Biology subjects

Hague, M. T. J.

Publications and source records attributed to Hague, M. T. J..

7 recordsLinked to original sources

bioRxiv2025

The contributions of host population size and maternal transmission rate to fluctuating Wolbachia frequencies

Many insects and other animals host heritable endosymbionts that alter host fitness and reproduction. The prevalence of facultative endosymbionts can fluctuate in host populations across time and geography for reasons that are poorly understood. This is particularly true for maternally transmitted Wolbachia bacteria, which infect roughly half of all insect species. For instance, the frequencies of several wMel-like Wolbachia, including wMel in host Drosophila melanogaster, fluctuate over time in certain host populations, but the specific conditions that generate temporal variation in Wolbachia prevalence are unresolved. We implemented a discrete generation model in the new R package symbiontmodeler to evaluate how finite-population stochasticity contributes to Wolbachia fluctuations over time in simulated host populations under a variety of conditions. Using empirical estimates from natural Wolbachia-Drosophila systems, we explored how stochasticity is determined by a broad range of factors, including host population size, maternal transmission rates, and Wolbachia effects on host fitness (modeled as fecundity) and reproduction (cytoplasmic incompatibility; CI). While stochasticity generally increases when host fitness benefits and CI are relaxed, we found that a decline in the maternal transmission rate had the strongest relative impact on increasing the size of fluctuations. We infer that non- or weak-CI-causing strains like wMel, which often show evidence of imperfect maternal transmission, tend to generate larger stochastic fluctuations compared to strains that cause strong CI, like wRi in D. simulans. Additional factors, such as fluctuating host fitness effects, are required to explain the largest examples of temporal variation in Wolbachia. The conditions we simulate here using symbiontmodeler serve as a jumping off point for understanding drivers of temporal and spatial variation in the prevalence of Wolbachia, the most common endosymbionts found in nature.

evolutionary biology↗

bioRxiv2024

Comparative analysis of Wolbachia maternal transmission and localization in host ovaries

Many insects and other animals carry microbial endosymbionts that influence their reproduction and fitness. These relationships only persist if endosymbionts are reliably transmitted from one host generation to the next. Wolbachia are maternally transmitted endosymbionts found in most insect species, but transmission rates can vary across environments. Maternal transmission of wMel Wolbachia depends on temperature in natural Drosophila melanogaster hosts and in transinfected Aedes aegypti, where wMel is used to block pathogens that cause human disease. In D. melanogaster, wMel transmission declines in the cold as Wolbachia become less abundant in host ovaries and at the posterior pole plasm (the site of germline formation) in mature oocytes. Here, we assess how temperature affects maternal transmission and underlying patterns of Wolbachia localization across 10 Wolbachia strains diverged up to 50 million years--including strains closely related to wMel--and their natural Drosophila hosts. Many Wolbachia maintain high transmission rates across temperatures, despite highly variable (and sometimes low) levels of Wolbachia in the ovaries and at the developing germline in late-stage oocytes. Identifying strains like closely related wMel-like Wolbachia with stable transmission across variable environmental conditions may improve the efficacy of Wolbachia-based biocontrol efforts as they expand into globally diverse environments.

evolutionary biology↗

bioRxiv2023

Coevolution with toxic prey produces functional trade-offs in sodium channels of predatory snakes

Seemingly unrelated traits often share the same underlying molecular mechanisms, potentially generating a pleiotropic relationship whereby selection shaping one trait can simultaneously compromise another. While such functional trade-offs are expected to influence evolutionary outcomes, their actual relevance in nature is masked by obscure links between genotype, phenotype, and fitness. Here, we describe functional trade-offs that likely govern a key adaptation and coevolutionary dynamics in a predator-prey system. Several garter snake (Thamnophis spp.) populations have evolved resistance to tetrodotoxin (TTX), a potent chemical defense in their prey, toxic newts (Taricha spp.). Snakes achieve TTX resistance through mutations occurring at toxin-binding sites in the pore of snake skeletal muscle voltage-gated sodium channels (NaV1.4). We hypothesized that these mutations impair basic NaV functions, producing molecular trade-offs that should ultimately scale up to compromised organismal performance. We investigate biophysical costs in two snake species with unique and independently evolved mutations that confer TTX resistance. We show electrophysiological evidence that skeletal muscle sodium channels encoded by toxin-resistant alleles are functionally compromised. Furthermore, skeletal muscles from snakes with resistance genotypes exhibit reduced mechanical performance. Lastly, modeling the molecular stability of these sodium channel variants partially explains the electrophysiological and muscle impairments. Ultimately, adaptive genetic changes favoring toxin resistance appear to negatively impact sodium channel function, skeletal muscle strength, and organismal performance. These functional trade-offs at the cellular and organ levels appear to underpin locomotor deficits observed in resistant snakes and may explain variation in the population-level success of toxin-resistant alleles across the landscape, ultimately shaping the trajectory of snake-newt coevolution.

evolutionary biology↗

bioRxiv2022

Distinct Wolbachia localization patterns in oocytes of diverse host species reveal multiple strategies of maternal transmission

A broad array of endosymbionts radiate through host populations via vertical transmission, yet much remains unknown concerning the cellular basis, diversity and routes underlying this transmission strategy. Here we address these issues, by examining the cellular distributions of Wolbachia strains that diverged up to 50 million years ago in the oocytes of 18 divergent Drosophila species. This analysis revealed three Wolbachia distribution patterns: 1) a tight clustering at the posterior pole plasm (the site of germline formation); 2) a concentration at the posterior pole plasm, but with a significant bacteria population distributed throughout the oocyte; 3) and a distribution throughout the oocyte, with none or very few located at the posterior pole plasm. Examination of this latter class indicates Wolbachia accesses the posterior pole plasm during the interval between late oogenesis and the blastoderm formation. We also find that one Wolbachia strain in this class concentrates in the posterior somatic follicle cells that encompass the pole plasm of the developing oocyte. In contrast, strains in which Wolbachia concentrate at the posterior pole plasm generally exhibit no or few Wolbachia in the follicle cells associated with the pole plasm. Taken together, these studies suggest that for some Drosophila species, Wolbachia invade the germline from neighboring somatic follicle cells. Phylogenomic analysis indicates that closely related Wolbachia strains tend to exhibit similar patterns of posterior localization, suggesting that specific localization strategies are a function of Wolbachia-associated factors. Previous studies revealed that endosymbionts rely on one of two distinct routes of vertical transmission: continuous maintenance in the germline (germline-to-germline) or a more circuitous route via the soma (germline-to-soma-to-germline). Here we provide compelling evidence that Wolbachia strains infecting Drosophila species maintain the diverse arrays of cellular mechanisms necessary for both of these distinct transmission routes. This characteristic may account for its ability to infect and spread globally through a vast range of host insect species.

cell biology↗

bioRxiv2021

Pervasive effects of Wolbachia on host activity

Heritable symbionts have diverse effects on the physiology, reproduction, and fitness of their hosts. Maternally transmitted Wolbachia are one of the most common endosymbionts in nature, infecting about half of all insect species. We test the hypothesis that Wolbachia alter host behavior by assessing the effects of 14 different Wolbachia strains on the locomotor activity of nine Drosophila host species. We find that Wolbachia alter the activity of six different host genotypes, including all hosts in our assay infected with wRi-like Wolbachia strains (wRi, wSuz, wAur), which have rapidly spread among Drosophila species in only the last 13,000 years. While Wolbachia effects on host activity were common, the direction of these effects varied unpredictability and sometimes depended on host sex. We hypothesize that the prominent effects of wRi-like Wolbachia may be explained by patterns of Wolbachia titer and localization within host somatic tissues, particularly in the central nervous system. Our findings support the view that Wolbachia have wide-ranging effects on host behavior. The fitness consequences of these behavioral modifications are important for understanding the evolution of host-symbiont interactions, including how Wolbachia spread within host populations.

evolutionary biology↗

bioRxiv2020

Divergent effects of Wolbachia on host temperature preference

Heritable symbionts can modify a range of ecologically important host traits, including behavior. About half of all insect species are infected with maternally transmitted Wolbachia, a bacterial endosymbiont known to alter host reproduction, nutrient acquisition, and virus susceptibility. Here, we broadly test the hypothesis that Wolbachia modify host behavior by assessing the effects of eight different Wolbachia strains on the temperature preference of six Drosophila melanogaster-subgroup species. Four of the seven host genotypes infected with A-group Wolbachia strains (wRi in D. simulans, wHa in D. simulans, wSh in D. sechellia, and wTei in D. teissieri) prefer significantly cooler temperatures relative to uninfected genotypes. Contrastingly, when infected with divergent B-group wMau, D. mauritiana prefer a warmer temperature. For most strains, changes to host temperature preference do not alter Wolbachia titer. However, males infected with wSh and wTei experience an increase in titer when shifted to a cooler temperature for 24 hours, suggesting that Wolbachia-induced changes to host behavior may promote bacterial replication and influence Wolbachia transmission rates. Modifications to host temperature preference likely influence host thermoregulation, and understanding the fitness consequences of these effects is crucial for predicting evolutionary outcomes of host-symbiont interactions, including how Wolbachia spread to become common.

evolutionary biology↗

bioRxiv2020

Environmental and genetic contributions to imperfect wMel-like Wolbachia transmission and frequency variation

Maternally transmitted Wolbachia bacteria infect about half of all insect species. They usually show imperfect maternal transmission and often produce cytoplasmic incompatibility (CI). Irrespective of CI, Wolbachia frequencies tend to increase when rare only if they benefit host fitness. Several Wolbachia, including wMel that infects Drosophila melanogaster cause weak or no CI and persist at intermediate frequencies. On the island of Sao Tome off West Africa, the frequencies of wMel-like Wolbachia infecting D. yakuba (wYak) and D. santomea (wSan) fluctuate, and the contributions of imperfect maternal transmission, fitness effects, and CI to these fluctuations are unknown. We demonstrate spatial variation in wYak frequency and transmission on Sao Tome. Concurrent field estimates of imperfect maternal transmission do not predict spatial variation in wYak frequencies, which are highest at high altitudes where maternal transmission is the most imperfect. Genomic and genetic analyses provide little support for D. yakuba effects on wYak transmission. Instead, rearing at cool temperatures reduces wYak titer and increases imperfect transmission to levels observed on Sao Tome. Using mathematical models of Wolbachia frequency dynamics and equilibria, we infer temporally variable imperfect transmission or spatially variable effects on host fitness and reproduction are required to explain wYak frequencies. In contrast, spatially stable wSan frequencies are plausibly explained by imperfect transmission, modest fitness effects, and weak CI. Our results provide insight into causes of wMel-like frequency variation in divergent hosts. Understanding this variation is crucial to explain Wolbachia spread and to improve wMel biocontrol of human disease in transinfected mosquito systems.

evolutionary biology↗