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- Wolbachia and host intrinsic reproductive barriers contribute additively to postmating isolation in spider mitesPublication . Cruz, Miguel; Magalhaes, S; Sucena, Élio; Zélé, FloreWolbachia are maternally-inherited bacteria that induce cytoplasmic incompatibility in many arthropod species. However, the ubiquity of this isolation mechanism for host speciation processes remains elusive, as only few studies have examined Wolbachia-induced incompatibilities when host populations are not genetically compatible. Here, we used three populations of two genetically differentiated colour forms of the haplodiploid spider mite Tetranychus urticae to dissect the interaction between Wolbachia-induced and host-associated incompatibilities, and their relative contribution to postmating isolation. We found that these two sources of incompatibility act through different mechanisms in an additive fashion. Host-associated incompatibility contributes 1.5 times more than Wolbachia-induced incompatibility in reducing hybrid production, the former through an overproduction of haploid sons at the expense of diploid daughters (ca. 75% decrease) and the latter by increasing the embryonic mortality of daughters (by ca. 49%). Furthermore, regardless of cross direction, we observed near-complete F1 hybrid sterility and complete F2 hybrid breakdown between populations of the two forms, but Wolbachia did not contribute to this outcome. We thus show mechanistic independence and an additive nature of host-intrinsic and Wolbachia-induced sources of isolation. Wolbachia may contribute to reproductive isolation in this system, thereby potentially affecting host differentiation and distribution in the field.
- Specific sequence of arrival promotes coexistence via spatial niche pre‐emption by the weak competitorPublication . De mendonça fragata almeida, Inês; Costa‐Pereira, Raul; Kozak, Mariya; Majer, Agnieszka; Godoy, Oscar; Magalhães, saraHistorical contingency, such as the order of species arrival, can modify competitive outcomes via niche modification or pre-emption. However, how these mechanisms ultimately modify stabilising niche and average fitness differences remains largely unknown. By experimentally assembling two congeneric spider mite species feeding on tomato plants during two generations, we show that order of arrival affects species’ competitive ability and changes the outcome of competition. Contrary to expectations, order of arrival did not cause positive frequency dependent priority effects. Instead, coexistence was predicted when the inferior competitor (Tetranychus urticae) arrived first. In that case, T. urticae colonised the preferred feeding stratum (leaves) of T. evansi leading to spatial niche pre-emption, which equalised fitness and reduced niche differences, driving community assembly to a close-to-neutrality scenario. Our study demonstrates how the order of species arrival and the spatial context of competitive interactions may jointly determine whether species can coexist.
- Consequences of population structure for sex allocation and sexual conflictPublication . Rodrigues, Leonor R; Torralba Sáez, Mario; Alpedrinha, João; Lefèvre, Sophie; Brengues, Muriel; Magalhães, Sara; Duncan, Alison B.Both sex allocation and sexual conflict can be modulated by spatial structure. However, how the interplay between the type of dispersal and the scale of competition simultaneously affects these traits in sub-divided populations is rarely considered. We investigated sex allocation and sexual conflict evolution in meta-populations of the spider mite Tetranychus urticae evolving under budding (pairing females from the same patch) or random (pairing females from different patches) dispersal and either local (fixed sampling from each subpopulation) or global (sampling as a function of subpopulation productivity) competition. Females evolving under budding dispersal produced less female-biased offspring sex ratios than those from the random dispersal selection regimes, contradicting theoretical predictions. In contrast, the scale of competition did not strongly affect sex allocation. Offspring sex ratio and female fecundity were unaffected by the number of mates, but female fecundity was highest when their mates evolved under budding dispersal, suggesting these males inflict less harm than those evolving under random dispersal. This work highlights that population structure can impact the evolution of sex allocation and sexual conflict. Moreover, selection on either trait may reciprocally affect the evolution of the other, for example via effects on fecundity.
- Population‐specific effect of Wolbachia on the cost of fungal infection in spider mitesPublication . Zélé, Flore; Altıntaş, Mustafa; Santos, Inês; Cakmak, Ibrahim; Magalhães, SMany studies have revealed the ability of the endosymbiotic bacterium Wolbachia to protect its arthropod hosts against diverse pathogens. However, as Wolbachia may also increase the susceptibility of its host to infection, predicting the outcome of a particular Wolbachia-host-pathogen interaction remains elusive. Yet, understanding such interactions and their eco-evolutionary consequences is crucial for disease and pest control strategies. Moreover, how natural Wolbachia infections affect artificially introduced pathogens for biocontrol has never been studied. Tetranychus urticae spider mites are herbivorous crop pests, causing severe damage on numerous economically important crops. Due to the rapid evolution of pesticide resistance, biological control strategies using entomopathogenic fungi are being developed. However, although spider mites are infected with various Wolbachia strains worldwide, whether this endosymbiont protects them from fungi is as yet unknown. Here, we compared the survival of two populations, treated with antibiotics or naturally harboring different Wolbachia strains, after exposure to the fungal biocontrol agents Metarhizium brunneum and Beauveria bassiana. To control for potential effects of the bacterial community of spider mites, we also compared the susceptibility of two populations naturally uninfected by Wolbachia, treated with antibiotics or not. In one population, Wolbachia-infected mites had a better survival than uninfected ones in absence of fungi but not in their presence, whereas in the other population Wolbachia increased the mortality induced by B. bassiana. In one naturally Wolbachia-uninfected population, the antibiotic treatment increased the susceptibility of spider mites to M. brunneum, but it had no effect in the other treatments. These results suggest that natural Wolbachia infections may not hamper and may even improve the success of biological control using entomopathogenic fungi. However, they also draw caution on the generalization of such effects, given the complexity of within-host-pathogens interaction and the potential eco-evolutionary consequences of the use of biocontrol agents for Wolbachia-host associations.
- Wolbachia and host intrinsic reproductive barriers contribute additively to postmating isolation in spider mitesPublication . Cruz, Miguel; Magalhães, sara; Sucena, Élio; Zélé, FloreWolbachia are maternally-inherited bacteria that induce cytoplasmic incompatibility in many arthropod species. However, the ubiquity of this isolation mechanism for host speciation processes remains elusive, as only few studies have examined Wolbachia-induced incompatibilities when host populations are not genetically compatible. Here, we used three populations of two genetically differentiated colour forms of the haplodiploid spider mite Tetranychus urticae to dissect the interaction between Wolbachia-induced and host-associated incompatibilities, and their relative contribution to postmating isolation. We found that these two sources of incompatibility act through different mechanisms in an additive fashion. Host-associated incompatibility contributes 1.5 times more than Wolbachia-induced incompatibility in reducing hybrid production, the former through an overproduction of haploid sons at the expense of diploid daughters (ca. 75% decrease) and the latter by increasing the embryonic mortality of daughters (by ca. 49%). Furthermore, regardless of cross direction, we observed near-complete F1 hybrid sterility and complete F2 hybrid breakdown between populations of the two forms, but Wolbachia did not contribute to this outcome. We thus show mechanistic independence and an additive nature of host-intrinsic and Wolbachia-induced sources of isolation. Wolbachia may contribute to reproductive isolation in this system, thereby potentially affecting host differentiation and distribution in the field.
- Next‐generation biological control: the need for integrating genetics and genomicsPublication . Leung, Kelley; Ras, Erica; Ferguson, Kim B.; Ariëns, Simone; Babendreier, Dirk; Bijma, Piter; Bourtzis, Kostas; Brodeur, Jacques; Bruins, Margreet A.; Centurión, Alejandra; Chattington, Sophie R.; Chinchilla‐Ramírez, Milena; Dicke, Marcel; Fatouros, Nina E.; González‐Cabrera, Joel; Groot, Thomas V. M.; Haye, Tim; Knapp, Markus; Koskinioti, Panagiota; Le Hesran, Sophie; Lyrakis, Manolis; Paspati, Angeliki; Pérez‐Hedo, Meritxell; Plouvier, Wouter N.; Schlötterer, Christian; Stahl, Judith M.; Thiel, Andra; Urbaneja, Alberto; Zande, Louis; Verhulst, Eveline C.; Vet, Louise E. M.; Visser, Sander; Werren, John H.; Xia, Shuwen; Zwaan, Bas J.; Magalhaes, S; Beukeboom, Leo W.; Pannebakker, Bart A.Biological control is widely successful at controlling pests, but effective biocontrol agents are now more difficult to import from countries of origin due to more restrictive international trade laws (the Nagoya Protocol). Coupled with increasing demand, the efficacy of existing and new biocontrol agents needs to be improved with genetic and genomic approaches. Although they have been underutilised in the past, application of genetic and genomic techniques is becoming more feasible from both technological and economic perspectives. We review current methods and provide a framework for using them. First, it is necessary to identify which biocontrol trait to select and in what direction. Next, the genes or markers linked to these traits need be determined, including how to implement this information into a selective breeding program. Choosing a trait can be assisted by modelling to account for the proper agro-ecological context, and by knowing which traits have sufficiently high heritability values. We provide guidelines for designing genomic strategies in biocontrol programs, which depend on the organism, budget, and desired objective. Genomic approaches start with genome sequencing and assembly. We provide a guide for deciding the most successful sequencing strategy for biocontrol agents. Gene discovery involves quantitative trait loci analyses, transcriptomic and proteomic studies, and gene editing. Improving biocontrol practices includes marker-assisted selection, genomic selection and microbiome manipulation of biocontrol agents, and monitoring for genetic variation during rearing and post-release. We conclude by identifying the most promising applications of genetic and genomic methods to improve biological control efficacy.
- No evidence for the evolution of mating behavior in spider mites due to Wolbachia‐induced cytoplasmic incompatibilityPublication . Rodrigues, Leonor R; Zélé, Flore; Santos, Inês; Magalhães, SaraArthropods are often infected with Wolbachia inducing cytoplasmic incompatibility (CI), whereby crosses between uninfected females and infected males yield unviable fertilized offspring. Although uninfected females benefit from avoiding mating with Wolbachia-infected males, this behavior is not always present in host populations and its evolution may hinge upon various factors. Here, we used spider mites to test whether CI could select for mate preference in uninfected females in absence of kin recognition. We found that uninfected females from several field-derived populations showed no preference for infected or uninfected males, nor evolved a preference after being exposed to CI for 12–15 generations by maintaining uninfected females with both infected and uninfected males (i.e., stable “infection polymorphism”). This suggests that Wolbachia-mediated mate choice evolution may require very specific conditions in spider mites. However, after experimental evolution, the copulation duration of Wolbachia-infected control males was significantly higher than that of uninfected control males, but not than that of uninfected males from the “infection polymorphism” regime. This result illustrates how gene flow may oppose Wolbachia-driven divergence between infected and uninfected hosts in natural populations.
- Competition for food affects the strength of reproductive interference and its consequences for species coexistencePublication . Cruz, Miguel A.; Godoy, Oscar; De mendonça fragata almeida, Inês; Sousa, Vitor C; Magalhães, Sara; Zélé, FloreCompetition for food and reproductive interference (negative interspecific sexual interactions) have been identified as major drivers of species exclusion. Still, how these biotic interactions jointly determine competitive dominance remains largely unknown. We tackle this by coupling population models and laboratory experiments with two sibling species of spider mites. Using experiments specifically designed to measure the single and combined effects of food competition and reproductive interference, we first show that the strength and symmetry of reproductive interference between species changes in the presence of food competition. Next, we show that population models incorporating each type of interaction alone lead to markedly different predictions, from systematic exclusion of one of the two species under food competition to priority effects instead favouring this same species (the inferior competitor for food) under the sole effect of reproductive interference. Moreover, accounting for the observed reduction in the strength of reproductive interference in the presence of food competition changes the threshold frequency determining the dominant competitor when both interactions are at play, from equal chances for the two species to exclude the other depending on their initial frequency to favouring the superior competitor for food except when it is extremely rare. Finally, we showed that the model generates accurate predictions for population dynamics in an independent population cage experiment, indicating that our approach captures the most relevant processes governing the outcomes of interactions between competing spider mite species. Altogether, our results suggest that trophic interactions can modulate sexual interactions, significantly impacting population dynamics and competitive outcomes. Hence, the joint consideration of food competition and reproductive interference is critical to accurately predict and understand species coexistence.
- Creating outbred and inbred populations in haplodiploids to measure adaptive responses in the laboratoryPublication . Godinho, Diogo; Cruz, Miguel A.; Charlery de la Masselière, Maud; Teodoro‐Paulo, Jéssica; Eira, Cátia; De mendonça fragata almeida, Inês; Rodrigues, Leonor R; Zélé, Flore; Magalhaes, SLaboratory 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.
- Effect of Cadmium Accumulation on the Performance of Plants and of Herbivores That Cope Differently With Organic DefensesPublication . Godinho, Diogo Prino; Serrano, Helena Cristina; Da Silva, Anabela Bernardes; Branquinho, Cristina; Magalhães, SaraSome plants are able to accumulate in their shoots metals at levels that are toxic to most other organisms. This ability may serve as a defence against herbivores. Therefore, both metal-based and organic defences may affect herbivores. However, how metal accumulation affects the interaction between herbivores and organic plant defences remains overlooked. To fill this gap, we studied the interactions between tomato (Solanum lycopersicum), a model plant that accumulates cadmium, and two spider-mite species, Tetranychus urticae and Tetranychus evansi that, respectively, induce and suppress organic plant defences, measurable via the activity of trypsin inhibitors. We exposed plants to different concentrations of cadmium and measured its effects on mites and plants. In the plant, despite clear evidence for cadmium accumulation, we did not detect any cadmium effects on traits that reflect the general response of the plant, such as biomass, water content, and carbon/nitrogen ratio. Still, we found effects of cadmium upon the quantity of soluble sugars and on leaf reflectance, where it may indicate structural modifications in the cells. These changes in plant traits affected the performance of spider mites feeding on those plants. Indeed, the oviposition of both spider mite species was higher on plants exposed to low concentrations of cadmium than on control plants, but decreased at concentrations above 0.5 mM. Therefore, herbivores with contrasting responses to organic defences showed a similar hormetic response to metal accumulation by the plants. Additionally, we show that the induction and suppression of plant defences by these spider-mite species was not affected by the amount of cadmium supplied to the plants. Furthermore, the effect of cadmium on the performance of spider mites was not altered by infestation with T. urticae or T. evansi. Together, our results suggest no interaction between cadmium-based and organic plant defences, in our system. This may be useful for plants living in heterogeneous environments, as they may use one or the other defence mechanism, depending on their relative performance in each environment.
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