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Verster, K. I.

Publications and source records attributed to Verster, K. I..

7 recordsLinked to original sources

Salinity is associated with habitat use and mitochondrial lineage diversity in halophilic Ephydra flies (Diptera: Ephydridae)

Brine flies of the genus Ephydra (Diptera: Ephydridae) are ubiquitous extremophile animals whose larval forms are able to thrive in high-stress environments, including hypersaline and high carbonate waters. Despite their historical and ecological importance, little is known about their evolutionary history. Here, we focus on an understudied population of Ephydra living in former industrial salt evaporation ponds of the San Francisco Bay Area (SFBA), a region which has undergone significant environmental changes in the past century. We observed and collected Ephydra specimens and took salinity measurements of waters they inhabited during a 6-month period in 2024. We found that E. millbrae and E. gracilis demonstrate strong salinity preferences. We also analyzed DNA from Ephydra spp. specimens from distant sites and a timespan of ~40 years, generating the most comprehensive gene genealogy of the group to date based on a single mitochondrial locus. Our analysis of phylogenetic signals suggests that salinity envelopes are influenced by evolutionary relationships in Ephydra. This study provides new information about the natural history of extremophile flies in the SFBA and fills in current gaps in our knowledge about the evolutionary history of the genus more broadly.

evolutionary biology↗

Retracing the horizontal transfer of a novel innate immune factor in Drosophila

Immune systems are among the most dynamically evolving traits across the tree of life, and long-lived macroparasites play an outsized role in shaping animal immunity. Even without adaptive immunity, insects have evolved potent innate immune strategies to neutralize such enemies, including nematodes and parasitoid wasps. One such strategy relies on endosymbioses between insects and toxin-expressing bacteria. Here, we use genome editing in Drosophila melanogaster to retrace the evolution of two of such toxins -- cytolethal distending toxin B (cdtB) and apoptosis inducing protein of 56kDa (aip56) -- that were horizontally transferred from bacteriophages to insects. We found that a cdtB::aip56 fusion gene (fusionB), which is conserved in Drosophila ananassae subgroup species, dramatically promoted fly survival and suppressed wasp development when expressed in D. melanogaster immune tissues. FusionB, a functional nuclease, was secreted into the host hemolymph where it targeted the parasitoid embryos serosal tissue and is to our knowledge the first humoral anti-parasitoid toxin in Drosophila. When expressed ubiquitously, fusionB slowed development in late stage fly larvae and eventually killed flies, pointing to the salience of regulatory constraint in preventing autoimmunity. Our findings demonstrate how horizontal gene transfer, in the right regulatory context, can instantly provide new and potent innate immune modules in animals.

evolutionary biology↗

Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae

Herbivorous insects are exceptionally diverse, accounting for a quarter of all known eukaryotic species, but the genetic basis of adaptations that enabled this dietary transition remains poorly understood. Many studies have suggested that expansions and contractions of chemosensory and detoxification gene families - genes directly mediating interactions with plant chemical defenses - underlie successful plant colonization. However, this hypothesis has been challenging to test because the origins of herbivory in many lineages are ancient (>150 million years ago [mya]), obscuring genomic evolutionary patterns. Here, we characterized chemosensory and detoxification gene family evolution across Scaptomyza, a genus nested within Drosophila that includes a recently derived (<15 mya) herbivore lineage of mustard (Brassicales) specialists and carnation (Caryophyllaceae) specialists, and several non-herbivorous species. Comparative genomic analyses revealed that herbivorous Scaptomyza have among the smallest chemosensory and detoxification gene repertoires across 12 drosophilid species surveyed. Rates of gene turnover averaged across the herbivore clade were significantly higher than background rates in over half of the surveyed gene families. However, gene turnover was more limited along the ancestral herbivore branch, with only gustatory receptors and odorant binding proteins experiencing strong losses. The genes most significantly impacted by gene loss, duplication, or changes in selective constraint were those involved in detecting compounds associated with feeding on plants (bitter or electrophilic phytotoxins) or their ancestral diet (yeast and fruit volatiles). These results provide insight into the molecular and evolutionary mechanisms of plant-feeding adaptations and highlight strong gene candidates that have also been linked to other dietary transitions in Drosophila.

evolutionary biology↗

Insights into the evolution of herbivory from a leaf-mining, drosophilid fly

Herbivorous insects and their host plants comprise most known species on Earth. Illuminating how herbivory repeatedly evolved in insects from non-herbivorous lineages is critical to understanding how this biodiversity is created and maintained. We characterized the trophic niche of Scaptomyza flava, a representative of a lineage nested within the Drosophila that transitioned to herbivory [~]15 million years ago. We used natural history studies to determine if S. flava is a true herbivore or a cryptic microbe-feeder. Specifically, we quantified oviposition substrate choice and larval viability across food-types, trophic-related morphological traits, and nitrogen isotope and sterol profiles across putatively herbivorous and non-herbivorous drosophilids. We confirmed that S. flava is an obligate herbivore of living plants. Paired with its genetic model host, Arabidopsis thaliana, S. flava is a novel and powerful system for exploring mechanisms underlying the evolution of herbivory, a complex trait that enabled the exceptional diversification of insects.

ecology↗

Horizontal transfer of microbial toxin genes to gall midge genomes

A growing body of evidence points to a role for horizontal gene transfer (HGT) in the evolution of animal novelties. Previously, we discovered the horizontal transfer of the gene encoding the eukaryotic genotoxin cytolethal distending toxin B (CdtB) from the Acyrthosiphon pisum Secondary Endosymbiont (APSE) bacteriophage to drosophilid and aphid genomes. Here, we report that cdtB is also found in the nuclear genome of the gall-forming swede midge Contarinia nasturtii (Diptera: Cecidomyiidae). We subsequently searched genome sequences of all available cecidomyiid species for evidence of microbe-to-insect HGT events. We found evidence of pervasive transfer of APSE-like toxin genes to cecidomyiid nuclear genomes. Many of the toxins encoded by these horizontally transferred genes target eukaryotic cells, rather than prokaryotes. In insects, catalytic residues important for toxin function are conserved. Phylogenetic analyses of HGT candidates indicated APSE phages were often not the ancestral donor of the toxin gene to cecidomyiid genomes, suggesting a broader pool of microbial donor lineages. We used a phylogenetic signal statistic to test a transfer-by-proximity hypothesis for HGT, which showed, that prokaryotic-to-insect HGT was more likely to occur between taxa in common environments. Our study highlights the horizontal transfer of genes encoding a new functional class of proteins in insects, toxins that target eukaryotic cells, which is potentially important in mediating interactions with eukaryotic pathogens and parasites. Significance StatementThe diversity of genes encoded by phages infecting bacterial symbionts of eukaryotes represents an enormous, relatively unexplored pool of new eukaryotic genes through horizontal gene transfer (HGT). In this study, we discovered pervasive HGT of toxin genes encoded by Acyrthosiphon pisum secondary endosymbiont (APSE) bacteriophages and other microbes to the nuclear genomes of gall midges (Diptera: Cecidomyiidae). We found five toxin genes were transferred horizontally from phage, bacteria, or fungi into genomes of several cecidomyiid species. These genes were aip56, cdtB, lysozyme, rhs, and sltxB. Most of the toxins encoded by these genes antagonize eukaryotic cells, and we posit that they may play a protective role in the insect immune system.

evolutionary biology↗

Evolution of herbivory remodels a Drosophila genome

One-quarter of extant Eukaryotic species are herbivorous insects, yet the genomic basis of this extraordinary adaptive radiation is unclear. Recently-derived herbivorous species hold promise for understanding how colonization of living plant tissues shaped the evolution of herbivore genomes. Here, we characterized exceptional patterns of evolution coupled with a recent (<15 mya) transition to herbivory of mustard plants (Brassicaceae, including Arabidopsis thaliana) in the fly genus Scaptomyza, nested within the paraphyletic genus Drosophila. We discovered a radiation of mustard-specialized Scaptomyza species, comparable in diversity to the Drosophila melanogaster species subgroup. Stable isotope, behavioral, and viability assays revealed these flies are obligate herbivores. Genome sequencing of one species, S. flava, revealed that the evolution of herbivory drove a contraction in gene families involved in chemosensation and xenobiotic metabolism. Against this backdrop of losses, highly targeted gains (\"blooms\") were found in Phase I and Phase II detoxification gene sub-families, including glutathione S-transferase (Gst) and cytochrome P450 (Cyp450) genes. S. flava has more validated paralogs of a single Cyp450 (N=6 for Cyp6g1) and Gst (N=5 for GstE5-8) than any other drosophilid. Functional studies of the Gst repertoire in S. flava showed that transcription of S. flava GstE5-8 paralogs was differentially regulated by dietary mustard oils, and of 22 heterologously expressed cytosolic S. flava GST enzymes, GSTE5-8 enzymes were exceptionally well-adapted to mustard oil detoxification in vitro. One, GSTE5-8a, was an order of magnitude more efficient at metabolizing mustard oils than GSTs from any other metazoan. The serendipitous intersection of two genetic model organisms, Drosophila and Arabidopsis, helped illuminate how an insect genome was remodeled during the evolutionary transformation to herbivory, identifying mechanisms that facilitated the evolution of the most diverse guild of animal life.\n\nSIGNIFICANCE STATEMENTThe origin of land plants >400 million years ago (mya) spurred the diversification of plant-feeding (herbivorous) insects and triggered an ongoing chemical co-evolutionary arms race. Because ancestors of most herbivorous insects first colonized plants >200 mya, the sands of time have buried evidence of how their genomes changed with their diet. We leveraged the serendipitous intersection of two genetic model systems: a close relative of yeast-feeding fruit fly (Drosophila melanogaster), the \"wasabi fly\" (Scaptomyza flava), that evolved to consume mustard plants including Arabidopsis thaliana. The yeast-to-mustard dietary transition remodeled the flys gene repertoire for sensing and detoxifying chemicals. Although many genes were lost, some underwent duplications that encode the most efficient detoxifying enzymes against mustard oils known from animals.

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↗