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), which significance is often interpreted as evidence for phylogenetic congruence, to simulations under three 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 two 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 three 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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Genome evolution in intracellular parasites: Microsporidia and Apicomplexa.

Microsporidia and Apicomplexa are eukaryotic, single-celled, intracellular parasites with huge public health and economic importance. Typically, these parasites are studied separately, emphasizing their uniqueness and diversity. In this review, we explore the huge amount of genomic data that has recently become available for the two groups. We compare and contrast their genome evolution and discuss how their transitions to intracellular life may have shaped it. In particular, we explore genome reduction and compaction, genome expansion and ploidy, gene shuffling and rearrangements, and the evolution of centromeres and telomeres.

Parasitic and predatory behavior of Alysia manducator (Hymenoptera: Braconidae) on blow fly larvae feeding on an adult pig carcass in the Western Cape Province of South Africa: preliminary observations and forensic implications.

Wasps are part of the entomofauna associated with vertebrate carrion. They are known to parasitize and prey on specific life stages of insect hosts such as eggs, larvae, pupae, and/or adults associated with vertebrate carrion. However, reports of parasitic behavior of wasps on carrion-associated insect life stages and their possible forensic implications are non-existent in the Western Cape Province of South Africa. This study is part of ongoing research investigating the entomofauna and their pattern of succession on an adult pig carcass in Cape Town, South Africa. During this study, the parasitic wasp Alysia manducator was noted parasitizing and preying on blow fly larvae associated with the decomposing carcass. The arrival of A. manducator coincides with the occurrence of blow fly eggs and/or larvae on the carcass. These wasps were seen in close association with the eggs and larvae of blow flies on various parts of the carcass and some wasps were seen dragging fly larvae attached to their ovipositors away from one part of the carcass to another. Some A. manducator were also observed walking over several larvae on the carcass while exhibiting a stabbing behavior presumably in search of a host for oviposition. We suggest that the observations recorded in this study are of considerable forensic importance as the dragging effect and predatory and stabbing behavior exhibited by A. manducator could potentially disrupt the feeding and development of the fly larvae on the carcass. This could subsequently alter the process of carcass decomposition and/or affect minimum post-mortem interval estimations.

With the dead under the mat: the zombie ant extended phenotype under a new perspective.

Some parasitic fungi can increase fitness by modifying the behavior of their hosts. These behaviors are known as extended phenotypes because they favor parasitic gene propagation. Here, we studied three lineages of Ophiocordyceps, a fungus that infects ants, altering their conduct before death. According to fungal strategy, ants may die in leaf litter, with entwined legs in branches, under the moss mat, or biting plant tissue. It is critical for parasites that the corpses stay at these places because Ophiocordyceps exhibit iteroparity, possibly releasing spores in multiple life cycles. Thus, we assumed substrate cadaver permanence as a fungi reproductive proxy and corpse height as a proxy of cadaver removal. We hypothesize that biting vegetation and dying in higher places may increase the permanence of ant corpses while avoiding possible corpse predation on the forest floor. We monitored over a year more than 4000 zombie ants in approximately 15 km2 of undisturbed tropical forest in central Amazonia. Our results show a longer permanence of corpses with increasing ground height, suggesting that the parasites may have better chances of releasing spores and infecting new hosts at these places. We found that the zombie ants that last longer on the substrate die under the moss mat in tree trunks, not necessarily biting vegetation. The biting behavior appears to be the most derived and complex mechanism among Ophiocordyceps syndromes. Our results put these findings under a new perspective, proposing that seemingly less complex behavioral changes are ecologically equivalent and adaptative for other parasite lineages.

Fostering innovation to solve the biomechanics of microbe-host interactions: Focus on the adhesive forces underlying Apicomplexa parasite biology.

The protozoa, Toxoplasma gondii and Plasmodium spp., are preeminent members of the Apicomplexa parasitic phylum in large part due to their public health and economic impact. Hence, they serve as model unicellular eukaryotes with which to explore the repertoire of molecular and cellular strategies that specific developmental morphotypes deploy to timely adjust to their host(s) in order to perpetuate. In particular, host tissue- and cell-invasive morphotypes termed zoites alternate extracellular and intracellular lifestyles, thereby sensing and reacting to a wealth of host-derived biomechanical cues over their partnership. In the recent years, biophysical tools especially related to real time force measurement have been introduced, teaching us how creative are these microbes to shape a unique motility system that powers fast gliding through a variety of extracellular matrices, across cellular barriers, in vascular systems or into host cells. Equally performant was this toolkit to start illuminating how parasites manipulate their hosting cell adhesive and rheological properties to their advantage. In this review, besides highlighting major discoveries along the way, we discuss the most promising development, synergy, and multimodal integration in active noninvasive force microscopy methods. These should in the near future unlock current limitations and allow capturing, from molecules to tissues, the many biomechanical and biophysical interplays over the dynamic host and microbe partnership.