High-throughput behavioral phenotyping of tiny arthropods: Chemosensory traits in a mesostigmatic hematophagous mite.

Pest management using attractive and/or repellent semiochemicals is a key alternative to synthetic insecticides. Its implementation requires a good understanding of the intra- and interspecific chemical interactions of arthropod pests, their interactions with their abiotic environment, as well as their evolutionary dynamics. Although mites include many pest species and biocontrol agents of economic importance in agriculture, their chemical ecology is largely understudied compared to insects. We developed a high-throughput ethomics system to analyze these small arthropods and conducted a study on Dermanyssus gallinae, a problematic poultry parasite in the egg industry. Our purpose was to elucidate the role played by host-derived odorants (synthetic kairomone) and conspecific odorants (mite body odors) in D. gallinae. After validating our nanocomputer controlled olfactometric system with volatile semiochemicals of known biological activity, we characterized response traits to kairomonal and/or pheromonal volatile blends in mites from different populations. We were able to accurately characterize the repulsion or attraction behaviors in >1000 individual specimens in a standardized way. Our results confirm the presence of a volatile aggregation pheromone emitted by D. gallinae and bring new elements to the effect of odor source presentation. Our results also confirm the attractive effect on Dermanyssus gallinae of a blend of volatile compounds contained in hen odor, while highlighting a repellent effect at high concentration. Significant interindividual and interpopulation variation was noted particularly in responses to synthetic kairomone. This information lays a valuable foundation for further exploring the emergence risk of resistance to semiochemicals.

Dispersal syndromes in challenging environments: A cross-species experiment.

Dispersal is a central biological process tightly integrated into life-histories, morphology, physiology and behaviour. Such associations, or syndromes, are anticipated to impact the eco-evolutionary dynamics of spatially structured populations, and cascade into ecosystem processes. As for dispersal on its own, these syndromes are likely neither fixed nor random, but conditional on the experienced environment. We experimentally studied how dispersal propensity varies with individuals' phenotype and local environmental harshness using 15 species ranging from protists to vertebrates. We reveal a general phenotypic dispersal syndrome across studied species, with dispersers being larger, more active and having a marked locomotion-oriented morphology and a strengthening of the link between dispersal and some phenotypic traits with environmental harshness. Our proof-of-concept metacommunity model further reveals cascading effects of context-dependent syndromes on the local and regional organisation of functional diversity. Our study opens new avenues to advance our understanding of the functioning of spatially structured populations, communities and ecosystems.

Genetically diverse populations spread faster in benign but not in challenging environments.

Population spread from a limited pool of founding propagules is at the basis of biological invasions. The size and genetic variation of these propagules eventually affect whether the invasion is successful or not. The inevitable bottleneck at introduction decreases genetic diversity, and therefore should affect population growth and spread. However, many heavily bottlenecked invasive populations have been successful in nature. Negative effects of a genetic bottleneck are typically considered to be relaxed in benign environments because of a release from stress. Despite its relevance to understand and predict invasions, empirical evidence on the role of genetic diversity in relation to habitat quality is largely lacking. We use the mite Tetranychus urticae Koch as a model to experimentally assess spread rate and size of genetically depleted inbred populations vs. enriched mixed populations. This was assessed in replicated linear patch systems consisting of benign (bean), challenging (tomato), or a gradient (bean to tomato) habitat. As expected, we found no effect of genetic diversity on population size in benign habitat but found that it increased population size in challenging habitat. However, we found that population spread rates were increased due to genetic diversity in the benign but not in the challenging habitat. Additionally, variance in spread was consistently higher in genetically poor populations and highest in the challenging habitat. Our experiment challenges the general view that a bottleneck in genetic variation decreases invasion success in challenging but not benign environments.

Spatial connectedness imposes local- and metapopulation-level selection on life history through feedbacks on demography.

Dispersal evolution impacts the fluxes of individuals and hence, connectivity in metapopulations. Connectivity is therefore decoupled from the structural connectedness of the patches within the spatial network. Because of demographic feedbacks, local selection also drives the evolution of other life history traits. We investigated how different levels of connectedness affect trait evolution in experimental metapopulations of the two-spotted spider mite. We separated local- and metapopulation-level selection and linked trait divergence to population dynamics. With lower connectedness, an increased starvation resistance and delayed dispersal evolved. Reproductive performance evolved locally by transgenerational plasticity or epigenetic processes. Costs of dispersal, but also changes in local densities and temporal fluctuations herein are found to be putative drivers. In addition to dispersal, demographic traits are able to evolve in response to metapopulation connectedness at both the local and metapopulation level by genetic and/or non-genetic inheritance. These trait changes impact the persistence of spatially structured populations.

The distinct phenotypic signatures of dispersal and stress in an arthropod model: from physiology to life history.

Dispersing individuals are expected to encounter costs during transfer and in the novel environment, and may also have experienced stress in their natal patch. Given this, a non-random subset of the population should engage in dispersal and show divergent stress-related responses. This includes physiological shifts as expressed in the metabolome, which form a major part of responses to stress. We analyzed how metabolic profiles and life-history traits varied between dispersers and residents of the model two-spotted spider mite Tetranychus urticae, and whether and how these syndromes varied with exposure to a stressful new host plant (tomato). Regardless of the effect of host plant, we found a physiological dispersal syndrome where, relative to residents, dispersers were characterized by lower leaf consumption and a lower concentration of several amino acids, indicating a potential dispersal-foraging trade-off. As a possible consequence of this lower food intake, dispersers also laid smaller eggs. Responses to tomato were consistent with this plant being a stressor for T.urticae, including reduced fecundity and reduced feeding. Tomato-exposed mites laid larger eggs, which we interpret as a plastic response to food stress, increasing survival to maturity. Contrary to what was expected from the costs of dispersal and from previous meta-population level studies, there was no interaction between dispersal status and host plant for any of the examined traits, meaning stress impacts were equally incurred by residents and dispersers. We thus provide novel insights into the processes shaping dispersal and the feedbacks on ecological dynamics in spatially structured populations.

Eco-evolutionary feedbacks following changes in spatial connectedness.

Humans are drastically changing the spatial configuration of habitats. The associated changes in habitat connectedness impose strong selection on dispersal, and dispersal related traits. Evolutionary responses do, however, strongly feedback on the metapopulation dynamics, by further constraining or improving connectivity and impacting local population and food web dynamics. Because these spatial eco-evolutionary interactions occur at contemporary time scales, unique evidence on its importance is especially emerging in the field of entomology as many insects have short generation times and a huge reproductive potential. We review the ecological feedbacks originating from the evolution of dispersal rate, dispersal syndromes and genetic diversity on metapopulation dynamics and range expansions. We thus close the eco-evolutionary loop for insect and arachnid spatial dynamics.

Bottom-up and top-down control of dispersal across major organismal groups.

Ecology and evolution unfold in spatially structured communities, where dispersal links dynamics across scales. Because dispersal is multicausal, identifying general drivers remains challenging. In a coordinated distributed experiment spanning organisms from protozoa to vertebrates, we tested whether two fundamental determinants of local dynamics, top-down and bottom-up control, generally explain active dispersal. We show that both factors consistently increased emigration rates and use metacommunity modelling to highlight consequences on local and regional dynamics.