THE EFFECT OF SEXUAL AND HOST-ENDOSYMBIONT CONFLITCTS OVER SEX ALLOCATION AND MATING STRATEGIES IN THE SPIDER MITE TETRANYCHUS URTICAE

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Polyandry and host-endosymbiont conflicts in the spider mite tetranychus urticae

Publication . Rodrigues, Ana Leonor Rapoula; Magalhães, Sara

Organisms compete for several resource types, the most studied being food, hosts and mates. Regrettably, the study of competition for each of these resource types belongs to different research fields that rarely overlaps, which might hamper a comprehensive understanding of competition as pervasive selective force. In this work, we begin by showing how experimental evolution can be transversally applied to the study of competition across research fields and attempt to extract general patterns and processes, as in all cases individuals are competing for the use of a limiting resource. The rest of this thesis is directed towards competition for mates, a type of competition that is shaped by sexual selection. The main goal of this work was to study the adaptations favoured by sexual selection at different stages of reproduction, namely prior and after mating, in order to better understand the occurrence of polyandry in species with first male sperm precedence. In these species, the first male that mates with a female will sire all her offspring. Consequently, it seems paradoxical that females mate multiply, except if this behaviour provides an advantage for females or males, if it correlates with other traits, or if it occurs inadvertently. In order to tackle this, we used the spider mite Tetranychus urticae, a haplodiploid species with first male sperm precedence in which polyandry is pervasive. First, we tested whether males distinguish between virgin and mated females and which type of cues they use to exert their preference. In fact, spider mite males preferred virgin over mated females and used chemical cues, namely volatiles and chemical trails, to distinguish them. These results indicate that polyandry does not occur due to a lack of ability to discriminate females of different matings status, suggesting this behaviour might be advantageous for either sex. Consequently, the next step was to test the potential costs and benefits of polyandry for males and females. Neither males, nor females benefited directly with polyandry. In fact, females that mated multiple times survived less and laid fewer eggs, compared to females that mated once or twice only. Nevertheless, males did not suffer longevity costs when they mated with mated females and they were able to decrease the fitness of first males, gaining an indirect benefit with this behaviour. Polyandry can thus be, even if partially, explained by this indirect benefit. Still, these results do not rule out the existence of other, indirect benefits. For instance, by mating multiply, individuals might reduce the risk of only mating with incompatible mates. Incompatible matings may be attributed to the presence of endosymbiotic bacteria. These organisms can employ various tactics, such as altering the reproduction of their hosts, in order to favour their own transmission. When these tactics are costly for the host, hosts are expected to evolve strategies to avoid or reduce such costs. Spider mite populations are often infected with Wolbachia, an endosymbiotic bacterium that induces cytoplasmic incompatibility (CI), whereby crosses between uninfected females and infected males yield reduced fertilized offspring. Here we tested whether T. urticae uninfected females evolve mate choice and multiple mating to circumvent the costs imposed by CI. To this aim, we performed experimental evolution on spider-mite populations with i) full Wolbachia infection, ii) no infection, or iii) mixed infection. In the latter, Wolbachia-uninfected females could copulate with both Wolbachia-infected and Wolbachia-uninfected males at each generation, which is expected to result in high costs for uninfected females, and hence promote the evolution of a compensatory mechanism. Evolving under mixed infection did not affect host mate choice, latency to copulation or copulation duration, after 12 generations of selection. Therefore, the role of Wolbachia in pre-copulatory reproductive isolation in spider mites, if present, is probably residual. However, after 20 generations of selection, uninfected females evolving under mixed infection that mated with Wolbachia-infected males presented a higher degree of CI than those mated first with Wolbachia-infected and then with Wolbachia-uninfected males evolving under mixed infection. Therefore, polyandry can be advantageous when there is the risk of incompatible matings, since it reduces the degree of CI. By doing so, spider mites break their sperm priority pattern in favour of the second male. However, this disruption of sperm precedence only occurred in one direction. Indeed, when the first mating was compatible, i.e., the first male was not infected with Wolbachia, individuals kept first male sperm precedence. The unidirectional disruption of the sperm precedence pattern might be a key factor for the evolution of CI-driven polyandry in species with skewed patterns of sperm precedence. Overall, the results obtained here contribute to improve our understanding of mating strategies by addressing important questions that have been largely neglected so far, namely the putative drivers of multiple mating in species with first male sperm precedence.

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Fundação para a Ciência e a Tecnologia

Número da atribuição

SFRH/BD/87628/2012