High fat diet alters Drosophila melanogaster sexual behavior and traits: decreased attractiveness and changes in pheromone profiles

Abstract

Sexual traits convey information about individual quality to potential mates. Environmental and genetic factors affect sexual trait expression and perception via effects on animal condition and health. High fat diet (HFD) is one environmental factor that adversely affects Drosophila melanogaster health, and its effects on animal health are mediated through conserved metabolic signaling pathways. HFD decreases female attractiveness, resulting in reduced male mating behaviors toward HFD females. HFD also affects the ability of males to judge mate attractiveness and likely alters fly condition and sexual traits to impact mating behavior. Here we show that HFD affects both visual (body size) and non-visual (pheromone profiles) sexual traits, which likely contribute to decreased fly attractiveness. We also demonstrate that adult-specific HFD effects on male mate preference can be rescued by changing metabolic signaling. These results demonstrate that HFD alters Drosophila sexual cues to reflect concurrent effects on condition and that less severe behavioral defects can be reversed by genetic manipulations that rescue fly health. This work expands on current knowledge of the role that metabolic signaling pathways play in linking animal health, sexual traits, and mating behavior, and provides a robust assay in a genetically tractable system to continue examining these processes.

Characterization of courtship behavior and copulation rate in adp60 mutant Drosophila melanogaster (Insecta: Diptera: Drosophilidae)

“…Surprisingly, courtship latency, and total courtship time, between the wildtype and adp 60 mutants were similar despite adp 60 exhibiting lower levels of courtship behaviors during courtship. Previous studies have shown that wildtype flies fed a high fat diet also accumulate triglycerides (but not glycogen) and have similar courtship latencies as wildtype flies fed a normal diet (Birse et al 2010;Schultzhaus et al 2017Schultzhaus et al , 2018. However, these high-fat fed flies have normal copulation frequencies (Schultzhaus et al 2017) unlike what was observed from our current study between adp 60 and wildtype flies (though Schultzhaus et al (2018) argues that high-fat fed flies are less attractive than wildtype flies fed a normal diet).…”

“…For the purposes of this study, wildtype female flies are used throughout in order to isolate any potential effects of the adp 60 mutation and obesity on male courtship decisions. Previous studies have shown that wildtype male flies fed a high-fat diet show no effect of the resulting obesity on reproductive behaviors if fed the high-fat diet throughout development (Schultzhaus et al 2017), but wildtype male flies do show reductions in some aspects of courtship if fed a high-fat diet only as an adult (Schultzhaus et al 2018). In both cases, however, copulation rate is not affected.…”

“…While much is known about the metabolic consequences due to the loss of the adipose gene, little is known about how the adp 60 mutation affects reproductive behaviors. Previous studies have characterized reproductive behaviors in flies with other metabolic perturbations such as wildtype flies with diet-induced obesity (Schultzhaus et al, 2017(Schultzhaus et al, , 2018, and characterizing the courtship of the adp 60 mutant, would complement these studies.…”

The effect of nutrient storage on courtship behavior and copulation frequency in the fruit fly, Drosophila melanogaster

“…For example, altering the amounts of protein and carbohydrates in the female diet will affect the rate of egg production in wild type D. melanogaster [30]. Schultzhaus [31] analyzed the effect of high fat diets on courtship in D. melanogaster and found that while feeding female flies a high fat diet had more negative effects on reproductive behavior than the same diet did on males, male judgment of female attractiveness was influenced by the high fat feeding. Considering only the wild type groups in the current study (food deprived, high fat fed, and normal fed), the nutrient storage data suggest that the reserves of glycogen, and not triglycerides, may serve as a cue for the change in sexual behavior we see in our study.…”

“…Size of the male could be another (see [25] for further discussion], as well as number or quality of the cuticular hydrocarbons, which are known chemical communicators between males and females and can be affected by nutritional regime (reviewed in [35]). While high fat diets are known to not alter male cuticular hydrocarbons [31], the effect of adp 60 and food deprivation is not known. Larger males may generally indicate better quality sperm based on nutrition; however, Partridge et al[25] also argued that larger males are more active and generally more persistent, so the increased copulation seen in the current study from the high fat fed group may be due to a form of male coercion.…”