Reproductive resource allocation correlates with successful global invasion of a mosquito species

Abstract

The understanding of traits favoring biological invasions has been considered an essential step to predict which species would become successful invaders. Classical approaches test for differences between invasive vs. not invasive species and emphasize reproduction as a critical phenotype for successful establishment of an invasive species. However, cross-species comparisons underestimate intraspecies differences, which may be relevant in invasive species with highly genetically diverse populations. Here we capitalize on the well-characterized invasion history of the arboviral vector Aedes albopictus, which resulted in genetically-distinct native, old and invasive populations, and compared the reproductive capacity (fertility and fecundity), development (timing of egg development, oviposition patterns and egg hatching) and physiology (blood digestion and nutrient movement during oogenesis) across populations. We observed that invasive mosquitoes optimize their nutrient investment during development and oogenesis, which leads to increased egg production with respect to native and long adapted laboratory mosquitoes. This higher fecundity results from a delay in oogenesis and is accompanied by higher fertility. We further tested inheritance of reproductive traits via reciprocal crosses, which showed a higher fertility and fecundity in hybrids with respect to parental strains and a potential contribution of males to the reproductive success of invasive mosquitoes. Our results provide evidence that resource allocation during development and oogenesis influences the reproductive capacity of Ae. albopictus and manifests in population differences that correlate with their invasion success. Significance StatementIn addition to being an essential process to ensure the survival of a species, reproduction is a key determinant for a species invasion success because it facilitates a species ability to establish in a new area. Reproduction is a complex phenotype that relies on intricate and timely interactions between genetic and physiological factors. Here we combined molecular, biochemical, and genetic approaches to show that efficient allocation of energetic resources during development and oogenesis fosters the reproductive output of Ae. albopictus mosquitoes and manifests as variation in the reproductive capacity of its geographic populations. These results are critical for predicting the invasion success of this species and tailoring effective control strategies.