Adaptations and counter-adaptations in <i>Drosophila</i> host-parasitoid interactions:Advances in the molecular mechanisms

Both hosts and parasitoids evolved a diverse array of traits and strategies for their antagonistic interactions, affecting their chances of encounter, attack and survival after parasitoid attack. This review summarizes the recent progress that has been made in elucidating the molecular mechanisms of these adaptations and counter-adaptations in various Drosophila host-parasitoid interactions. For the hosts, it focuses on the neurobiological and genetic control of strategies in Drosophila adults and larvae of avoidance or escape behaviours upon sensing the parasitoids, and the immunological defences involving diverse classes of haemocytes. For the parasitoids, it highlights their behavioural strategies in host finding, as well as the rich variety of venom components that evolved and were partially acquired through horizontal gene transfer. Recent studies revealed the mechanisms by which these venom components manipulate their parasitized hosts in exhibiting escape behaviour to avoid superparasitism, and their counter-strategies to evade or obstruct the hosts' immunological defences

Genomic basis of evolutionary change:evolving immunity

Complex traits are manifestations of intricate gene interaction networks. Evolution of complex traits revolves around the genetic variation in such networks. Genomics has increased our ability to investigate the complex gene interaction networks, and characterize the extent of genetic variation in these networks. Immunity is a complex trait, for which the ecological drivers and molecular networks are fairly well understood in Drosophila. By characterizing the natural variation in immunity, and mapping how the genome changes during the evolution of immunity in Drosophila, we can integrate our knowledge on the complex genetic architecture of traits and the molecular basis of evolutionary processes

Rapid but narrow:Evolutionary adaptation and transcriptional response of <i>Drosophila melanogaster</i> to toxic mould

Insects have adapted to a multitude of environmental conditions, including the presence of xenobiotic noxious substances. Environmental microorganisms, particularly rich on ephemeral resources, employ these noxious chemicals in a chemical warfare against predators and competitors, driving co-evolutionary adaptations. In order to analyse how environmental microbes may be driving such evolutionary adaptations, we experimentally evolved Drosophila melanogaster populations by exposing larvae to the toxin-producing mould Aspergillus nidulans that infests the flies' breeding substrate. To disentangle the effects of the mycotoxin Sterigmatocystin from other substrate modifications inflicted by the mould, we used the following four selection regimes: (i) control without fungus, (ii) A. nidulans wild type, (iii) a mutant of A. nidulans ΔlaeA with impaired toxin production, (iv) synthetic Sterigmatocystin. Experimental evolution was carried out in five independent D. melanogaster populations each, for a total of 11 generations. We further combined our evolution experiment with transcriptome analysis to identify evolutionary shifts in gene expression due to the selection regimes and mould confrontation. Populations that evolved in presence of the toxin-producing mould or the pure mycotoxin rapidly adapted to the respective conditions and showed higher viability in subsequent confrontations. Yet, mycotoxin-selected populations had no advantage in A. nidulans wild type confrontation. Moreover, distinctive changes in gene expression related to the selection-regime contrast were only associated with the toxin-producing-fungus regime and comprised a narrow set of genes. Thus, it needs the specific conditions of the selection agent to enable adaptation to the fungus.</p

Context-dependence and the development of push-pull approaches for integrated management of <i>Drosophila suzukii</i>

Sustainable pest control requires a systems approach, based on a thorough ecological understanding of an agro-ecosystem. Such fundamental understanding provides a basis for developing strategies to manipulate the pest's behaviour, distribution, and population dynamics, to be employed for crop protection. This review focuses on the fundamental knowledge required for the development of an effective push-pull approach. Push-pull is a strategy to repel a pest from a crop, while attracting it toward an external location. It often relies on infochemicals (e.g., pheromones or allelochemicals) that are relevant in the ecology of the pest insect and can be exploited as lure or repellent. Importantly, responsiveness of insects to infochemicals is dependent on both the insect's internal physiological state and external environmental conditions. This context-dependency reflects the integration of cues from different sensory modalities, the effect of mating and/or feeding status, as well as diurnal or seasonal rhythms. Furthermore, when the costs of responding to an infochemical outweigh the benefits, resistance can rapidly evolve. Here, we argue that profound knowledge on context-dependence is important for the development and implementation of push-pull approaches. We illustrate this by discussing the relevant fundamental knowledge on the invasive pest species Drosophila suzukii as an example

Transcriptomic Analysis of Light-Induced Genes in Nasonia vitripennis:Possible Implications for Circadian Light Entrainment Pathways

Circadian entrainment to the environmental day–night cycle is essential for the optimal use of environmental resources. In insects, opsin-based photoreception in the compound eye and ocelli and CRYPTOCHROME1 (CRY1) in circadian clock neurons are thought to be involved in sensing photic information, but the genetic regulation of circadian light entrainment in species without light-sensitive CRY1 remains unclear. To elucidate a possible CRY1-independent light transduction cascade, we analyzed light-induced gene expression through RNA-sequencing in Nasonia vitripennis. Entrained wasps were subjected to a light pulse in the subjective night to reset the circadian clock, and light-induced changes in gene expression were characterized at four different time points in wasp heads. We used co-expression, functional annotation, and transcription factor binding motif analyses to gain insight into the molecular pathways in response to acute light stimulus and to form hypotheses about the circadian light-resetting pathway. Maximal gene induction was found after 2 h of light stimulation (1432 genes), and this included the opsin gene opblue and the core clock genes cry2 and npas2. Pathway and cluster analyses revealed light activation of glutamatergic and GABA-ergic neurotransmission, including CREB and AP-1 transcription pathway signaling. This suggests that circadian photic entrainment in Nasonia may require pathways that are similar to those in mammals. We propose a model for hymenopteran circadian light-resetting that involves opsin-based photoreception, glutamatergic neurotransmission, and gene induction of cry2 and npas2 to reset the circadian clock.</p

Coevolutionary feedback elevates constitutive immune defence: a protein network model

Background: Organisms have evolved a variety of defence mechanisms against natural enemies, which are typically used at the expense of other life history components. Induced defence mechanisms impose minor costs when pathogens are absent, but mounting an induced response can be time-consuming. Therefore, to ensure timely protection, organisms may partly rely on constitutive defence despite its sustained cost that renders it less economical. Existing theoretical models addressing the optimal combination of constitutive versus induced defence focus solely on host adaptation and ignore the fact that the efficacy of protection depends on genotype-specific host-parasite interactions. Here, we develop a signal-transduction network model inspired by the invertebrate innate immune system, in order to address the effect of parasite coevolution on the optimal combination of constitutive and induced defence. Results: Our analysis reveals that coevolution of parasites with specific immune components shifts the host's optimal allocation from induced towards constitutive immunity. This effect is dependent upon whether receptors (for detection) or effectors (for elimination) are subjected to parasite counter-evolution. A parasite population subjected to a specific immune receptor can evolve heightened genetic diversity, which makes parasite detection more difficult for the hosts. We show that this coevolutionary feedback renders the induced immune response less efficient, forcing the hosts to invest more heavily in constitutive immunity. Parasites diversify to escape elimination by a specific effector too. However, this diversification does not alter the optimal balance between constitutive and induced defence: the reliance on constitutive defence is promoted by the receptor's inability to detect, but not the effectors' inability to eliminate parasites. If effectors are useless, hosts simply adapt to tolerate, rather than to invest in any defence against parasites. These contrasting results indicate that evolutionary feedback between host and parasite populations is a key factor shaping the selection regime for immune networks facing antagonistic coevolution. Conclusion: Parasite coevolution against specific immune defence alters the prediction of the optimal use of defence, and the effect of parasite coevolution varies between different immune components

Houseflies harbor less diverse microbiota under laboratory conditions but maintain a consistent set of host-associated bacteria

The housefly (Musca domestica) is a wide-ranging insect, often associated with decaying matter from livestock and humans. The septic environments in which houseflies live are believed to be a rich source for microbial acquisition. Although the housefly can harbor a wide range of microorganisms, it is not yet well known which microbes are always recurrent, which are dispensable and which environmentally dependent. In the present study, we aim at identifying which microbes are recurrently associated with the housefly gut throughout the species' life cycle and whether their acquisition relies on the fly's living environment. We surveyed three housefly strains-two of them kept under standard laboratory conditions for a long time and one wild-caught. To track any shifts happening throughout the lifecycle of the housefly and to test the consistency of the revealed microbial communities, we sampled houseflies at five developmental stages over the course of four consecutive generations. Both the bacterial and fungal microbiota of five developmental stages were studied for all samples, using amplicon sequencing for the 16S and ITS1 rRNA gene, respectively. Results revealed diverse microbial communities yet consistent for each of the two distinct sampling environments. The wild-caught population showed a more diverse and more distinct gut microbiota than the two laboratory strains, even though the strain was phylogenetically similar and shared geographic origin with one of them. Two bacterial genera, Myroides and Providencia, and two yeasts, Trichosporon and Candida tropicalis, were present in all sampled larvae and pupae, regardless of the strain. Analysis of the provided diet revealed that the flies acquired the yeasts through feeding. Our main findings show that houseflies might lose microbial diversity when reared in controlled environments, however they can maintain a consistent set of bacteria. We conclude that although the environment can facilitate certain microbial transmission routes for the housefly, and despite the fungal microbiota being largely acquired through diet, the larval bacterial gut microbiome remains relatively consistent within the same developmental stage

Evolution of parasitoid host preference and performance in response to an invasive host acting as evolutionary trap

The invasion of a novel host species can create a mismatch in host choice and offspring survival (performance) when native parasitoids attempt to exploit the invasive host without being able to circumvent its resistance mechanisms. Invasive hosts can therefore act as evolutionary trap reducing parasitoids' fitness and this may eventually lead to their extinction. Yet, escape from the trap can occur when parasitoids evolve behavioral avoidance or a physiological strategy compatible with the trap host, resulting in either host-range expansion or a complete host-shift. We developed an individual based model to investigate which conditions promote parasitoids to evolve behavioral preference that matches their performance, including host-trap avoidance, and which conditions lead to adaptations to the unsuitable hosts. The model was inspired by solitary endo-parasitoids attacking larval host stages. One important aspect of these conditions was reduced host survival during incompatible interaction, where a failed parasitization attempt by a parasitoid resulted not only in death of her offspring but also in host killing. This non-reproductive host mortality had a strong influence on the likelihood of establishment of novel host-parasitoid relationship, in some cases constraining adaptation to the trap host species. Moreover, our model revealed that host-search efficiency and genetic variation in host-preference play a key role in the likelihood that parasitoids will include the suboptimal host in their host range, or will evolve behavioral avoidance resulting in specialization and host-range conservation, respectively. Hence, invasive species might change the evolutionary trajectory of native parasitoid species, which is important for predicting biocontrol ability of native parasitoids towards novel hosts

Regulatory and sequence evolution in response to selection for improved associative learning ability in Nasonia vitripennis

BACKGROUND: Selection acts on the phenotype, yet only the genotype is inherited. While both the phenotypic and genotypic response to short-term selection can be measured, the link between these is a major unsolved problem in evolutionary biology, in particular for complex behavioural phenotypes.RESULTS: Here we characterize the genomic and the transcriptomic basis of associative learning ability in the parasitic wasp Nasonia vitripennis and use gene network analysis to link the two. We artificially selected for improved associative learning ability in four independent pairs of lines and identified signatures of selection across the genome. Allele frequency diverged consistently between the selected and control lines in 118 single nucleotide polymorphisms (SNPs), clustering in 51 distinct genomic regions containing 128 genes. The majority of SNPs were found in regulatory regions, suggesting a potential role for gene expression evolution. We therefore sequenced the transcriptomes of selected and control lines and identified 36 consistently differentially expressed transcripts with large changes in expression. None of the differentially expressed genes also showed sequence divergence as a result of selection. Instead, gene network analysis showed many of the genes with consistent allele frequency differences and all of the differentially expressed genes to cluster in a single co-expression network. At a functional level, both genomic and transcriptomic analyses implicated members of gene networks known to be involved in neural plasticity and cognitive processes.CONCLUSIONS: Taken together, our results reveal how specific cognitive abilities can readily respond to selection via a complex interplay between regulatory and sequence evolution.</p