The evolution of sex peptide: sexual conflict, cooperation, and coevolution

Abstract

A central paradigm in evolutionary biology is that the fundamental divergence in the fitness interests of the sexes ('sexual conflict') can lead to both the evolution of sex-specific traits that reduce fitness for individuals of the opposite sex, and sexually antagonistic coevolution between the sexes. However, clear examples of traits that evolved in this way - where a single trait in one sex demonstrably depresses the fitness of members of the opposite sex, resulting in antagonistic coevolution - are rare. The Drosophila seminal protein 'sex peptide' (SP) is perhaps the most widely cited example of a trait that appears to harm females while benefitting males. Transferred in the ejaculate by males during mating, SP triggers profound and wide-ranging changes in female behaviour and physiology. Early studies reported that the transfer of SP enhances male fitness while depressing female fitness, providing the foundations for the widespread view that SP has evolved to manipulate females for male benefit. Here, we argue that this view is (i) a simplification of a wider body of contradictory empirical research, (ii) narrow with respect to theory describing the origin and maintenance of sexually selected traits, and (iii) hard to reconcile with what we know of the evolutionary history of SP's effects on females. We begin by charting the history of thought regarding SP, both at proximate (its production, function, and mechanism of action) and ultimate (its fitness consequences and evolutionary history) levels, reviewing how studies of SP were central to the development of the field of sexual conflict. We describe a prevailing paradigm for SP's evolution: that SP originated and continues to evolve to manipulate females for male benefit. In contrast to this view, we argue on three grounds that the weight of evidence does not support the view that receipt of SP decreases female fitness: (i) results from studies of SP's impact on female fitness are mixed and more often neutral or positive, with fitness costs emerging only under nutritional extremes; (ii) whether costs from SP are appreciable in wild-living populations remains untested; and (iii) recently described confounds in genetic manipulations of SP raise the possibility that measures of the costs and benefits of SP have been distorted. Beyond SP's fitness effects, comparative and genetic data are also difficult to square with the idea that females suffer fitness costs from SP. Instead, these data - from functional and evolutionary genetics and the neural circuitry of female responses to SP - suggest an evolutionary history involving the evolution of a dedicated SP-sensing apparatus in the female reproductive tract that is likely to have evolved because it benefits females, rather than harms them. We end by exploring theory and evidence that SP benefits females by functioning as a signal of male quality or of sperm receipt and storage (or both). The expanded view of the evolution of SP that we outline recognises the context-dependent and fluctuating roles played by both cooperative and antagonistic selection in the origin and maintenance of reproductive traits.

Keywords: coevolution; condition dependence; ejaculates; post-mating responses; seminal fluid; sex peptide; sexual conflict; sexual selection; signalling; sperm competition.

Fig. 1

A wide variety of behavioural and physiological changes take place in females upon receipt of sex peptide (SP), including shifts in feeding (Carvalho et al., ; Ribeiro & Dickson, ; Walker et al., 2015), memory (Scheunemann et al., 2019), sleep and movement (Isaac et al., 2010), aggression (Bath et al., 2017), sexual receptivity and egg‐laying (Chen et al., ; Aigaki et al., ; Chapman et al., ; Liu & Kubli, 2003), gut activity (Cognigni et al., ; Reiff et al., ; White et al., 2021), sperm use (Avila et al., 2010), immune activity (Peng et al., ; Domanitskaya et al., ; Schwenke & Lazzaro, 2017), and, presumably underlying much of this, changes in gene expression (Gioti et al., 2012) and endocrine activity (Soller et al., 1999). Figure adapted from the Hallmarks of Cancer: Circle template, by BioRender.com. Retrieved from https://app.biorender.com/biorender‐templates.

Fig. 2

(A) Hypothetical fitness curves that illustrate how the fitness benefits of short‐term support of female reproduction by sex peptide (SP) could be offset by reduced long‐term gains (e.g. due to accelerated reproductive ageing or early death). A female that receives SP (blue) initially shows a greater rate of offspring production compared to a female that does not (gold). However, the female that does not receive SP continues to produce offspring over a longer period, perhaps due to a longer lifespan. The conclusion we reach about whether SP increases or decreases female fitness will depend on whether we measure female offspring production up to, or the female dies at, point t or t + 1. (B) The weight of evidence is consistent with a model by which the sign and magnitude of female fitness outcomes from receipt of SP depend on the quality of a female's diet. A positive effect is experienced on intermediate diets with neutral effects under limited nutrient availability and negative effects at excess nutrient availability (Wigby & Chapman, ; Rogina, ; Fricke et al., 2010). The effects of SP are presented relative to females that do not receive SP.

Fig. 3

Loss of sex peptide (SP) disrupts the structure of seminal microcarriers and changes seminal fluid composition (Wainwright et al., 2021). (i) SP is produced in the male accessory glands, a pair of seminal fluid‐producing glands that branch off from the ejaculatory duct at the base of the testes. (ii) Within the lumen of the male accessory gland, SP (green) is carried on lipid‐containing microcarriers. Microcarriers are transferred to females during mating and rapidly disassemble within the female reproductive tract. SP is integral to their normal assembly and disassembly. (iii) In the absence of SP, microcarriers fail to form correctly and are highly enlarged. (iv) In normal matings, males transfer a suite of seminal proteins (coloured circles), including SP, and sperm to females. (v) When SP is absent, the dysfunction in microcarriers leads to changes in the composition of the seminal proteome. Some seminal fluid proteins (SFPs) are transferred in greater quantities, others are reduced. (vi) Seminal proteins and sperm are transferred to the female. (vii) In normal matings, some SP enters directly into the female haemolymph shortly after mating. SP also binds to the surface of sperm, a process facilitated by a network of male‐derived, co‐factor ‘network proteins’. Sperm, along with bound SP, are transported into the storage organs: the seminal receptacle and paired spermathecae. Here, SP is required for the long‐term, multi‐day maintenance of post‐mating responses, as well as the normal release and use of sperm from storage. (viii) Although sperm accumulation into storage is not affected by the absence of SP, the subsequent release of sperm is reduced and the duration of post‐mating responses is truncated (Avila et al., 2010).

Fig. 4

(A) The sex peptide (SP)‐sensing apparatus within the female reproductive tract consists of two bilateral clusters of three sex peptide receptor (SPR)‐expressing neurons (Häsemeyer et al., ; Yang et al., ; Rezával et al., 2012). These neurons are necessary and sufficient for the reduction in receptivity and stimulation of egg‐laying induced by SP and co‐express doublesex, fruitless, and pickpocket. Figure redrawn and modified from Rezával et al. (2012). (B) A schematic of the neural circuitry underlying the female post‐mating response, modified from Jang et al. (2017). SP enters the uterus where it is detected by SP‐sensing neurons (see A). Myoinhibitory peptide (MIP)‐expressing interneurons relay the detection of SP to SP abdominal ganglion neurons, which in turn extend to the brain.