Coinfection accelerates transmission to new hosts despite no effects on virulence and parasite growth.

One of the fundamental aims of ecological, epidemiological and evolutionary studies of host-parasite interactions is to unravel which factors affect parasite virulence. Theory predicts that virulence and transmission are correlated by a trade-off, as too much virulence is expected to hamper transmission owing to excessive host damage. Coinfections may affect each of these traits and/or their correlation. Here, we used inbred lines of the spider mite Tetranychus urticae to test how coinfection with T. evansi impacted virulence-transmission relationships at different conspecific densities. The presence of T. evansi on a shared host did not change the relationship between virulence (leaf damage) and the number of transmitting stages (i.e. adult daughters). The relationship between these traits was hump-shaped across densities, both in single and coinfections, which corresponds to a trade-off. Moreover, transmission to adjacent hosts increased in coinfection, but only at low T. urticae densities. Finally, we tested whether virulence and the number of daughters were correlated with measures of transmission to adjacent hosts, in single and coinfections at different conspecific densities. Traits were mostly independent, meaning that interspecific competitors may increase transmission without affecting virulence. Thus, coinfections may impact epidemiology and parasite trait evolution, but not necessarily the virulence-transmission trade-off.This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

Limits to the adaptation of herbivorous spider mites to metal accumulation in homogeneous and heterogeneous environments.

Metal accumulation is used by some plants as a defence against herbivores. Yet, herbivores may adapt to these defences, becoming less susceptible. Moreover, ecosystems often contain plants that do and do not accumulate metals, but whether such heterogeneity affects herbivore adaptation remains understudied. Here, we performed experimental evolution to test whether the spider mite Tetranychus evansi adapts to plants with high cadmium concentrations, in homogeneous (plants with cadmium) or heterogeneous (plants with or without cadmium) environments. For that we used tomato plants, which accumulate cadmium, thus affecting the performance of these spider mites. We measured mite fecundity, hatching rate, and the number of adult offspring after 12 and 33 generations and habitat choice after 14 and 51 generations, detecting no trait change, which implies the absence of adaptation. We then tested whether this was due to a lack of genetic variation in the traits measured and, indeed, additive genetic variance was low. Interestingly, despite no signs of adaptation, we observed a decrease in fecundity and number of adult offspring produced on cadmium-free plants, in the populations evolving in environments with cadmium. Therefore, evolving in environments with cadmium reduces the growth rate of spider mite populations on non-accumulating plants. Possibly, other traits contributed to population persistence on plants with cadmium. This calls for more studies addressing herbivore adaptation to plant metal accumulation.

Limited host availability disrupts the genetic correlation between virulence and transmission.

Virulence is expected to be linked to parasite fitness via transmission. However, it is not clear whether this relationship is genetically determined, nor if it differs when transmission occurs continuously during, or only at the end of, the infection period. Here, we used inbred lines of the macroparasitic spider mite Tetranychus urticae to disentangle genetic vs. nongenetic correlations among traits, while varying parasite density and opportunities for transmission. A positive genetic correlation between virulence and the number of transmitting stages produced was found under continuous transmission. However, if transmission occurred only at the end of the infection period, this genetic correlation disappeared. Instead, we observed a negative relationship between virulence and the number of transmitting stages, driven by density dependence. Thus, within-host density dependence caused by reduced opportunities for transmission may hamper selection for higher virulence, providing a novel explanation as to why limited host availability leads to lower virulence.

Concurrent herbivory and metal accumulation: The outcome for plants and herbivores.

The effects of metals on plants and herbivores, as well as the interaction among the latter, are well documented. However, the effects of simultaneous herbivory and metal accumulation remain poorly studied. Here, we shed light on this topic by infesting cadmium-accumulating tomato plants (Solanum lycopersicum), either exposed to cadmium or not, with herbivorous spider mites, Tetranychus urticae or T. evansi during 14 days. Whereas on plants without cadmium T. evansi had higher growth rate than T. urticae, on plants with cadmium both mite species had similar growth rates, which were lower than on plants without metal. Plants were affected by both cadmium toxicity and by herbivory, as shown by leaf reflectance, but not on the same wavelengths. Moreover, changes in leaf reflectance on the wavelength affected by herbivores were similar on plants with and without cadmium, and vice versa. Long-term effects of cadmium and herbivory did not affect H2O2 concentrations in the plant. Finally, plants infested with spider mites did not accumulate more cadmium, suggesting that metal accumulation is not induced by herbivory. We thus conclude that cadmium accumulation affects two congeneric herbivore species differently and that the effects of herbivory and cadmium toxicity on plants may be disentangled, via leaf reflectance, even during simultaneous exposure.

The distribution of herbivores between leaves matches their performance only in the absence of competitors.

Few studies have tested how plant quality and the presence of competitors interact in determining how herbivores choose between different leaves within a plant. We investigated this in two herbivorous spider mites sharing tomato plants: Tetranychus urticae, which generally induces plant defenses, and Tetranychus evansi, which suppresses them, creating asymmetrical effects on coinfesting competitors. On uninfested plants, both herbivore species preferred young leaves, coinciding with increased mite performance. On plants with heterospecifics, the mites did not prefer leaves on which they had a better performance. In particular, T. urticae avoided leaves infested with T. evansi, which is in agreement with T. urticae being outcompeted by T. evansi. In contrast, T. evansi did not avoid leaves with the other species, but distributed itself evenly over plants infested with heterospecifics. We hypothesize that this behavior of T. evansi may prevent further spread of T. urticae over the shared plant. Our results indicate that leaf age determines within-plant distribution of herbivores only in absence of competitors. Moreover, they show that this distribution depends on the order of arrival of competitors and on their effects on each other, with herbivores showing differences in behavior within the plant as a possible response to the outcome of those interactions.

Creating outbred and inbred populations in haplodiploids to measure adaptive responses in the laboratory.

Laboratory studies are often criticized for not being representative of processes occurring in natural populations. One reason for this is the fact that laboratory populations generally do not capture enough of the genetic variation of natural populations. This can be mitigated by mixing the genetic background of several field populations when creating laboratory populations. From these outbred populations, it is possible to generate inbred lines, thereby freezing and partitioning part of their variability, allowing each genotype to be characterized independently. Many studies addressing adaptation of organisms to their environment, such as those involving quantitative genetics or experimental evolution, rely on inbred or outbred populations, but the methodology underlying the generation of such biological resources is usually not explicitly documented. Here, we developed different procedures to circumvent common pitfalls of laboratory studies, and illustrate their application using two haplodiploid species, the spider mites Tetranychus urticae and Tetranychus evansi. First, we present a method that increases the chance of capturing high amounts of variability when creating outbred populations, by performing controlled crosses between individuals from different field-collected populations. Second, we depict the creation of inbred lines derived from such outbred populations, by performing several generations of sib-mating. Third, we outline an experimental evolution protocol that allows the maintenance of a constant population size at the beginning of each generation, thereby preventing bottlenecks and diminishing extinction risks. Finally, we discuss the advantages of these procedures and emphasize that sharing such biological resources and combining them with available genetic tools will allow consistent and comparable studies that greatly contribute to our understanding of ecological and evolutionary processes.

Rapid host-plant adaptation in the herbivorous spider mite Tetranychus urticae occurs at low cost.

The herbivorous spider mite Tetranychus urticae is a generalist world crop pest. Early evidence for host races, its fully sequenced genome resolved to the chromosome level, and the development of other molecular tools in this species suggest that this arthropod can be a good model to address host plant adaptation and early stages of speciation. Here, we evaluate this possibility by reviewing recent studies of host-plant adaptation in T. urticae. We find that evidence for costs of adaptation are relatively scarce and that studies involving molecular-genetics and genomics are mostly disconnected from those with phenotypic tests. Still, with the ongoing development of genetic and genomic tools for this species, T. urticae is becoming an attractive model to understand the molecular basis of host-plant adaptation.

Wolbachia both aids and hampers the performance of spider mites on different host plants.

In the last few decades, many studies have revealed the potential role of arthropod bacterial endosymbionts in shaping the host range of generalist herbivores and their performance on different host plants, which, in turn, might affect endosymbiont distribution in herbivore populations. We tested this by measuring the prevalence of endosymbionts in natural populations of the generalist spider mite Tetranychus urticae on different host plants. Focusing on Wolbachia, we then analysed how symbionts affected mite life-history traits on the same host plants in the laboratory. Overall, the prevalences of Cardinium and Rickettsia were low, whereas that of Wolbachia was high, with the highest values on bean and eggplant and the lowest on morning glory, tomato and zuchini. Although most mite life-history traits were affected by the plant species only, Wolbachia infection was detrimental for the egg-hatching rate on morning glory and zucchini, and led to a more female-biased sex ratio on morning glory and eggplant. These results suggest that endosymbionts may affect the host range of polyphagous herbivores, both by aiding and hampering their performance, depending on the host plant and on the life-history trait that affects performance the most. Conversely, endosymbiont spread may be facilitated or hindered by the plants on which infected herbivores occur.

Suppression of Plant Defenses by Herbivorous Mites Is Not Associated with Adaptation to Host Plants.

Some herbivores suppress plant defenses, which may be viewed as a result of the coevolutionary arms race between plants and herbivores. However, this ability is usually studied in a one-herbivore-one-plant system, which hampers comparative studies that could corroborate this hypothesis. Here, we extend this paradigm and ask whether the herbivorous spider-mite Tetranychus evansi, which suppresses the jasmonic-acid pathway in tomato plants, is also able to suppress defenses in other host plants at different phylogenetic distances from tomatoes. We test this using different plants from the Solanales order, namely tomato, jimsonweed, tobacco, and morning glory (three Solanaceae and one Convolvulaceae), and bean plants (Fabales). First, we compare the performance of T. evansi to that of the other two most-commonly found species of the same genus, T. urticae and T. ludeni, on several plants. We found that the performance of T. evansi is higher than that of the other species only on tomato plants. We then showed, by measuring trypsin inhibitor activity and life history traits of conspecific mites on either clean or pre-infested plants, that T. evansi can suppress plant defenses on all plants except tobacco. This study suggests that the suppression of plant defenses may occur on host plants other than those to which herbivores are adapted.

Down-regulation of plant defence in a resident spider mite species and its effect upon con- and heterospecifics.

Herbivorous spider mites occurring on tomato plants (Solanum lycopersicum L.) cope with plant defences in various manners: the invasive Tetranychus evansi reduces defences below constitutive levels, whereas several strains of T. urticae induce such defences and others suppress them. In the Mediterranean region, these two species co-occur on tomato plants with T. ludeni, another closely related spider mite species. Unravelling how this third mite species affects plant defences is thus fundamental to understanding the outcome of herbivore interactions in this system. To test the effect of T. ludeni on tomato plant defences, we measured (1) the activity of proteinase inhibitors, indicating the induction of plant defences, in those plants, and (2) mite performance on plants previously infested with each mite species. We show that the performance of T. evansi and T. ludeni on plants previously infested with T. ludeni or T. evansi was better than on clean plants, indicating that these two mite species down-regulate plant defences. We also show that plants attacked by these mite species had lower activity of proteinase inhibitors than clean plants, whereas herbivory by T. urticae increased the activity of these proteins and resulted in reduced spider mite performance. This study thus shows that the property of down-regulation of plant defences below constitutive levels also occurs in T. ludeni.