In agricultural systems, spatially and temporally heterogeneous environments are expected to favour the evolution of generalist pests and pathogens, yet the genomic mechanisms underlying niche‐breadth expansion remain poorly understood. Here, we address this gap by assembling one of the smallest known eukaryotic genomes - from the global cereal pest Aceria tosichella - and by resequencing generalist and specialist populations which evolved in the lab on constant versus fluctuating hosts. A previous study demonstrated that generalist populations retained a wider niche, including the ability to exploit a refuge host, compared to specialist populations that showed a narrowing of the ecological niche. Genomic scans identified 640 SNPs that significantly differed in frequency between treatments, including a single highly differentiated 120-kbp region containing 13 genes. Allele-frequency shifts across many SNPs in this region paralleled phenotypic divergence in the ability to utilise refuge hosts, and gene annotations suggested their roles in starvation resistance and nutrient signalling. However, experimental validation of the top candidate gene did not support its strong direct effect on survival on the refuge host, implying a more complex, likely polygenic basis for adaptation. Consistent with this interpretation, numerous significant SNPs occurred outside the focal region, with enrichment for genes involved in xenobiotic transport, detoxification pathways, and ABC transporters. Together, these results indicate that generalism in A. tosichella relies on complex molecular mechanisms that enable survival on suboptimal or refuge hosts, relying to a considerable extent on the ability to deal with stress arising, for example, from toxic compounds present in suboptimal hosts. ### Competing Interest Statement The authors have declared no competing interest. National Science Centre, https://ror.org/03ha2q922, 2017/27/N/NZ8/00305, 2019/32/T/NZ8/00151, 2021/41/B/NZ8/01703

Animals must decode environmental information to make adaptive decisions. In passive dispersers, for whom only departure timing is under control, the mechanisms of take-off remain poorly understood. Using experimental evolution, we tested how niche breadth modulates passive dispersal in phytophagous mites by exposing specialist and generalist lineages to host-derived kairomones. Dispersal was highly context-dependent. Generalists exhibited higher baseline dispersal and increased take-off when detecting familiar target cues; however, they were inhibited by complex mixtures of unfamiliar cues (low signal-to-noise ratio). Conversely, specialists primarily tracked current host quality, departing significantly more frequently from unfamiliar plants, yet showing little modulation by target cue identity. These results demonstrate that divergent host specialisation in homogeneous versus heterogeneous environments fundamentally alters the way in which organisms integrate information from current and future habitats to drive dispersal. Niche breadth dictates the baseline propensity for informed departure, while olfactory context provides the final trigger for passive take-off.

ABSTRACT In an ever-changing world, organisms are subject to selective pressures that shape their ecological niches. Niche theory predicts that environmental heterogeneity selects for niche expansion, yet niches are inherently multidimensional, and expansion in one dimension may impose severe constrains on others. In this study, we employed rigorous experimental evolution to investigate these cross-dimensional trade-offs in the wheat curl mite, Aceria tosichella . By adapting replicated lineages to either stable (single-host) or alternating (two-host) environments for hundreds of generations, we successfully expanded the mites’ fundamental biotic host niche, enabling lineages to exploit diverse host species, including those unencountered during their evolutionary history. Crucially, however, this biotic generalization incurred a significant cost in the abiotic niche dimension. Lineages adapted to alternating hosts exhibited significantly reduced thermal tolerance compared to host specialists, which maintained superior performance across a wider thermal range. This trade-off appears to be driven by a combination of genetically based metabolic constraints and behavioral dispersal strategies. Our results provide compelling experimental evidence for the “Jack-of-all-trades is master of none” hypothesis across niche dimensions. We demonstrate that physiological trade-offs between biotic versatility and abiotic resilience strictly constrain the evolution of the multidimensional niche, with critical implications for forecasting species’ distributions and invasion potential under climate change.

Animals must acquire and decode information to make the right decisions. While active dispersers can evaluate habitats en route , passive dispersers can only control their departure timing. Although the passive strategy is ubiquitous among arthropods, the mechanisms behind their take-off decisions remain poorly understood. We tested whether host niche breadth shapes passive dispersal in phytophagous mites by exposing them to host-derived kairomones and measuring departure rates. Using experimentally evolved specialist and generalist lineages, we found that dispersal depends more on the context in which cues are encountered that on the kairomones themselves. Host specialisation strongly shaped responses: mites left plants more readily when exposed to unfamiliar hosts, with generalists dispersing over twice as often as specialists. Increased number of unfamiliar kairomones strongly inhibited generalists dispersal but barely affected specialists. This suggests specialists use environmental novelty to trigger exploration, whereas generalists need multiple cues to confirm host suitability, revealing a trade-off between host range and environmental sensitivity. ### Competing Interest Statement The authors have declared no competing interest. National Science Centre, 2019/35/N/NZ8/03377

Species interact in different ways, including competition, facilitation and predation. These interactions can be non-linear or higher order and may depend on time or species densities. Although these higher-order interactions are virtually ubiquitous, they remain poorly understood, as they are challenging both theoretically and empirically. We propose to adapt niche and fitness differences from modern coexistence theory and apply them to species interactions over time. As such, they may not merely inform about coexistence, but provide a deeper understanding of how species interactions change. Here, we investigated how the exploitation of a biotic resource (plant) by phytophagous arthropods affects their interactions. We performed monoculture and competition experiments to fit a generalized additive mixed model to the empirical data, which allowed us to calculate niche and fitness differences. We found that species switch between different types of interactions over time, including intra- and interspecific facilitation, and strong and weak competition.

trajectories.csv (the raw data) id: replicate identifiervariant: co-existence status ("competition" or "monoculture")day: day of experimentspecies: mite species ("CRM" or "WCM")n: population density model.R The R script with the GAMM fitted to the trajectory data; also produces simulations from this model (saved as sim.csv). sim.csv (simulations from the GAMM) day: day of experimentspec_var: combination of co-existence status ("competition" or "monoculture") and species ("CRM" or "WCM")X1:X1000: population densities simulated from the fitted GAMM (on the log scale) reg.RData The GAMM for growth rates. NFD_over_time_monte_carlo_gam.py Python script to compute niche and fitness differences. Takes sim.csv (densities over time for different instantiations) and reg.RData ( stores the GAMM from R for the growth rates) as input and generates the file Data_NFD_monte_carlo_multi_c.csv which stores the niche and fitness differences computed for these communities. figures.R The R script that produces Figures 2-5. plot_biotic_model.py Python code to generate the figures S3 and S4 showing the simulations of a biotic resource competition model. plot_abiotic_model.py Python code to generate the figures S1 and S2 showing simulations of an abiotic resource competition model.

The wood warbler, Phylloscopus sibilatrix (Aves: Passeriformes), is a well-known model organism for studying bird migration, breeding habitat selection and nest predation. The nest acarofauna of this bird species has not been extensively studied so far. To provide a comprehensive report on mite species inhabiting wood warbler nests and to assess infestation parameters (prevalence, intensity, and abundance) for mite species and orders, we collected 45 nests of this bird species in the Wielkopolska National Park in western Poland. Analyses revealed a huge diversity (198 species) of mites inhabiting wood warbler nests. We found individuals belonging to the Mesostigmata, Trombidiformes and Sarcoptiformes. The Trombidiformes, represented in our study only by the Prostigmata, achieved statistically significantly lower intensity and abundance, compared to representatives of other orders. However, the number of recorded prostigmatid species was high (65). The most common were: Stigmaeus sphagneti (22 nests), Stigmaeus longipilis (16), Eupodes voxencollinus (15), Cunaxa setirostris (14), Stigmaeus pilatus (11), and Linopodes sp. 2 (10). The prevalence of Mesostigmata and Sarcoptiformes was equal, reaching 91.1%. Most of Gamasina (Mesostigmata) species found in this study were more characteristic of the soil environment and forest litter than bird nests, but there was also a typical bird parasite, viz. Ornithonyssus sylviarum. None of the observed species of Uropodina (Mesostigmata) or Oribatida (Sarcoptiformes) was typical for bird nests. Among the Uropodina, the highest parameters of nest infestation were achieved by Oodinychus ovalis, whereas among the Oribatida, they were achieved by Metabelba pulverosa. We discuss the importance of wood warbler nests for mite dispersal, survival and reproduction.

Theory generally predicts that host specialisation and dispersal should evolve jointly. Indeed, many models predict that specialists should be poor dispersers to avoid landing on unsuitable hosts while generalists will have high dispersal abilities. Phytophagous arthropods are an excellent group to test this prediction, given extensive variation in their host range and dispersal abilities. Here, we explore the degree to which the empirical literature on this group is in accordance with theoretical predictions. We first briefly outline the theoretical reasons to expect such a correlation. We then report empirical studies that measured both dispersal and the degree of specialisation in phytophagous arthropods. We find a correlation between dispersal and levels of specialisation in some studies, but with wide variation in this result. We then review theoretical attributes of species and environment that may blur this correlation, namely environmental grain, temporal heterogeneity, habitat selection, genetic architecture, and coevolution between plants and herbivores. We argue that theoretical models fail to account for important aspects, such as phenotypic plasticity and the impact of selective forces stemming from other biotic interactions, on both dispersal and specialisation. Next, we review empirical caveats in the study of this interplay. We find that studies use different measures of both dispersal and specialisation, hampering comparisons. Moreover, several studies do not provide independent measures of these two traits. Finally, variation in these traits may occur at scales that are not being considered. We conclude that this correlation is likely not to be expected from large-scale comparative analyses as it is highly context dependent and should not be considered in isolation from the factors that modulate it, such as environmental scale and heterogeneity, intrinsic traits or biotic interactions. A stronger crosstalk between theoretical and empirical studies is needed to understand better the prevalence and basis of the correlation between dispersal and specialisation.

Dispersal is an important process affecting the survival of organisms and the structure and dynamics of communities and ecosystems in space and time. It is a multiphase phenomenon influenced by many internal and external factors. Dispersal syndromes can be complicated, but they are vital to our knowledge of the biology of any organism. We analysed dispersal ability in mites (Acariformes and Parasitiformes), a highly diverse group of wingless arthropods, taking into consideration various modes of dispersal, feeding strategies, body size and the number of articles published for each species. Based on 174 articles summarized for this study, it appears that mites are opportunistic when it comes to dispersal, regardless of their feeding habits, and are often able to adopt several different strategies as needs arise. Moreover, we find a significant positive relationship between the amount of research effort that was put into studying a given species and the number of modes of dispersal that were described. The most salient conclusion to be drawn from this positive correlation is that additional studies are needed, especially on a broader set of mite taxa, until the aforementioned correlation is no longer demonstrably significant.

One of the most phylogenetically enigmatic taxa of Trombidiformes is the supercohort Eupodides (=Eupodina) consists of five superfamilies: Bdelloidea, Eriophyoidea, Eupodoidea, Halacaroidea, and Tydeoidea. However, this taxonomic system has not been supported by formal reconstruction of the phylogeny of these mite groups. In this paper, we present the results of the phylogenetic relationships of major lineages of Eupodides based on 18S rDNA, 28S rDNA, and COI sequences. By critically analysing the key morphological features of the mite taxa indicated by molecular analysis as the main eupodine lineages, we reconstructed a cladogram showing the cladistic hypothesis of the internal phylogenetic structure of Eupodides. Subsequently, the result was compared to the character evolution course suggested by tracing the morphological characters of eupodine mites on the reconstructed molecular tree. According to our data, Eupodides should still be classified as a monophyletic taxon grouping representatives of Bdelloidea, Eupodoidea, Tydeoidea, and Eriophyoidea; however, the taxonomic status of some superfamilies was not confirmed. Particularly, only the bdelloid clade with Cunaxidae nested within Bdellidae may correspond to the superfamily in the current taxonomic view. Additionally, the superfamilies Eupodoidea and Tydeoidea were demonstrated to be paraphyletic. Moreover, morphological, as well as molecular, data recovered Eriophyoidea nested within Tydeoidea.

Understanding pest evolution in agricultural systems is crucial for developing effective and innovative pest control strategies. Types of cultivation, such as crop mono-cultures versus polycultures or crop rotation, may act as a selective pressure on pests' capability to exploit the host's resources. In this study, we examined the herbivorous mite Aceria tosichella (commonly known as wheat curl mite), a widespread wheat pest, to understand how fluctuating versus stable environments influence its niche breadth and ability to utilize different host plant species. We subjected a wheat-bred mite population to replicated experimental evolution in a single-host environment (either wheat or barley), or in an alternation between these two plant species every three mite generations. Next, we tested the fitness of these evolving populations on wheat, barley, and on two other plant species not encountered during experimental evolution, namely rye and smooth brome. Our results revealed that the niche breadth of A. tosichella evolved in response to the level of environmental variability. The fluctuating environment expanded the niche breadth by increasing the mite's ability to utilize different plant species, including novel ones. Such an environment may thus promote flexible host-use generalist phenotypes. However, the niche expansion resulted in some costs expressed as reduced performances on both wheat and barley as compared to specialists. Stable host environments led to specialized phenotypes. The population that evolved in a constant environment consisting of barley increased its fitness on barley without the cost of utilizing wheat. However, the population evolving on wheat did not significantly increase its fitness on wheat, but decreased its performance on barley. Altogether, our results indicated that, depending on the degree of environmental heterogeneity, agricultural systems create different conditions that influence pests' niche breadth evolution, which may in turn affect the ability of pests to persist in such systems.

Dispersal and colonisation determine the survival and success of organisms, and influence the structure and dynamics of communities and ecosystems in space and time. Both affect the gene flow between populations, ensuring sufficient level of genetic variation and improving adaptation abilities. In haplodiploids, such as Aceria tosichella (wheat curl mite, WCM), a population may be founded even by a single unfertilised female, so there is a risk of heterozygosity loss (i.e. founder effect). It may lead to adverse outcomes, such as inbreeding depression. Yet, the strength of the founder effect partly depends on the genetic variation of the parental population. WCM is an economically important pest with a great invasive potential, but its dispersal and colonisation mechanisms were poorly studied before. Therefore, here we assessed WCM dispersal and colonisation potential in relation to the genetic variation of the parental population. We checked whether this potential may be linked to specific pre-dispersal actions (e.g. mating before dispersal and collective behaviour). Our study confirms that dispersal strategies of WCM are not dependent on heterozygosity in the parental population, and the efficient dispersal of this species depends on collective movement of fertilised females.

In seasonal environments, sinks that are more persistent than sources may serve as temporal stepping stones for specialists. However, this possibility has to our knowledge, not been demonstrated to date, as such environments are thought to select for generalists, and the role of sinks, both in the field and in the laboratory, is difficult to document. Here, we used laboratory experiments to show that herbivorous arthropods associated with seasonally absent main (source) habitats can endure on a suboptimal (sink) host for several generations, albeit with a negative growth rate. Additionally, they dispersed towards this host less often than towards the main host and accepted it less often than the main host. Finally, repeated experimental evolution attempts revealed no adaptation to the suboptimal host. Nevertheless, field observations showed that arthropods are found in suboptimal habitats when the main habitat is unavailable. Together, these results show that evolutionary rescue in the suboptimal habitat is not possible. Instead, the sink habitat functions as a temporal stepping stone, allowing for the persistence of a specialist when the source habitat is gone.

Quantifying basic biological data, such as the effects of variable temperatures on development and survival, is crucial to predicting and monitoring population growth rates of pest species, many of which are highly invasive. One of the most globally important pests of cereals is the eriophyoid wheat curl mite (WCM), Aceria tosichella, which is the primary vector of several plant viruses. The aim of this study was to evaluate temperature-dependent development and survival of WCM at a wide range of constant temperatures in the laboratory (17–33 °C). The development time of each stage depended significantly on temperature and it was negatively correlated with temperature increase. At high temperatures (27–33 °C), individuals had shorter developmental times, with the shortest (6 days) at 33 °C, whereas at the lowest tested temperatures (17–19 °C), developmental time was almost 3× longer. Moreover, temperature had a clear effect on survival: the higher the temperature, the lower the survival rate. These data provide information promoting more efficient and effective manipulation of WCM laboratory colonies, and further our understanding of the ramifications of temperature change on WCM physiology and implications for the growth and spread of this globally invasive pest.

1. Colonisation, i.e. the establishment of dispersed individuals in an unoccupied area, is a fundamental biological process that drives the distribution and range dynamics of organisms. It is crucial to understand the basic mechanisms of colonisation, especially in invasive species. 2. In this study, we investigated the importance of dispersal success (the proportion of settlers and founders) and intrinsic population growth rate for colonisation ability in phytophagous mites that spread both passively and actively. We performed laboratory experiments using two eriophyid mite species: Aceria tosichella [wheat curl mite (WCM)] and Abacarus hystrix [cereal rust mite (CRM)]. These are obligate herbivores of economic importance because they feed on cereal plants, including wheat. 3. To test the colonisation ability of WCMand CRM on wheat when dispersed actively by walking and passively when blown by air currents, we estimated the number of individuals that established new populations after dispersal and calculated the intrinsic population growth rate (r) for both species. 4. WCM had a higher colonisation ability on wheat than CRM. This resulted from the higher dispersal success of WCM; however, the two species did not differ in r. This pattern was consistent for both dispersal modes. Moreover, both species had higher colonisation success when dispersing actively, albeit with a very limited spatial range. 5. These results underline the role of successful dispersal in the colonisation ability of species. The knowledge of the colonisation process of WCM and CRM is important for understanding their invasiveness and for predicting their potential geographical distributions.

Dispersal shapes the dynamics of populations, their genetic structure and species distribution; therefore, knowledge of an organisms' dispersal abilities is crucial, especially in economically important and invasive species. In this study, we investigated dispersal strategies of two phytophagous eriophyoid mite species: Aceria tosichella (wheat curl mite, WCM) and Abacarus hystrix (cereal rust mite, CRM). Both species are obligatory plant parasites that infest cereals and are of economic significance. We investigated their dispersal success using different dispersal agents: wind and vectors. We hypothesised that in both mite species the main mode of dispersal is moving via wind, whereas phoretic dispersal is rather accidental, as the majority of eriophyoid mite species do not possess clear morphological or behavioural adaptations for phoresy. Results confirmed our predictions that both species dispersed mainly with wind currents. Additionally, WCM was found to have a higher dispersal success than CRM. Thus, this study contributes to our understanding of the high invasive potential of WCM.

Dispersal is a fundamental biological process that operates at different temporal and spatial scales with consequences for individual fitness, population dynamics, population genetics, and species distributions. Studying this process is particularly challenging when the focus is on microscopic organisms that disperse passively, whilst controlling neither the transience nor the settlement phase of their movement. In this work we propose a comprehensive approach for studying passive dispersal of microscopic invertebrates and demonstrate it using wind and phoretic vectors. The protocol includes the construction of versatile, modifiable dispersal tunnels as well as a theoretical framework quantifying the movement of species via wind or vectors, and a hierarchical Bayesian approach appropriate to the structure of the dispersal data. The tunnels were used to investigate the three stages of dispersal (viz., departure, transience, and settlement) of two species of minute, phytophagous eriophyid mitesAceria tosichellaandAbacarus hystrix. The proposed devices are inexpensive and easy to construct from readily sourced materials. Possible modifications enable studies of a wide range of mite species and facilitate manipulation of dispersal factors, thus opening a new important area of ecological study for many heretofore understudied species.

Phytophagous mites belonging to the Eriophyoidea are extremely diverse and highly host-specific. Their accurate morphological identification is hampered by their reduced size and simplified bodies and by the existence of cryptic species complexes. Previous studies have demonstrated the urgency of applying multisource methods to accurate taxonomic identification of eriophyoid mites, especially species belonging to the genus Abacarus. This genus comprises 65 species, of which 37 are associated with grasses and four with sugarcane Saccharum (Poaceae). Recently, Abacarus specimens very similar to Abacarus sacchari were collected from the sugarcane crop in Brazil; however, their taxonomic placement was uncertain. In this study, we used an integrative approach to determine whether A. aff. sacchari specimens belong to A. sacchari or constitute a cryptic species. Morphological data were combined with molecular phylogeny based on the nucleotide sequences of three markers, one mitochondrial (COI) and two nuclear (D2 region of 28S and ITS). Morphological differences were observed between A. aff. sacchari, A. sacchari and A. doctus. The phylogenetic relationships among these three taxa and the genetic distances separating them revealed an interspecific divergence. The results of the morphological and molecular methods were congruent and supported the existence of a new species: Abacarus neosacchari n. sp. Duarte and Navia, herein described. This species belongs to the Abacarus cryptic species complex associated with sugarcane in the Americas. The results of this study, presenting the occurrence of multiple Abacarus species associated with sugarcane, contribute to the knowledge on plants and mites diversity by adding up one more clue highlighting that plant hybridization can be an important mechanism contributing to the speciation of plant-feeding arthropods.