Effective specialist or jack of all trades? Experimental evolution of a crop pest in fluctuating and stable environments.

Understanding pest evolution in agricultural systems is crucial for developing effective and innovative pest control strategies. Types of cultivation, such as crop monocultures 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.

Mechanisms of dispersal and colonisation in a wind-borne cereal pest, the haplodiploid wheat curl mite.

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.

A sink host allows a specialist herbivore to persist in a seasonal source.

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.

Temperature-dependent development and survival of an invasive genotype of wheat curl mite, Aceria tosichella.

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.

A comprehensive and cost-effective approach for investigating passive dispersal in minute invertebrates with case studies of phytophagous eriophyid mites.

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 mites Aceria tosichella and Abacarus 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.

A novel experimental approach for studying life-history traits of phytophagous arthropods utilizing an artificial culture medium.

Experimental approaches to studying life-history traits in minute herbivorous arthropods are hampered by the need to work with detached host plant material and the difficulty of maintaining that material in a suitable condition to support the animal throughout the duration of the test. In order to address this shortcoming, we developed a customizable agar-based medium modified from an established plant cell-culture medium to nourish detached leaves laid atop it while also preventing arthropods from escaping the experimental arena. The artificial culture medium was tested with two herbivorous mite species: the wheat curl mite (Aceria tosichella; Eriophyidae) and two-spotted spider mite (Tetranychus urticae; Tetranychidae). The proposed approach was a major improvement over a standard protocol for prolonged studies of individual eriophyid mites and also provided some benefits for experiments with spider mites. Moreover, the described method can be easily modified according to the requirements of host plant species and applied to a wide range of microherbivore species. Such applications include investigations of life-history traits and other ecological and evolutionary questions, e.g. mating or competitive behaviours or interspecific interactions, assessing invasiveness potential and predicting possible outbreaks. The approach presented here should have a significant impact on the advancement of evolutionary and ecological research on microscopic herbivores.

Cryptic diversity within grass-associated Abacarus species complex (Acariformes: Eriophyidae), with the description of a new species, Abacarus plumiger n. sp.

Accurate estimation of species richness is often complex as genetic divergence is not always accompanied by appreciable morphological differentiation. In consequence, cryptic lineages or species evolve. Cryptic speciation is common especially in taxa characterized by small and simplified bodies, what makes their proper identification challenging. The cereal rust mite, Abacarus hystrix, was regarded for a long time as a species associated with a wide range of grass hosts, whereas wide host ranges are rather rare in eriophyoid mites. Therefore, the generalist status of A. hystrix was questioned. In this paper we demonstrate that the diversity within Abacarus species associated with grasses is more complex than it was previously thought. The 78 Abacarus mtDNA COI sequences used in this study formed 10 highly supported clades (bootstrap value 99%) and four more distinct genetic lineages were represented by unique sequences. The genetic distances between them ranged from 6.6 to 26.5%. Moreover, morphological study and genetic approach based on the combination of the Poisson Tree Processes model for species delimitation (PTP) and a Bayesian implementation of PTP (bPTP), and Neighbour Joining analyses led to delimitation of a new species within the Abacarus complex: Abacarus plumiger, specialized on smooth brome (Bromus inermis). Furthermore, our analyses demonstrated a pattern of host-associated differentiation within the complex. Overall, our study indicates that cryptic speciation occurs in the grass-associated Abacarus genus, and suggests the need for more extensive sampling using integrative methods.