Male sexual behaviour and ethanol consumption from an evolutionary perspective: A comment on “Sexual Deprivation Increases Ethanol Intake in Drosophila”

Abstract

Shohat-Ophir et al.¹ demonstrate a connection between sexual behaviour and ethanol consumption in male Drosophila flies, and how the neuropeptide F system regulates ethanol preference. Their results are rightly discussed only in a physiological context, but this has facilitated erroneous anthropomorphic interpretations by the media. Here we discuss the link between male sexual behaviour and ethanol consumption from an evolutionary perspective, providing a broader context to interpret their results.

In their paper, Shohat-Ophir et al.¹ show that rejected virgin fruit fly males are more prone to consume ethanol than mated males. The authors present a series of elegant experiments in which they disentangle the potential factors involved in this ethanol preference, concluding that sexual deprivation is the major factor. Then, the authors focused on the neuropeptide F (NPF)-NPF receptor (NPFR) system as a potential mediator of both the effects of sexual experience and ethanol preference in Drosophila. Using several experimental approaches, Shohat-Ophir et al.¹ found a causal relationship between sexual experience, NPF levels and ethanol preference. Furthermore, using independent assays they show that mating, ethanol intoxication and the activation of the NPF-NPFR pathway are rewarding experiences to male flies. Altogether, these results are an important contribution to understanding a physiological link between social experiences and drug reward.

Because the authors' objective was to understand the role of the neuropeptide F system as a regulator of ethanol consumption, their results were discussed only in a physiological context. This has facilitated erroneous anthropomorphic interpretations by the media.^2-11 We believe that an ecological and evolutionary perspective is important to understand why virgin male flies are attracted to alcohol and why this attraction cannot be compared to alcohol consumption in humans.

The use of model species has certainly advanced our knowledge of how animals function in different situations. For example, using Drosophila to determine the physiological mechanisms that underline addiction to ethanol can inform us how alcohol consumption exerts its addictive properties in mammalian systems, including humans. However, it is perilous to ignore the evolution and ecology of each species. Although humans have a similar rewarding system that regulates both sexual experiences and ethanol consumption (the neuropeptide Y,^12,13) the relationship that humans and flies have with ethanol is very different. Therefore it is erroneous to suggest that, because alcoholism is harmful to humans, ethanol consumption by sexually deprived males is negative for flies (i.e..¹⁴)

In their natural habitat, Drosophila flies are exposed to environmental alcohol, including ethanol, in all stages of their life history because it is strongly associated with food resources.^15-18 Females show a clear preference to oviposit onto fermenting fruits, larvae develop to adulthood in this substrate, and courtship and mating also takes place there.^19-22 It is not surprising that D. melanogaster shows a strong tolerance to high ethanol concentrations, given that ethanol metabolism was selected to improve the use of rich sugary environments.^23-25 Indeed, ethanol is more caloric than unfermented carbohydrates, and flies are able to use ethanol as an energy source.^18,26

The evolution of an efficient alcohol metabolism in Drosophila has maximised the fitness benefits from being exposed to environmental alcohol. Tolerance of Drosophila to high ethanol levels has evolved both naturally (populations in wineries show higher tolerance to ethanol than populations from other areas^27,28,29), and artificially (populations have been selected to increase tolerance to alcohol²⁶),. Flies that live in low concentrations of ethanol have better survival and increased longevity than flies that lack ethanol in their environment.^30-32 Although high concentrations of ethanol can be toxic, Drosophila can develop tolerance to ethanol, so that they improve recovery after subsequent ethanol consumption.³³ Furthermore, Drosophila consume ethanol to self-medicate against parasites³⁴ and they can balance the concentration of ethanol intake to avoid harmful intoxication.³⁴

In Drosophila, it is likely that the NPF pathway has evolved as a natural reward pathway ¹, because finding and consuming ethanol benefits flies. The fact that males with low reproductive success are more attracted to food with ethanol than males with high reproductive success¹ reflects, in our view, a behaviour that is only part of a complex process of adaptation to ethanol rich habitats. Thus, in the ecological context we outlined above, by eating ethanol-enriched food, which is more nutritious than food lacking alcohol, virgin males might increase their fitness, which may positively affect their mating success in the future.³⁵ For example, an increase in food quality could improve male courtship displays in subsequent encounters with females, and could allow males to keep courting for longer if receptive females are scarce in the environment. Increased fitness may also positively affect sperm production.

We note that the levels of alcohol used in Shohat-Ophir et al.¹ are well above anything that Drosophila would encounter in nature (15% ethanol in Shohat-Ophir et al. study vs 6% in rotting fruits.³⁶) It is possible that virgin males are keen to pay the costs of consuming high concentrations of ethanol if ethanol-enriched food is more caloric than food without ethanol (i.e. a trade-off between current and future reproduction³⁵),. This idea can be tested by investigating whether rejected males prefer higher calorie food when given food with different caloric values but without ethanol, and how this enhanced feeding regime affects courtship display in virgin males. Virgin males could also be more attracted to ethanol than mated males because ethanol not only signals food but the congregation of other flies, including females. In this circumstance,¹ an increased attraction to ethanol may increase the probability to encounter a potential mate. It would also be interesting to test whether females are more attracted to males that smell like ethanol than males that lack that odour. A male that can bear the costs of consuming high concentration of ethanol and still be able to court females could be signalling higher levels of fitness to a females.³⁷ This can be easily tested by allowing females to choose between males that experimentally differ in the concentration of ethanol on their cuticle.

Because the neuropeptide Y is the NPF homolog in mammals,^12,13 it is easy to interpret Shohat-Ophir et al.'s results in the context of what human experience with ethanol intoxication. Indeed, this is the general interpretation by the media and the public: associating sexual deprivation and ethanol intoxication between humans and flies without considering their obvious ecological and evolutionary differences.^2-11 We believe that comparing the physiology involved in the regulation of reward systems in both flies and mammals could be an effective way of increasing our understanding of how addictions work in humans. However, anthropomorphic interpretations of results obtained using animals without considering their evolutionary history and ecology could have negative consequences, not only for scientists, by biasing their research questions in function of those anthropomorphisms, but also to the general public, that lacks a clear understanding of how different behaviours evolve.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.