Dataset Information

Larval foraging decisions in competitive heterogeneous environments accommodate diets that support egg-to-adult development in a polyphagous fly.

ABSTRACT: In holometabolous insects, larval nutrition is a key factor underpinning development and fitness. Heterogeneity in the nutritional environment and larval competition can force larvae to forage in suboptimal diets, with potential downstream fitness effects. Little is known about how larvae respond to competitive heterogeneous environments, and whether variation in these responses affects current and next generations. Here, we designed nutritionally heterogeneous foraging arenas by modifying nutrient concentration, where groups of the polyphagous fruit fly Bactrocera tryoni could forage freely at various levels of larval competition. Larval foraging preferences were highly consistent and independent of larval competition, with greatest foraging propensity for high (100%) followed by intermediate (80% and 60%) nutrient concentration diets, and avoidance of lower concentration diets (less than 60%). We then used these larval preferences (i.e. 100%, 80% and 60% diets) in fitness assays in which larvae competition was maintained constant, and showed that nutrient concentrations selected by the larvae in the foraging trials had no effect on fitness-related traits such as egg hatching and pupation success, adult flight ability, sex ratio, percentage of emergence, nor on adult cold tolerance, fecundity and next-generation pupal weight. These results support the idea that polyphagous species can exploit diverse hosts and nutritional conditions with minimal fitness costs to thrive in new environments.

SUBMITTER: Morimoto J

PROVIDER: S-EPMC6502372 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Larval foraging decisions in competitive heterogeneous environments accommodate diets that support egg-to-adult development in a polyphagous fly.

Morimoto Juliano J Tabrizi Shabnam Tarahi ST Lundbäck Ida I Mainali Bishwo B Taylor Phillip W PW Ponton Fleur F

Royal Society open science 20190417 4

In holometabolous insects, larval nutrition is a key factor underpinning development and fitness. Heterogeneity in the nutritional environment and larval competition can force larvae to forage in suboptimal diets, with potential downstream fitness effects. Little is known about how larvae respond to competitive heterogeneous environments, and whether variation in these responses affects current and next generations. Here, we designed nutritionally heterogeneous foraging arenas by modifying nutri ...[more]

PMID: 31183148

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Project description:Egg-laying decisions are critical for insects, and particularly those competing for limited resources. Sensory information used by females to mediate egg-laying decisions has been reported to be primarily chemical, but the role of vibration has received little attention. We tested the hypothesis that vibrational cues produced by feeding larvae occupying a seed influences egg-laying decisions amongst female cowpea beetles. This hypothesis is supported by three lines of evidence using two strains of the cowpea beetle (Callosobruchus maculatus), an Indian strain with choosy females and aggressively competing larvae and a Brazilian strain with less choosy females and larvae exhibiting an "accommodating" type of competition. First, in free-choice bioassays of seed selection, choosy Indian females selected control seeds (free of eggs, larvae, or egg-laying marker) over seeds with live larvae (free of eggs and egg-laying marker), but did not discriminate between control seeds and those with dead larvae. In contrast, less choosy Brazilian females showed no preference for seeds containing live or dead larvae over controls. Second, laser-doppler vibrometer recordings confirmed that larvae feeding inside seeds generate vibrations that are available to the female during egg-laying decisions. Third, during dichotomous choice experiments where artificial vibrations approximating those produced by feeding larvae were played back during seed selection, Indian females preferred immobile control seeds over vibrating seeds, but Brazilian females showed no preference. These results support the hypothesis that females use larval vibrations in their egg-laying decisions; whether these vibrations are passive cues exploited by the female, or active signals that 'steer' the behaviour of the female is unknown. We propose that vibration cues and signals could be important for host selection in insects, particularly those laying on substrates where visual or chemical cues may be unreliable. This seems to be the case with females of the cowpea beetle since visual cues are not important and chemical egg-marking does not last more than two weeks, allowing vibration cues to improve discrimination of egg-laying substrate particularly by choosy females.

Project description: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.

Dataset Information

Larval foraging decisions in competitive heterogeneous environments accommodate diets that support egg-to-adult development in a polyphagous fly.

Publications

Larval foraging decisions in competitive heterogeneous environments accommodate diets that support egg-to-adult development in a polyphagous fly.

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