Mating Behavior: When structure meets function
A new study upturns the long-held belief that in fruit flies, the yellow gene determines sex-specific behaviors by acting in the brain.
- North Dakota State University, United States
It is a truism to say that in many organisms, body structure matters for behavior: jumping is not possible without legs, or flying without wings. However, scientists sometimes overlook morphology when trying to understand behavior, preferring instead to favor explanations that involve the brain and the nervous system. For instance, for decades it was thought that the yellow gene in fruit flies, which gives them their black color, was important for courtship behaviors because it is also expressed in the central nervous system (Drapeau et al., 2003; Drapeau et al., 2006). Male flies deficient in this gene mate less, and it was assumed that this was a consequence of changes in the neuronal wiring of the behavior controlled by yellow.
This makes intuitive sense in many ways because pigmentation genes such as yellow are derived from – and can bind to – dopamine, a chemical that has many neurological roles. However, in addition to creating color, pigments can also shape the structural properties of the external skeleton (Wittkopp and Beldade, 2009). Now in eLife, Patricia Wittkopp (University of Michigan), David Stern (Janelia Research Campus) and colleagues, including Jonathan Massey as first author, report the results of elegant experiments that rule out a neurological role for yellow in altering courtship behavior (Massey et al., 2019).
During courtship, male fruit flies perform a number of actions such as singing and extending their wings. Massey et al. found that the insects that lacked yellow also displayed the same mating behaviors, but they spent less time initiating copulation with females. This suggests that yellow might be important for this process, so the researchers set out to identify the types of cells in which the absence of yellow would have an impact on the beginning of copulation. They used two genes which regulate sex-specific behaviors and sexual dimorphism to manipulate where yellow was expressed in the body. Fruitless controls the expression of yellow in the central nervous system of larvae, while doublesex acts indirectly on yellow and is responsible, among other roles, for sex-specific pigmentation (Drapeau et al., 2006; Kopp et al., 2000; Williams et al., 2008; Signor et al., 2016).
First, flies were genetically engineered so that yellow was only expressed in the central nervous system, under the control of fruitless. This did not restore normal mating behavior. Massey et al. then used doublesex to control the expression of yellow. When the gene was not expressed in the tissues where doublesex is present, the flies failed to start mating; however, they also showed lack of mating when yellow was expressed in the nervous system under the control of doublesex. The insects only mated normally when yellow was expressed in other, non-neuronal cells.
To find out which non-neuronal cells might be responsible for the difference in mating success, Massey et al. examined the sequences that regulate the expression of doublesex, looking for regions that had an effect on reproductive behavior in male flies. A region was identified, which drove the expression of doublesex in the sex combs. This structure is formed of bristles on the forelegs of male flies and contains large amounts of melanin pigment. Removing the combs does not influence courtship behavior, but it does reduce mating success (Ng and Kopp, 2008). Moreover, it had been shown previously that the expression of doublesex is involved in the development and diversification of sex combs in fruit flies (Tanaka et al., 2011). In the latest work, Massey et al. showed that these structures are present when yellow is not expressed, but that they are not melanized: this prevents male flies from efficiently grasping female flies and starting to mate.
For many years, yellow was thought to influence courtship behavior through its expression in the central nervous system, and its role in the structural properties of the sex comb was entirely overlooked. By showing that neuronal sources of yellow do not affect courtship, the work of Massey et al. is both an exciting reminder that structure determines function, and a cautionary tale about the dangers of overlooking the physical aspects of behavior.
References
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Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropySeminars in Cell & Developmental Biology 20:65–71.https://doi.org/10.1016/j.semcdb.2008.10.002
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- Version of Record published: October 15, 2019 (version 1)
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© 2019, Signor
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Mating Behavior: When structure meets function
eLife 8:e51746.
https://doi.org/10.7554/eLife.51746
Further reading
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A hundred years after the discovery of yellow mutant flies, new experiments expose why they reproduce so badly.
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- Evolutionary Biology
- Genetics and Genomics
In many species, meiotic recombination events tend to occur in narrow intervals of the genome, known as hotspots. In humans and mice, double strand break (DSB) hotspot locations are determined by the DNA-binding specificity of the zinc finger array of the PRDM9 protein, which is rapidly evolving at residues in contact with DNA. Previous models explained this rapid evolution in terms of the need to restore PRDM9 binding sites lost to gene conversion over time, under the assumption that more PRDM9 binding always leads to more DSBs. This assumption, however, does not align with current evidence. Recent experimental work indicates that PRDM9 binding on both homologs facilitates DSB repair, and that the absence of sufficient symmetric binding disrupts meiosis. We therefore consider an alternative hypothesis: that rapid PRDM9 evolution is driven by the need to restore symmetric binding because of its role in coupling DSB formation and efficient repair. To this end, we model the evolution of PRDM9 from first principles: from its binding dynamics to the population genetic processes that govern the evolution of the zinc finger array and its binding sites. We show that the loss of a small number of strong binding sites leads to the use of a greater number of weaker ones, resulting in a sharp reduction in symmetric binding and favoring new PRDM9 alleles that restore the use of a smaller set of strong binding sites. This decrease, in turn, drives rapid PRDM9 evolutionary turnover. Our results therefore suggest that the advantage of new PRDM9 alleles is in limiting the number of binding sites used effectively, rather than in increasing net PRDM9 binding. By extension, our model suggests that the evolutionary advantage of hotspots may have been to increase the efficiency of DSB repair and/or homolog pairing.
