Search bioRxiv⌕ Search

Biology subjects

Minard, G.

Publications and source records attributed to Minard, G..

9 recordsLinked to original sources

Friend or foe: A mosquito parasite with mixed transmission mode displays mutualistic traits promoting oogenesis.

Mutualism is often selected in vertically transmitted symbionts due to their fitness interdependence with hosts. However, the evolution of mutualism remains unclear in symbionts using both vertical and horizontal transmission. In this study, we show that Ascogregarina taiwanensis, previously known as a weak horizontally transmitted parasite of the Asian tiger mosquito (Aedes albopictus), exhibits mutualistic traits that enhance mosquito reproduction. The symbiont improves embryogenesis and extends the egg-laying period while most females are pseudo-vertically transmitting symbiont oocysts to their progeny at oviposition sites. Dual transcriptomic analyses reveal that early oogenesis in infected females involves increased nitrogen metabolism in both partners, enhanced detoxification of blood waste, and activation of egg development pathways. These changes lead to improved assimilation of blood proteins essential for egg production. Our findings provide rare empirical evidence of a symbiont displaying both parasitic and mutualistic traits, offering new insights into the evolutionary dynamics of mixed-mode transmission symbioses. Significance StatementHow mutualism evolves from parasitism remains a central question in evolutionary biology, particularly for symbionts that combine vertical and horizontal transmission. We show that Ascogregarina taiwanensis, an Apicomplexan parasite previously known to be costly for developing Aedes albopictus mosquitoes, is also pseudo-vertically transmitted: most females release oocysts into the water during oviposition, exposing their offspring. Surprisingly, infection enhances host reproduction by promoting oogenesis through protein assimilation, leading to the production of larger larvae. Dual transcriptomic analyses reveal coordinated shifts in host and parasite metabolism, especially in nitrogen assimilation. Our findings provide rare evidence that mutualistic traits can emerge in a symbiont with mixed-mode transmission, offering new insights into the evolutionary transitions shaping host-microbe interactions.

evolutionary biology↗

Contrasting genetic differentiation of urban and rural populations of two grassland lepidopterans across Europe

Urbanisation is transforming environments globally. The altered abiotic conditions and biotic interactions in urban habitats impose divergent selection pressures on urban versus rural populations, while genetic drift may also be significant in typically small urban populations. A key question in urban evolution concerns the origin and spread of urban genotypes. Examples exist of both single and multiple origins of urban genotypes, but these have proven difficult to generalize. Here, we address genetic differentiation among urban populations, among rural populations, and between urban and rural populations. We conducted an extensive population genomic double digest restriction-site associated DNA sequencing analysis of two non-model grassland lepidopterans, Coenonympha pamphilus and Chiasmia clathrata, across Europe. The genetic population structures of the study species were strikingly different: Co. pamphilus showed strong population differentiation, while this was almost absent in Ch. clathrata, which instead showed signs of high current and past gene flow among populations. Results of Co. pamphilus are consistent with multiple origins of urban populations, and multiple origins seem plausible also in Ch. clathrata. These results suggest that past and large-scale population dynamics need to be integrated into urban evolution research, because population history affects urban evolutionary dynamics.

evolutionary biology↗

A major entomoparasite interferes with Chikungunya transmission by Aedes albopictus

The Asian tiger mosquito, Aedes albopictus, spreads diseases like Chikungunya and has caused outbreaks worldwide. Studies show that mosquitoes-associated microbes can affect how well they spread diseases. One of those microbes, the parasite As. taiwanensis, is common in older mosquito populations but rare in newer ones. We found that this parasite slows down the spread of Chikungunya within the mosquito and decreases its transmission rate by half. Unparasitized mosquitoes spread the virus more easily, suggesting that changes in mosquito microbes could impact disease outbreaks and public health.

microbiology↗

Discovery and functional analysis of a novel ALPK1 variant causing ROSAH syndrome

ROSAH syndrome is an autosomal dominant autoinflammatory disorder characterised by visual disturbance caused by pathogenic variation in the protein kinase ALPK1. Only two such variants have been reported to cause ROSAH syndrome to date: 66 out of 67 patients harbour the Thr237Met variant, while a single patient carries a Tyr254Cys variant. Here we identify a family in which ROSAH syndrome is caused by a Ser277Phe variant in ALPK1. The phenotypic variability in this family is high, with four of the seven individuals legally blind. Hypohidrosis, splenomegaly and arthritis were present in several family members. In contrast to wildtype ALPK1, which is activated specifically by the bacterial metabolite ADP-heptose during bacterial infection, ALPK1[Ser277Phe] was also activated by the human metabolites UDP-mannose and ADP-ribose, even more strongly than the ALPK1[Thr237Met] variant. However, unlike ALPK1[Thr237Met], ALPK1[Ser277Phe] could additionally be activated by GDP-mannose. These observations can explain why these ALPK1 variants are active in cells in the absence of ADP-heptose and hence why patients have episodes of autoinflammation. Examination of the three-dimensional structure of ALPK1 revealed that the sidechains of Ser277 and Tyr254 interact but mutational analysis established that this interaction is not critical for the integrity of the ADP-heptose binding site. Instead, it is replacement of Ser277 by a large hydrophobic phenylalanine residue or the replacement of Tyr254 by a much smaller cysteine residue that is responsible for altering the specificity of the ADP-heptose-binding pocket. The characterisation of ALPK1 variants that cause ROSAH syndrome suggests ways in which drugs that inhibit these disease-causing variants selectively can be developed.

genetics↗

Human-aided dispersal facilitates parasitism escape in the most invasive mosquito species

During biological invasion process, species encounter new environments and partially escape some ecological constraints they faced in their native range, while they face new ones. The Asian tiger mosquito Aedes albopictus is one of the most iconic invasive species introduced in every inhabited continent due to international trade. It has also been shown to be infected by a prevalent yet disregarded microbial entomoparasite Ascogregarina taiwanensis. In this study, we aimed at deciphering the factors that shape the global dynamics of As. taiwanensis infection in natural Ae. albopictus populations. We showed that Ae. albopictus populations are highly colonized by several parasite genotypes but recently introduced ones are escaping it. We further performed experiments based on the invasion process to explain such pattern. To that end, we hypothesized that (i) mosquito passive dispersal (i.e. human-aided egg transportation) may affect the parasite infectiveness, (ii) founder effects (i.e. population establishment by a small number of mosquitoes) may influence the parasite dynamics and (iii) unparasitized mosquitoes are more prompt to found new populations through active flight dispersal. The two first hypotheses were supported as we showed that parasite infection decreases over time when dry eggs are stored and that experimental increase in mosquitoes density improves the parasite horizontal transmission to larvae. Surprisingly, parasitized mosquitoes tend to be more active than their unparasitized relatives. Finally, this study highlights the importance of global trade as a driver of biological invasion of the most invasive arthropod vector species. SignificanceGlobal trade expansion has facilitated the introduction of invasive species such as the Asian tiger mosquito Aedes albopictus. Eventually, invasive species might escape their natural enemies and this phenomenon exemplifies their invasion success. In this study, we combined field observations and laboratory experiments to decipher the ecological consequences of the invasion process on the interaction dynamics between Ae. albopictus and its most prevalent natural parasite As. taiwanensis. We observed a decrease in parasitism in recently introduced populations and provide experimental evidence to explain how human-aided mosquito transportation and mosquito population bottlenecks were a burden for the parasite.

microbiology↗

Variation in diet and microbial exposure shape the performance of the Asian tiger mosquito, Aedes albopictus

Along their life cycle, mosquitoes colonize different ecological niches with various microorganisms and diet sources that likely modulate their performance (i.e. a set of mosquito fitness-related traits). However, which ecological parameters and how their variations modulate mosquito performance is not completely understood. In this study, we used Ae. albopictus surface-sterilized eggs re-associated or not to conventional bacterial microbiota upon a range of diet concentrations and addressed the impact of microbial inoculum and diet concentration variation on several mosquito performance traits. Results showed that mosquito juvenile survival depends on the interaction between bacterial inoculum load and diet concentration in the breeding water. Exposure to bacteria in rearing water shorten larval development time although it impacted larvae survival in an inoculum and diet concentration-dependent manner. Bacterial composition of larval rearing water was mainly structured by the bacterial inoculum concentration, with some Operational Taxonomic Units abundances correlating with larval traits. Ae. albopictus survival, development and bacterial community patterns upon gradients of diet and bacterial inoculum illustrated the complex impact of diet-microbiota interaction on mosquito performance. These findings argue the importance of deciphering host-microbe-environment interactions and open promising perspectives to improve Ae. albopictus control measures in the field. IMPORTANCEMicrobiota is increasingly recognized as a driving force of metazoan biology, impacting diverse traits including nutrition, behaviour or reproduction. The microbial impact on host nutrition is among the most studied host-microbe interactions although it remains poorly understood in arthropod vectors like mosquitoes. Here, we manipulated mosquito microbiota using gnotobiology to decipher the impact of bacteria and diet on the Asian tiger mosquito, Ae. albopictus. These results are key to understand the link between diet and bacteria concentration on juvenile mosquitoes as well as carry-over effects in adults. They unveil some specific aspects of mosquito-bacteria interactions while opening interesting avenues for vector management of this vector of arboviruses.

microbiology↗

Alternative developmental and transcriptomic responses to host plant water limitation in a butterfly metapopulation

Predicting how climate change affects biotic interactions and their evolution poses a challenge. Plant-insect herbivore interactions are particularly sensitive to climate change, as climate-induced changes in plant quality cascade into the performance of insect herbivores. Whereas the immediate survival of herbivore individuals depends on plastic responses to climate change induced nutritional stress, long-term population persistence via evolutionary adaptation requires genetic variation for these responses. In order to assess the prospects for population persistence under climate change, it is therefore crucial to characterise response mechanisms to climate change induced stressors, and quantify their variability in natural populations. Here, we test developmental and transcriptomic responses to water limitation induced host plant quality change in a Glanville fritillary butterfly (Melitaea cinxia) metapopulation. We combine nuclear magnetic resonance spectroscopy on the plant metabolome, larval developmental assays and an RNA seq analysis of the larval transcriptome. We observed that responses to feeding on water limited plants, in which amino acids and aromatic compounds are enriched, showed marked intrapopulation variation, with individuals of some families performing better on control and others on water limited plants. The transcriptomic responses were concordant with the developmental responses: Families exhibiting opposite developmental responses also produced opposite transcriptomic responses, e.g. in growth associated intracellular signalling. The opposite developmental and transcriptomic responses are associated with between families differences in organic compound catabolism and storage protein production. The results reveal heritable intrapopulation variability in plasticity, suggesting potential for evolutionary responses to drought-induced changes in host plant quality in the Finnish M. cinxia metapopulation.

ecology↗

Variation in Melitaea cinxia gut microbiota is phylogenetically highly structured but only mildly driven by host plant microbiota, sex or parasitism.

Originality-Significance StatementThe factors contributing to the assembly of microbiota in animals are extremely complex, and thus a comprehensive understanding of the mechanisms shaping host-associated microbial communities in natural ecosystems requires extensive ecological studies and appropriate statistical methods. In this study, we investigated the bacterial microbiota associated with the caterpillars of the Glanville fritillary (Melitaea cinxia), which is a long-term-studied ecological model system. We assessed the structure of variation in both occurrence and abundance of gut microbial communities of individuals collected in the wild with joint-species modelling, with the aim to relate the microbial community structure with multiple potentially impacting covariates: host plant microbiota and metabolites, hosts sex, potential parasitoid infection, and family structure. These covariates exhibited substantial correlation with multiple microbial taxas occurrences, which correlations were consistent for phylogenetically related groups of taxa, but varied across the whole microbial community; on the contrary, only few correlations were found with taxas abundances. The dominating co-occurrence pattern of microbiota assembly, which effectively split caterpillar individuals into two distinct groups, was, however, unrelated to any of the considered covariates.\n\nSummaryUnderstanding of what ecological factors shape intraspecific variation of insect microbiota is still relatively poor. In Lepidopteran caterpillars, microbiota is assumed to be mainly composed of transient bacterial symbionts acquired from the host plant. We sampled Glanville fritillary (Melitaea cinxia) caterpillars from natural populations to describe the microbiome and to identify potential factors that determine the structure of the microbial community, including the sex of the host, the impact of parasitoid infection, and the possible link between host plant and caterpillar microbiota. Our results demonstrate high variability of microbiota composition even among caterpillars that shared the same host plant individual. The observed variation in microbiota composition is partially attributed to the measured properties of the host or its plant microbial and chemical composition, and is aligned with microbial phylogenetic structure, with related taxa exhibiting similar patterns. However, the prevailing part of the observed variation was not associated with any of the assessed characteristics, although it followed a pronounced segregation structure: in some caterpillars the microbial communities were dominated by several related Enterobacteriaceae taxa, while in others these taxa were absent. Our results challenge previous findings that the host plant properties are the major drivers of microbiota communities of insect herbivores.

ecology↗

Every cloud has a silver lining: Moderate plant water stress positively impacts development, immunity, and gut microbiota of a specialist herbivore

The ongoing global temperature rise has led to increasing frequency of drought events, negatively impacting vegetation and the living organisms relying on it. Extreme drought killing host plants can clearly reduce herbivore fitness, but the impact of moderate host plant water stress on insect herbivores can vary, and may even be beneficial. The Finnish Glanville fritillary butterfly (Melitaea cinxia) has faced reduced precipitation in recent years, which has impacted population dynamics. However, whether the negative effects depend on extreme desiccation killing the host plant or moderate drought impacting plant quality remains unclear. We assessed the performance of larvae fed on moderately water-stressed Plantago lanceolata in terms of growth, gut microbial composition and immune response. We found that larvae fed on water-stressed plants had better growth, a more heterogeneous bacterial community and a shifted fungal community in the gut, and up-regulated the expression of one candidate immune gene (pelle), whereas survival remained unaffected. Most of the measured traits showed considerable variation due to family structure. Our data suggest that in temperate regions moderate host plant water stress can positively shape resource acquisition of this specialized insect herbivore, potentially by increasing nutrient accessibility or concentration. Potentially, the better larval performance may be mediated by a shift of the microbiota on water-stressed plants, calling for further research especially on the understudied gut fungal community.

ecology↗