Adaptation in heterogeneous environments

Evolution of sex allocation strategies in the mite Tetranychus urticae, a major crop pest

  • FCT-ANR/BIA-EVF/0013/2012
  • National Research Project
  • 2013 to 2016

Sex allocation is a crucial trait with tremendous effects on population dynamics1. Indeed, female-biased sex ratios entail high population growth rates, relative to a 1:1 sex ratio. Therefore, unravelling sex allocation strategies will help us managing populations of undesirable species (invasive species, crop pests, disease-carrying vectors, etc). Moreover, the evolution of sex ratio is a fertile ground to put Evolutionary Theory to a critical test, given the precise predictions that have been generated (e.g., 2). For these reasons, sex allocation has been a prolific research area for the past 40 years3-5. Despite the abundance of studies, however, several research avenues remain unexplored.
Female-biased sex ratios are observed in many species. Two major explanations for such biased sex ratios have been provided: Local mate competition (LMC) and sex ratio distorters. Under LMC, the main fuel driving biased sex allocation is population structure. Indeed, in populations founded by few females, a female-biased sex ratio is expected, as males will incur competition with related males2. This highly popular hypothesis has been tested using within-generation plasticity studies (e.g., 6) or by a comparative approach across species (e.g., 7). However, to directly test theory, it is necessary to perform experimental evolution. We have recently adopted this approach8, by creating populations with different numbers of foundresses at each generation, and this has been viewed as a groundbreaking result in the field9. Indeed, novel research avenues can be followed using this approach, some of which will be undertaken in this project.

The endosymbiontic bacteria Wolbachia is the most widespread sex ratio distorter10. Although its effects on hosts have been extensively studied, the mechanism by which Wolbachia manipulates the host sex ratio is unknown, and our understanding of the reciprocal effects between the host mating system and Wolbachia is in its infancy11. The knowledge we have gathered in our study system will be instrumental to the advancement of this research area.
The information on sex allocation strategies and Wolbachia infection can be used to design management policies for host populations1,17,18,20. This approach has been recently successfully undertaken for the dengue-carrying mosquito18,20, and its extension to other systems is highly desirable.

In this project, we will use the haplodiploid spider mite Tetranychus urticae to shed light on the evolution of sex allocation and its consequences for population dynamics and pest management. T. urticae is a major crop pests worldwide12, in which resistance to pesticides evolves at a rapid pace13. Hence, novel control measures are needed. The project builds on an ongoing collaboration with the University of Montpellier, that has already contributed substantially to the knowledge of sex allocation strategies8,14,15. Indeed, so far, we have (a) provided the first direct test of Hamiltons' LMC theory8; (b) unravelled a mechanism by which females control the sex ratio of their offspring (i.e., egg size)14; and (c) provided a complete analysis of resource allocation strategies of virgin and mated females in absence of sexual conflicts15. These results provide a solid ground upon which this project is built. Together, we gather a unique set of experimental tools (isogenic lines, experimental evolution populations, natural populations with and without sex ratio distorters, and access to all genomic tools developed by the spider mite genome consortium16, to which we belong). This places us at the forefront of research in this field.

The Portuguese team aims to cover the following aspects:
-Perform experimental evolution of sex ratio adjustment using different number of patches, to complement our results on evolution with different foundresses numbers8.
- Analyse the consequences of the mating system of spider mites, following our previous work15, in terms of sex allocation and population dynamics;
- Test the role of Wolbachia in sex allocation and sexual conflict in spider mites and their consequences for the invasion of this symbiont;
- Perform greenhouse experiments to (a) manipulate population structure, affecting the sex ratio and hence population growth and (b) test the effect of Wolbachia on host population growth. Both these approaches can subsequently be used as potential biocontrol measures17-20.
This project provides groundbreaking tests of evolutionary theory of sex allocation, and has the potential to develop novel biocontrol measures. The complementary knowledge and resources of the French and the Portuguese team, as well as their long lasting collaboration (since 2004), ensures its feasibility.

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