Niche construction initiates the evolution of mutualistic interactions

Buser, Claudia C.; Newcomb, Richard D.; Gaskett, Anne C.; Goddard, Matthew R.

doi:10.1111/ele.12331

Cited by 112 publications

(146 citation statements)

References 54 publications

(167 reference statements)

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“…P:C 1:10 to P:C 10,000:1 over the course of 27 days, with P and C concentrations varying between 10 and 10,000 g l −1 (Matavelli et al, 2015). These nutritional modifications of food resources are likely favoured by the fact that females inoculate the fruit substrate with yeast during oviposition (Buser et al, 2014;Stamps et al, 2012) and tend to lay eggs in aggregations (Navarro and del Solar, 1975;Prokopy and Roitberg, 2001;Wertheim et al, 2005; see also experiment 2). In many cases, multiple fly species may also breed in the same fruits (Matavelli et al, 2015).…”

Section: Discussionmentioning

confidence: 97%

Drosophila females trade off good nutrition with high quality oviposition sites when choosing foods

Lihoreau

Poissonnier

Isabel

et al. 2016

Journal of Experimental Biology

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Animals, from insects to humans, select foods to regulate their acquisition of key nutrients in amounts and balances that maximise fitness. In species in which the nutrition of juveniles depends on parents, adults must make challenging foraging decisions that simultaneously address their own nutrient needs as well as those of their progeny. Here, we examined how the fruit fly Drosophila melanogaster, a species in which individuals eat and lay eggs in decaying fruits, integrate feeding decisions (individual nutrition) and oviposition decisions (offspring nutrition) when foraging. Using cafeteria assays with artificial diets varying in concentrations and ratios of protein to carbohydrates, we show that D. melanogaster females exhibit complex foraging patterns, alternating between laying eggs on high carbohydrate foods and feeding on foods with different nutrient contents depending on their own nutritional state. Although larvae showed faster development on high protein foods, both survival and learning performance were higher on balanced foods. We suggest that the apparent mismatch between the oviposition preference of females for high carbohydrate foods and the high performances of larvae on balanced foods reflects a natural situation where high carbohydrate ripened fruits gradually enrich in proteinaceous yeast as they start rotting, thereby yielding optimal nutrition for the developing larvae. Our findings that animals with rudimentary parental care uncouple feeding and egg-laying decisions in order to balance their own diet and provide a nutritionally optimal environment to their progeny reveal unsuspected levels of complexity in the nutritional ecology of parent-offspring interactions.

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Section: Discussionmentioning

confidence: 97%

Drosophila females trade off good nutrition with high quality oviposition sites when choosing foods

Lihoreau

Poissonnier

Isabel

et al. 2016

Journal of Experimental Biology

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“…The apparent absence of a taxonomically defined core microbiota in Drosophila (21) suggests that such coevolutionary interactions would be diffuse, involving guilds of microorganisms interacting with multiple animal taxa associated with a diversity of fruits. In addition, Drosophila-associated yeasts have been proposed to modify the fruit habitat to the benefit of Drosophila, a process interpreted as niche construction, and release volatiles that are utilized as foraging and oviposition cues by the insect host (41). Bacterial partners may also contribute to these effects.…”

Section: Discussionmentioning

confidence: 99%

The Host as the Driver of the Microbiota in the Gut and External Environment of Drosophila melanogaster

Wong

Luo

Jing

et al. 2015

Appl Environ Microbiol

118

120

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Most associations between animals and their gut microbiota are dynamic, involving sustained transfer of food-associated microbial cells into the gut and shedding of microorganisms into the external environment with feces, but the interacting effects of host and microbial factors on the composition of the internal and external microbial communities are poorly understood. This study on laboratory cultures of the fruit fly Drosophila melanogaster reared in continuous contact with their food revealed timedependent changes of the microbial communities in the food that were strongly influenced by the presence and abundance of Drosophila. When germfree Drosophila eggs were aseptically added to nonsterile food, the microbiota in the food and flies converged to a composition dramatically different from that in fly-free food, showing that Drosophila has microbiota-independent effects on the food microbiota. The microbiota in both the flies that developed from unmanipulated eggs (bearing microorganisms) and the associated food was dominated by the bacteria most abundant on the eggs, demonstrating effective vertical transmission via surface contamination of eggs. Food coinoculated with a four-species defined bacterial community of Acetobacter and Lactobacillus species revealed the progressive elimination of Lactobacillus from the food bearing few or no Drosophila, indicating the presence of antagonistic interactions between Acetobacter and Lactobacillus. Drosophila at high densities ameliorated the Acetobacter/Lactobacillus antagonism, enabling Lactobacillus to persist. This study with Drosophila demonstrates how animals can have major, coordinated effects on the composition of microbial communities in the gut and immediate environment. F rom a microbiological perspective, an animal is a transient, nutrient-rich patch. The capacity of various microorganisms to exploit the animal habitat involves multiple traits, including mechanisms that evade or modulate the animal immune system (1-3) and metabolic adaptations to utilize host resources (4, 5). Animal-associated microorganisms include pathogens, whose fitness is coupled to host disease and debility, and beneficial forms that variously contribute nutrients, confer protection, and deliver effectors that promote host performance (6). Consequently, the composition of animal-associated microorganisms is an important determinant of animal fitness.Many animal-microbe associations are open systems, meaning that external microorganisms have access to the host habitat and members of the host microbiota are released back to the external environment via feces, sloughed skin, fluid secretions, etc. (7). Open symbioses can be invaded by external microorganisms that are compatible with the host and are competitive with resident microbiota. As a result, the host is potentially more exposed to parasites and cheats than in a closed system but also has an enhanced capacity to modify the composition of its microbiota adaptively to changes in environmental circumstances (8, 9). The shedding of ...

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“…While yeasts are the major source of protein for Drosophilids, the flies, in turn, are the major inoculators of yeasts in the fruits and the primary vectors for yeast dispersal (Begon, 1982;Buser et al, 2014). Furthermore, different species of Drosophilids prefer to consume different species of yeasts (Dobzhansky, 1956;Phaff et al, 1956;Fogleman et al, 1981;Morais et al, 1995;Barker and Starmer, 1999).…”

Section: Discussionmentioning

confidence: 99%

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

Matavelli

Carvalho

Martins

et al. 2015

Journal of Insect Physiology

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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.

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Niche construction initiates the evolution of mutualistic interactions

Cited by 112 publications

References 54 publications

Drosophila females trade off good nutrition with high quality oviposition sites when choosing foods

Drosophila females trade off good nutrition with high quality oviposition sites when choosing foods

The Host as the Driver of the Microbiota in the Gut and External Environment of Drosophila melanogaster

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

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