In many animal species, males guard females to prevent rivals from mating so that they can be sure that they fathered the female’s offspring. Some guarding methods work even when the male is not present. For example, the semen of some male insects contains chemicals known as antiaphrodisiacs that repel other males from females who have recently mated. Over the course of several days or weeks, the females expel or degrade the antiaphrodisiacs, making themselves attractive to other mates again. How long it takes to eliminate the antiaphrodisiacs depends on how much of the chemicals were deposited in the first place. Therefore, males could gain an advantage in fertilizing more eggs by depositing excess antiaphrodisiac to make the females unattractive to other mates for a long time.

The Western tarnished plant bug(Lygus hesperus) is an agricultural pest that targets cotton, strawberries and other crops. One antiaphrodisac had already been identified in the semen of male Lygus bugs. To investigate whether the males produced any others, Brent et al. tested the molecules emitted by recently mated females. This search identified another potential antiaphrodisiac. However, females are able to convert this second chemical into a third one that neither attracts nor repels males. This “anti-antiaphrodisiac” acts against the males’ two antiaphrodisiacs, and allows the females to more accurately signal when they are ready to mate again, giving them more control over their reproduction.

Anti-antiaphrodisiacs were not previously known to exist, but now that scientists know where to look, more are likely to be found in other species. A better understanding of how different chemicals interact to influence the mating behavior of insects could also lead to new methods of targeting pests of crops, which are safer for the environment than existing chemical pesticides.

Chemical signaling is an essential part of the regulation of mating in many insects, with a combination of pheromonal attractants and repellents indicating the suitability of prospective mates (Gillott, 2003). Several species have been shown to rely upon the transfer of an antiaphrodisiac from male to female during mating, the effect of which is to reduce the sexual attractiveness of females concurrent with a post-copulatory ovipositional period (Happ, 1969; Gilbert, 1976; Kukuk, 1985; Tompkins and Hall, 1981a, 1981b; Jallon et al., 1981; Scott, 1986; Andersson et al., 2000, 2003; Schulz et al., 2008; Yew et al., 2009). The mating male benefits from a reduced risk of sperm competition, while potential successor suitors avoid sperm competition as well as reduce the energetic costs and predation risks associated with courting a female that is unlikely to be receptive (Gillott, 2003; Malouines, 2016). Females benefit from this change in their chemical signature by a reduction in male harassment, which might otherwise negatively impact longevity, ovipositional opportunities, and predation avoidance (Forsberg and Wiklund, 1989; Magnhagen, 1991; Cook et al., 1994; Clutton-Brock and Langley, 1997; Bateman et al., 2006; den Hollander and Gwynne, 2009). This system is particularly useful for species in which females mate only once and for whom a protracted or permanent loss of attractiveness has no negative consequences (Gillott, 2003). Similarly, mated females can also cease releasing their attractant pheromones (Raina, 1989; Kingan et al., 1993; Ayasse et al., 1999; Eliyahu et al., 2003; Fukuyama et al., 2007; Oku and Yasuda, 2010), potentially adding to the impact of an antiaphrodisiac. However, in species with females that can or need to mate multiple times over their lives, the antiaphrodisiac might actually fail to accurately convey a female’s reproductive state to conspecific males (Malouines, 2016).

Often the antiaphrodisiac consists of just one or at most a few chemicals that are repellant to males (Jallon et al., 1981; Andersson et al., 2000; Schulz et al., 2008; Yew et al., 2009; Zawistowski and Richmond, 1986; Krueger et al., 2016) or that mask a female’s attractants (Andersson et al., 2003; Zhang and Aldrich, 2003; Zhang et al., 2007). These pheromones are emitted from the female over days or weeks until fully discharged or degraded, at which point the female can attract a new mate. One disadvantage of such a simple signaling system is that the amount of antiaphrodisiac being emitted by a female may not coincide with her readiness to mate again. A male’s maturity, health, or the interval between insemination events can all influence the amount of antiaphrodisiac that he can transfer along with his sperm. There is even evidence that males can intentionally bias the size of their spermatophore in response to female mating history and the local level of intrasexual competition (Larsdotter-Mellström et al., 2016). Such variability in the starting amount can result in a female being ready to mate well before a large load of antiaphrodisiac is sufficiently depleted for her to be attractive again, or being prematurely courted if the male transfers too little. Such signaling uncertainty is potentially costly to the fitness of both females and males, and should create selective pressure to produce a more accurate signaling system that incorporates information beyond the amount of remaining antiaphrodisiac (Estrada et al., 2011). To date, the only mechanism shown to allow females to counteract the effect of an antiaphrodisiac is in Drosophila, in which females actively eject mating-transferred cis-vaccenyl acetate from their reproductive tract (Laturney and Billeter, 2016).

Females of the western tarnished plant bug, Lygus hesperus Knight, are polyandrous, mating repeatedly throughout their lives to ensure a steady supply of sperm and to maintain an elevated rate of oviposition (Strong et al., 1970; Brent, 2010a; Brent and Spurgeon, 2011; Brent et al., 2011). Mating also causes these females to become less attractive than virgins to males (Strong et al., 1970; Brent, 2010a). A sex-pheromone has been identified for this species (Byers et al., 2013), but there is no evidence that the release rate of this chemical blend is affected by the mating status of a female. All evidence suggests that L. hesperus female attractiveness is instead modulated by myristyl acetate (MA), a volatile compound transferred during insemination that is released via the female’s vaginal pore, where it is detected by antennating males and acts as an antiaphrodisiac (Brent and Byers, 2011). Mated females remain unattractive to males for a 4–5 day post-copulatory period during which they also become sexually unreceptive and increase their rate of oviposition (Brent, 2010b). MA is produced in the male accessory glands and transferred along with other components in the spermatophore during mating (Brent and Byers, 2011). Some of these other seminal components may also play a role in male assessment of female mating history during courtship. Although females regain their attractiveness to prospective mates over time (Strong et al., 1970; Brent, 2010b), the mechanism by which this is accomplished, either by passive degradation or active countermeasure, had not been determined.

Here, we undertook a detailed analysis of the composition of L. hesperus spermatophores and the compounds emitted by mated females to determine what other volatiles might shape male reproductive behavior and how the compounds change over time. We used gas-chromatography-mass spectrometry coupled with behavioral assays to identify compounds, in addition to MA, that are involved in modulating male responses to potential mates and to monitor their changing concentrations. We obtained the first evidence of a complex sexual communication system that actively counters the male chemical mate-guarding through use of an anti-antiaphrodisiac, to produce an honest indicator of female readiness to mate.

Mating causes a precipitous decline in the attractiveness of an L. hesperus female (Strong et al., 1970), but over the course of several days she becomes increasingly likely to be courted by males (Brent, 2010a). Our previous investigation of this phenomenon led us to conclude that when a male inseminates a female, he transfers an antiaphrodisiac that is slowly released through the female’s gonopore and dissuades other males from courting her, and that the gradual dissipation of this antiaphrodisiac restores the female’s attractiveness (Brent and Byers, 2011). This simple picture was consistent with the conclusions of previous antiaphrodisiac studies (Andersson et al., 2000, Andersson et al., 2003; Schulz et al., 2008; Forsberg and Wiklund, 1989; Carlson and Langley, 1986; Schlechter-Helas et al., 2011), however the results of our current investigation indicate a more complicated signaling system regulating L. hesperus reproductive behavior. Three compounds appear to be involved: myristyl acetate, the previously identified antiaphrodisiac (Brent and Byers, 2011), geranylgeranyl acetate and geranylgeraniol. The final compound, rather than being transferred directly from the male like the first two, is primarily produced within the female via chemical conversion of the GGA. While MA’s role has been reconfirmed here, GGOH appears to play a counteracting role, diminishing or negating the effect of MA. In no instance did application of GGOH result in courtship rates being elevated above that for solvent controls, indicating that the compound does not act as an attractant or excitatory agent. The only observable effect was to counteract the antiaphrodisiac effect, thus GGOH appears to serve as an anti-antiaphrodisiac.

The signaling function of GGA is not as easily categorized. When applied by itself, GGA did not significantly affect male courtship rates, although some depression is visible. GGA also did not make females less likely to be courted when combined with MA. Of course the dose of MA used in the mixture may have been sufficient to achieve the maximal level of repellency to males by itself, leaving little room for an additive effect to be observed. However, when added to a mix of MA and GGOH, GGA was able to counteract the anti-antiaphrodisiac effect of GGOH. The resulting reduction in female attractiveness suggests that GGA contributes towards the antiaphrodisiac effect, but only in a context-specific manner. The depletion of GGA over time will diminish this repellant effect, and when combined with the commensurate increase in GGOH, will accelerate the process of the female again becoming attractive.

Compared to our previously hypothesized single-compound signal communication system of L. hesperus, the greater complexity we have found could facilitate much better coordination between male courtship and the cessation of the female refractory period. During this three to seven day span subsequent to insemination, a female refrains from interaction with courting males (Brent, 2010a), a behavioral transition largely driven by male seminal products (Brent, 2010a; Brent et al., 2016). Because the female may copulate several times throughout her life (Strong et al., 1970; Brent et al., 2011), she cannot afford to have prospective mates repelled by an overly persistent antiaphrodisiac. For a certain period after mating an antiaphrodisiac would be an honest indicator of a female’s receptivity and would help prevent males from engaging in unnecessary sperm competition (Estrada et al., 2011; Malouines, 2016). However, given that the amount of MA that a male transfers can be highly variable, the signal would not be a reliable indicator of a female’s suitability and readiness to mate over the natural refractory period. Like females of Pieris napi (Andersson et al., 2004), there is no indication that L. hesperus females can modulate the rate of antiaphrodisiac release, so they are unlikely to have control over how quickly the supply can be depleted. Thus, if the initial MA concentration in a spermatophore is quite high, such as when contributed by a male that has not mated for a week or more, the female would be rendered unattractive well past when she again becomes reproductively receptive such that both sexes lose out on potential mating opportunities. If the initial MA is quite low, such as when contributed by a male that had already mated within the past day, a still refractory female would be harassed by unwanted suitors.

By utilizing additional signaling elements in this reproductive communication system, males can more accurately estimate the likelihood that a female is suitable to mate again, an added capability that would have been selectively favored (Arak and Enquist, 1995; Estrada et al., 2011). During the first couple of days after mating when male courtship is inhibited (Brent, 2010b), the combined emissions of MA and GGA are greater than GGOH. Once there is sufficient GGOH produced to offset the antiaphrodisiac effect, subsequent males will try to court a mated female. The starting concentration of MA and GGA can vary, so long as they are above activation thresholds needed to repel other males. The relative quantities of MA and GGA transferred from a male are consistently similar although absolute amounts can vary between males. The amount of GGOH ultimately produced within the female is intrinsically tied to the starting quantity of GGA. Thus the signaling system is not affected by the variability between males in the quantities of pheromones transferred because only the time-dependent ratios are what matter. A high starting concentration of GGA will eventually produce a commensurately high concentration of GGOH to offset a high starting level of MA. So long as the conversion of GGA to GGOH occurs at a predictable rate, males will be able to accurately determine when a female is ending her refractory period.

It is likely that a combination of absolute quantities and relative proportions of these chemicals determine female attractiveness. This is suggested by some apparent inconsistency in the data. By the second day after mating, the concentration of GGOH appears comparable to that of MA, and GGA is substantially reduced. Despite these early shifts in proportions, the courtship rates remain suppressed until the fifth day after mating. GGA at this late stage may have fallen to such a low level that it no longer has a synergistic effect with MA to counteract the GGOH. We show here that MA has an activation threshold to be effective, but after that relative amounts of GGA and GGOH may be key modulators. Relative amounts of other, as yet unidentified, minor seminal constituents might also influence female attractiveness. Another consideration is that the threshold concentration identified for MA, and activation concentrations of the other compounds, may be substantially lower than our tests indicate. The external application of the chemical compounds does not fully mimic their normal release from the female gonopore. Applied chemicals can rapidly degrade, volatilize, or bind with chemicals on the cuticle. This would quickly diminish the perceivable amounts of the regulatory pheromones during the course of the bioassay, so that females avoided by males at the start were attractive again by the end. With each compound having different chemical properties, the effects of external application will not necessarily be consistent in these tests. Additional assays are needed to sort out the contributions toward female attractiveness of concentrations and proportions.

Another noteworthy finding was the variability in the responsiveness of males to these compounds. Even under the highest topical dosages of MA some males did not stop courting. This may be the result of diminished odorant receptor expression in males that cannot detect the antiaphrodisiac. Alternatively, a subgroup of males may employ a different mating strategy from the norm and are willing to tolerate sperm competition by indiscriminately courting every female encountered regardless of indicators of recent mating. This can be periodically rewarding as they are likely to be the first to access a female coming out of her refractory period earlier than her release of MA would otherwise indicate. We have also found a small but consistent subset of females that fail to enter into a refractory period, mating multiple times within a short span. Males willing to mate with one of these promiscuous females may benefit by fertilizing at least a portion of her eggs.

Although this is the first recorded instance of a pheromone being utilized as an anti-antiaphrodisiac, such compounds may not be rare. Just as it is likely that the occurrence of antiaphrodisiacs is far more widespread than has been reported due to a lack of thorough investigations (Malouines, 2016), anti-antiaphrodisiacs may have been overlooked until now because no one knew to search for them. Given the advantages of a two-dimensional chemical signaling system, it is quite likely that this is not the only instance. In fact, the evolution of a controlled antiaphrodisiac expulsion mechanism in Drosophila females (Laturney and Billeter, 2016), supports the likely occurrence of other such active counter measures to chemical mate guarding.

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Author details

1. Colin S Brent

   Arid Land Agricultural Research Center, United States Department of Agriculture-Agricultural Research Service, Maricopa, United States

   Contribution

   CSB, Conceptualization, Resources, Data curation, Formal analysis, Investigation, Methodology, Writing—original draft, Project administration

   For correspondence

   colin.brent@ars.usda.gov

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0003-2078-1417

2. John A Byers

   1. Arid Land Agricultural Research Center, United States Department of Agriculture-Agricultural Research Service, Maricopa, United States
   2. Department of Entomology, Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel

   Contribution

   JAB, Conceptualization, Resources, Investigation, Methodology, Writing—review and editing

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0002-7233-6334

3. Anat Levi-Zada

   Department of Entomology-Chemistry Unit, Agricultural Research Organization, Volcani Center, Rishon LeZion, Israel

   Contribution

   AL-Z, Resources, Writing—review and editing

   Competing interests

   The authors declare that no competing interests exist.

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