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Zele, F.

Publications and source records attributed to Zele, F..

12 recordsLinked to original sources

Unexpected changes in reproductive barriers between incipient species after experimental evolution in sympatry

Hybridization is generally considered a temporary phenomenon, but it is actually widespread and may last for large time periods between species that stably coexist. Here, to test whether evolving with a closely-related species modifies or maintains partial reproductive isolation, we performed experimental evolution in artificial sympatry vs. allopatry with two closely-related colour forms of spider mites (Tetranychus urticae) that exhibit an asymmetrical pattern of pre-mating isolation despite almost complete post-zygotic isolation. We assessed whether evolutionary changes occurred in traits associated to (i) pre-mating isolation, (ii) post-mating pre-zygotic and early post-zygotic isolation, and (iii) late post-zygotic isolation. Our results revealed that reinforcement did not occur even under forced long-term sympatric evolution. Instead, the strength of some reproductive barriers decreased (e.g., premating isolation and fertilization failure), and some trait changes indicated convergence rather than divergence between species (e.g., mating propensity, latency to copulation). In fact, both types of males showed the same decreased preference for red-form females across generations in sympatry. In line with this, traits underlying fertilization success evolved in the same direction and with similar amplitude in heterotypic crosses and in their homotypic control, as the offspring sex ratio of green-form females decreased in sympatry irrespective of the male they mated with. Finally, other changes in reproductive barriers resulted from trait correlations (e.g., decreased zygote mortality but increased juvenile mortality). Hence, despite very high costs of hybridization, responses occurring following evolution in sympatry were unrelated to selection directly associated to hybridization, but rather the by-product of other evolutionary forces, with cascading consequences for reproductive barriers. In particular, these results support the underappreciated hypothesis that within-species sexual interactions can constrain population diver-gence, or even drive trait convergence between species, thereby playing a role in the maintenance of partial reproductive isolation.

evolutionary biology↗

Genetic variance in spider mites reveals trade-offs: lines with higher growth rate suffer stronger competition but exert stronger reproductive interference

O_LIWithin-species individual variation has been gaining increased attention in ecological studies of species interactions. Yet, these studies rarely consider genetic variation and potential genetic correlations among traits. Moreover, traits beyond those associated with trophic interactions are mostly overlooked. Filling these gaps is important to fully understand the relevance of trait variation in both the ecology and evolution of species interactions. C_LIO_LIWe addressed this using inbred lines of Tetranychus cinnabarinus, a spider mite species that often engages in antagonistic interactions with its congeneric T. urticae. Specifically, we measured (a) the intrinsic growth rate and the sex ratio in the absence of food competition and reproductive interference; (b) food competition against a density gradient of con- or heterospecific competitors in absence of reproductive interference; (c) reproductive interference in absence of food competition; and (d) the body size of adult females and males. C_LIO_LIWe found significant genetic variance (i.e., broad-sense heritability) among lines for all variables except for the effect of T. cinnabarinus on its heterospecific competitor via food competition. Moreover, we showed that lines with higher intrinsic growth were more sensitive to intra- and inter-specific competition for food but exerted stronger reproductive interference on heterospecifics. In addition, the higher the proportion of sons produced by a line, the more resilient it was to reproductive interference but also the lower its growth rate. No genetic correlations were found between any variable and body size. C_LIO_LIOur results indicate that considering the genetic correlations among traits involved in both trophic and sexual interactions is key to understanding the role of individual variation in species interactions and their evolution. C_LI

evolutionary biology↗

Wolbachia strengthens the match between pre-mating and early post-mating isolation in spider mites

Endosymbiotic reproductive manipulators are widely studied as sources of post-zygotic isolation in arthropods, but their effect on pre-zygotic isolation between genetically differentiated populations has garnered less attention. We tested this using two partially isolated populations of the red and green colour forms of Tetranychus urticae, either uninfected or infected with different Wolbachia strains, one inducing cytoplasmic incompatibility and the other not. We first investigated male and female preferences, and found that, in absence of infection, females were not choosy but all males preferred red-form females. Wolbachia effects were more subtle, with only the CI-inducing strain slightly strengthening colour-form based preferences. We then performed a double-mating experiment to test how incompatible matings affect subsequent mating behaviour and offspring production, as compared to compatible matings. Females mated with an incompatible male (infected and/or heterotypic) were more attractive and/or receptive to subsequent (compatible) matings, although analyses of offspring production revealed no clear benefit for this re-mating behaviour (i.e., apparently unaltered first male sperm precedence). Finally, by computing the relative contributions of each reproductive barrier to total isolation, we showed that pre-mating isolation matches both host-associated and Wolbachia-induced post-mating isolation, suggesting that Wolbachia could contribute to reproductive isolation in this system.

evolutionary biology↗

Sex in the kitchen: non-additive effects of competition for food and reproductive interference on coexistence outcomes between closely related species.

Competition 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 presence of food competition. Next, we show that population models incorporating each type of interaction alone lead to markedly different predictions, from exclusion of the inferior competitor for food, to priority effects instead favouring the latter 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 outcome 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.

ecology↗

Evolution in abiotic environments shapes coexistence between two spider mite species

Adaptation to abiotic stresses generally relies on traits that are not independent from those affecting species interactions. Still, the impact of such evolutionary processes on coexistence remains elusive. Here, we studied two spider mite species evolving separately on tomato plants that hyper-accumulated cadmium, a stressful environment for herbivores, or on plants without cadmium. Through experimental evolution and structural stability theory, we found that both species coexist in the cadmium environment, but evolution of a single species in cadmium leads to exclusion. However, when both species evolve in cadmium they can coexist. This shift occured due to a simultaneous increase in intra and a decrease in interspecific competition in that environment. These predictions were further confirmed with complementary experiments of population dynamics. Therefore, population shifts to novel environments, even in absence of interspecific competitors, may have unforeseen evolutionary consequences for community composition and the maintenance of species diversity.

evolutionary biology↗

Wolbachia and host intrinsic reproductive barriers contribute additively to post-mating isolation in spider mites

AO_SCPLOWBSTRACTC_SCPLOWWolbachia are widespread maternally-inherited bacteria suggested to play a role in arthropod host speciation through induction of cytoplasmic incompatibility, but this hypothesis remains controversial. Most studies addressing Wolbachia-induced incompatibilities concern closely-related populations, which are intrinsically 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 to assess their relative contribution to post-mating 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 daugters (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 that Wolbachia did not contribute to this outcome. This study identifies the mechanistic independence and additive nature of host-intrinsic and Wolbachia-induced sources of isolation. It suggests that Wolbachia could drive reproductive isolation in this system, thereby potentially affecting host differentiation and distribution in the field.

evolutionary biology↗

Creating outbred and inbred populations of haplodiploid mites to measure adaptive responses in the lab

Laboratory studies are often criticized for not being representative of processes occurring in natural populations. This can be partially mitigated by using lab populations that capture large amounts of variation. Additionally, many studies addressing adaptation of organisms to their environment are done with laboratory populations, using quantitative genetics or experimental evolution methodologies. Such studies rely on populations that are either highly outbred or inbred. However, the methodology underlying the generation of such biological resources are usually not explicitly documented. Given their small size, short generation time, amenability to laboratory experimentation and knowledge of their ecological interactions, haplodiploid spider mites are becoming a widely used model organism. Here, we describe the creation of outbred populations of two species of spider mites, Tetranychus urticae and T. evansi, obtained by performing controlled crosses between individuals from field-collected populations. Subsequently, from the outbred population of T. evansi, we derived inbred lines, by performing several generations of sib-mating. These can be used to measure broad-sense heritability as well as correlations among traits. Finally, we outline an experimental evolution protocol that can be widely used in other systems. Sharing these biological resources with other laboratories and combining them with the available powerful genetic tools for T. urticae (and other species) will allow consistent and comparable studies that greatly contribute to our understanding of ecological and evolutionary processes.

evolutionary biology↗

Population-specific effect of Wolbachia on the cost of fungal infection in spider mites

Many studies have revealed the ability of the endosymbiotic bacteria 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 is crucial for disease and pest control strategies. 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 generalist entomopathogenic 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 harbouring different Wolbachia strains, after exposure to the fungal biocontrol agents Metarhizium brunneum and Beauveria bassiana. In one population, Wolbachia affected survival in absence of fungi but not in their presence, whereas in the other population Wolbachia increased the mortality induced by B. 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. The antibiotic treatment increased the susceptibility of spider mites to M. brunneum in one naturally Wolbachia-uninfected population, but it had no effect in the other treatments. These results highlight the complexity of within-host pathogens interactions, and the importance of considering the whole bacterial community of arthropods when assessing the effect of Wolbachia in a particular system.

ecology↗

Inter- and intra-specific variation of spider mite susceptibility to fungal infections: implications for the long-term success of biological control

Spider mites are severe pests of several annual and perennial crops worldwide, often causing important economic damages. Moreover, rapid evolution of pesticide resistance in this group hampers the efficiency of chemical control. Alternative control strategies, such as the use of entomopathogenic fungi, are thus being developed. However, while several studies have focussed on the evaluation of the control potential of different fungal species and/or isolates as well as their compatibility with other control methods (e.g. predators or chemical pesticides), knowledge on the extent of inter- and intraspecific variation in spider mite susceptibility to fungal infection is as yet incipient. Here, we measured the mortality induced by two generalist fungi, Beauveria bassiana and Metarhizium brunneum, in 12 spider mite populations belonging to different Tetranychus species: T. evansi, T. ludeni, the green form of T. urticae and the red form of T. urticae, within a full factorial experiment. We found that spider mite species differed in their susceptibility to infection to both fungal species. Moreover, we also found important intraspecific variation for this trait. These results draw caution on the development of single strains as biocontrol agents. Indeed, the high level of intraspecific variation suggests that (a) the one-size-fits-all strategy will probably fail to control spider-mite populations and (b) hosts resistance to infection may evolve at a rapid pace. Finally, we propose future directions to better understand this system and improve the long-term success of spider mite control strategies based on entomopathogenic fungi.

ecology↗

Spider mites escape bacterial infection by avoiding contaminated food

To fight infection, arthropods rely on the deployment of an innate immune response but also upon physical/chemical barriers and avoidance behaviours. However, most studies focus on immunity, with other defensive mechanisms being relatively overlooked.\n\nWe have previously shown that the spider mite Tetranychus urticae does not mount an induced immune response towards systemic bacterial infections, entailing very high mortality rates. Therefore, we hypothesized that other defence mechanisms may be operating to minimize infection risk. Here, we test (a) if spider mites are also highly susceptible to other infection routes - spraying and feeding - and (b) if they display avoidance behaviours towards infected food. Individuals sprayed with or fed on Escherichia coli or Pseudomonas putida survived less than the control, pointing to a deficient capacity of the gut epithelium, and possibly of the cuticle, to contain bacteria. Additionally, we found that spider mites prefer uninfected food to food contaminated with bacteria, a choice that probably does not rely on olfactory cues.\n\nOur results suggest that spider mites may rely mostly on avoidance behaviours to minimize bacterial infection and highlight the multi-layered nature of immune strategies present in arthropods.

ecology↗

Environments with a high probability of incompatible crosses do not select for mate avoidance in spider mites

Arthropods 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 behaviour is not present in all host species. Here we measured the prevalence of this behaviour across populations of the spider mite Tetranychus urticae. Females from five populations originally fully infected with Wolbachia showed no preference, possibly because they did not face the choice between compatible and incompatible mates in their environment. Hence, to determine whether this behaviour could be selected in populations with intermediate Wolbachia infection frequency, we performed 15 generations of experimental evolution of spider-mite populations under i) full Wolbachia infection, ii) no infection, or iii) mixed infection. In the latter selection regime, where uninfected females were exposed to infected and uninfected males at every generation, mating duration increased relative to the uninfected regime, suggesting the presence of genetic variation for mating traits. However, mate choice did not evolve. Together, these results show that CI-inducing Wolbachia alone does not necessarily lead to the evolution of pre-copulatory strategies in uninfected hosts, even at intermediate infection frequency.

evolutionary biology↗

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

In the last decades, many studies had 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 herbivores 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 purple, tomato and zuchini. Although most mite life-history traits were affected by the plant species only, Wolbachia infection was detrimental for egg hatching rate on purple and zucchini, and led to a more female-biased sex ratio on purple 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.

ecology↗