Biology subjects

Chaston, J.

Publications and source records attributed to Chaston, J..

4 recordsLinked to original sources

bioRxiv2024

Humidity determines penetrance of a latitudinal gradient in genetic selection on the microbiota by Drosophila melanogaster

The fruit fly Drosophila melanogaster is a model for understanding how hosts and their microbial partners interact as the host adapts to wild environments. These interactions are readily interrogated because of the low taxonomic and numeric complexity of the flies bacterial communities. Previous work has established that host genotype, the environment, diet, and interspecies microbial interactions can all influence host fitness and microbiota composition, but the specific processes and characters mediating these processes are incompletely understood. Here, we compared the variation in microbiota composition between wild-derived fly populations when flies could choose between the microorganisms in their diets and when flies were reared under environmental perturbation (different humidities). We also compared the colonization of the resident and transient microorganisms. We show that the ability to choose between microorganisms in the diet and the environmental condition of the flies can influence the relative abundance of the microbiota. There were also key differences in the abundances of the resident and transient microbiota. However, the microbiota only differed between populations when the flies were reared at humidities at or above 50% relative humidity. We also show that elevated humidity determined the penetrance of a gradient in host genetic selection on the microbiota that is associated with the latitude the flies were collected from. Finally, we show that the treatment-dependent variation in microbiota composition is associated with variation in host stress survival. Together, these findings emphasize that host genetic selection on the microbiota composition of a model animal host can be patterned with the source geography, and that such variation has the potential to influence their survival in the wild. ImportanceThe fruit fly Drosophila melanogaster is a model for understanding how hosts and their microbial partners interact as hosts adapt in wild environments. Our understanding of what causes geographic variation in the fruit fly microbiota remains incomplete. Previous work has shown that the D. melanogaster microbiota has relatively low numerical and taxonomic complexity. Variation in the fly microbiota composition can be attributed to environmental characters and host genetic variation, and variation in microbiota composition can be patterned with the source location of the flies. In this work we explored three possible causes of patterned variation in microbiota composition. We show that host feeding choices, the host niche colonized by the bacteria, and a single environmental character can all contribute to variation in microbiota composition. We also show that penetrance of latitudinally-patterned host genetic selection is only observed at elevated humidities. Together, these results identify several factors that influence microbiota composition in wild fly genotypes and emphasize the interplay between environmental and host genetic factors in determining the microbiota composition of these model hosts.

microbiology↗

bioRxiv2022

Flagellar genes are associated with the colonization persistence phenotype of the Drosophila melanogaster microbiota

In this work we use Drosophila melanogaster as a model to identify bacterial genes necessary for bacteria to colonize their hosts independent of the bulk flow of diet. Early work on this model system established that dietary replenishment drives the composition of the D. melanogaster gut microbiota, and subsequent research has shown that some bacterial strains can stably colonize, or persist with, the fly independent of dietary replenishment. Here we reveal transposon insertions in specific bacterial genes that influence the bacterial colonization persistence phenotype by using a gene association approach. We initially established that different bacterial strains persist at varying levels, independent of dietary replenishment. We then repeated the analysis with an expanded panel of bacterial strains and performed a metagenome wide association (MGWA) to identify distinct bacterial genes that are significantly correlated with the colonization level of persistent bacterial strains. Based on the MGWA, we tested if 44 bacterial transposon insertion mutants from 6 gene categories affect bacterial persistence with the flies. We identified that transposon insertions in four flagellar genes, one urea carboxylase gene, one phosphatidyl inositol gene, one bacterial secretion gene, and one antimicrobial peptide (AMP) resistance gene each significantly influenced the colonization of an Acetobacter fabarum strain with D. melanogaster. Follow-up experiments revealed that each flagellar mutant was non-motile, even though the wild-type strain was motile. Taken together, these results reveal transposon insertions in specific bacterial genes, including motility genes, are necessary for at least one member of the fly microbiota to persistently colonize the fly. IMPORTANCEDespite the growing body of research on the microbiota, the mechanisms by which the microbiota colonizes a host can still be further elucidated. This study identifies bacterial genes that are associated with colonization persistence phenotype of the microbiota in Drosophila melanogaster, which reveals specific bacterial factors that influence establishment of the microbiota with its host. Identification of specific genes that affect persistence can help inform how the microbiota colonizes a host. Furthermore, a deeper understanding of the genetic mechanisms of the establishment of the microbiota could aid in further developing the Drosophila microbiota as a model for microbiome research.

microbiology↗

bioRxiv2019

Microbiome composition shapes rapid genomic adaptation of Drosophila melanogaster

Population genomic data has revealed patterns of genetic variation associated with adaptation in many taxa. Yet understanding the adaptive process that drives such patterns is challenging - it requires disentangling the ecological agents of selection, determining the relevant timescales over which evolution occurs, and elucidating the genetic architecture of adaptation. Doing so for the adaptation of hosts to their microbiome is of particular interest with growing recognition of the importance and complexity of host-microbe interactions. Here, we track the pace and genomic architecture of adaptation to an experimental microbiome manipulation in replicate populations of Drosophila melanogaster in field mesocosms. Manipulation of the microbiome altered population dynamics and increased divergence between treatments in allele frequencies genome-wide, with regions showing strong divergence found on all chromosomes. Moreover, at divergent loci previously associated with adaptation across natural populations, we found that the more common allele in fly populations experimentally enriched for a certain microbial group was also more common in natural populations with high relative abundance of that microbial group. These results suggest that microbiomes may be an agent of selection that shapes the pattern and process of adaptation and, more broadly, that variation in a single ecological factor within a complex environment can drive rapid, polygenic adaptation over short timescales.\n\nSignificance statementNatural selection can drive evolution over short timescales. However, there is little understanding of which ecological factors are capable of driving rapid evolution and how this rapid evolution alters allele frequencies across the genome. Here we combine a field experiment with population genomic data from natural populations across a latitudinal gradient to assess whether and how microbiome composition drives rapid genomic evolution of host populations. We find that differences in microbiome composition cause divergence in allele frequencies genome-wide, including in genes previously associated with local adaptation. Moreover, we observed concordance between experimental and natural populations in terms of the direction of allele frequency change, suggesting that microbiome composition may be an agent of selection that drives adaptation in the wild.

evolutionary biology↗

bioRxiv2018

The microbiota influences the Drosophila melanogaster life history strategy

AbstractOrganismal life history traits are ideally adapted to local environments when an organism has a fitness advantage in one location relative to conspecifics from other geographies. Local adaptation has been best studied across, for example, latitudinal gradients, where organisms may tradeoff between investment in traits that maximize one, but not both, fitness components of somatic maintenance or reproductive output in the context of finite environmental resources. Latitudinal gradients in life history strategies are traditionally attributed to environmentally mediated selection on an animals genotype, without any consideration of the possible impact of associated microorganisms ( microbiota) on life history traits. Here we show that in Drosophila melanogaster, a key organism for studying local adaptation and life history strategies, associated microorganisms can drive life history variation. First, we reveal that an isogenic fly line reared with different bacteria vary the investment in early reproduction versus somatic maintenance, with little resultant variation in lifetime fitness. Next, we show that in wild Drosophila the abundance of these same bacteria was correlated with the latitude and life history strategy of the flies, and bacterial abundance was driven at least in part by host genetic selection. Finally, by eliminating or manipulating the microbiota of fly lines collected across a latitudinal gradient, we reveal that host genotype contributes to latitude-specific life history traits independent of the microbiota; but that the microbiota can override these host genetic adaptations. Taken together, these findings establish the microbiota as an essential consideration in local adaptation and life history evolution.\n\nSignificance statementExplanations of local adaptation have historically focused on how animal genotypes respond to environmental selection. Although the impact of variation in host life histories on the composition of the microbiota has been investigated for many associations, the scale and pattern of microbial effects on host life history strategy are largely unknown. Here we demonstrate in the fruit fly Drosophila melanogaster that microbiota effects on host life history strategy in the laboratory are matched by patterns of microbiota composition in wild host populations. In particular, microbiota composition varies with latitude and the effects of the microbiota on life history traits are greater than host genetic adaptations. Together, these findings demonstrate that the microbiota plays an important role in local adaptation.

evolutionary biology↗