Developmental mechanisms underlying the ontogeny of foraging behaviour in fruit fly larvae

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Differences in larval nutritional requirements and female oviposition preference reflect the order of fruit colonization of Zaprionus indianus and Drosophila simulans

Publication . Matavelli, Cristiane; Carvalho, Maria João A.; Martins, Nelson E.; Mirth, Christen K.

Species coexist using the same nutritional resource by partitioning it either in space or time, but few studies explore how species-specific nutritional requirements allow partitioning. Zaprionus indianus and Drosophila simulans co-exist in figs by invading the fruit at different stages; Z. indianus colonizes ripe figs, whereas D. simulans oviposits in decaying fruit. Larvae feed on yeast growing on the fruit, which serves as their primary protein source. Because yeast populations increase as fruit decays, we find that ripe fruit has lower protein content than rotting fruit. Therefore, we hypothesized that Z. indianus and D. simulans larvae differ in their dietary requirements for protein. We used nutritional geometry to assess the effects of protein and carbohydrate concentration in the larval diet on life history characters in both species. Survival, development time, and ovariole number respond differently to the composition of the larval diet, with Z. indianus generally performing better across a wider range of protein concentrations. Correspondingly, we found that Z. indianus females preferred to lay eggs on low protein foods, while D. simulans females chose higher protein foods for oviposition when competing with Z. indianus. We propose the different nutritional requirements and oviposition preference of these two species allows them to temporally partition their habitat.

2015-11Journal article

Open access

Drosophila melanogaster larvae make nutritional choices that minimize developmental time

Publication . Rodrigues, Marisa A.; Martins, Nelson E.; Balancé, Lara F.; Broom, Lara N.; Dias, António J.S.; Fernandes, Ana Sofia D.; Rodrigues, Fábio; Sucena, Élio; Mirth, Christen K.

Organisms from slime moulds to humans carefully regulate their macronutrient intake to optimize a wide range of life history characters including survival, stress resistance, and reproductive success. However, life history characters often differ in their response to nutrition, forcing organisms to make foraging decisions while balancing the trade-offs between these effects. To date, we have a limited understanding of how the nutritional environment shapes the relationship between life history characters and foraging decisions. To gain insight into the problem, we used a geometric framework for nutrition to assess how the protein and carbohydrate content of the larval diet affected key life history traits in the fruit fly, Drosophila melanogaster. In no-choice assays, survival from egg to pupae, female and male body size, and ovariole number - a proxy for female fecundity - were maximized at the highest protein to carbohydrate (P:C) ratio (1.5:1). In contrast, development time was minimized at intermediate P:C ratios, around 1:2. Next, we subjected larvae to two-choice tests to determine how they regulated their protein and carbohydrate intake in relation to these life history traits. Our results show that larvae targeted their consumption to P:C ratios that minimized development time. Finally, we examined whether adult females also chose to lay their eggs in the P:C ratios that minimized developmental time. Using a three-choice assay, we found that adult females preferentially laid their eggs in food P:C ratios that were suboptimal for all larval life history traits. Our results demonstrate that D. melanogaster larvae make foraging decisions that trade-off developmental time with body size, ovariole number, and survival. In addition, adult females make oviposition decisions that do not appear to benefit the larvae. We propose that these decisions may reflect the living nature of the larval nutritional environment in rotting fruit. These studies illustrate the interaction between the nutritional environment, life history traits, and foraging choices in D. melanogaster, and lend insight into the ecology of their foraging decisions.

2015-07-04Journal article

Open access

The Ol1mpiad: concordance of behavioural faculties of stage 1 and stage 3 Drosophila larvae.

Publication . Almeida-Carvalho, Maria J.; Berh, Dimitri; Braun, Andreas; Chen, Yi-chun; Eichler, Katharina; Eschbach, Claire; Fritsch, Pauline M. J.; Gerber, Bertram; Hoyer, Nina; Jiang, Xiaoyi; Kleber, Jörg; Klämbt, Christian; König, Christian; Louis, Matthieu; Michels, Birgit; Miroschnikow, Anton; Mirth, Christen; Miura, Daisuke; Niewalda, Thomas; Otto, Nils; Paisios, Emmanouil; Pankratz, Michael J.; Petersen, Meike; Ramsperger, Noel; Randel, Nadine; Risse, Benjamin; Saumweber, Timo; Schlegel, Philipp; Schleyer, Michael; Soba, Peter; Sprecher, Simon G.; Tanimura, Teiichi; Thum, Andreas S.; Toshima, Naoko; Truman, Jim W.; Yarali, Ayse; Zlatic, Marta

Mapping brain function to brain structure is a fundamental task for neuroscience. For such an endeavour, the Drosophila larva is simple enough to be tractable, yet complex enough to be interesting. It features about 10,000 neurons and is capable of various taxes, kineses and Pavlovian conditioning. All its neurons are currently being mapped into a light-microscopical atlas, and Gal4 strains are being generated to experimentally access neurons one at a time. In addition, an electron microscopic reconstruction of its nervous system seems within reach. Notably, this electron microscope-based connectome is being drafted for a stage 1 larva - because stage 1 larvae are much smaller than stage 3 larvae. However, most behaviour analyses have been performed for stage 3 larvae because their larger size makes them easier to handle and observe. It is therefore warranted to either redo the electron microscopic reconstruction for a stage 3 larva or to survey the behavioural faculties of stage 1 larvae. We provide the latter. In a community-based approach we called the Ol1mpiad, we probed stage 1 Drosophila larvae for free locomotion, feeding, responsiveness to substrate vibration, gentle and nociceptive touch, burrowing, olfactory preference and thermotaxis, light avoidance, gustatory choice of various tastants plus odour-taste associative learning, as well as light/dark-electric shock associative learning. Quantitatively, stage 1 larvae show lower scores in most tasks, arguably because of their smaller size and lower speed. Qualitatively, however, stage 1 larvae perform strikingly similar to stage 3 larvae in almost all cases. These results bolster confidence in mapping brain structure and behaviour across developmental stages.

2017-07-05Journal article

Open access

Coordinating morphology with behavior during development: an integrative approach from a fly perspective

Publication . Carvalho, Maria João A.; Mirth, Christen K.

Animals in the wild live in highly variable and unpredictable environments. This variation in their habitat induces animals, at all stages of their development, to make decisions about what to eat, where to live, and with whom to associate. Additionally, animals like insects show dramatic restructuring of their morphology across life stages, which is accompanied by alterations in their behavior to match stage-specific functions. Finally, in a process called developmental plasticity, environmental conditions feed back onto developmental mechanisms producing animals with stage-specific variation in both morphological and behavioral traits. In this review, we use examples from insects to explore the idea that animals are integrated units where stage-specific morphological and neurological traits develop together to increase individual fitness within their natural environments. We hypothesize that the same mechanisms act to alter both morphological and behavioral traits in response to the environment in which an organism develops. For example, in insects the steroid hormone ecdysone orchestrates the restructuring of the body from larva to adult form during metamorphosis at the same time as it rebuilds the central nervous system. The remodeling of both body form and nervous system structure results in behavioral alterations that match the morphological functions of the emerging adult. We review relevant findings from the fruit fly Drosophila melanogaster, combining insights from different fields like developmental biology, neurobiology and developmental plasticity. Finally, we highlight how insights drawn from D. melanogaster can be used as a model in future efforts to understand how developmental processes modify behavioral responses to environmental change in a stage-specific manner in other animals.

2015-02-03Journal article

Open access