High promiscuity among females of the invasive pest species Drosophila suzukii.

Drosophila suzukii (Matsumura, 1931), the spotted-wing drosophila, is a highly invasive fruit fly that spread from Southern Asia across most regions of Asia and, in the last 15 years, has invaded Europe and the Americas. It is an economically important pest of small fruits such as berries and stone fruits. Drosophila suzukii speciated by adapting to cooler, mountainous, and forest environments. In temperate regions, it evolved seasonal polyphenism traits which enhanced its survival during stressful winter population bottlenecks. Consequently, in these temperate regions, the populations undergo seasonal reproductive dynamics. Despite its economic importance, no data are available on the behavioural reproductive strategies of this fly. The presence of polyandry, for example, has not been determined despite the important role it might play in the reproductive dynamics of populations. We explored the presence of polyandry in an established population in Trentino, a region in northern Italy. In this area, D. suzukii overcomes the winter bottleneck and undergoes a seasonal reproductive fluctuation. We observed a high remating frequency in females during the late spring demographic explosion that led to the abundant summer population. The presence of a high degree of polyandry and shared paternity associated with the post-winter population increase raises the question of the possible evolutionary adaptive role of this reproductive behaviour in D. suzukii.

Microbiota acquisition and transmission in Drosophila flies.

Understanding the ecological and evolutionary dynamics of host-microbiota associations notably involves exploring how members of the microbiota assemble and whether they are transmitted along host generations. Here, we investigate the larval acquisition of facultative bacterial and yeast symbionts of Drosophila melanogaster and Drosophila suzukii in ecologically realistic setups. Fly mothers and fruit were major sources of symbionts. Microorganisms associated with adult males also contributed to larval microbiota, mostly in D. melanogaster. Yeasts acquired at the larval stage maintained through metamorphosis, adult life, and were transmitted to offspring. All these observations varied widely among microbial strains, suggesting they have different transmission strategies among fruits and insects. Our approach shows microbiota members of insects can be acquired from a diversity of sources and highlights the compound nature of microbiotas. Such microbial transmission events along generations should favor the evolution of mutualistic interactions and enable microbiota-mediated local adaptation of the insect host.

Microbiota-mediated competition between Drosophila species.

BACKGROUND: The influence of microbiota in ecological interactions, and in particular competition, is poorly known. We studied competition between two insect species, the invasive pest Drosophila suzukii and the model Drosophila melanogaster, whose larval ecological niches overlap in ripe, but not rotten, fruit. RESULTS: We discovered D. suzukii females prevent costly interspecific larval competition by avoiding oviposition on substrates previously visited by D. melanogaster. More precisely, D. melanogaster association with gut bacteria of the genus Lactobacillus triggered D. suzukii avoidance. However, D. suzukii avoidance behavior is condition-dependent, and D. suzukii females that themselves carry D. melanogaster bacteria stop avoiding sites visited by D. melanogaster. The adaptive significance of avoiding cues from the competitor's microbiota was revealed by experimentally reproducing in-fruit larval competition: reduced survival of D. suzukii larvae only occurred if the competitor had its normal microbiota. CONCLUSIONS: This study establishes microbiotas as potent mediators of interspecific competition and reveals a central role for context-dependent behaviors under bacterial influence. Video Abstract.

Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly.

Both local adaptation and adaptive phenotypic plasticity can influence the match between phenotypic traits and local environmental conditions. Theory predicts that environments stable for multiple generations promote local adaptation, whereas highly heterogeneous environments favor adaptive phenotypic plasticity. However, when environments have periods of stability mixed with heterogeneity, the relative importance of local adaptation and adaptive phenotypic plasticity is unclear. Here, we used Drosophila suzukii as a model system to evaluate the relative influence of genetic and plastic effects on the match of populations to environments with periods of stability from three to four generations. This invasive pest insect can develop within different fruits, and persists throughout the year in a given location on a succession of distinct host fruits, each one being available for only a few generations. Using reciprocal common environment experiments of natural D. suzukii populations collected from cherry, strawberry, and blackberry, we found that both oviposition preference and offspring performance were higher on medium made with the fruit from which the population originated than on media made with alternative fruits. This pattern, which remained after two generations in the laboratory, was analyzed using a statistical method we developed to quantify the contributions of local adaptation and adaptive plasticity in determining fitness. Altogether, we found that genetic effects (local adaptation) dominate over plastic effects (adaptive phenotypic plasticity). Our study demonstrates that spatially and temporally variable selection does not prevent the rapid evolution of local adaptation in natural populations. The speed and strength of adaptation may be facilitated by several mechanisms including a large effective population size and strong selective pressures imposed by host plants.

Influence of bacteria on the maintenance of a yeast during Drosophila melanogaster metamorphosis.

Interactions between microorganisms associated with metazoan hosts are emerging as key features of symbiotic systems. Little is known about the role of such interactions on the maintenance of host-microorganism association throughout the host's life cycle. We studied the influence of extracellular bacteria on the maintenance of a wild isolate of the yeast Saccharomyces cerevisiae through metamorphosis of the fly Drosophila melanogaster reared in fruit. Yeasts maintained through metamorphosis only when larvae were associated with extracellular bacteria isolated from D. melanogaster faeces. One of these isolates, an Enterobacteriaceae, favoured yeast maintenance during metamorphosis. Such bacterial influence on host-yeast association may have consequences for the ecology and evolution of insect-yeast-bacteria symbioses in the wild.

Yeast facilitates the multiplication of Drosophila bacterial symbionts but has no effect on the form or parameters of Taylor's law.

Interactions between microbial symbionts influence their demography and that of their hosts. Taylor's power law (TL)-a well-established relationship between population size mean and variance across space and time-may help to unveil the factors and processes that determine symbiont multiplications. Recent studies suggest pervasive interactions between symbionts in Drosophila melanogaster. We used this system to investigate theoretical predictions regarding the effects of interspecific interactions on TL parameters. We assayed twenty natural strains of bacteria in the presence and absence of a strain of yeast using an ecologically realistic set-up with D. melanogaster larvae reared in natural fruit. Yeast presence led to a small increase in bacterial cell numbers; bacterial strain identity largely affected yeast multiplication. The spatial version of TL held among bacterial and yeast populations with slopes of 2. However, contrary to theoretical prediction, the facilitation of bacterial symbionts by yeast had no detectable effect on TL's parameters. These results shed new light on the nature of D. melanogaster's symbiosis with yeast and bacteria. They further reveal the complexity of investigating TL with microorganisms.