Chapter One - Neurogenetics of Female Reproductive Behaviors in Drosophila melanogaster
Introduction
The study of the genetics of the vinegar fly Drosophila melanogaster has taught us a lot about the mechanisms that control reproductive behaviors. Male reproductive behavior in particular has been dissected using the fine scalpel of genetics for many decades. This approach has yielded tremendous insights in the cellular and physiological mechanisms underlying sensory transduction, as well as the neuronal connectivity and processing underlying male sexual behavior, providing general lessons for understanding the mechanistic and evolutionary basis of behavior (for recent reviews, see Billeter & Levine, 2013; Dickson, 2008; Pavlou & Goodwin, 2013; Siwicki & Kravitz, 2009; Villella & Hall, 2008; Yamamoto & Koganezawa, 2013). However, when it comes to understanding reproductive behaviors, the complement of this story is missing as we have inadequate knowledge of how females receive and interpret information communicated by males (Ferveur, 2010). This asymmetric level of understanding hampers the study of the interactive processes fundamental to sexual communication and reproduction.
The importance of studying female reproductive behaviors is obvious. From an ultimate perspective, understanding female mate choice is important for our understanding of the evolutionary process. Females are the gatekeeper of gene flow between species and show strong behavioral isolation when courted by nonconspecifics. Understanding the reproductive behaviors of D. melanogaster females thus not only sheds light on the genetic architecture of species-specific behavior, the molecular and neural basis of conspecific interactions, and the processes of selection within this species; but it also holds the key to evolutionary questions such as species formation and isolation by means of sexual selection. From a proximate perspective, one of the outstanding challenges of neuroscience is to understand how individuals identify others (e.g., member of the same species, sex, kin versus unrelated individuals, and familiar versus novel) and treat them differentially on the basis of their own identity (e.g., their genotype, sex, and experience) (Insel, 2010). Drosophila female reproductive behavior is a particularly ideal system in which to unravel such a quandary. The female brain must receive complex sensory signals about conspecifics, the physical environment, and her internal state; and process the information to control the differential treatment of individuals in a given social environment. What is perhaps less well appreciated is that females continue their choosy reproductive behavior beyond mate choice into postcopulatory feeding habits and choice of egg-laying sites. The study of female behaviors thus has the potential to tell us how complex cues from various sources are sensed, and how this information is integrated and processed, ultimately leading to a variety of behavioral outputs.
Here we attempt to review what we know about the genetic, cellular, and chemical basis of female reproductive behaviors: how virgin females locate their habitat, select their first love, and transition into maternal behaviors. While writing this review, we noticed that genetic and neurobiological data on female behavior is often missing or anecdotal. As in-depth neurobiological studies of the female nervous system and the behaviors it supports are slowly beginning to emerge, we hope that this review, which contains more questions than hard facts, will isolate gaps in our knowledge that should be filled. We highlight evolutionary studies in female behavior that have postulated many interesting features of female reproductive neurobiology, whose mechanistic basis is still unknown. By intersecting work generated from a more evolutionary angle with work aimed at a stronger mechanistic understanding of the neurogenetic and neurobiological basis of female reproductive behaviors, we hope to highlight potential new areas we hope it will spur greater dialog between evolution and neurosciences. By trying to be Jack of all Trades, we are bound to miss several works of importance, and more worryingly, to have made some factual mistakes. We apologize in advance to those colleagues whose work we have overlooked.
We have structured this chapter around an imaginary adult female, whom we will follow from the moment of her choosing of a local habitat (Section 2). We next see how, once settled, she chooses her first mate (Section 3), transitions into producing offspring (Section 4) or chooses to mate with more males (Section 5), to finish on her choice of a site to have offspring (Section 6).
Section snippets
Habitat Selection
Drosophila melanogaster females feed, mate, and produce progeny on the same site predictive of a strong interplay between habitat and behavior (Ferveur, 2010; Markow & O’Grady, 2005, 2008; Spieth, 1974; Zhu, Park, & Baker, 2003). The strong association of D. melanogaster with human activities, such as wine making and agriculture, probably explains how flies are introduced into new areas and why they are found throughout the world (Keller, 2007). Habitat selection for fruit flies might be as
First Love
Once landing on a fruit fly-colonized food patch, females are almost immediately courted by males (Wertheim et al., 2006). Despite the lack of conspicuous solicitation behavior by females, males are drawn to them and display intense courtship. Male courtship consists of approaching the female, mostly from the back, tapping her abdomen, extending one wing, and vibrating it to produce a song, circling the female while doing so, extending his proboscis to make contact with the female genitals and
The Postmating Response
A mated female is fundamentally different from a virgin. Once mated, females exhibit a host of changes at almost all systemic levels. Compared to a virgin, a mated female has a different transcriptome, proteome, pattern of neuronal activity, and exhibits different behaviors. The postmating response (PMR) is a collection of behaviors that are consistently produced by mated females. In the literature, the classic PMR highlights two main behavioral changes: virgin females are sexually receptive
Female Postcopulatory Mate Choice: Cryptic vs Noncryptic
It is not always appreciated that sexual selection continues after copulation. What the female does after the virginal mating, and each subsequent mating, can impact the fertilization success of the first male she mated with. Postcopulatory mate choice (PCMC) is any decision regarding reproductive behavior that is made after mating and includes not only decisions that can be clearly observed such as the degree to which a female is polyandrous (noncryptic PCMC) but also decisions that are made
Egg-Laying and Oviposition Site Selection
After successful copulation, ovulation, and fertilization of an egg, females must start the process of oviposition site selection. This choice represents the only form of overt maternal care that Drosophila mothers extend to their offspring because once laid, a Drosophila egg is left to its own devises. The developmental time from egg to larva is about 22 h at 24 °C (Markow, Beall, & Matzkin, 2009). The larva that will hatch from this egg will therefore experience the microenvironment that its
Conclusion
In this chapter, we set out to review female reproductive behavior not only considering the ultimate and proximate perspective but also an integration of the two. We compiled the literature regarding the genetic, cellular, and chemical basis of how females make decisions that influence not only herself but also the genotype and environment of her offspring in hope of resolving the evolutionary processes that contribute to species-wide behavior. One apparent theme that occurred but was not
Acknowledgments
We thank Bregje Wertheim and Joel Levine for feedback on some of the sections of this review. ML and JCB are funded by an Open Programma grant from the Dutch organization for scientific research (NWO).
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2021, Advances in Insect PhysiologyCitation Excerpt :It is not known if specific aspects of male courtship elicit immature rejection and which sensory modalities are involved. The neuronal control of female receptivity has been studied in great detail, but mostly in mature virgins and mated females, and with a focus on how the nervous system mediates the transition between these two stages (the so-called post-mating switch) (reviewed in: Aranha and Vasconcelos, 2018; Ellendersen and von Philipsborn, 2017; Ishimoto and Kamikouchi, 2021; Laturney and Billeter, 2014; von Philipsborn, 2020). Since mated females and immature virgins respond to male courtship in a different way, with ovipositor extrusion and rejection wing flicks, respectively, there is the notion that the low receptivity in these two types of females depends on different neuronal mechanisms.
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2017, Current Opinion in Insect ScienceCitation Excerpt :Drosophila courtship is close range, with the male following the female, singing by wing vibration, tapping her with his foreleg, licking her genitalia and attempting copulation. Receptive virgins accept males by slowing down, pausing and opening of the vaginal plates [17,18]. The two male stimuli thought to be most important (since required for a swift acceptance response), courtship song and the pheromone cis-vaccenyl acetate (cVA), are relayed by interconnected neurons narrowly tuned to the stimulus, so called ‘labelled lines’ [19–21], and likely to be integrated by Dsx+ brain neuronal class pC1.