Biology subjects

Matzkin, L. M.

Publications and source records attributed to Matzkin, L. M..

13 recordsLinked to original sources

bioRxiv2025

Evolution of the reproductive interactome: proteomic divergence and the origins of postmating-prezygotic reproductive incompatibilities

Reproductive proteins evolve rapidly, making them strong candidates for driving postmating-prezygotic (PMPZ) reproductive incompatibilities between populations. While most previous studies have focused on protein sequence divergence as a likely driver of PMPZ incompatibilities, reproductive proteomes may also diverge compositionally and/or quantitatively. Here, we combine quantitative proteomics, molecular evolutionary analyses, and protein-protein interaction (PPI) modeling to predict the molecular basis of reproductive incompatibilities between Drosophila mojavensis and D. arizonae. We demonstrate multidimensional divergence in reproductive proteomes including changes at the sequence, compositional, and quantitative levels. We further demonstrate that three divergent male seminal fluid proteins affect the size of the insemination reaction mass and/or fertilization success in D. arizonae. Despite high sequence divergence, predicted protein-protein interactions involving a conserved set of proteases and/or protease inhibitors were predicted to be maintained in heterospecific crosses. In contrast, predicted interspecies protein incompatibilities arose from proteome compositional divergence, suggesting that such changes may play a disproportionate role in PMPZ incompatibilities, at least for the subset of the interactome that we tested. Furthermore, extensive quantitative divergence, particularly for proteases and inhibitors, suggests pervasive stoichiometric mismatches in heterospecific matings. Altogether, our findings indicate that reproductive proteins are evolutionarily labile at multiple levels, and that compositional and quantitative divergence, rather than sequence changes alone, may be central to the early evolution of reproductive isolation.

evolutionary biology↗

bioRxiv2024

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↗

bioRxiv2023

A pooled-sample draft genome assembly provides insights into host plant-specific transcriptional responses of a Solanaceae-specializing pest, Tupiocoris notatus (Hemiptera: Miridae)

The assembly of genomes from pooled samples of genetically heterogenous samples of conspecifics remains challenging. In this study we show that high-quality genome assemblies can be produced from samples of multiple wild-caught individuals. We sequenced DNA extracted from a pooled sample of conspecific herbivorous insects (Hemiptera: Miridae: Tupiocoris notatus) acquired from a greenhouse infestation in Tucson, Arizona (in the range of 30-100 individuals; 0.5 mL tissue by volume) using PacBio highly accurate long reads (HiFi). The initial assembly contained multiple haplotigs (>85% BUSCOs duplicated), but duplicate contigs could be easily purged to reveal a highly complete assembly (95.6% BUSCO, 4.4% duplicated) that is highly contiguous by short-read assembly standards (N50 = 675 kb; Largest contig = 4.3 Mb). We then used our assembly as the basis for a genome-guided differential expression study of host-plant specific transcriptional responses. We found thousands of genes (N = 4982) to be differentially expressed between our new data from individuals feeding on Datura wrightii (Solanaceae) and existing RNA-seq data from Nicotiana attenuata (Solanaceae) fed individuals. We identified many of these genes as previously documented detoxification genes such as glutathione-S-transferases, cytochrome P450s, UDP-glucosyltransferases. Together our results show that long-read sequencing of pooled samples can provide a cost-effective genome assembly option for small insects and provide insights into the genetic mechanisms underlying interactions between plants and herbivorous pests.

genomics↗

bioRxiv2023

Females translate male mRNA transferred during mating

Although RNA is found in the seminal fluid of diverse organisms, it is unknown whether this RNA is functional within females. Here, we develop an experimental proteomic method called VESPA (Variant Enabled SILAC Proteomic Analysis) to test the hypothesis that Drosophila male seminal fluid RNA is translated by females. We find strong evidence for 67 male-derived, female-translated proteins (mdFTPs) in female lower reproductive tracts at six hours postmating, many with predicted functions relevant to reproduction. Gene knockout experiments indicate that genes coding for mdFTPs play diverse roles in postmating interactions, with effects on fertilization efficiency, and the formation and persistence of the insemination reaction mass, a trait hypothesized to be involved in sexual conflict. These findings advance our understanding of reproduction by revealing a novel mechanism of postmating molecular interactions between the sexes that strengthens and extends male influences on reproductive outcomes in previously unrecognized ways. Given the diverse species known to carry RNA in seminal fluid, this discovery has broad significance for understanding molecular mechanisms of cooperation and conflict during reproduction.

evolutionary biology↗

bioRxiv2022

Chromosome-length genome assemblies of cactophilic Drosophila illuminate links between structural and sequence evolution.

A thorough understanding of adaptation and speciation requires model organisms with both a history of ecological and phenotypic study as well as a robust set of genomic resources. For decades, the cactophilic Drosophila species of the southwestern US and northern Mexico have fit this profile, serving as a crucial model system for understanding ecological adaptation, particularly in xeric environments, as well as the evolution of reproductive incompatibilities and speciation. Here, we take a major step towards gaining a complete molecular description of this system by assembling and annotating seven chromosome-length de novo genomes across the three species D. mojavensis, D. arizonae, and D. navojoa. Using this data, we present the most accurate reconstruction of the phylogenetic history of this clade to date. We further demonstrate a relationship between structural evolution and coding evolution both within and between species in this clade, and use this relationship to generate novel hypotheses for adaptation genes. All of our data are presented in a new public database (cactusflybase.arizona.edu), providing one of the most in-depth resources for the analysis of inter- and intraspecific evolutionary genomic data.

genomics↗

bioRxiv2022

Phylogenomics provides insights into the evolution of cactophily and host plant shifts in Drosophila

Cactophilic species of the Drosophila buzzatii cluster (repleta group) comprise an excellent model group to investigate genomic changes underlying adaptation to extreme climate conditions and host plants. In particular, these species offer a subject to study the transition from chemically simpler breeding sites (like prickly pears of the genus Opuntia) to chemically more complex hosts (columnar cacti). Here, we report four highly contiguous genome assemblies of three species of the buzzatii cluster. Based on this genomic data and inferred phylogenetic relationships, we identified candidate taxonomically restricted genes (TRGs) likely involved in the evolution of cactophily and cactus host specialization in internal branches of the subgenus Drosophila. Functional enrichment analyses of TRGs within the buzzatii cluster identified genes involved in detoxification, water preservation, immune system response, anatomical structure development, and morphogenesis. In contrast, processes that regulate responses to stress, as well as the metabolism of nitrogen compounds, transport, and secretion were found in the set of species that are columnar cacti dwellers. These findings are in line with the hypothesis that those genomic innovations brought about instrumental mechanisms underlying adaptation in a group of species that speciated in the arid regions of South America.

evolutionary biology↗

bioRxiv2021

Propagation of seminal toxins through binary expression gene drives can suppress polyandrous populations

Gene drives can be highly effective in controlling a target population by disrupting a female fertility gene. To spread across a population, these drives require that disrupted alleles be largely recessive so as not to impose too high of a fitness penalty. We argue that this restriction may be relaxed by using a double gene drive design to spread a split binary expression system. One drive carries a dominant lethal/toxic effector alone and the other a transactivator factor, without which the effector will not act. Only after the drives reach sufficiently high frequencies would individuals have the chance to inherit both system components and the effector be expressed. We explore through mathematical modeling the potential of this design to spread dominant lethal/toxic alleles and suppress populations. We show that this system could be implemented to spread engineered seminal proteins designed to kill females, making it highly effective against polyandrous populations.

bioinformatics↗

bioRxiv2021

Physiological and life history changes associated with seasonal adaptation in the cactophilic Drosophila mojavensis

Many insects inhabiting temperate climates are faced with changing environmental conditions throughout the year. Depending on the species, these environmental fluctuations can be experienced within a single generation or across multiple generations. Strategies for dealing with these seasonal changes vary across populations. Drosophila mojavensis is a cactophilic Drosophila species endemic to the Sonoran Desert. The Sonoran Desert regularly reaches temperatures of 50{degrees}C in the summer months. As individuals of this population are rare to collect in the summer months, we therefore simulated in a temperature and light controlled chamber the cycling temperatures experienced by D. mojavensis in the Sonoran Desert from April to July (four generations) to understand the physiological and life history changes that allow this population to withstand these conditions. In contrast to our hypothesis of a summer aestivation, we found that D. mojavensis continue to reproduce during the summer months, albeit with lower viability, but the longevity of the population is highly reduced during this period. As expected, stress resistance increased during the summer months in both the adult and the larval stages. This study examines several strategies for withstanding the Sonoran Desert summer conditions which may be informative in the study of other desert endemic species.

evolutionary biology↗

bioRxiv2021

Novel genetic basis of resistance to Bt toxin Cry1Ac in Helicoverpa zea

Crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) have advanced pest management, but their benefits are diminished when pests evolve resistance. Elucidating the genetic basis of pest resistance to Bt toxins can improve resistance monitoring, resistance management, and design of new insecticides. Here, we investigated the genetic basis of resistance to Bt toxin Cry1Ac in the lepidopteran Helicoverpa zea, one of the most damaging crop pests in the United States. To facilitate this research, we built the first chromosome-level genome assembly for this species, which has 31 chromosomes containing 375 Mb and 15,482 predicted proteins. Using a genome-wide association study, fine-scale mapping, and RNA-seq, we identified a 250-kb quantitative trait locus (QTL) on chromosome 13 that was strongly associated with resistance in a strain of H. zea that had been selected for resistance in the field and lab. The mutation in this QTL contributed to but was not sufficient for resistance, which implies alleles in more than one gene contributed to resistance. This QTL contains no genes with a previously reported role in resistance or susceptibility to Bt toxins. However, in resistant insects, this QTL has a premature stop codon in a kinesin gene which is a primary candidate as a mutation contributing to resistance. We found no changes in gene sequence or expression consistently associated with resistance for 11 genes previously implicated in lepidopteran resistance to Cry1Ac. Thus, the results reveal a novel and polygenic basis of resistance.

genetics↗

bioRxiv2021

Divergent evolutionary trajectories shape the postmating transcriptional profiles of conspecific and heterospecifically mated females

Postmating-prezygotic (PMPZ) reproductive isolation is hypothesized to result from divergent coevolutionary trajectories of sexual selection and/or sexual conflict in isolated populations (coevolutionary divergence model). However, the genetic basis of PMPZ incompatibilities between species is poorly understood. Here, we use a comparative framework to test predictions of the coevolutionary divergence model using a large transcriptomic dataset generated from con- and heterospecifically mated Drosophila mojavensis and D. arizonae female reproductive tracts. We found striking divergence between the species in the female postmating transcriptional response to conspecific mating, including differences in differential expression (DE), alternative splicing (AS), and intron retention (IR). As predicted, heterospecific matings produced disrupted transcriptional profiles, but the overall patterns of misregulation were different between the reciprocal crosses. Moreover, we found a positive correlation between postmating transcriptional divergence between species and levels of transcriptional disruption in heterospecific crosses, indicating that mating-responsive genes that have diverged more in expression also have more disrupted transcriptional profiles in heterospecifically mated females. Overall, our results are consistent with predictions of the coevolutionary divergence model and lay the foundation for future studies aimed at identifying specific genes involved in PMPZ incompatibilities and the evolutionary forces that have contributed to their divergence in closely related species.

evolutionary biology↗

bioRxiv2019

Mate discrimination among subspecies through a conserved olfactory pathway

Signaling mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of Drosophila mojavensis as a model, we identify two behaviorally active male-specific pheromones. One functions as a conserved male anti-aphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an important role for this sensory pathway in promoting sexual isolation of subspecies, in collaboration with auditory signals. Surprisingly, the peripheral sensory pathway detecting this pheromone is conserved molecularly, physiologically and anatomically across subspecies. These observations imply that subspecies-specific behaviors arise from differential interpretation of the same peripheral cue, reminiscent of sexually conserved detection but dimorphic interpretation of male pheromones in D. melanogaster. Our results reveal that, during incipient speciation, pheromone production, detection and interpretation do not necessarily evolve in a coordinate manner.

neuroscience↗

bioRxiv2019

Chromosome-level hybrid de novo genome assemblies as an attainable option for non-model organisms

The emergence of third generation sequencing (3GS; long-reads) is making closer the goal of chromosome-size fragments in de novo genome assemblies. This allows the exploration of new and broader questions on genome evolution for a number of non-model organisms. However, long-read technologies result in higher sequencing error rates and therefore impose an elevated cost of sufficient coverage to achieve high enough quality. In this context, hybrid assemblies, combining short-reads and long-reads provide an alternative efficient and cost-effective approach to generate de novo, chromosome-level genome assemblies. The array of available software programs for hybrid genome assembly, sequence correction and manipulation is constantly being expanded and improved. This makes it difficult for non-experts to find efficient, fast and tractable computational solutions for genome assembly, especially in the case of non-model organisms lacking a reference genome or one from a closely related species. In this study, we review and test the most recent pipelines for hybrid assemblies, comparing the model organism Drosophila melanogaster to a non-model cactophilic Drosophila, D. mojavensis. We show that it is possible to achieve excellent contiguity on this non-model organism using the DBG2OLC pipeline.

genomics↗

bioRxiv2019

Genomic analysis of the four ecologically distinct cactus host populations of Drosophila mojavensis

BackgroundRelationships between an organism and its environment can be fundamental in the understanding how populations change over time and species arise. Local ecological conditions can shape variation at multiple levels, among these are the evolutionary history and trajectories of coding genes. This study examines the rate of molecular evolution at protein-coding genes throughout the genome in response to host adaptation in the cactophilic Drosophila mojavensis. These insects are intimately associated with cactus necroses, developing as larvae and feeding as adults in these necrotic tissues. Drosophila mojavensis is composed of four isolated populations across the deserts of western North America and each population has adapted to utilize different cacti that are chemically, nutritionally, and structurally distinct. ResultsHigh coverage Illumina sequencing was performed on three previously unsequenced populations of D. mojavensis. Genomes were assembled using the previously sequenced genome of D. mojavensis from Santa Catalina Island (USA) as a template. Protein coding genes were aligned across all four populations and rates of protein evolution were determined for all loci using a several approaches. ConclusionsLoci that exhibited elevated rates of molecular evolution tended to be shorter, have fewer exons, low expression, be transcriptionally responsive to cactus host use and have fixed expression differences across the four cactus host populations. Fast evolving genes were involved with metabolism, detoxification, chemosensory reception, reproduction and behavior. Results of this study gives insight into the process and the genomic consequences of local ecological adaptation.

genomics↗