Sugar-rich larval diet promotes lower adult pathogen load and higher survival after infection in a polyphagous fly.

Nutrition is a central factor influencing immunity and resistance to infection, but the extent to which nutrition during development affects adult responses to infections is poorly understood. Our study investigated how the nutritional composition of the larval diet affects the survival, pathogen load and food intake of adult fruit flies, Bactrocera tryoni, after septic bacterial infection. We found a sex-specific effect of larval diet composition on survival post-infection: survival rate was higher and bacterial load was lower for infected females raised on a sugar-rich larval diet than for females raised on a protein-rich larval diet, an effect that was absent in males. Both males and females were heavier when fed a balanced larval diet compared with a protein- or sugar-rich diet, while body lipid reserves were higher for those that had consumed the sugar-rich larval diet compared with other diets. Body protein reserves were lower for flies that had been raised on the sugar-rich larval diet compared with other diets in males, but not females. Both females and males shifted their nutrient intake to ingest a sugar-rich diet when infected compared with sham-infected flies without any effect of the larval diet, suggesting that sugar-rich diets can be beneficial to fight off bacterial infection as shown in previous literature. Overall, our findings show that nutrition during early life can shape individual fitness in adulthood.

Density-by-Diet Interactions during Larval Development Shape Adult Life History Trait Expression and Fitness in a Polyphagous Fly.

AbstractHabitat quality early in life determines individual fitness, with possible long-term evolutionary effects on groups and populations. In holometabolous insects, larval ecology plays a major role in determining the expression of traits in adulthood, but how ecological conditions during the larval stage interact to shape adult life history and fitness, particularly in nonmodel organisms, remains subject to scrutiny. Consequently, our knowledge of the interactive effects of ecological factors on insect development is limited. Here, using the polyphagous fly Bactrocera tryoni, we conducted a fully factorial design where we manipulated larval density and larval diet (protein rich, standard, and sugar rich) to gain insights into how these ecological factors interact to modulate adult fitness. As expected, a protein-rich diet resulted in faster larval development and heavier and leaner adults that were more fecund compared with the standard and sugar-rich diets, irrespective of larval density. Females from the protein-rich larval diet had overall higher reproductive rate (i.e., eggs per day) than females from other diets, and reproductive rate decreased linearly with density for females from the protein-rich diet but nonlinearly for females from the standard and sugar-rich diets over time. Surprisingly, adult lipid reserve increased with larval density for adults from the sugar-rich diet (as opposed to decreasing as in other diets), possibly because of a stress response to an extremely adverse condition during development (i.e., high intraspecific competition and poor nutrition). Together, our results provide insights into how ecological factors early in life interact and shape the fate of individuals through life stages in holometabolous insects.

Parental Microbiota Modulates Offspring Development, Body Mass and Fecundity in a Polyphagous Fruit Fly.

The commensal microbiota is a key modulator of animal fitness, but little is known about the extent to which the parental microbiota influences fitness-related traits of future generations. We addressed this gap by manipulating the parental microbiota of a polyphagous fruit fly (Bactrocera tryoni) and measuring offspring developmental traits, body composition, and fecundity. We generated three parental microbiota treatments where parents had a microbiota that was non-manipulated (control), removed (axenic), or removed-and-reintroduced (reinoculation). We found that the percentage of egg hatching, of pupal production, and body weight of larvae and adult females were lower in offspring of axenic parents compared to that of non-axenic parents. The percentage of partially emerged adults was higher, and fecundity of adult females was lower in offspring of axenic parents relative to offspring of control and reinoculated parents. There was no significant effect of parental microbiota manipulation on offspring developmental time or lipid reserve. Our results reveal transgenerational effects of the parental commensal microbiota on different aspects of offspring life-history traits, thereby providing a better understanding of the long-lasting effects of host-microbe interactions.

Effects of carbohydrate types on larval development and adult traits in a polyphagous fruit fly.

Nutrition is a major mediator of insect life-history trait expression. While the role of macronutrient (carbohydrate and protein) balance on trait expression has received substantial attention, the implications of different classes of specific macronutrients remains virtually unexplored. Here, we addressed this gap by varying the type of carbohydrate in larval diets of the polyphagous fruit fly Bactrocera tryoni (aka 'Queensland fruit fly'). Sourcing insects from a colony maintained using larval diets that contain sucrose, we assessed the effects of sucrose, maltose, and lactose on larval development and adult traits. Replacement of sucrose with lactose resulted in slow larval growth, as well as decreases in pupation, adult emergence and adult body weight for both sexes, although adult lipid reserves were unaffected. Sucrose and maltose were equivalent in terms of larval growth, pupation, adult emergence and adult weight of both sexes. Surprisingly, adults from larvae reared on diets containing maltose had lower lipid reserves than adults from larvae reared on diets containing either lactose or sucrose. The sex ratio of adults at emergence from larvae reared on diets containing lactose and maltose was balanced, but was female-biased in adults from larvae reared on diets containing sucrose. Our results show that carbohydrate sources are not equivalent for development of the Queensland fruit fly, affecting both larval development and adult traits. These findings have implications for understanding the ecology of this highly polyphagous species which infests fruits with highly diverse carbohydrate contents, as well as for the rearing and management of this pest species.

Interactions between ecological factors in the developmental environment modulate pupal and adult traits in a polyphagous fly.

In holometabolous insects, adult fitness depends on the quantity and quality of resource acquired at the larval stage. Diverse ecological factors can influence larval resource acquisition, but little is known about how these factors in the larval environment interact to modulate larval development and adult traits.Here, we addressed this gap by considering how key ecological factors of larval density, diet nutritional composition, and microbial growth interact to modulate pupal and adult traits in a polyphagous tephritid fruit fly, Bactrocera tryoni (aka "Queensland fruit fly").Larvae were allowed to develop at two larval densities (low and high), on diets that were protein-rich, standard, or sugar-rich and prepared with or without preservatives to inhibit or encourage microbial growth, respectively.Percentage of adult emergence and adult sex ratio were not affected by the interaction between diet composition, larval density, and preservative treatments, although low preservative content increased adult emergence in sugar-rich diets but decreased adult emergence in protein-rich and standard diets.Pupal weight, male and female adult dry weight, and female (but not male) body energetic reserves were affected by a strong three-way interaction between diet composition, larval density, and preservative treatment, whereby in general, low preservative content increased pupal weight and female lipid storage in sugar-rich diets particularly at low-larval density and differentially modulated the decrease in adult body weight caused by larval density across diets.Our findings provide insights into the ecological factors modulating larval development of a polyphagous fly species and shed light into the ecological complexity of the larval developmental environment in frugivorous insects.

Crowded developmental environment promotes adult sex-specific nutrient consumption in a polyphagous fly.

BACKGROUND: The fitness of holometabolous insects depends largely on resources acquired at the larval stage. Larval density is an important factor modulating larval resource-acquisition, influencing adult survival, reproduction, and population maintenance. To date, however, our understanding of how larval crowding affects adult physiology and behaviour is limited, and little is known about how larval crowding affects adult non-reproductive ecological traits. Here, larval density in the rearing environment of the polyphagous fruit fly Bactrocera tryoni ('Queensland fruit-fly') was manipulated to generate crowded and uncrowded larval treatments. The effects of larval crowding on pupal weight, adult emergence, adult body weight, energetic reserves, fecundity, feeding patterns, flight ability, as well as adult predation risk were investigated. RESULTS: Adults from the crowded larval treatment had lower adult emergence, body weight, energetic reserves, flight ability and fecundity compared to adults from the uncrowded larval treatment. Adults from the crowded larval treatment had greater total food consumption (i.e., consumption of yeast plus sucrose) relative to body weight for both sexes compared to adults from the uncrowded treatment. Furthermore, males from the crowded treatment consumed more yeast relative to their body weight than males from the uncrowded treatment, while females from the crowded treatment consumed more sucrose relative to their body weight than females from the uncrowded treatment. Importantly, an interaction between the relative consumptions of sucrose and yeast and sex revealed that the density of conspecifics in the developmental environment differentially affects feeding of adult males and females. We found no effect of larval treatment on adult predation probability. However, males were significantly more likely to be captured by ants than females. CONCLUSION: We show that larvae crowding can have important implications to ecological traits in a polyphagous fly, including traits such as adult energetic reserve, flight ability, and adult sex-specific nutrient intake. Our findings contextualise the effects of larval developmental conditions into a broad ecological framework, hence providing a better understanding of their significance to adult behaviour and fitness. Furthermore, the knowledge presented here can help us better understanding downstream density-dependent effects of mass rearing conditions of this species, with potential relevance to Sterile Insect Technique.