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DuBose, J. G.

Publications and source records attributed to DuBose, J. G..

9 recordsLinked to original sources

The roles of dispersal limitation and pre-adaptation in shaping Paraburkholderia endosymbiont frequencies in social amoeba communities

Endosymbiotic interactions have long played fundamental roles in shaping the evolution and diversification of eukaryotes. However, we still have a limited understanding of how ecological processes govern the distribution of endosymbionts that are still segregating in host populations. To contribute to this understanding, here we use the interactions between Paraburkholderia endosymbionts and their Dictyostelid social amoeba hosts as a model system to investigate the role of dispersal, a fundamental ecological process, in shaping the distribution and evolution of endosymbiotic interactions. We first found that patterns of endosymbiont diversification were highly biogeographic, suggesting a significant degree of dispersal limitation. We then experimentally mediated the dispersal of several endosymbiont species into environments with multiple host species and found that each symbiont was able to sustain a high prevalence in each host population. The benefit/detriment of these mediated interactions did not change with increasing phylogenetic distance from what is suspected to be the focal amoeba host species in nature. Taken together, our findings suggest Paraburkholderia endosymbionts are generally pre-adapted to occupy a variety of Dictyostelid host environments, and their distribution among host populations is subject to a high degree of dispersal limitation. Overall, our findings have significant implications for our understanding of how ecological processes facilitate and limit the evolution of endosymbiotic interactions. ImportanceEndosymbiotic interactions are ubiquitous in complex eukaryotes, as organelles such as mitochondria and chloroplasts represent the remnants of what were once free-living prokaryotes. However, how ecological processes facilitate the transition from free-living to host-associated is less understood. Selection is the most commonly invoked process to explain this transition: symbionts that are better at infecting hosts and potentially confer some benefit rise in frequency because they are selected for (and otherwise selected against). However, this only describes one fundamental process that can shape the ecology of symbiotic interactions. Here we present evidence that the importance of dispersal (and its limitations) likely exceeds that of selection in shaping the distribution and frequency of Paraburkholderia endosymbionts in their Dictyostelid social amoeba host communities. These findings highlight the need to consider the interaction between ecological processes, rather than individual processes, when understanding the ecology and evolution of endosymbiotic interactions.

evolutionary biology↗

Evaluating the use of Monte Carlo simulation for statistically assessing topological congruence of phylogenetic trees

Variation in host-associated microbial communities often parallels patterns of phylogenetic divergence between hosts, a pattern known as phylosymbiosis. Understanding of this phenomenon relies initially on quantifying phylosymbiotic signals from across a broad range of host taxa. Quantifying signals of phylosymbiosis is typically achieved by calculating how congruent a hosts phylogenetic tree is with a dendrogram that represents patterns of dissimilarity in their associated microbial communities. To statistically assess the degree of congruence, several studies have constructed null models using a Monte Carlo approach to randomly sample trees. Although this approach is becoming more common, it has several features that warrant benchmarking to advise its further use. This approach relies on quantification of congruence between a hosts phylogenetic tree its microbial community dendrogram. Therefore, it is important to establish how choice of congruence metric influences null model-based inferences. Furthermore, phylosymbiotic signals may manifest at different scales of host divergence, and it is important to establish the extent of host phylogenetic breadth needed to reliably detect a phylosymbiotic signal. To help improve our study of phylosymbiosis, here I examine how power and type 1 error (false positive) rates associated with this approach varies with choice of congruence metric and host phylogenetic coverage. Furthermore, I examine variation in sensitivity given uncertainty in tree estimation, as well as how well null congruence models align with expectations of community assembly that is completely neutral with respect to host phylogeny. I generally found that model performance increased rapidly with increasing tree sizes, suggesting lower limits on the host phylogenetic breadth needed to reliably detect phylosymbiotic signals with this approach. Furthermore, I found several notable variations in performance between congruence metrics, which translated into different inferences regarding signal detection. Overall, these findings suggest that Monte Carlo sampling across tree space can be an effective way to quantify phylosymbiotic signals and highlight key considerations for its implementation.

bioinformatics↗

Reduced signatures of gene duplication and non-random gene organization in shaping stage-specific patterns of gene expression across a relatively simple life cycle

Complex eukaryotes generally experience some degree of ecological transition as they develop, which is usually accompanied by the expression of different traits across their ontogeny. Theory suggests the evolution of differentiation between life stages is facilitated by the expression of different genes at different points throughout ontogeny, which alleviates pleiotropic evolutionary constraints. Therefore, ascertaining what contributes to specialized patterns of gene expression across ontogeny is fundamental to understanding the evolution of ontogenetic complexity. Expression divergence between duplicate genes and gene organization on chromosomes have been identified as important features of relatively complex ontogenies. Therefore, one could predict that their link to transcriptional specialization across ontogeny may be weaker in relatively simpler life cycles. Here, we investigated the links between gene duplication, gene organization, and stage-specific patterns of expression across the relatively simple Caenorhabditis elegans life cycle. We found that signatures of stage-biased chromosomal regions were weaker in C. elegans than what has been previously described in organisms with more complex ontogenies. Furthermore, we found the extent that duplicate genes varied in ontogenetic expression pattern was more constrained in C. elegans. Overall, our findings add to a body of evidence that suggests a link between gene duplication and gene organization and the evolution of complex ontogenies.

evolutionary biology↗

The role of a non-native host plant in altering the seasonal dynamics of monarch development

The development and life history of many organisms have evolved to align with annual seasonal changes, but anthropogenic ecological changes have started to disrupt phenological dynamics. To understand the implications of these changes, tractable model systems are needed to identify the causes and consequences of phenological-seasonal asynchrony. Here, we investigate the potential of a non-native and tropical host plant whose phenology has been tuned to different seasonal dynamics to influence the seasonal developmental dynamics of the migratory monarch butterfly Danaus plexippus. Consistent with predictions, we found that the non-native host plant facilitated successful monarch development later into the fall and early winter, which is typically the season North American monarchs enter reproductive diapause and migrate to over-wintering locations. Furthermore, we found evidence that this success could partly be attributed to decreased thermal constraints on development experienced by monarchs reared on A. curassavica.

ecology↗

Extensive transcriptional differentiation and specialization of a parasite across its host's metamorphosis

Foundational theory on life cycle evolution suggests that given genetic independence, the phenotypes presented by different life stages will diverge more when they occupy more dissimilar niches. When divergence between stages is significant and punctual, we typically consider the life cycle complex. In parasites, the delineation between simple and complex life cycles is usually made between those that occupy single and multiple host species. However, many parasites can experience significant niche shifts in a single host. To explore the potential for a hosts metamorphosis to shape divergence between stages across its parasites life cycle, we quantified the transcriptional differentiation and specialization that the protozoan parasite Ophryocystis elektroscirrha exhibits across the metamorphosis of its host the monarch butterfly. We found evidence that O. elektroscirrha differentiates in concordance with the ecological turnover imposed by monarch transitions to different stages, and that patterns of transcriptional decoupling across the O. elektroscirrha exceeded even that of its host. However, because of its greater gene content, the monarch exhibited greater total transcriptional turnover than its parasite. These findings highlight that synthesis of evolutionary theory pertaining to free-living and parasitic life cycles could be facilitated by more nuanced and continuous descriptions of life cycle complexity.

evolutionary biology↗

The relative importance of host phylogeny and dietary convergence in shaping the bacterial communities hosted by several Sonoran Desert Drosophila species

Complex eukaryotes vary greatly in the mode and extent that their evolutionary histories have been shaped by the microbial communities that they host. A general understanding of the evolutionary consequences of host-microbe symbioses requires that we understand the relative importance of host phylogenetic divergence and other ecological processes in shaping variation in host-associated microbial communities. To contribute to this understanding, we described the bacterial communities hosted by several Drosophila species native to the Sonoran Desert of North America. Our sampling consisted of four species that span multiple dietary shifts to cactophily, as well as the dietary generalist D. melanogaster, allowing us to partition the influences of host phylogeny and extant ecology. We found that bacterial communities were compositionally indistinguishable when considering incidence only but varied when considering the relative abundances of bacterial taxa. Variation in community composition was not explained by host phylogenetic divergence but could be partially explained by dietary variation. In support for an important role of diet as a source of ecological selection, we found that specialist cactophilic Drosophila deviated more from neutral predictions than dietary generalists. Overall, our findings provide insight into the evolutionary and ecological factors that shape host-associated microbial communities in a natural context.

evolutionary biology↗

The role of gene duplication in facilitating divergent patterns of gene expression across a complex life cycle

Explaining the processes that facilitate divergence in the morphologies and functions expressed by organisms throughout their life cycles is fundamental for understanding life cycle evolution. Theory suggests that the expression of traits is decoupled across life stages, thus allowing for evolutionary independence. Although trait decoupling between stages has been described in many studies, explanations of how said decoupling evolves have seldom been considered. Here, we propose evolutionary divergence between duplicate genes as an important mechanism by which life cycle complexity evolves. Because the different phenotypes expressed by organisms throughout their life cycles are coded by the same genome, trait decoupling between stages must be mediated through their divergence in gene expression. Gene duplication has been identified as an important mechanism that enables divergence in gene function and expression between cells and tissues. Here, we examined the temporal changes in gene expression across the monarch butterfly (Danaus plexippus) metamorphosis. We found that within homologous groups, more phylogenetic divergent genes exhibited more distinct temporal expression patterns, and that this relationship scaled such that more phylogenetically diverse homologous groups showed more diverse patterns of gene expression. Furthermore, we found that duplicate genes showed increased stage-specificity relative to singleton genes. Overall, our findings suggest an important role of gene duplication in the evolution of trait decoupling across complex life cycles. SignificanceThe proliferation of many of the worlds most diverse groups of eukaryotes is frequently attributed to their life cycle complexity. By allowing organisms to express different traits throughout their lives, complex life cycles enable individuals to utilize multiple ecological niches. However, the mechanisms that facilitate life cycle evolution are not well understood. We drew inspiration from studies on functional divergence between different tissues and examined the role of gene duplication in generating different patterns of gene expression between stages across the metamorphosis of Danaus plexippus (the monarch butterfly). Our findings suggest that the role of gene duplication in generating differences between cell and tissue types likely extends to trait differentiation between stages within complex life cycles.

evolutionary biology↗

Clonal development, not aggregation, drives the transition to multicellularity in an isogenic model system

A key step in the evolutionary transition to multicellularity is the origin of multicellular groups as biological individuals capable of adaptation. Comparative work, supported by theory, suggests clonal development should facilitate this transition, though this hypothesis has never been tested in a single model system. We evolved 20 replicate populations of otherwise isogenic clonally-reproducing snowflake yeast ({Delta}ace2/{Delta}ace2) and aggregative floc yeast (GAL1p::FLO1/ GAL1p::FLO1) with daily selection for rapid growth in liquid media, which favors faster cell division, followed by selection for rapid sedimentation, which favors larger multicellular groups. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Aggregative floc yeast obtained nearly all of their increased fitness from faster growth, not improved group survival; indicating that selection acted primarily at the level of cells. In contrast, clonal snowflake yeast mainly benefited from higher group-dependent fitness, indicating a shift in the level of biological individuality from cells to groups. Through genome sequencing and mathematical modeling, we show that the genetic bottlenecks in a clonal life cycle also drive much higher rates of genetic drift--a result with complex implications for this evolutionary transition. Our results highlight the central role that early multicellular life cycles play in the process of multicellular adaptation.

evolutionary biology↗

The complexities of inferring symbiont function: Paraburkholderia symbiont dynamics in social amoeba populations and its impact on the amoeba microbiome

The relationship between the social amoeba Dictyostelium discoideum and its endosymbiotic bacteria Paraburkholderia provides a model system for studying the development of symbiotic relationships. Laboratory experiments have shown that any of three species of Paraburkholderia symbiont allow D. discoideum food bacteria to persist through the amoeba lifecycle and survive in amoeba spores, rather than being fully digested. This phenomenon is termed "farming", as it potentially allows spores dispersed to food poor locations to grow their own. The occurrence and impact of farming in natural populations, however, has been a challenge to measure. Here, we surveyed natural D. discoideum populations and found that only one of the three symbiont species, P. agricolaris, remained prevalent. We then explored the effect of Paraburkholderia on the amoeba microbiota, expecting that by facilitating bacterial food carriage it would diversify the microbiota. Contrary to our expectations, Paraburkholderia tended to infectiously dominate the D. discoideum microbiota, in some cases decreasing diversity. Similarly, we found little evidence for Paraburkholderia facilitating the carriage of particular food bacteria. These findings highlight the complexities of inferring symbiont function in nature and suggest the possibility that Paraburkholderia could be playing multiple roles for its host.

evolutionary biology↗