hybridization and that selection against the minor species genome might be similar across experimental replicates

Supplemental Material for Matute et al., 2020

Supplementary tables for Matute et al. Rapid and predictable evolution of admixed populations between two Drosophila species pair