Evolutionary compromises to metabolic toxins: Ammonia and urea tolerance in Drosophila suzukii and Drosophila melanogaster

Abstract

The invasive pest Drosophila suzukii has evolved morphological and behavioural adaptations to lay eggs under the skin of fresh fruits. This results in severe damage to a wide range of small fruits. Drosophila suzukii females typically lay few eggs per fruit, preferring healthy fruits. Hence, larvae are exposed to a reduced amount of nitrogenous waste. Differently, the innocuous Drosophila melanogaster lays eggs on fermented fruits already infested by conspecifics, with larvae developing in a crowded environment with the accumulation of nitrogenous waste such as ammonia and urea. These compounds derive from nitrogen metabolism, protein degradation, and amino acids catabolism and are relatively toxic at high concentrations in an organism. The observed differences in oviposition site and larval ecological niche suggest that these species might differ in behavioural and physiological mechanisms used to cope with nitrogenous waste. We investigated how different concentrations of ammonia and urea affect oviposition and larval development in both species. Females and larvae of D. suzukii showed greater susceptibility to high concentrations of both compounds, with a dramatic decrease in the number of eggs laid and egg viability. Moreover, we tested the chemotactic response of third instar larvae to high concentrations of the compounds. Interestingly, ammonia resulted in a repulsive behaviour in respect of the control and urea groups. To better understand the pathways underlying these differences, we evaluated the effect on ornithine aminotransferase and glutathione-S-transferase, two enzymes involved in nitrogen metabolism and stress response that are expressed during larval development. Both ammonia and urea significantly reduced the expression of these enzymes in D. suzukii compared to D. melanogaster. This shows how the ecological shift of D. suzukii to fresh fruit is accompanied by less efficient detoxifying and excretory mechanisms, with important implications for evolutionary biology and applied research. Our data suggest that the ecological shift of D. suzukii to fresh fruit as oviposition substrate is accompanied by a reduced tolerance to metabolic toxins during larval development.

Integrative developmental ecology: a review of density-dependent effects on life-history traits and host-microbe interactions in non-social holometabolous insects

“…(Mueller and Ayala 1981;Mueller et al 1991); this is evidence for the evolution of increased population carryingcapacity at high population densities. In addition, D. melanogaster larval feeding rates (a measure of larval competitive ability), cannibalism, and ability to withstand toxic waste (i.e., ammonia and urea) also increase (although not for all species) in populations experiencing or evolving high larval densities [(Belloni et al 2018;Borash et al 1998;Borash and Shimada 2001;Vijendravarma et al 2013); see also review in (Joshi et al 2001)], albeit creating a trade-off with larval energy efficiency (Joshi and Mueller 1996;Joshi et al 2001;Mueller 1990). However, this trade-off is not necessarily observed in other Drosophila species (Nagarajan et al 2016) suggesting that the natural history of species may lead to different responses to population density.…”

Drosophila ammonium transporter Rh50 is required for integrity of larval muscles and neuromuscular system

“…Wild‐type larvae were exposed to high ammonia concentration (350 mM) in the food, from the first to the third stage. This concentration is similar to that used to study ammonia tolerance in Drosophila (Belloni et al, ; Borash, Pierce, Gibbs, & Mueller, ). The treated larvae consistently showed a ~26 and 14% decrease in synaptic and extrasynaptic GluRIIA levels in muscles, respectively (Supporting Information Figure S3a,b).…”

Composting susceptible fruit wastes reduces Drosophila suzukii (Diptera: Drosophilidae) reproductive habitat

“…developmental delay or modified feeding rate. 23 In contrast, when fruit waste was composted with 1% chicken manure in the laboratory, D. suzukii reproduction increased by 28.5% compared to pure apple pomace. The nitrogenous wastes exuded from this minute quantity of chicken manure were potentially too low to cause acute toxicity in D. suzukii, but may have permitted an accelerated growth of microbes beneficial to larval development.…”

“…22 High concentrations of dietary urea and ammonia have been shown to decrease oviposition and egg viability in D. suzukii. 23,24 Furthermore, the enzymes ornithine aminotransferase and glutathione-S-transferase expression are suppressed in D. suzukii, and control nitrogen metabolism and stress response. 23 This potentially leaves D. suzukii larvae susceptible to high levels of nitrogenous wastes because they may not have adequate detoxification or excretory mechanisms to regulate their nitrogen intake, e.g.…”

“…As chicken manure decomposes, uric acid forms urea, which subsequently forms ammonia 22 . High concentrations of dietary urea and ammonia have been shown to decrease oviposition and egg viability in D. suzukii 23,24 . Furthermore, the enzymes ornithine aminotransferase and glutathione‐ S ‐transferase expression are suppressed in D. suzukii , and control nitrogen metabolism and stress response 23 .…”