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Price, D. K.

Publications and source records attributed to Price, D. K..

8 recordsLinked to original sources

Microbiome composition shapes temperature tolerance in a Hawaiian picture-winged Drosophila

Hawaiian picture-winged Drosophila are undergoing rapid biodiversity loss, with twelve species listed as endangered and others in decline. Gut microbiota are increasingly recognized as contributors to host adaptation that are capable of influencing stress tolerance, reproduction, and other fitness-related traits. We investigated the role of microbial communities in local adaptation using two populations of Drosophila basisetae from Hawaiian rainforests at 900 m and 1200 m elevation. Microbiome profiling of wild flies by high throughput amplicon sequencing revealed distinct bacterial and fungal communities between sites. Whole-genome resequencing of the two Drosophila populations identified weak but significant population genetic structure, with evidence of admixture and gene flow. Despite this connectivity, 16 outlier SNPs across 18 genes showed patterns consistent with divergent selection, suggesting localized adaptation. To test microbiome effects on host physiology experimentally, we conducted a fully factorial research design with microbiome inoculations in laboratory-reared flies acclimated to 18 {degrees}C (control) or 24 {degrees}C (stressful). Flies treated with low-elevation microbiota had higher survival across temperatures, whereas those treated with high-elevation microbiota produced more eggs, indicating microbiome-mediated differences in reproductive investment. Activity levels at 18 {degrees}C were higher when flies received microbiota from their native population. Measures of critical thermal maximum (CTmax) and male accessory gland size showed complex interactions among microbiome source, temperature, and fly population. These results indicate that microbes may modulate host thermal tolerance and reproduction in environmentally-dependent and population-specific ways. Our findings suggest that microbiome-host-environment interactions may contribute to both phenotypic plasticity and evolutionary adaptation to enhance resilience to environmental stress, with important implications for conservation in rapidly changing Hawaiian ecosystems. Summary statementThis study demonstrates that microbiome composition influences thermal tolerance through alterations in survival and reproduction in the Hawaiian picture wing, Drosophila basisetae, potentially contributing to adaptive phenotypic changes between populations.

evolutionary biology↗

Abiotic factors are the primary determinants of endemic Hawaiian Drosophila microbiome assembly

The Hawaiian Drosophila radiation exemplifies rapid adaptation and species diversification. Many factors have been attributed to these phenomena, including allopatry, sexual selection, and ecological specialization. In recent years, the microbiome has come to the forefront as an important driver of adaptation that is capable of facilitating host survivorship, enhancing resilience to local environmental challenges, and enabling the use of different dietary resources. To determine how microbial communities assemble in natural populations and potentially contribute to the rapid adaptation of Hawaiian drosophilids, we conducted a survey of bacterial and fungal communities from over 500 wild flies collected from across six islands of the Hawaiian archipelago. These samples represent a breadth of host plant specializations, habitats, lifestyles, and endemicity. Our findings reveal that microbiome assembly is largely driven by abiotic factors including elevation, temperature, rainfall, and evapotranspiration, but is not strongly constrained by phylogenetic relatedness. Identical species inhabiting two separate locations exhibited different microbiomes. By contrast, distantly related species inhabiting the same site had more similar microbiomes. The microbiomes of native species also differ from recently introduced, non-native Drosophila in terms of diversity, composition, and function. Given the myriad roles of the microbiome in nutrition, reproduction, and mate choice, these results support a role for the microbiome in the remarkable ecological divergence of Hawaiian Drosophila.

ecology↗

Single-fly assemblies fill major phylogenomic gaps across the Drosophilidae Tree of Life

Long-read sequencing is driving rapid progress in genome assembly across all major groups of life, including species of the family Drosophilidae, a longtime model system for genetics, genomics, and evolution. We previously developed a cost-effective hybrid Oxford Nanopore (ONT) long-read and Illumina short-read sequencing approach and used it to assemble 101 drosophilid genomes from laboratory cultures, greatly increasing the number of genome assemblies for this taxonomic group. The next major challenge is to address the laboratory culture bias in taxon sampling by sequencing genomes of species that cannot easily be reared in the lab. Here, we build upon our previous methods to perform amplification-free ONT sequencing of single wild flies obtained either directly from the field or from ethanol-preserved specimens in museum collections, greatly improving the representation of lesser studied drosophilid taxa in whole-genome data. Using Illumina Novaseq X Plus and ONT P2 sequencers with R10.4.1 chemistry, we set a new benchmark for inexpensive hybrid genome assembly at US $150 per genome while assembling genomes from as little as 35 ng of genomic DNA from a single fly. We present 183 new genome assemblies for 179 species as a resource for drosophilid systematics, phylogenetics, and comparative genomics. Of these genomes, 62 are from pooled lab strains and 121 from single adult flies. Despite the sample limitations of working with small insects, most single-fly diploid assemblies are comparable in contiguity (>1Mb contig N50), completeness (>98% complete dipteran BUSCOs), and accuracy (>QV40 genome-wide with ONT R10.4.1) to assemblies from inbred lines. We present a well-resolved multi-locus phylogeny for 360 drosophilid and 4 outgroup species encompassing all publicly available (as of August 2023) genomes for this group. Finally, we present a Progressive Cactus whole-genome, reference-free alignment built from a subset of 298 suitably high-quality drosophilid genomes. The new assemblies and alignment, along with updated laboratory protocols and computational pipelines, are released as an open resource and as a tool for studying evolution at the scale of an entire insect family.

evolutionary biology↗

Bacterial and fungal components of the gut microbiome have distinct, sex-specific roles in Hawaiian Drosophila reproduction

Gut microbiomes provide numerous physiological benefits for host animals. The role of bacterial members of microbiomes in host physiology is well-documented. However, much less is known about the contributions and interactions of fungal members of the microbiome even though fungi are significant components of many microbiomes, including those of humans and insects. Here, we used antibacterial and antifungal drugs to manipulate the gut microbiome of a Hawaiian picture-wing Drosophila species, D. grimshawi, and identified distinct, sex-specific roles for the bacteria and fungi in microbiome community stability and reproduction. Female oogenesis, fecundity and mating drive were significantly diminished when fungal communities were suppressed. By contrast, male fecundity was more strongly affected by bacterial but not fungal populations. For males and females, suppression of both bacteria and fungi severely reduced fecundity and altered fatty acid levels and composition, implicating the importance of interkingdom interactions on reproduction and lipid metabolism. Overall, our results reveal that bacteria and fungi have distinct, sexually-dimorphic effects on host physiology and interkingdom dynamics in the gut help to maintain microbiome community stability and enhance reproduction.

microbiology↗

Widespread introgression across a phylogeny of 155 Drosophila genomes

Genome-scale sequence data have invigorated the study of hybridization and introgression, particularly in animals. However, outside of a few notable cases, we lack systematic tests for introgression at a larger phylogenetic scale across entire clades. Here we leverage 155 genome assemblies, from 149 species, to generate a fossil-calibrated phylogeny and conduct multilocus tests for introgression across nine monophyletic radiations within the genus Drosophila. Using complementary phylogenomic approaches, we identify widespread introgression across the evolutionary history of Drosophila. Mapping gene-tree discordance onto the phylogeny revealed that both ancient and recent introgression has occurred across most of the nine clades that we examined. Our results provide the first evidence of introgression occurring across the evolutionary history of Drosophila and highlight the need to continue to study the evolutionary consequences of hybridization and introgression in this genus and across the Tree of Life.

evolutionary biology↗

Highly contiguous assemblies of 101 drosophilid genomes

Over 100 years of studies in Drosophila melanogaster and related species in the genus Drosophila have facilitated key discoveries in genetics, genomics, and evolution. While high-quality genome assemblies exist for several species in this group, they only encompass a small fraction of the genus. Recent advances in long read sequencing allow high quality genome assemblies for tens or even hundreds of species to be generated. Here, we utilize Oxford Nanopore sequencing to build an open community resource of high-quality assemblies for 101 lines of 95 drosophilid species encompassing 14 species groups and 35 sub-groups with an average contig N50 of 10.5 Mb and greater than 97% BUSCO completeness in 97/101 assemblies. These assemblies, along with detailed wet lab protocol and assembly pipelines, are released as a public resource and will serve as a starting point for addressing broad questions of genetics, ecology, and evolution within this key group.

evolutionary biology↗

Horizontal transfer of prokaryotic cytolethal distending toxin B genes to eukaryotes

Cytolethal distending toxins (CDTs) are tripartite eukaryotic genotoxins encoded in diverse bacterial and phage genomes. The cdtB subunit is a DNAse that causes eukaryotic cell cycle arrest and apoptosis, and in one context, is associated with resistance against parasitoid wasp infections. Here we report the discovery of functional cdtB copies in the nuclear genomes of insect species from two distantly related insect orders, including fruit flies (Diptera: Drosophilidae) and aphids (Hemiptera: Aphididae). Insect cdtB copies are most closely related to bacteriophage copies, were horizontally transferred to insect genomes > 40 million years ago and encode a protein that retains ancestral DNase activity. This phage-derived toxin has been domesticated by diverse insects and we hypothesize that it is used as a defensive weapon against parasitoid wasps. One Sentence SummaryWe report horizontal transfer of the gene cytolethal distending toxin B, which encodes a DNase, into eukaryotic genomes from bacteriophage. SignificanceCytolethal distending toxins (CDTs) are secreted by diverse pathogenic bacterial species to kill animal cells. The cdtB subunit enters cell nuclei, damaging the DNA and leading to mitotic arrest and apoptosis. In the pea aphid, a bacterial endosymbiont provides protection against wasp attack, possibly via cdtB. We discovered that this same endosymbiont-encoded lineage of cdtB was transferred to the genomes of Diptera and Hemiptera species and retains ancestral DNase activity. This is the first report of cdtB outside of bacteria or phages. A toxin that first evolved to kill eukaryotic cells has been co-opted by insects, potentially to their benefit.

evolutionary biology↗

Reproductive capacity evolves in response to ecology through common developmental mechanisms in Hawaiian Drosophila

Lifetime reproductive capacity, or the total number of offspring that an individual can give rise to in its lifetime, is a fitness component critical to the evolutionary process. In insects, female reproductive capacity is largely determined by the number of ovarioles, the egg-producing subunits of the ovary. Recent work has provided insights into the genetic and environmental control of ovariole number in Drosophila melanogaster. However, whether regulatory mechanisms discovered under laboratory conditions also explain evolutionary variation in natural populations is an outstanding question. Here we report, for the first time, insights into the mechanisms regulating ovariole number and its evolution among Hawaiian Drosophila, a large adaptive radiation of fruit flies in which the highest and lowest ovariole numbers of the genus have evolved within 25 million years. Using phylogenetic comparative methods, we show that ovariole number variation among Hawaiian Drosophila is best explained by adaptation to specific oviposition substrates. Further, we show that evolution of oviposition on ephemeral egg-laying substrates is linked to changes the allometric relationship between body size and ovariole number. Finally, we provide evidence that the developmental mechanism principally responsible for controlling ovariole number in D. melanogaster also regulates ovariole number in natural populations of Hawaiian drosophilids. By integrating ecology, organismal growth, and cell behavior during development to understand the evolution of ovariole number, this work connects the ultimate and proximate mechanisms of evolutionary change in reproductive capacity.

evolutionary biology↗