Parasitic fish embryos do a "front-flip" on the yolk to resist expulsion from the host.

Embryonic development is often considered shielded from the effects of natural selection, being selected primarily for reliable development. However, embryos sometimes represent virulent parasites, triggering a coevolutionary "arms race" with their host. We have examined embryonic adaptations to a parasitic lifestyle in the bitterling fish. Bitterlings are brood parasites that lay their eggs in the gill chamber of host mussels. Bitterling eggs and embryos have adaptations to resist being flushed out by the mussel. These include a pair of projections from the yolk sac that act as an anchor. Furthermore, bitterling eggs all adopt a head-down position in the mussel gills which further increases their chances of survival. To examine these adaptations in detail, we have studied development in the rosy bitterling (Rhodeus ocellatus) using molecular markers, X-ray tomography, and time-lapse imaging. We describe a suite of developmental adaptations to brood parasitism in this species. We show that the mechanism underlying these adaptions is a modified pattern of blastokinesis-a process unique, among fish, to bitterlings. Tissue movements during blastokinesis cause the embryo to do an extraordinary "front-flip" on the yolk. We suggest that this movement determines the spatial orientation of the other developmental adaptations to parasitism, ensuring that they are optimally positioned to help resist the ejection of the embryo from the mussel. Our study supports the notion that natural selection can drive the evolution of a suite of adaptations, both embryonic and extra-embryonic, via modifications in early development.

Distinguishing Cophylogenetic Signal from Phylogenetic Congruence Clarifies the Interplay Between Evolutionary History and Species Interactions.

Interspecific interactions, including host-symbiont associations, can profoundly affect the evolution of the interacting species. Given the phylogenies of host and symbiont clades and knowledge of which host species interact with which symbiont, two questions are often asked: "Do closely related hosts interact with closely related symbionts?" and "Do host and symbiont phylogenies mirror one another?." These questions are intertwined and can even collapse under specific situations, such that they are often confused one with the other. However, in most situations, a positive answer to the first question, hereafter referred to as "cophylogenetic signal," does not imply a close match between the host and symbiont phylogenies. It suggests only that past evolutionary history has contributed to shaping present-day interactions, which can arise, for example, through present-day trait matching, or from a single ancient vicariance event that increases the probability that closely related species overlap geographically. A positive answer to the second, referred to as "phylogenetic congruence," is more restrictive as it suggests a close match between the two phylogenies, which may happen, for example, if symbiont diversification tracks host diversification or if the diversifications of the two clades were subject to the same succession of vicariance events. Here we apply a set of methods (ParaFit, PACo, and eMPRess), whose significance is often interpreted as evidence for phylogenetic congruence, to simulations under 3 biologically realistic scenarios of trait matching, a single ancient vicariance event, and phylogenetic tracking with frequent cospeciation events. The latter is the only scenario that generates phylogenetic congruence, whereas the first 2 generate a cophylogenetic signal in the absence of phylogenetic congruence. We find that tests of global-fit methods (ParaFit and PACo) are significant under the 3 scenarios, whereas tests of event-based methods (eMPRess) are only significant under the scenario of phylogenetic tracking. Therefore, significant results from global-fit methods should be interpreted in terms of cophylogenetic signal and not phylogenetic congruence; such significant results can arise under scenarios when hosts and symbionts had independent evolutionary histories. Conversely, significant results from event-based methods suggest a strong form of dependency between hosts and symbionts evolutionary histories. Clarifying the patterns detected by different cophylogenetic methods is key to understanding how interspecific interactions shape and are shaped by evolution.

Genomic diversification of the specialized parasite of the fungus-growing ant symbiosis.

Fungi shape the diversity of life. Characterizing the evolution of fungi is critical to understanding symbiotic associations across kingdoms. In this study, we investigate the genomic and metabolomic diversity of the genus Escovopsis, a specialized parasite of fungus-growing ant gardens. Based on 25 high-quality draft genomes, we show that Escovopsis forms a monophyletic group arising from a mycoparasitic fungal ancestor 61.82 million years ago (Mya). Across the evolutionary history of fungus-growing ants, the dates of origin of most clades of Escovopsis correspond to the dates of origin of the fungus-growing ants whose gardens they parasitize. We reveal that genome reduction, determined by both genomic sequencing and flow cytometry, is a consistent feature across the genus Escovopsis, largely occurring in coding regions, specifically in the form of gene loss and reductions in copy numbers of genes. All functional gene categories have reduced copy numbers, but resistance and virulence genes maintain functional diversity. Biosynthetic gene clusters (BGCs) contribute to phylogenetic differences among Escovopsis spp., and sister taxa in the Hypocreaceae. The phylogenetic patterns of co-diversification among BGCs are similarly exhibited across mass spectrometry analyses of the metabolomes of Escovopsis and their sister taxa. Taken together, our results indicate that Escovopsis spp. evolved unique genomic repertoires to specialize on the fungus-growing ant-microbe symbiosis.

Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts.

Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources. We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production. A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential.

Orientia tsutsugamushi infection reduces host gluconeogenic but not glycolytic substrates.

Orientia tsutsugamushi a causal agent of scrub typhus, is an obligate intracellular bacterium that, akin to other rickettsiae, is dependent on host cell-derived nutrients for survival and thus pathogenesis. Based on limited experimental evidence and genome-based in silico predictions, O. tsutsugamushi is hypothesized to parasitize host central carbon metabolism (CCM). Here, we (re-)evaluated O. tsutsugamushi dependency on host cell CCM as initiated by glucose and glutamine. Orientia infection had no effect on host glucose and glutamine consumption or lactate accumulation, indicating no change in overall flux through CCM. However, host cell mitochondrial activity and ATP levels were reduced during infection and correspond with lower intracellular glutamine and glutamate pools. To further probe the essentiality of host CCM in O. tsutsugamushi proliferation, we developed a minimal medium for host cell cultivation and paired it with chemical inhibitors to restrict the intermediates and processes related to glucose and glutamine metabolism. These conditions failed to negatively impact O. tsutsugamushi intracellular growth, suggesting the bacterium is adept at scavenging from host CCM. Accordingly, untargeted metabolomics was utilized to evaluate minor changes in host CCM metabolic intermediates across O. tsutsugamushi infection and revealed that pathogen proliferation corresponds with reductions in critical CCM building blocks, including amino acids and TCA cycle intermediates, as well as increases in lipid catabolism. This study directly correlates O. tsutsugamushi proliferation to alterations in host CCM and identifies metabolic intermediates that are likely critical for pathogen fitness.IMPORTANCEObligate intracellular bacterial pathogens have evolved strategies to reside and proliferate within the eukaryotic intracellular environment. At the crux of this parasitism is the balance between host and pathogen metabolic requirements. The physiological basis driving O. tsutsugamushi dependency on its mammalian host remains undefined. By evaluating alterations in host metabolism during O. tsutsugamushi proliferation, we discovered that bacterial growth is independent of the host's nutritional environment but appears dependent on host gluconeogenic substrates, including amino acids. Given that O. tsutsugamushi replication is essential for its virulence, this study provides experimental evidence for the first time in the post-genomic era of metabolic intermediates potentially parasitized by a scrub typhus agent.

Immune system modulation & virus transmission during parasitism identified by multi-species transcriptomics of a declining insect biocontrol system.

BACKGROUND: The Argentine stem weevil (ASW, Listronotus bonariensis) is a significant pasture pest in Aotearoa New Zealand, primarily controlled by the parasitoid biocontrol agent Microctonus hyperodae. Despite providing effective control of ASW soon after release, M. hyperodae parasitism rates have since declined significantly, with ASW hypothesised to have evolved resistance to its biocontrol agent. While the parasitism arsenal of M. hyperodae has previously been investigated, revealing many venom components and an exogenous novel DNA virus Microctonus hyperodae filamentous virus (MhFV), the effects of said arsenal on gene expression in ASW during parasitism have not been examined. In this study, we performed a multi-species transcriptomic analysis to investigate the biology of ASW parasitism by M. hyperodae, as well as the decline in efficacy of this biocontrol system. RESULTS: The transcriptomic response of ASW to parasitism by M. hyperodae involves modulation of the weevil's innate immune system, flight muscle components, and lipid and glucose metabolism. The multispecies approach also revealed continued expression of venom components in parasitised ASW, as well as the transmission of MhFV to weevils during parasitism and some interrupted parasitism attempts. Transcriptomics did not detect a clear indication of parasitoid avoidance or other mechanisms to explain biocontrol decline. CONCLUSIONS: This study has expanded our understanding of interactions between M. hyperodae and ASW in a biocontrol system of critical importance to Aotearoa-New Zealand's agricultural economy. Transmission of MhFV to ASW during successful and interrupted parasitism attempts may link to a premature mortality phenomenon in ASW, hypothesised to be a result of a toxin-antitoxin system. Further research into MhFV and its potential role in ASW premature mortality is required to explore whether manipulation of this viral infection has the potential to increase biocontrol efficacy in future.

Urban socioeconomic variation influences the ecology and evolution of trophic interactions.

As urbanization expands, it is becoming increasingly important to understand how anthropogenic activity is affecting ecological and evolutionary processes. Few studies have examined how human social patterns within cities can modify eco-evolutionary dynamics. We tested how socioeconomic variation corresponds with changes in trophic interactions and natural selection on prey phenotypes using the classic interaction between goldenrod gall flies (Eurosta solidaginis) and their natural enemies: birds, beetles, and parasitoid wasps. We sampled galls from 84 sites across neighbourhoods with varying socioeconomic levels, and quantified the frequency of predation/parasitism on flies and natural selection by each enemy. We found that bird predation was higher in the highest income neighbourhoods, increasing the strength of selection for smaller galls. Wasp and beetle attack, but not their strength of selection, increased in lower income neighbourhoods. We show that socioeconomic variation in cities can have strong unintended consequences for the ecology and evolution of trophic interactions.

Variations and reduction of plastome are associated with the evolution of parasitism in Convolvulaceae.

Parasitic lifestyle can often relax the constraint on the plastome, leading to gene pseudogenization and loss, and resulting in diverse genomic structures and rampant genome degradation. Although several plastomes of parasitic Cuscuta have  been reported, the evolution of parasitism in the family Convolvulaceae which is linked to structural variations and reduction of plastome has not been well investigated. In this study, we assembled and collected 40 plastid genomes belonging to 23 species representing four subgenera of Cuscuta and ten species of autotrophic Convolvulaceae. Our findings revealed nine types of structural variations and six types of inverted repeat (IR) boundary variations in the plastome of Convolvulaceae spp. These structural variations were associated with the shift of parasitic lifestyle, and IR boundary shift, as well as the abundance of long repeats. Overall, the degradation of Cuscuta plastome proceeded gradually, with one clade exhibiting an accelerated degradation rate. We observed five stages of gene loss in Cuscuta, including NAD(P)H complex → PEP complex → Photosynthesis-related → Ribosomal protein subunits → ATP synthase complex. Based on our results, we speculated that the shift of parasitic lifestyle in early divergent time promoted relaxed selection on plastomes, leading to the accumulation of microvariations, which ultimately resulted in the plastome reduction. This study provides new evidence towards a better understanding of plastomic evolution, variation, and reduction in the genus Cuscuta.

Transcriptomic Approach for Investigation of Solanum spp. Resistance upon Early-Stage Broomrape Parasitism.

Tomato (Solanum lycopersicum) is a major horticultural crop of high economic importance. Phelipanche and Orobanche genera (broomrapes) are parasitic weeds, constituting biotic stressors that impact tomato production. Developing varieties with tolerance to broomrapes has become imperative for sustainable agriculture. Solanum pennellii, a wild relative of cultivated tomato, has been utilized as breeding material for S. lycopersicum. In the present study, it is the first time that an in-depth analysis has been conducted for these two specific introgression lines (ILs), IL6-2 and IL6-3 (S. lycopersicum X S. pennellii), which were employed to identify genes and metabolic pathways associated with resistance against broomrape. Comparative transcriptomic analysis revealed a multitude of differentially expressed genes (DEGs) in roots, especially in the resistant genotype IL6-3, several of which were validated by quantitative PCR. DEG and pathway enrichment analysis (PEA) revealed diverse molecular mechanisms that can potentially be implicated in the host's defense response and the establishment of resistance. The identified DEGs were mostly up-regulated in response to broomrape parasitism and play crucial roles in various processes different from strigolactone regulation. Our findings indicate that, in addition to the essential role of strigolactone metabolism, multiple cellular processes may be involved in the tomato's response to broomrapes. The insights gained from this study will enhance our understanding and facilitate molecular breeding methods regarding broomrape parasitism. Moreover, they will assist in developing sustainable strategies and providing alternative solutions for weed management in tomatoes and other agronomically important crops.

Dominant-negative KAI2d paralogs putatively attenuate strigolactone responses in root parasitic plants.

Many root parasitic plants in the Orobanchaceae use host-derived strigolactones as germination cues. This adaptation facilitates attachment to a host and is particularly important for the success of obligate parasitic weeds that cause substantial crop losses globally. Parasite seeds sense strigolactones through "divergent" KARRIKIN INSENSITIVE2 (KAI2d)/HYPOSENSITIVE TO LIGHT (HTL) α/ß-hydrolases that have undergone substantial duplication and diversification in Orobanchaceae genomes. After germination, chemotropic growth of parasite roots toward a strigolactone source also occurs in some species. We investigated which of the seven KAI2d genes found in a facultative hemiparasite, Phtheirospermum japonicum, may enable chemotropic responses to strigolactones. To do so, we developed a triple mutant Nbd14a,b kai2i line of Nicotiana benthamiana in which strigolactone-induced degradation of SMAX1, an immediate downstream target of KAI2 signaling, is disrupted. In combination with a transiently expressed, ratiometric reporter of SMAX1 protein abundance, this mutant forms a system for the functional analysis of parasite KAI2d proteins in a plant cellular context. Using this system, we unexpectedly found three PjKAI2d proteins that do not trigger SMAX1 degradation in the presence of strigolactones. Instead, these PjKAI2d inhibit the perception of low strigolactone concentrations by strigolactone-responsive PjKAI2d in a dominant-negative manner that depends upon an active catalytic triad. Similar dominant-negative KAI2d paralogs were identified in an obligate hemiparasitic weed, Striga hermonthica. These proteins suggest a mechanism for attenuating strigolactone signaling in parasites, which might be used to enhance the perception of shallow strigolactone gradients during root growth toward a host or to restrict germination responses to specific strigolactones.

Genetic and Phenotypic Consequences of Local Transitions between Sexual and Parthenogenetic Reproduction in the Wild.

AbstractTransitions from sexual to asexual reproduction have occurred in numerous lineages, but it remains unclear why asexual populations rarely persist. In facultatively parthenogenetic animals, all-female populations can arise when males are absent or become extinct, and such populations could help to understand the genetic and phenotypic changes that occur in the initial stages of transitions to asexuality. We investigated a naturally occurring spatial mosaic of mixed-sex and all-female populations of the facultatively parthenogenetic Australian phasmid Megacrania batesii. Analysis of single-nucleotide polymorphisms indicated multiple independent transitions between reproductive modes. All-female populations had much lower heterozygosity and allelic diversity than mixed-sex populations, but we found few consistent differences in fitness-related traits between population types. All-female populations exhibited more frequent and severe deformities in their (flight-incapable) wings but did not show higher rates of appendage loss. All-female populations also harbored more ectoparasites in swamp (but not beach) habitats. Reproductive mode explained little variation in female body size, fecundity, or egg hatch rate. Our results suggest that transitions to parthenogenetic reproduction can lead to dramatic genetic changes with little immediate effect on performance. All-female M. batesii populations appear to consist of high-fitness genotypes that might be able to thrive for many generations in relatively constant and benign environments but could be vulnerable to environmental challenges, such as increased parasite abundance.

A Mosquito Parasite Is Locally Adapted to Its Host but Not Temperature.

AbstractClimate change will alter interactions between parasites and their hosts. Warming may affect patterns of local adaptation, shifting the environment to favor the parasite or host and thus changing the prevalence of disease. We assessed local adaptation to hosts and temperature in the facultative ciliate parasite Lambornella clarki, which infects the western tree hole mosquito Aedes sierrensis. We conducted laboratory infection experiments with mosquito larvae and parasites collected from across a climate gradient, pairing sympatric or allopatric populations across three temperatures that were either matched or mismatched to the source environment. Lambornella clarki parasites were locally adapted to their hosts, with 2.6 times higher infection rates on sympatric populations compared with allopatric populations, but they were not locally adapted to temperature. Infection peaked at the intermediate temperature of 12.5°C, notably lower than the optimum temperature for free-living L. clarki growth, suggesting that the host's immune response can play a significant role in mediating the outcome of infection. Our results highlight the importance of host selective pressure on parasites, despite the impact of temperature on infection success.

Comparative and phylogenetic analyses of Loranthaceae plastomes provide insights into the evolutionary trajectories of plastome degradation in hemiparasitic plants.

BACKGROUND: The lifestyle transition from autotrophy to heterotrophy often leads to extensive degradation of plastomes in parasitic plants, while the evolutionary trajectories of plastome degradation associated with parasitism in hemiparasitic plants remain poorly understood. In this study, phylogeny-oriented comparative analyses were conducted to investigate whether obligate Loranthaceae stem-parasites experienced higher degrees of plastome degradation than closely related facultative root-parasites and to explore the potential evolutionary events that triggered the 'domino effect' in plastome degradation of hemiparasitic plants. RESULTS: Through phylogeny-oriented comparative analyses, the results indicate that Loranthaceae hemiparasites have undergone varying degrees of plastome degradation as they evolved towards a heterotrophic lifestyle. Compared to closely related facultative root-parasites, all obligate stem-parasites exhibited an elevated degree plastome degradation, characterized by increased downsizing, gene loss, and pseudogenization, thereby providing empirical evidence supporting the theoretical expectation that evolution from facultative parasitism to obligate parasitism may result in a higher degree of plastome degradation in hemiparasites. Along with infra-familial divergence in Loranthaceae, several lineage-specific gene loss/pseudogenization events occurred at deep nodes, whereas further independent gene loss/pseudogenization events were observed in shallow branches. CONCLUSIONS: The findings suggest that in addition to the increasing levels of nutritional reliance on host plants, cladogenesis can be considered as another pivotal evolutionary event triggering the 'domino effect' in plastome degradation of hemiparasitic plants. These findings provide new insights into the evolutionary trajectory of plastome degradation in hemiparasitic plants.

Trophic interactions in microbiomes influence plant host population size and ecosystem function.

Plant microbiomes that comprise diverse microorganisms, including prokaryotes, eukaryotes and viruses, are the key determinants of plant population dynamics and ecosystem function. Despite their importance, little is known about how species interactions (especially trophic interactions) between microbes from different domains modify the importance of microbiomes for plant hosts and ecosystems. Using the common duckweed Lemna minor, we experimentally examined the effects of predation (by bacterivorous protists) and parasitism (by bacteriophages) within microbiomes on plant population size and ecosystem phosphorus removal. Our results revealed that the addition of predators increased plant population size and phosphorus removal, whereas the addition of parasites showed the opposite pattern. The structural equation modelling further pointed out that predation and parasitism affected plant population size and ecosystem function via distinct mechanisms that were both mediated by microbiomes. Our results highlight the importance of understanding microbial trophic interactions for predicting the outcomes and ecosystem impacts of plant-microbiome symbiosis.

Genus-wide analysis of Trichoderma antagonism toward Pythium and Globisporangium plant pathogens and the contribution of cellulases to the antagonism.

Parasitism is an important lifestyle in the Trichoderma genus but has not been studied in a genus-wide way toward Pythium and Globisporangium hosts. Our approach screened a genus-wide set of 30 Trichoderma species in dual culture assays with two soil-borne Pythium and three Globisporangium plant-parasitic species and used exo-proteomic analyses, with the aim to correlate Trichoderma antagonism with potential strategies for attacking Pythium and Globisporangium. The Trichoderma spp. showed a wide range of antagonism from strong to weak, but the same Trichoderma strain showed similar levels toward all the Pythium and Globisporangium species. The Trichoderma enzymes from strong (Trichoderma asperellum, Trichoderma atroviride, and Trichoderma virens), moderate (Trichoderma cf. guizhouense and Trichoderma reesei), and weak (Trichoderma parepimyces) antagonists were induced by the autoclaved mycelia of one of the screened Pythium species, Pythium myriotylum. The variable proportions of putative cellulases, proteases, and redox enzymes suggested diverse as well as shared strategies amongst the antagonists. There was a partial positive correlation between antagonism from microscopy and the cellulase activity induced by autoclaved P. myriotylum mycelia in different Trichoderma species. The deletion of the cellulase transcriptional activator XYR1 in T. reesei led to lower antagonism toward Pythium and Globisporangium. The antagonism of Pythium and Globisporangium appears to be a generic property of Trichoderma as most of the Trichoderma species were at least moderately antagonistic. While a role for cellulases in the antagonism was uncovered, cellulases did not appear to make a major contribution to T. reesei antagonism, and other factors are also likely contributing.IMPORTANCETrichoderma is an important genus widely distributed in nature with broad ecological impacts and applications in the biocontrol of plant diseases. The Pythium and Globisporangium genera of fungus-like water molds include many important soil-borne plant pathogens that cause various diseases. Most of the Trichoderma species showed at least a moderate ability to compete with or antagonize the Pythium and Globisporangium hosts, and microscopy showed examples of parasitism (a slow type of killing) and predation (a fast type of killing). Hydrolytic enzymes such as cellulases and proteases produced by Trichoderma likely contribute to the antagonism. A mutant deficient in cellulase activity had reduced antagonism. Interestingly, Pythium and Globisporangium species contain cellulose in their cell walls (unlike true fungi such as Trichoderma), and the cellulolytic ability of Trichoderma appears beneficial for antagonism of water molds.

Host avian species and environmental conditions influence the microbial ecology of brood parasitic brown-headed cowbird nestlings: What rules the roost?

The role of species interactions, as well as genetic and environmental factors, all likely contribute to the composition and structure of the gut microbiome; however, disentangling these independent factors under field conditions represents a challenge for a functional understanding of gut microbial ecology. Avian brood parasites provide unique opportunities to investigate these questions, as brood parasitism results in parasite and host nestlings being raised in the same nest, by the same parents. Here we utilized obligate brood parasite brown-headed cowbird nestlings (BHCO; Molothrus ater) raised by several different host passerine species to better understand, via 16S rRNA sequencing, the microbial ecology of brood parasitism. First, we compared faecal microbial communities of prothonotary warbler nestlings (PROW; Protonotaria citrea) that were either parasitized or non-parasitized by BHCO and communities among BHCO nestlings from PROW nests. We found that parasitism by BHCO significantly altered both the community membership and community structure of the PROW nestling microbiota, perhaps due to the stressful nest environment generated by brood parasitism. In a second dataset, we compared faecal microbiotas from BHCO nestlings raised by six different host passerine species. Here, we found that the microbiota of BHCO nestlings was significantly influenced by the parental host species and the presence of an inter-specific nestmate. Thus, early rearing environment is important in determining the microbiota of brood parasite nestlings and their companion nestlings. Future work may aim to understand the functional effects of this microbiota variability on nestling performance and fitness.

Genomic basis of adaptation to climate and parasite prevalence and the importance of odorant perception in the ant Temnothorax longispinosus.

A co-evolutionary arms race ensues when parasites exhibit exploitative behaviour, which prompts adaptations in their hosts, in turn triggering counter-adaptations by the parasites. To unravel the genomic basis of this coevolution from the host's perspective, we collected ants of the host species Temnothorax longispinosus, parasitized by the social parasite Temnothorax americanus, from 10 populations in the northeastern United States exhibiting varying levels of parasite prevalence and living under different climatic conditions. We conducted a genome-wide association study (GWAS) to identify single nucleotide polymorphisms (SNPs) associated with both prevalence and climate. Our investigation highlighted a multitude of candidate SNPs associated with parasite prevalence, particularly in genes responsible for sensory perception of smell including odorant receptor genes. We further focused on population-specific compositions of cuticular hydrocarbons, a complex trait important for signalling, communication and protection against desiccation. The relative abundances of n-alkanes were correlated with climate, while there was only a trend between parasite prevalence and the relative abundances of known recognition cues. Furthermore, we identified candidate genes likely involved in the synthesis and recognition of specific hydrocarbons. In addition, we analysed the population-level gene expression in the antennae, the primary organ for odorant reception, and established a strong correlation with parasite prevalence. Our comprehensive study highlights the intricate genomic patterns forged by the interplay of diverse selection factors and how these are manifested in the expression of various phenotypes.

Phylogenomic analysis of Stylops reveals the evolutionary history of a Holarctic Strepsiptera radiation parasitizing wild bees.

Holarctic Stylops is the largest genus of the enigmatic insect order Strepsiptera, twisted winged parasites. Members of Stylops are obligate endoparasites of Andrena mining bees and exhibit extreme sexual dimorphism typical of Strepsiptera. So far, molecular studies on Stylops have focused on questions on species delimitation. Here, we utilize the power of whole genome sequencing to infer the phylogeny of this morphologically challenging genus from thousands of loci. We use a species tree method, concatenated maximum likelihood analysis and Bayesian analysis with a relaxed clock model to reconstruct the phylogeny of 46 Stylops species, estimate divergence times, evaluate topological consistency across methods and infer the root position. Furthermore, the biogeographical history and coevolutionary patterns with host species are assessed. All methods recovered a well resolved topology with close to all nodes maximally supported and only a handful of minor topological variations. Based on the result, we find that included species can be divided into 12 species groups, seven of them including only Palaearctic species, three Nearctic and two were geographically mixed. We find a strongly supported root position between a clade formed by the spreta, thwaitesi and gwynanae species groups and the remaining species and that the sister group of Stylops is Eurystylops or Eurystylops + Kinzelbachus. Our results indicate that Stylops originated in the Western Palaearctic or Western Palaearctic and Nearctic in the early Neogene or late Paleogene, with four independent dispersal events to the Nearctic. Cophylogenetic analyses indicate that the diversification of Stylops has been shaped by both significant coevolution with the mining bee hosts and host-shifting. The well resolved and strongly supported phylogeny will provide a valuable phylogenetic basis for further studies into the fascinating world of Strepsipterans.

Phylogenomics including new sequence data of phytoplankton-infecting chytrids reveals multiple independent lifestyle transitions across the phylum.

Parasitism is the most common lifestyle on Earth and has emerged many times independently across the eukaryotic tree of life. It is frequently found among chytrids (Chytridiomycota), which are early-branching unicellular fungi that feed osmotrophically via rhizoids as saprotrophs or parasites. Chytrids are abundant in most aquatic and terrestrial environments and fulfil important ecosystem functions. As parasites, they can have significant impacts on host populations. They cause global amphibian declines and influence the Earth's carbon cycle by terminating algal blooms. To date, the evolution of parasitism within the chytrid phylum remains unclear due to the low phylogenetic resolution of rRNA genes for the early diversification of fungi, and because few parasitic lineages have been cultured and genomic data for parasites is scarce. Here, we combine transcriptomics, culture-independent single-cell genomics and a phylogenomic approach to overcome these limitations. We newly sequenced 29 parasitic taxa and combined these with existing data to provide a robust backbone topology for the diversification of Chytridiomycota. Our analyses reveal multiple independent lifestyle transitions between parasitism and saprotrophy among chytrids and multiple host shifts by parasites. Based on these results and the parasitic lifestyle of other early-branching holomycotan lineages, we hypothesise that the chytrid last common ancestor was a parasite of phytoplankton.

Modelling suggests Wolbachia-induced cytoplasmic incompatibility in oak gall wasps with cyclical parthenogenesis.

Oak gall wasps typically exhibit a life cycle with one sexual and one asexual generation each year. These wasps can carry various endosymbionts, one of which is the maternally inherited bacterium Wolbachia that can induce several reproductive manipulations on its host. Cytoplasmic incompatibility (CI) has been described as the most prominent of these manipulations. CI leads to embryonic mortality in the hosts' offspring when infected males mate with either uninfected females or with females that harbour different Wolbachia strains. It has been hypothesized that Wolbachia can induce CI in oak gall wasps. To address this hypothesis, we derived a mathematical model to investigate the spread of a bacterial infection in naive populations and to determine the plausibility of CI occurrence. To validate our model, we used published data from Wolbachia-infected Belonocnema kinseyi populations in two approaches. Our first approach uses measurements of infection frequencies and maternal transmission in the sexual generation. For the second approach, we extended the model to compare predictions to estimates of mtDNA-haplotypes, which, like Wolbachia, are maternally inherited, and can therefore be associated with the infection. Both approaches indicate that CI is present in these populations. Our model can be generalized to investigate the occurrence of CI not only for oak gall wasps but also for other species.