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Parasite-mediated selection can rapidly drive up resistance levels in host populations, but fixation of resistance traits may be prevented by costs of resistance. Black bean aphids (Aphis fabae) benefit from increased resistance to parasitoids when carrying the defensive bacterial endosymbiont Hamiltonella defensa. However, due to fitness costs that come with symbiont infection, symbiont-conferred resistance may result in either a net benefit or a net cost to the aphid host, depending on parasitoid presence as well as on the general ecological context. Balancing selection may therefore explain why in natural aphid populations, H. defensa is often found at intermediate frequencies. Here we present a 2-year field study where we set out to look for signatures of balancing selection in natural aphid populations. We collected temporally well-resolved data on the prevalence of H. defensa in A. f. fabae and estimated the risk imposed by parasitoids using sentinel hosts. Despite a marked and consistent early-summer peak in parasitism risk, and significant changes in symbiont prevalence over time, we found just a weak correlation between parasitism risk and H. defensa frequency dynamics. H. defensa prevalence in the populations under study was, in fact, better explained by the number of heat days that previous aphid generations were exposed to. Our study grants an unprecedentedly well-resolved insight into the dynamics of endosymbiont and parasitoid communities of A. f. fabae populations, and it adds to a growing body of empirical evidence suggesting that not only parasitism risk, but rather multifarious selection is shaping H. defensa prevalence in the wild., Molecular Ecology, 32 (14), ISSN:0962-1083, ISSN:1365-294X

Human impacts such as habitat loss, climate change and biological invasions are radically altering biodiversity, with greater effects projected into the future. Evidence suggests human impacts may differ substantially between terrestrial and freshwater ecosystems, but the reasons for these differences are poorly understood. We propose an integrative approach to explain these differences by linking impacts to four fundamental processes that structure communities: dispersal, speciation, species-level selection and ecological drift. Our goal is to provide process-based insights into why human impacts, and responses to impacts, may differ across ecosystem types using a mechanistic, eco-evolutionary comparative framework. To enable these insights, we review and synthesise (i) how the four processes influence diversity and dynamics in terrestrial versus freshwater communities, specifically whether the relative importance of each process differs among ecosystems, and (ii) the pathways by which human impacts can produce divergent responses across ecosystems, due to differences in the strength of processes among ecosystems we identify. Finally, we highlight research gaps and next steps, and discuss how this approach can provide new insights for conservation. By focusing on the processes that shape diversity in communities, we aim to mechanistically link human impacts to ongoing and future changes in ecosystems., Ecology Letters, 26 (2), ISSN:1461-023X, ISSN:1461-0248

Aim Biological invasions are a major threat to biodiversity in aquatic and terrestrial habitats. Insects represent an important group of species in freshwater and terrestrial habitats, and they constitute a large proportion of non-native species. However, while many non-native insects are known from terrestrial ecosystems, they appear to be less represented in freshwater habitats. Comparisons between freshwater and terrestrial habitats of invader richness relative to native species richness are scarce, which hinders syntheses of invasion processes. Here, we used data from three regions on different continents to determine whether non-native insects are indeed under-represented in freshwater compared with terrestrial assemblages. Location Europe, North America, New Zealand. Methods We compiled a comprehensive inventory of native and non-native insect species established in freshwater and terrestrial habitats of the three study regions. We then contrasted the richness of non-native and native species among freshwater and terrestrial insects for all insect orders in each region. Using binomial regression, we analysed the proportions of non-native species in freshwater and terrestrial habitats. Marine insect species were excluded from our analysis, and insects in low-salinity brackish water were considered as freshwater insects. Results In most insect orders living in freshwater, non-native species were under-represented, while they were over-represented in a number of terrestrial orders. This pattern occurred in purely aquatic orders and in orders with both freshwater and terrestrial species. Overall, the proportion of non-native species was significantly lower in freshwater than in terrestrial species. Main conclusions Despite the numerical and ecological importance of insects among all non-native species, non-native insect species are surprisingly rare in freshwater habitats. This is consistent across the three investigated regions. We review hypotheses concerning species traits and invasion pathways that are most likely to explain these patterns. Our findings contribute to a growing appreciation of drivers and impacts of biological invasions., Diversity and Distributions, 28 (11), ISSN:1366-9516, ISSN:1472-4642

The phylogeographic patterns of many taxa on New Zealand's South Island are characterized by disjunct distributions that have been attributed to Pleistocene climatic cycles and the formation of the Southern Alps. Pleistocene glaciation has been implicated in shaping the contemporary genetic differentiation between populations of the aquatic snail Potamopyrgus antipodarum. We investigated whether similar phylogeographic patterns exist for the snail's locally adapted trematode parasite, Atriophallophorus winterbourni. We found evidence for a barrier to gene-flow in sympatry between cryptic, but ecologically divergent species. When focusing on the most common of these species, disjunct geographic distributions are found for mitochondrial lineages that diverged during the Pleistocene. The boundary between these distributions is found in the central part of the South Island and is reinforced by low cross-alpine migration. Further support for a vicariant origin of the phylogeographic pattern was found when assessing nuclear multilocus SNP data. Nuclear and mitochondrial population differentiation was concordant in pattern, except for populations in a potential secondary contact zone. Additionally, we found larger than expected differentiation between nuclear- and mitochondrial-based empirical Bayes FST estimates (global FST: 0.02 vs. 0.39 for nuclear and mitochondrial data, respectively). Population subdivision is theoretically expected to be stronger for mitochondrial genomes due to a smaller effective population size, but the strong difference here, together with mitonuclear discordance in a putative contact zone, is potentially indicative of divergent gene flow of nuclear and mitochondrial genomes., Molecular Ecology, 31 (15), ISSN:0962-1083, ISSN:1365-294X

Monitoring the occurrence and density of parasites and pathogens can identify high infection-risk areas and facilitates disease control and eradication measures. Environmental DNA (eDNA) techniques are increasingly used for pathogen detection due to their relative ease of application. Since many factors affect the reliability and efficacy of eDNA-based detection, rigorous validation and assessment of method limitations is a crucial first step. We evaluated an eDNA detection method usingin situfiltration of large-volume water samples, developed to detect and quantify aquatic wildlife parasites by quantitative PCR (qPCR). We assessed method reliability usingBatrachochytrium dendrobatidis,a pathogenic fungus of amphibians and the myxozoanTetracapsuloides bryosalmonae, causative agent of salmonid proliferative kidney disease, in a controlled experimental setup. Different amounts of parasite spores were added to tanks containing either clean tap water or water from a semi-natural mesocosm community. Overall detection rates were higher than 80%, but detection was not consistent among replicate samples. Within-tank variation in detection emphasises the need for increased site-level replication when dealing with parasites and pathogens. Estimated parasite DNA concentrations in water samples were highly variable, and a significant increase with higher spore concentrations was observed only forB. dendrobatidis. Despite evidence for PCR inhibition in DNA extractions from mesocosm water samples, the type of water did not affect detection rates significantly. Direct spiking controls revealed that the filtration step reduced detection sensitivity. Our study identifies sensitive quantification and sufficient replication as major remaining challenges for the eDNA-based methods for detection of parasites in water.

Protective symbionts can provide effective and specific protection to their hosts. This protection can differ between different symbiont strains with each strain providing protection against certain components of the parasite and pathogen community their host faces. Protective symbionts are especially well known from aphids where, among other functions, they provide protection against different parasitoid wasps. However, most of the evidence for this protection comes from laboratory experiments. Our aim was to understand how consistent protection is across different symbiont strains under natural field conditions and whether symbiont diversity enhanced the species diversity of colonizing parasitoids, as could be expected from the specificity of their protection. We used experimental colonies of the black bean aphid Aphis fabae to investigate symbiont-conferred protection under natural field conditions over two seasons. Colonies differed only in their symbiont composition, carrying either no symbionts, a single strain of the protective symbiont Hamiltonella defensa, or a mixture of three H. defensa strains. These aphid colonies were exposed to natural parasitoid communities in the field. Subsequently, we determined the parasitoids hatched from each aphid colony. The evidence for a protective effect of H. defensa was limited and inconsistent between years, and aphid colonies harbouring multiple symbiont strains did not support a more diverse parasitoid community. Instead, parasitoid diversity tended to be highest in the absence of H. defensa. Symbiont-conferred protection, although a strong and repeatable effect under laboratory conditions may not always cause the predicted bottom-up effects under natural conditions in the field.

Invasive species can facilitate the spread of pathogens by first providing asymptomatic host reservoirs, and then driving disease outbreaks in native populations through pathogen spillover. An example of this are invasive crayfish species in Europe (Faxonius limosus, Pacifastacus leniusculus, Procambarus clarkii), which carry the deadly plague agent (Aphanomyces astaci). Effective disease management requires comprehensive monitoring, however, pathogen detection in carrier populations with low pathogen prevalence and intensities is challenging. We simultaneously collected and analysed crayfish tissue samples of invasive crayfish populations and water samples to compare A. astaci detection in different sample types using quantitative PCR. Combined, the two sampling methods revealed A. astaci presence with DNA concentrations above limit of detection (LOD; the lowest concentration which can be detected with reasonable certainty) in 13 of 23 invasive crayfish populations. In four additional sites, A. astaci DNA concentrations below LOD were found in water. In four populations only were A. astaci concentrations above LOD detected in both sample types and in three populations in concentrations above LOD in tissue but below LOD in water. The likely reason for these discrepancies is the low A. astaci prevalence and concentration in resistant invasive crayfish, which limit detection reliability. Consistency may be improved by timing surveys with seasonal periods of high A. astaci abundance and by increasing water sampling effort. Considering the ease of collecting eDNA samples, compared to crayfish tissue sampling, eDNA methods would facilitate frequent and comprehensive surveys. However, remaining uncertainties in eDNA-based detection reveal the relevance of combining monitoring tools to improve detection of invasive pathogens and their management., Biological Invasions, 24 (1), ISSN:1387-3547, ISSN:1573-1464

Insect host–parasitoid interactions abound in nature and are characterized by a high degree of host specialization. In addition to their behavioral and immune defenses, many host species rely on heritable bacterial endosymbionts for defense against parasitoids. Studies on aphids and flies show that resistance conferred by symbionts can be very strong and highly specific, possibly as a result of variation in symbiont-produced toxins. I argue that defensive symbionts are therefore an important source of diversifying selection, promoting the evolution of host specialization by parasitoids. This is likely to affect the structure of host–parasitoid food webs. I consider potential changes in terms of food web complexity, although the nature of these effects will also be influenced by whether maternally transmitted symbionts have some capacity for lateral transfer. This is discussed in the light of available evidence for horizontal transmission routes. Finally, I propose that defensive mutualisms other than microbial endosymbionts may also exert diversifying selection on insect parasitoids.

Insect hosts and parasitoids are engaged in an intense struggle of antagonistic coevolution. Infection with heritable bacterial endosymbionts can substantially increase the resistance of aphids to parasitoid wasps, which exerts selection on parasitoids to overcome this symbiont-conferred protection (counteradaptation). Experimental evolution in the laboratory has produced counteradapted populations of the parasitoid wasp Lysiphlebus fabarum. These populations can parasitize black bean aphids (Aphis fabae) protected by the bacterial endosymbiont Hamiltonella defensa, which confers high resistance against L. fabarum. We used two experimentally evolved parasitoid populations to study the genetic architecture of the counteradaptation to symbiont-conferred resistance by QTL analysis. With simple crossing experiments, we showed that the counteradaptation is a recessive trait depending on the maternal genotype. Based on these results, we designed a customized crossing scheme to genotype a mapping population phenotyped for the ability to parasitize Hamiltonella-protected aphids. Using 1835 SNP markers obtained by ddRAD sequencing, we constructed a high-density linkage map consisting of six linkage groups (LGs) with an overall length of 828.3 cM and an average marker spacing of 0.45 cM. We identified a single QTL associated with the counteradaptation to Hamiltonella in L. fabarum on linkage group 2. Out of 120 genes located in this QTL, several genes encoding putative venoms may represent candidates for counteradaptation, as parasitoid wasps inject venoms into their hosts during oviposition., Heredity, 127 (2), ISSN:0018-067x, ISSN:1365-2540

Virtually all higher organisms form holobionts with associated microbiota. To understand the biology of holobionts we need to know how species assemble and interact. Controlled experiments are suited to study interactions between particular symbionts, but they only accommodate a tiny portion of the diversity within each species. Alternatively, interactions can be inferred by testing if associations among symbionts in the field are more or less frequent than expected under random assortment. However, random assortment may not be a valid null hypothesis for maternally transmitted symbionts since drift alone can result in associations. Here, we analyse a European field survey of endosymbionts in pea aphids (Acyrthosiphon pisum), confirming that symbiont associations are pervasive. To interpret them, we develop a model simulating the effect of drift on symbiont associations. We show that drift induces apparently nonrandom assortment, even though horizontal transmissions and maternal transmission failures tend to randomise symbiont associations. We also use this model in the approximate Bayesian computation framework to revisit the association between Spiroplasma and Wolbachia in Drosophila neotestacea. New field data reported here reveal that this association has disappeared in the investigated location, yet a significant interaction between Spiroplasma and Wolbachia can still be inferred. Our study confirms that negative and positive associations are pervasive and often induced by symbiont-symbiont interactions. Nevertheless, some associations are also likely to be driven by drift. This possibility needs to be considered when performing such analyses, and our model is helpful for this purpose.

Parasites and pathogens are crucial in shaping immune systems. Many animals and especially insects have outsourced part of their immune function to protective symbionts. There is good evidence that, akin to immune systems, parasites shape the occurrence and diversity of protective symbionts and that likewise, protective symbionts can shape the occurrence and diversity of parasites. Such a relationship should result in a correlation between symbiont and parasite diversity in nature. Aphids are well known for possessing symbionts that provide specific and effective protection against parasitoid wasps. We compared symbiont and parasitoid diversity across multiple populations of different aphid species of the genus Aphis and their parasitoid wasps. The diversity of protective symbionts and parasitoids was indeed positively associated. Even though this association was very noisy, it is in line with the hypothesis that parasitoids and symbionts promote each other’s diversity. © 2021 The Authors. ISSN:2150-8925

The dynamics of coevolution between hosts and parasites are influenced by their genetic interactions. Highly specific interactions, where the outcome of an infection depends on the precise combination of host and parasite genotypes (G x G interactions), have the potential to maintain genetic variation by inducing negative frequency-dependent selection. The importance of this effect also rests on whether such interactions are consistent across different environments or modified by environmental variation (G x G x E interaction). In the black bean aphid, Aphis fabae, resistance to its parasitoid Lysiphlebus fabarum is largely determined by the possession of a heritable bacterial endosymbiont, Hamiltonella defensa, with strong G x G interactions between H. defensa and L. fabarum. A key environmental factor in this system is the host plant on which the aphid feeds. Here, we exposed genetically identical aphids harbouring three different strains of H. defensa to three asexual genotypes of L. fabarum and measured parasitism success on three common host plants of A. fabae, namely Vicia faba, Chenopodium album and Beta vulgaris. As expected, we observed the pervasive G x G interaction between H. defensa and L. fabarum, but despite strong main effects of the host plants on average rates of parasitism, this interaction was not altered significantly by the host plant environment (no G x G x E interaction). The symbiont-conferred specificity of resistance is thus likely to mediate the coevolution of A. fabae and L. fabarum, even when played out across diverse host plants of the aphid., Journal of Evolutionary Biology, 34 (12), ISSN:1010-061X, ISSN:1420-9101

Secondary endosymbionts of aphids have an important ecological and evolutionary impact on their host, as they provide resistance to natural enemies but also reduce the host’s lifespan and reproduction. While secondary symbionts of aphids are faithfully transmitted from mother to offspring, they also have some capacity to be transmitted horizontally between aphids. Here we explore whether 11 isolates from 3 haplotypes of the secondary endosymbiont Hamiltonella defensa differ in their capacity for horizontal transmission. These isolates vary in the protection they provide against parasitoid wasps as well as the costs they inflict on their host, Aphis fabae. We simulated natural horizontal transmission through parasitoid wasps by stabbing aphids with a thin needle and assessed horizontal transmission success of the isolates from one shared donor clone into three different recipient clones. Specifically, we asked whether potentially costly isolates reaching high cell densities in aphid hosts are more readily transmitted through this route. This hypothesis was only partially supported. While transmissibility increased with titre for isolates from two haplotypes, isolates of the H. defensa haplotype 1 were transmitted with greater frequency than isolates of other haplotypes with comparable titres. Thus, it is not sufficient to be merely frequent—endosymbionts might have to evolve specific adaptations to transmit effectively between hosts.

Immune systems have repeatedly diversified in response to parasite diversity. Many animals have outsourced part of their immune defence to defensive symbionts, which should be affected by similar evolutionary pressures as the host's own immune system. Protective symbionts provide efficient and specific protection and respond to changing selection pressure by parasites. Here we use the aphid Aphis fabae, its protective symbiont Hamiltonella defensa, and its parasitoid Lysiphlebus fabarum to test whether parasite diversity can maintain diversity in protective symbionts. We exposed aphid populations with the same initial symbiont composition to parasitoid populations that differed in their diversity. As expected, single parasitoid genotypes mostly favoured a single symbiont that was most protective against that particular parasitoid, while multiple symbionts persisted in aphids exposed to more diverse parasitoid populations, which in turn affected aphid population density and rates of parasitism. Parasite diversity may be crucial to maintaining symbiont diversity in nature.

There is increasing demand for sustainable pest management to reduce harmful effects of pesticides on the environment and human health. For pest aphids, biological control with parasitoid wasps provides a welcome alternative, particularly in greenhouses. However, aphids are frequently infected with the heritable bacterial endosymbiont Hamiltonella defensa, which increases resistance to parasitoids and thereby hampers biological control. Using the black bean aphid (Aphis fabae) and its main parasitoid Lysiphlebus fabarum, we tested whether prior adaptation of parasitoids can improve the control of symbiont‐protected pests. We had parasitoid lines adapted to two different strains of H. defensa by experimental evolution, as well as parasitoids evolved on H. defensa‐free aphids. We compared their ability to control caged aphid populations comprising 60% unprotected and 40% H. defensa‐protected aphids, with both H. defensa strains present in the populations. Parasitoids that were not adapted to H. defensa had virtually no effect on aphid population dynamics compared to parasitoid‐free controls, but one of the adapted lines and a mixture of both adapted lines controlled aphids successfully, strongly benefitting plant growth. Selection by parasitoids altered aphid population composition in a very specific manner. Aphid populations became dominated by H. defensa‐protected aphids in the presence of parasitoids, and each adapted parasitoid line selected for the H. defensa strain it was not adapted to. This study shows, for the first time, that prior adaptation of parasitoids improves biological control of symbiont‐protected pests, but the high specificity of parasitoid counter‐resistance may represent a challenge for its implementation.

Coevolving taxa offer the opportunity to study the genetic basis of rapid reciprocal adaptation. We have used experimental evolution to examine adaptation in the parasitoid waspLysiphlebus fabarumto resistance conferred by the protective endosymbiontHamiltonella defensain its aphid hostAphis fabae. To examine a key stage in parasitoid infection, we have used RNA-seq to study gene expression in 4-5 day old parasitoid larvae contained in still living aphids. With this dual RNA-seq we can simultaneously view expression in individual experimentally evolved parasitoids and the aphids that house them. This gives a view of the sweeping changes in both taxa accompanying successful or unsuccessful infections. Among successful larvae, we find that experimentally evolved populations adapted toH. defensa-protected hosts differ in the expression of genes that include putative toxins and genes to cope with stress. These differences remain even when the larvae are developing in aphids possessing no defensive endosymbionts, suggesting that they are genetically based. In contrast, plastic responses between parasitoids reared in hosts with and withoutH. defensaare relatively small. Although aphids rely largely on their secondary endosymbionts for defense against parasitoids, we identify expression differences in aphids housing different parasitoid phenotypes. Together, these results demonstrate that wild parasitoid populations possess the genetic variation for rapid adaptation to host resistance, resulting in genetically based differences in gene expression that increase their success in parasitizing symbiont-protected host aphids.

We report on a novel RNA virus infecting the wasp Lysiphlebus fabarum, a parasitoid of aphids. This virus, tentatively named “Lysiphlebus fabarum virus” (LysV), was discovered in transcriptome sequences of wasps from an experimental evolution study in which the parasitoids were allowed to adapt to aphid hosts (Aphis fabae) with or without resistance-conferring endosymbionts. Based on phylogenetic analyses of the viral RNA-dependent RNA polymerase (RdRp), LysV belongs to the Iflaviridae family in the order of the Picornavirales, with the closest known relatives all being parasitoid wasp-infecting viruses. We developed an endpoint PCR and a more sensitive qPCR assay to screen for LysV in field samples and laboratory lines. These screens verified the occurrence of LysV in wild parasitoids and identified the likely wild-source population for lab infections in Western Switzerland. Three viral haplotypes could be distinguished in wild populations, of which two were found in the laboratory. Both vertical and horizontal transmission of LysV were demonstrated experimentally, and repeated sampling of laboratory populations suggests that the virus can form persistent infections without obvious symptoms in infected wasps.

BackgroundParasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol, and infecting aphids requires overcoming both aphid defenses and their defensive endosymbionts.ResultsWe present thede novogenome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids:Aphidius erviandLysiphlebus fabarum(Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage, and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and age-specific energy demands. We identify expansions of F-box/Leucine-rich-repeat proteins, suggesting that diversification in this gene family may be associated with their broad host range or with countering defenses from aphids’ endosymbionts. The absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids.ConclusionsThese findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available athttps://bipaa.genouest.org.

Understanding the coevolution of hosts and parasites is a long-standing goal of evolutionary biology. There is a well-developed theoretical framework to describe the evolution of host-parasite interactions under the assumption of direct, two-species interactions, which can result in arms race dynamics or sustained genotype fluctuations driven by negative frequency dependence (Red Queen dynamics). However, many hosts rely on symbionts for defence against parasites. Whilst the ubiquity of defensive symbionts and their potential importance for disease control are increasingly recognized, there is still a gap in our understanding of how symbionts mediate or possibly take part in host-parasite coevolution. Herein we address this question by synthesizing information already available from theoretical and empirical studies. First, we briefly introduce current hypotheses on how defensive mutualisms evolved from more parasitic relationships and highlight exciting new experimental evidence showing that this can occur very rapidly. We go on to show that defensive symbionts influence virtually all important determinants of coevolutionary dynamics, namely the variation in host resistance available to selection by parasites, the specificity of host resistance, and the trade-off structure between host resistance and other components of fitness. In light of these findings, we turn to the limited theory and experiments available for such three-species interactions to assess the role of defensive symbionts in host-parasite coevolution. Specifically, we discuss under which conditions the defensive symbiont may take over from the host the reciprocal adaptation with parasites and undergo its own selection dynamics, thereby altering or relaxing selection on the hosts' own immune defences. Finally, we address potential effects of defensive symbionts on the evolution of parasite virulence. This is an important problem for which there is no single, clear-cut prediction. The selection on parasite virulence resulting from the presence of defensive symbionts in their hosts will depend on the underlying mechanism of defence. We identify the evolutionary predictions for different functional categories of symbiont-conferred resistance and we evaluate the empirical literature for supporting evidence. We end this review with outstanding questions and promising avenues for future research to improve our understanding of symbiont-mediated coevolution between hosts and parasites.

ISSN:0269-8463 ISSN:1365-2435

Reciprocal selection between aphids, their protective endosymbionts, and the parasitoid wasps that prey upon them offers an opportunity to study the basis of their coevolution. We investigated adaptation to symbiont-conferred defense by rearing the parasitoid wasp Lysiphlebus fabarum on aphids (Aphis fabae) possessing different defensive symbiont strains (Hamiltonella defensa). After ten generations of experimental evolution, wasps showed increased abilities to parasitize aphids possessing the H. defensa strain they evolved with, but not aphids possessing the other strain. We show that the two symbiont strains encode different toxins, potentially creating different targets for counter-adaptation. Phenotypic and behavioral comparisons suggest that neither life-history traits nor oviposition behavior differed among evolved parasitoid lineages. In contrast, comparative transcriptomics of adult female wasps identified a suite of differentially expressed genes among lineages, even when reared in a common, symbiont-free, aphid host. In concurrence with the specificity of each parasitoid lineages' infectivity, most differentially expressed parasitoid transcripts were also lineage-specific. These transcripts are enriched with putative venom toxins and contain highly expressed, potentially defensive viral particles. Together, these results suggest that wild populations of L. fabarum employ a complicated offensive arsenal with sufficient genetic variation for wasps to adapt rapidly and specifically to their hosts' microbial defenses.

Specialization on different host plants can promote evolutionary diversification of herbivorous insects. Work on pea aphids (Acyrthosiphon pisum) has contributed significantly to the understanding of this process, demonstrating that populations associated with different host plants exhibit performance trade-offs across hosts, show adaptive host choice and genetic differentiation and possess different communities of bacterial endosymbionts. Populations specialized on different secondary host plants during the parthenogenetic summer generations are also described for the black bean aphid (Aphis fabae complex) and are usually treated as different (morphologically cryptic) subspecies. In contrast to pea aphids, however, host choice and mate choice are decoupled in black bean aphids, because populations from different summer hosts return to the same primary host plant to mate and lay overwintering eggs. This could counteract evolutionary divergence, and it is currently unknown to what extent black bean aphids using different summer hosts are indeed differentiated. We addressed this question by microsatellite genotyping and endosymbiont screening of black bean aphids collected in summer from the goosefoot Chenopodium album (subspecies A. f. fabae) and from thistles of the genus Cirsium (subspecies A. f. cirsiiacanthoides) across numerous sites in Switzerland and France. Our results show clearly that aphids from Cirsium and Chenopodium exhibit strong and geographically consistent genetic differentiation and that they differ in their frequencies of infection with particular endosymbionts. The dependence on a joint winter host has thus not prevented the evolutionary divergence into summer host-adapted populations that appear to have evolved mechanisms of reproductive isolation within a common mating habitat.

1. Insects are commonly infected with bacterial endosymbionts. In addition to the costs and benefits associated with harbouring these symbionts, their rates of vertical and horizontal transmission are important determinants of symbiont prevalence. 2. Aphids are cyclical parthenogens and show virtually perfect maternal transmission of endosymbionts during asexual reproduction. Less clear is the role of the annual sexual generation, during which overwintering eggs are produced. Data from pea aphids (Acyrthosiphon pisum Harris) suggest that maternal transmission failures and horizontal transmission via males may occur under sexual reproduction at least occasionally. No such data exist for other aphid species. 3. In the present study, the rates of maternal and paternal transmission of facultative endosymbionts during sexual reproduction in the black bean aphid, Aphis fabae (Scopoli) were examined. Crosses were performed between clones infected with Hamiltonella defensa, clones infected with Regiella insecticola and clones without facultative endosymbionts, and eggs were overwintered under three different conditions. 4. Only one of 205 offspring from crosses testing for maternal transmission failed to inherit the symbiont present in the maternal clone, and in crosses testing for horizontal transmission, only one of 412 offspring acquired a facultative symbiont from the father. 5. These results show that in A. fabae, maternal transmission of H. defensa and R. insecticola is extremely reliable also during sexual reproduction, indicating that maternal transmission failures are unlikely to exert a significant influence on frequencies of infection in the field. Paternal transmission of endosymbionts was exceedingly rare, suggesting that this route of horizontal transmission may be less important than hitherto assumed.

International audience; The heritable endosymbiont Spiroplasma infects many insects and has repeatedly evolved the ability to protect its hosts against different parasites. Defenses do not come for free to the host, and theory predicts that more costly symbionts need to provide stronger benefits to persist in host populations. We investigated the costs and benefits of Spiroplasma infections in pea aphids (Acyrthosiphon pisum), testing 12 bacterial strains from three different clades. Virtually all strains decreased aphid lifespan and reproduction, but only two had a (weak) protective effect against the parasitoid Aphidius ervi, an important natural enemy of pea aphids. Spiroplasma-induced fitness costs were variable, with strains from the most slowly evolving clade reaching higher titers and curtailing aphid lifespan more strongly than other strains. Some Spiroplasma strains shared their host with a second endosymbiont, Regiella insecticola. Although the result of an unfortunate handling error, these co-infections proved instructive, because they showed that the cost of infection with Spiroplasma may be attenuated in the presence of Regiella. These results suggest that mechanisms other than protection against A. ervi maintain pea aphid infections with diverse strains of Spiroplasma, and that studying them in isolation will not provide a complete picture of their effects on host fitness.

Anthropogenic river fragmentation has the potential to alter fish population structure and diversity, but it can be difficult to infer whether observed effects reflect the obstruction of fish movement or population responses to altered flow regimes or habitat structure concomitant with fragmentation. We addressed the influence of habitat fragmentation on the European Chub (Squalius cephalus), a large-bodied fish with strong swimming ability that is a ubiquitous habitat generalist that occurs at high densities in lentic and lotic habitats. European Chub populations have never been stocked and are little affected by habitat alterations. Thus, they are good sentinels for the effects of fragmentation per se. We used microsatellite genotyping of 1726 fish from 38 sites to compare the genetic structure and diversity of European Chub populations from 3 Swiss midland rivers that are unequally affected by man-made fragmentation. The Thur is unfragmented, the adjacent Glatt is strongly fragmented by tall ba...

Drawing insights from multiple disciplines is essential for finding integrative solutions that are required to tackle complex environmental problems. Human activities are causing unprecedented influence on global ecosystems, culminating in the loss of species and fundamental changes in the selective environments of organisms across the tree of life. Our collective understanding about biological evolution can help identify and mitigate many of the environmental problems in the Anthropocene. To this end, we propose a stronger integration of environmental sciences with evolutionary biology., Graphical abstract Unlabelled Image, Highlights • Evolutionary theory is not widely used to address environmental problems. • Evolutionary processes can both ameliorate and exacerbate environmental problems. • Evolution can be informative about disease dynamics, biofuel production, adaptation to pollution, and harmful algal blooms. • We propose a stronger integration of evolutionary biology with environmental sciences to help solve environmental problems.

Insects commonly possess heritable microbial symbionts that increase their resistance to particular parasites. A diverse community of defensive symbionts may thus provide hosts with effective and specific protection against multiple parasites, although costs might constrain the accumulation of many symbionts. In parallel to the allelic diversity in the MHC complex of the vertebrate immune system, parasite diversity could be the driving force behind symbiont diversity. There is indeed evidence that parasites have the ability to drive frequencies of defensive symbionts in their hosts, and that these symbionts influence parasite communities, but direct evidence that parasite diversity can promote symbiont diversity is still lacking. We provide suggestions to investigate this potential link.