Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene

Fitzpatrick, Mark; Feder, Elah; Rowe, Locke; Sokolowski, Marla B.

doi:10.1038/nature05764

Cited by 189 publications

(186 citation statements)

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“…The non-GFP males do not have this transgene, but are otherwise in the same foraging s wild-type background. These males were chosen because they had been shown to be equivalent despite the GFP transgene [33]. This experiment was otherwise performed and scored as in experiment 1.…”

Section: Methodsmentioning

confidence: 99%

Drosophila melanogaster females change mating behaviour and offspring production based on social context

et al. 2012

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In Drosophila melanogaster, biological rhythms, aggression and mating are modulated by group size and composition. However, the fitness significance of this group effect is unknown. By varying the composition of groups of males and females, we show that social context affects reproductive behaviour and offspring genetic diversity. Firstly, females mating with males from the same strain in the presence of males from a different strain are infecund, analogous to the Bruce effect in rodents, suggesting a social context-dependent inbreeding avoidance mechanism. Secondly, females mate more frequently in groups composed of males from more than one strain; this mitigates last male sperm precedence and increases offspring genetic diversity. However, smell-impaired Orco mutant females do not increase mating frequency according to group composition; this indicates that social context-dependent changes in reproductive behaviour depend on female olfaction, rather than direct male-male interactions. Further, variation in mating frequency in wild-type strains depends on females and not males. The data show that group composition can affect variance in the reproductive success of its members, and that females play a central role in this process. Social environment can thus influence the evolutionary process.

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Section: Methodsmentioning

confidence: 99%

Drosophila melanogaster females change mating behaviour and offspring production based on social context

et al. 2012

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“…Rover and sitter natural variants are described by Fitzpatrick et al (29). Fly populations were maintained in 50-mL plastic vials at 23°C on a 12:12 light/dark cycle, with 10 mL of food medium.…”

Section: Methodsmentioning

confidence: 99%

“…In these nutrient-poor environments, rover larvae have higher survivorship and faster development than sitter larvae when grown in groups composed of single variants (19). Although not examined in the present paper, complex interactions between for genotype and the nutritive and social environments can influence fitness (28,29).…”

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confidence: 96%

Gene–environment interplay inDrosophila melanogaster: Chronic food deprivation in early life affects adult exploratory and fitness traits

Burns

Svetec

Rowe

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Early life adversity has known impacts on adult health and behavior, yet little is known about the gene-environment interactions (GEIs) that underlie these consequences. We used the fruit fly Drosophila melanogaster to show that chronic early nutritional adversity interacts with rover and sitter allelic variants of foraging (for) to affect adult exploratory behavior, a phenotype that is critical for foraging, and reproductive fitness. Chronic nutritional adversity during adulthood did not affect rover or sitter adult exploratory behavior; however, early nutritional adversity in the larval period increased sitter but not rover adult exploratory behavior. Increasing for gene expression in the mushroom bodies, an important center of integration in the fly brain, changed the amount of exploratory behavior exhibited by sitter adults when they did not experience early nutritional adversity but had no effect in sitters that experienced early nutritional adversity. Manipulation of the larval nutritional environment also affected adult reproductive output of sitters but not rovers, indicating GEIs on fitness itself. The natural for variants are an excellent model to examine how GEIs underlie the biological embedding of early experience.genotype-environment interaction | plasticity T he question of how individual differences arise is fundamental to biology, psychology, and precision medicine (1, 2). From studies on mammals, we know that early adversity places individuals on developmental trajectories for health and behavior that can last a lifetime (3, 4). However, for the most part, this idea has not been investigated in simple model genetic organisms, such as the worm Caenorhabditis elegans or the fruit fly Drosophila melanogaster, in which gene manipulation can be readily accomplished. Two biological mechanisms that can underlie individual differences, and that go beyond the obsolete notion of nature or nurture, are gene-environment interactions (GEIs) and epigenetics. Here, we explore GEIs in the context of early adversity. In particular, we address how early adversity interacts with natural variants of the foraging (for) gene to affect adult behavior and fitness in D. melanogaster.Within human populations, nutritional adversity can lead to substantive effects on cognitive and behavioral development (5, 6). The question of how early adversities perturb normal development is a difficult one, because both the strength and timing of adversity can matter. For example, in humans, detrimental effects are seen after chronic protein or carbohydrate deprivation, yet one or a few acute deprivations have little long-term effect (7). Similarly, in fruit flies, levels of hemolymph carbohydrate affected by 3 h of food deprivation return to normal levels after just 2 h of refeeding (8). Moreover, not all individuals are affected equally by early nutritional adversity (9, 10), and these individual differences arise from GEIs.In evolutionary biology, GEIs can be important for the maintenance and expression of both phenotypic plasticit...

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“…The allele associated with higher levels of PKG ("rover"; for R ) results in larvae with longer foraging trails between food patches, whereas the allele associated with lower levels of PKG ("sitter"; for s ) results in larvae with shorter foraging trails; a mutant of for (for s2 ) generated in the for R background also displays shorter foraging trails. Different foraging patterns appear beneficial in discrete situations, so neither allele has achieved a consistent advantage, suggesting an explanation for their persistence over time (4). Interestingly, for is highly pleiotropic and is known to influence many behaviors in multiple species (5), including sleep (6, 7) and learning and memory (8), to name only a few.…”

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confidence: 99%

foraging alters resilience/vulnerability to sleep disruption and starvation in Drosophila

Donlea

Leahy

Thimgan

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Recent human studies suggest that genetic polymorphisms allow an individual to maintain optimal cognitive functioning during sleep deprivation. If such polymorphisms were not associated with additional costs, selective pressures would allow these alleles to spread through the population such that an evolutionary alternative to sleep would emerge. To determine whether there are indeed costs associated with resiliency to sleep loss, we challenged natural allelic variants of the foraging gene (for) with either sleep deprivation or starvation. Flies with high levels of Protein Kinase G (PKG) (for R ) do not display deficits in short-term memory following 12 h of sleep deprivation. However, short-term memory is significantly disrupted when for R flies are starved overnight. In contrast, flies with low levels of PKG (for s , for s2 ) show substantial deficits in short-term memory following sleep deprivation but retain their ability to learn after 12 h of starvation. We found that for R phenotypes could be largely recapitulated in for s flies by selectively increasing the level of PKG in the α/β lobes of the mushroom bodies, a structure known to regulate both sleep and memory. Together, these data indicate that whereas the expression of for may appear to provide resilience in one environmental context, it may confer an unexpected vulnerability in other situations. Understanding how these tradeoffs confer resilience or vulnerability to specific environmental challenges may provide additional clues as to why an evolutionary alternative to sleep has not emerged.A lthough sleep is a behavioral state that is conserved across a diverse range of species, the biological functions of sleep remain unknown. Sleep deprivation (SD) has been shown to negatively impact cognition, but individual responses to sleep loss can vary significantly within a population (1). Recent studies suggest that a portion of this variability may be influenced by genetic factors (2). For example, polymorphisms for PERIOD 3 (PER3), a circadian clock gene, can predict the magnitude of cognitive impairment and sleep homeostasis in response to a night of SD in humans (2). Although these genetic contributions may attenuate impairments following SD, the tradeoffs associated with resistance to sleep loss remain unknown. Presumably, the potential costs must be substantial. Thus, it is likely that the price of protection from sleep loss that can be conferred by allelic variation in one environment may induce a cost when manifested in a different environment. To date, putative costs of resiliency to sleep loss have not been identified in humans or any model organism.foraging (for), which codes for Protein Kinase G (PKG), is maintained in wild-type populations as a genetic polymorphism that results in either higher or lower levels of PKG activity (3). The allele associated with higher levels of PKG ("rover"; for R ) results in larvae with longer foraging trails between food patches, whereas the allele associated with lower levels of PKG ("sitter"; for s ) results i...

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Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene

Cited by 189 publications

References 29 publications

Drosophila melanogaster females change mating behaviour and offspring production based on social context

Drosophila melanogaster females change mating behaviour and offspring production based on social context

Gene–environment interplay inDrosophila melanogaster: Chronic food deprivation in early life affects adult exploratory and fitness traits

foraging alters resilience/vulnerability to sleep disruption and starvation in Drosophila

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