Mating Experience Research Articles

Mating experience modifies locomotor performance and promotes episodic motor activity in Drosophila melanogaster

Sexual behavior is a routine among animal species. Sexual experience has several behavioral consequences in insects, but its physiological basis is less well-understood. The episodic motor activity with a periodicity around 19 s was unintentionally observed in the wildtype Canton-S flies and was greatly reduced in the white-eyed mutant w1118 flies. Episodic motor activity co-exists with several consistent locomotor performances in Canton-S flies whereas reduced episodic motor activity is accompanied by neural or behavioral abnormalities in w1118 flies. The improvements of both episodic motor activity and locomotor performance are co-inducible by a pulsed light illumination in w1118. Here we show that mating experience of w1118 males promoted fast and consistent locomotor activities and increased the power of episodic motor activities. Compared with virgin males, mated ones showed significant increases of boundary preference, travel distance over 60 s, and increased path increments per 0.2 s. In contrast, mated males of Canton-S showed decreased boundary preference, increased travel distance over 60 s, and increased path increments per 0.2 s. Additionally, mated males of w1118 displayed increased power amplitude of periodic motor activities at 0.03-0.1 Hz. These data indicated that mating experience promoted fast and consistent locomotion and improved episodic motor activities in w1118 male flies.

Mating and parenting experiences sculpture mood-modulating effects of oxytocin-MCH signaling

The two hypothalamic neuropeptides oxytocin and melanin concentrating hormone (MCH) share several physiological actions such as the control of maternal care, sexual behavior, and emotions. In this study, we uncover the role for the oxytocin-MCH signaling pathway in mood regulation. We identify discrete effects of oxytocin-MCH signaling on depressive behavior and demonstrate that parenting and mating experiences shape these effects. We show that the selective deletion of OXT receptors from MCH neurons increases and decreases depressive behavior in sexually naïve and late postpartum female mice respectively, with no effect on sexually naïve male mice. We demonstrate that both parenting experience and mood-regulating effects of oxytocin-MCH are associated with synaptic plasticity in the reward and fear circuits revealed by the alterations of Arc expressions, which are associated with the depressive behavior. Finally, we uncover the sex-dependent effects of mating on depressive behavior; while the sexual activity reduces the basal levels of depressive behavior in male mice, it reduces in female mice evoked-depression only. We demonstrate that the oxytocin-MCH pathway mediates the effects of sexual activity on depressive behavior. Our data suggest that the oxytocin-MCH pathway can serve as a potential therapeutic target for the treatment of major depression and postpartum mood disorders.

Beetle-robot hybrid interaction: sex, lateralization and mating experience modulate behavioural responses to robotic cues in the larger grain borer Prostephanus truncatus (Horn)

Ethorobotics, a new fascinating field of biorobotics, proposes the use of robotic replicas as an advanced method for investigating animal behaviour. This novel research approach can also encourage the development of advanced bioinspired robots. In the present study, we investigated the pushing behaviour, a particular display occurring in several beetle species, such as the larger grain borer, Prostephanus truncatus, during both male-female and male-male contexts. We developed a robotic apparatus actuating female and male-mimicking dummies to study if sex, mating experience and asymmetries of robotic cues can modulate the escalation of pushing behaviour. Results showed that the time needed by P. truncatus to react to female-smelling biomimetic dummies was chiefly affected by their mating experience and the dummy odour. This was likely due to reduce waste of costly sperm in mated males during the subsequent sexual interactions. The pushing behaviour was performed longer and with a higher number of acts when virgin females were approached from their right side. More and longer pushing acts were noted when virgin males were approached from their left side. Dedicated neural circuits would likely act in opposite direction in females and males producing population-level lateralized sensory-motor displays, which may be evolved to promote male approaches from the left side of females, thus improving short-distance sex recognition. Overall, this study provides new insights on the behavioural ecology of stored-product beetles, as well as on self-organization and decentralized decision making that can be exploited to develop bioinspired algorithms for task optimization, involving real-world scenarios.

Objective and subjective components of resource value in lethal fights between male entomopathogenic nematodes

Males sometimes engage in fights over contested resources such as access to mates; in this case, fighting behaviour may be adjusted based on the value they place on the females. Resource value (RV) can have two components. First, males can assess the quality of females, which constitutes an objective assessment of RV. Second, internal state such as previous mating experience can also influence motivation to fight thus constituting a subjective assessment of RV. If mating opportunities are scarce and available females have a major impact on the lifetime reproductive success of males, then fighting can be fatal; in this situation it is uncertain whether males would adjust fighting behaviour based on RV. We found that both female quality, that is, virginity (objective component of RV) and male mating status (subjective component of RV) influenced fighting intensity between males of the entomopathogenic nematode Steinernema longicaudum which engage in lethal fights. Male nematodes were more likely to engage in fighting and fought longer and more frequently in the presence of virgin (high-quality) females than in the presence of mated (lower-quality) females. Male mating status was also found to influence fighting behaviour: mated males were the winners in staged fights between mated and virgin males. Mated males may have superior fighting ability (greater resource-holding potential), but RV asymmetries between mated and virgin males cannot be excluded. Males were more likely to win when they were resident, but we did not find a significant interaction effect between male mating and residency status.

Personality traits change after an opportunity to mate.

There is growing evidence that personality traits can change throughout the life course in humans and nonhuman animals. However, the proximate and ultimate causes of personality trait change are largely unknown, especially in adults. In a controlled, longitudinal experiment, we tested whether a key life event for adults--mating--can cause personality traits to change in female threespine sticklebacks. We confirmed that there are consistent individual differences in activity, sociability and risk-taking, and then compared these personality traits among three groups of females: (i) control females; (ii) females that had physically mated, and (iii) females that had socially experienced courtship but did not mate. Both the physical experience of mating and the social experience of courtship caused females to become less willing to take risks and less social. To understand the proximate mechanisms underlying these changes, we measured levels of excreted steroids. Both the physical experience of mating and the social experience of courtship caused levels of dihydroxyprogesterone (17α,20β-P) to increase, and females with higher 17α,20β-P were less willing to take risks and less social. These results provide experimental evidence that personality traits and their underlying neuroendocrine correlates are influenced by formative social and life-history experiences well into adulthood.

Limits to male reproductive potential across mating bouts in Drosophila melanogaster

Understanding the sources of variation in reproductive fitness is a central goal of sexual selection research. Research investigating factors limiting male reproductive potential typically focus on limited mate availability or mate access. This focus often minimizes the potential relevance of physiological or other limitations on male reproductive potential, in contrast to the emphasis on studying such limitations in females. This gap in knowledge leaves open questions about how variation in male reproductive success emerges across successive mating bouts. Here, we contribute to bridging this gap by examining male reproductive potential across successive matings and across time. To reveal limits to male reproductive potential, and sources of variation in these limits, we measured mating rate and offspring production in Drosophila melanogaster males under conditions in which mate limitation was abrogated and food was abundant. Even under these ideal conditions, we discovered distinct limits to male reproductive potential after just a few mating bouts. After males mated two to five times on a given day, additional matings often resulted in zero progeny. Furthermore, we found nonlinear relationships between the number of females a male mated with and the number of progeny he sired; and these relationships depended on the male's genotype, early life social environment and recent mating experience. These findings suggest that males who obtain more mates do not always sire the most offspring and that males who are highly successful in obtaining mates during one time period may not be able to continue this success on subsequent mating bouts and days. Together, these findings suggest trade-offs between current and future reproduction for males. More broadly, these results highlight how sexual selection studies may be expanded across individuals' lifetimes to develop a fuller picture of how sexual selection shapes variation.

Neuropeptide F regulates courtship in Drosophila through a male-specific neuronal circuit.

Male courtship is provoked by perception of a potential mate. In addition, the likelihood and intensity of courtship are influenced by recent mating experience, which affects sexual drive. Using Drosophila melanogaster, we found that the homolog of mammalian neuropeptide Y, neuropeptide F (NPF), and a cluster of male-specific NPF (NPFM) neurons, regulate courtship through affecting courtship drive. Disrupting NPF signaling produces sexually hyperactive males, which are resistant to sexual satiation, and whose courtship is triggered by sub-optimal stimuli. We found that NPFM neurons make synaptic connections with P1 neurons, which comprise the courtship decision center. Activation of P1 neurons elevates NPFM neuronal activity, which then act through NPF receptor neurons to suppress male courtship, and maintain the proper level of male courtship drive.

Molecular characterization and expression of sensory neuron membrane proteins in the parasitoid Microplitis mediator (Hymenoptera: Braconidae)

Sensory neuron membrane proteins (SNMPs), homologs of the human fatty acid transport protein CD36 family, are observed to play a significant role in chemoreception, especially in detecting sex pheromone in Drosophila and some lepidopteran species. In the current study, two full‐length SNMP transcripts, MmedSNMP1 and MmedSNMP2, were identified in the parasitoid Microplitis mediator (Hymenoptera: Braconidae). Quantitative real‐time polymerase chain reaction analysis showed that the expression of MmedSNMP1 was significantly higher in antennae than in other tissues of both sexes. In addition, the MmedSNMP1 transcript was increased dramatically in newly emerged adults and there were no significant differences between adults with or without mating and parasitic experiences. However, compared with MmedSNMP1, the expression of MmedSNMP2 was widely found in various tissues, significantly increased at half‐pigmented pupae stage and remained at a relatively constant level during the following developmental stages. It was found that MmedSNMP1 contained eight exons and seven introns, which was highly conserved compared with other insect species. In situ hybridization assay demonstrated that MmedSNMP1 transcript was distributed widely in antennal flagella. Among selected chemosensory genes (odorant binding protein, odorant receptor, and ionotropic receptor genes), MmedSNMP1 only partially overlapped with MmedORco in olfactory sensory neurons of antennae. Subsequent immunolocalization results further indicated that MmedSNMP1 was mainly expressed in sensilla placodea of antennae and possibly involved in perceiving plant volatiles and sex pheromones. These findings lay a foundation for further investigating the roles of SNMPs in the chemosensation of parasitoids.

Sexually experienced, but not naïve, female rats show a conditioned object preference (COP) for mating after a single training trial

Female rats with mating experience spend more time with the male rat, exhibit shorter contact-return latency to intromission, and display more proceptive behaviors in the male rat's compartment than during the first mating experience. The present study tested 1) whether mating induced conditioned object preference (COP) is possible with a single conditioning trial and 2) whether a preference is induced for an object associated with the first mating encounter or the fifth mating encounter in female rats. Ovariectomized, Long-Evans female rats were primed with estradiol benzoate + progesterone and either exposed to an empty paced mating chamber for 15 min (Naïve) or received a 15 intromission test of paced mating behavior (Experienced) on four separate occasions before undergoing the COP procedure. Experienced, but not Naïve, female rats developed a COP for a single mating bout, indicating that mating is highly rewarding for sexually experienced female rats. The findings raise questions about the effect of sexual experience on reward regions in the brain, the responsiveness of genital tissue, and learning mechanisms.

Sexual activity modulates neuroinflammatory responses in male rats

Immune activity influences reproduction, however, the extent to which mating experience may inversely alter immune pathways is poorly understood. A few studies in humans suggest that mating triggers a circulating immune and hypothalamic-pituitary-adrenal axis response. In male rats, mating experience enhances neuroplasticity and improves cognitive function and affective-like behavior, independent of the physical activity component. Yet, the extent to which mating experience may influence immune responses in the brain remain unexplored. Here, we hypothesized that recent mating experience in male rats increases neuroinflammatory signaling (via lipopolysaccharide [LPS] stimulation, i.p.) and associated sickness behaviors (i.e., food intake, weight loss) relative to sexually-naïve controls. Virgin male rats were exposed to a sexually non-receptive (control) or sexually-receptive female for 30 min for six consecutive days. Immediately following the last mating experience, rats were administered a saline or LPS injection and euthanized four hours later. Mating increased Tnfα responses to LPS in the brain, which positively correlated with LPS-induced weight loss. Mating also increased peripheral corticosterone among saline-treated rats, but this corticosterone response was attenuated in the most proficient copulators (e.g., shortest latencies). Thus, recent mating experience may be a unique modulator of select stimulated inflammatory signals that are relevant to adaptive neuroimmune responses and behavior.

A post-ingestive amino acid sensor promotes food consumption in Drosophila

Adequate protein intake is crucial for the survival and well-being of animals. How animals assess prospective protein sources and ensure dietary amino acid intake plays a critical role in protein homeostasis. By using a quantitative feeding assay, we show that three amino acids, L-glutamate (L-Glu), L-alanine (L-Ala) and L-aspartate (L-Asp), but not their D-enantiomers or the other 17 natural L-amino acids combined, rapidly promote food consumption in the fruit fly Drosophila melanogaster. This feeding-promoting effect of dietary amino acids is independent of mating experience and internal nutritional status. In vivo and ex vivo calcium imagings show that six brain neurons expressing diuretic hormone 44 (DH44) can be rapidly and directly activated by these amino acids, suggesting that these neurons are an amino acid sensor. Genetic inactivation of DH44+ neurons abolishes the increase in food consumption induced by dietary amino acids, whereas genetic activation of these neurons is sufficient to promote feeding, suggesting that DH44+ neurons mediate the effect of dietary amino acids to promote food consumption. Single-cell transcriptome analysis and immunostaining reveal that a putative amino acid transporter, CG13248, is enriched in DH44+ neurons. Knocking down CG13248 expression in DH44+ neurons blocks the increase in food consumption and eliminates calcium responses induced by dietary amino acids. Therefore, these data identify DH44+ neuron as a key sensor to detect amino acids and to enhance food intake via a putative transporter CG13248. These results shed critical light on the regulation of protein homeostasis at organismal levels by the nervous system.

Female receptivity affects subsequent mating effort and mate choice in male guppies

High mating effort leads to choosiness because each mating event reduces future reproductive potential. Many studies have shown that males adjust their sexual behaviour relative to female fecundity and encounter rate. However, little is known about the effects of a male's past mating experiences. We used guppies, Poecilia reticulata, to investigate how males change their sexual behaviour after experiencing high or low mating success. Each male was tested with two differently sized unreceptive females before and after encountering either four indiscriminate receptive virgin females or four nonreceptive pregnant females. Males that experienced high mating success with receptive females decreased their courtship displays but increased the frequency of sneaky behaviour, whereas low mating success males previously repetitively rejected by nonreceptive females showed an increase in courtship and a decrease in sneaky copulation attempts. Mating history also influenced male choosiness, with successful males showing stronger preferences for larger females than unsuccessful males. This overall adjustment in behaviour may be attributed to a reduction of resources, such as energy and gametes, as well as prior social interaction with receptive and nonreceptive females. Males that adjust their effort and choosiness based on their recent mating history and their own condition could optimize reproductive trade-offs.

Physiological status ofDrosophila suzukii(Diptera: Drosophilidae) affects their response to attractive odours

AbstractAn improved understanding of the biology of the invasive pest,Drosophila suzukii(Matsumura) (Diptera: Drosophilidae), is critical for the development of effective management strategies. Trapping is one technique used for both detection and control; however, the efficacy of trapping can vary depending on the target insect's physiological state, its behavioural priorities and the type of attractant used in the trap. We conducted a series of caged trapping experiments and a greenhouse trapping experiment to investigate the effects ofD. suzukiifeeding status, age, mating status, ovipositional status and seasonal morph type on the capture rate of traps baited with fermentation odours. Starved flies were trapped at greater rates compared to fed flies; more virgin flies were trapped than mated flies; flies deprived of an oviposition substrate were trapped more frequently than flies given an oviposition substrate. It is still unclear whether age or seasonal morphology affect bait response. Lastly, a caged choice experiment investigated the relationship between female reproductive status and attraction to fermentation or fruit odours. Fermentation‐based traps captured female flies regardless of their reproductive status but, ripe fruit‐based traps were more attractive to flies with more than seven eggs. In summary, studies that use fermentation‐based traps should recognize that capture rates ofD. suzukiiwill depend on the feeding, mating and oviposition experiences of the population; also, fruit‐based traps may better target gravid females.

Mating experience influences mate choice and reproductive output in an aphidophagous ladybird, Menochilus sexmaculatus

AbstractInformation about mating status can be used to decide about whether to invest resources in mating with a particular partner. In the present study, we evaluated mate choice in relation to the mating experience of males and females ofMenochilus sexmaculatus. We subjected both unmated and multiply mated males and females to different mate choice trials. The mating experience of the adults includes unmated, once-mated, twice-mated and multiply mated. The mate choice trials revealed that unmated adults were preferred over mated adults by both unmated and multiply mated partners. This preference for unmated partners also had consequences for mating behaviour and reproductive output. Unmated and multiply mated females commenced mating with unmated males earlier. In addition, unmated and multiply mated males invested more time in copula with unmated females. Moreover, females mated with unmated males were more fecund than those mated with previously mated males. This suggests that mating experience of mates may influence mating and reproductive behaviour in this species.

Changes in courtship behaviour following rejection: The influence of female phenotype in Drosophila melanogaster

AbstractCourtship can be costly and so selection should favour individual males that reduce courtship towards female types that have a low probability of resulting in copulation. One way males can do this is by associating previous courtship failure with the traits of particular rejecting females. We characterised changes in male Drosophila melanogaster courtship behaviour following a failed mating attempt with one of the four female phenotypes that varied in size, age or mating status. To do this, we assessed individual courtship behaviour for each male presented again with a female of the same phenotype that previously rejected him. Males reduced subsequent courtship most strongly for recently mated (sexually non‐receptive) females. More interestingly, males also significantly reduced courtship activity following a failed mating experience from old females but did not do so for control (large, young, virgin) or small females. As such, males significantly reduced courtship towards both female types possessing chemical cues associated with their phenotype (age and mating status), but not towards a female phenotype based on physical characteristics (body size). Our results suggest that males are able to modify their courtship behaviour following experience, but that they are better prepared to associate chemical traits that may be more reliable indicators of the likelihood of courtship failure.

Effect of Ovarian Hormones and Mating Experience on the Preference of Female Mice to Investigate Male Urinary Pheromones.

In female mice, the expression of receptive lordosis behavior requires estradiol and progesterone actions in the nervous system; however, the contribution of these hormones to females' motivation to seek out male pheromones is less clear. In an initial experiment, sexually naïve ovary-intact female mice preferred to investigate (make nasal contact with) testes-intact male as opposed to estrous female urine, provided they were in vaginal estrus. In a second experiment, groups of sexually naïve and mating-experienced, ovariectomized females were tested for urinary pheromone preference first without and then with ovarian hormone replacement. Without hormone replacement, sexually naïve ovariectomized females showed no preference for male over female urinary pheromones whereas mating-experienced females preferred to investigate male pheromones. Ovariectomized females in both groups preferred male over female urine after sequential s.c. injections with estradiol benzoate followed 2 days later with progesterone and after prolonged (7 days) exposure to estradiol alone. Our results indicate that in sexually naïve female mice estradiol, perhaps aided by progesterone, is required to motivate a preference to seek out male pheromones whereas after mating experience females' preference to investigate male pheromones persists even in the absence of ovarian hormone action.

Mechanisms of sleep plasticity due to sexual experience in Drosophila melanogaster

Sleep can be altered by an organism's previous experience. For instance, female Drosophila melanogaster experience a post-mating reduction in daytime sleep that is purportedly mediated by sex peptide (SP), one of many seminal fluid proteins (SFPs) transferred from male to female during mating. In the present study, we first characterized this mating effect on sleep more fully, as it had previously only been tested in young flies under 12h light/12h dark conditions. We found that mating reduced sleep equivalently in 3-day-old or 14-day-old females, and could even occur in females who had been mated previously, suggesting that there is not a developmental critical period for the suppression of sleep by mating. In conditions of constant darkness, circadian rhythms were not affected by prior mating. In either constant darkness or constant light, the sleep reduction due to mating was no longer confined to the subjective day but could be observed throughout the 24-hour period. This suggests that the endogenous clock may dictate the timing of when the mating effect on sleep is expressed.We recently reported that genetic elimination of SP only partially blocked the post-mating female siesta sleep reduction, suggesting that the effect was unlikely to be governed solely by SP. We found here that the daytime sleep reduction was also reduced but not eliminated in females mated to mutant males lacking the vast majority of SFPs. This suggested that SFPs other than SP play a minimal role in the mating effect on sleep, and that additional non-SFP signals from the male might be involved. Males lacking sperm were able to induce a normal initial mating effect on female sleep, although the effect declined more rapidly in these females. This result indicated that neither the presence of sperm within the female reproductive tract nor female impregnation are required for the initial mating effect on sleep to occur, although sperm may serve to prolong the effect.Finally, we tested for contributions from other aspects of the mating experience. NorpA and eya2 mutants with disrupted vision showed normal mating effects on sleep. By separating males from females with a mesh, we found that visual and olfactory stimuli from male exposure, in the absence of physical contact, could not replicate the mating effect. Further, in ken/barbie male flies lacking external genitalia, courtship and physical contact without ejaculation were also unable to replicate the mating effect. These findings confirmed that the influence of mating on sleep does in fact require male/female contact including copulation, but may not be mediated exclusively by SP transfer.

Effect of Body Size, Age, and Premating Experience on Male Mating Success in Bactrocera tryoni (Diptera: Tephritidae).

Variation in male body size, age, and prior sexual experience may all influence male mating success in tephritid fruit flies. Bactrocera tryoni (Froggatt) is an Australian pest tephritid for which the sterile insect technique (SIT) is being actively pursued, and for which information on what makes males more competitive is urgently needed. Pair-wise competitive mating trials were run using laboratory-reared flies in walk-in field cages, evaluating young, large, and virgin B. tryoni males against old, small, and nonvirgin males, respectively. Analysis of male sexual competitiveness indices revealed that young and large males obtained significantly more copulations compared to old and small males; there was no significant difference between virgin and nonvirgin males in obtaining mates. While SIT programs will always release young males, the results do show that rearing programs which focus on producing larger males, rather than greater numbers of smaller males, will produce more sexually competitive males. After release, virgin SIT males will not be at a competitive disadvantage with sexually experienced males based on prior mating experience.

Female mate preference in an invasive phytopathogen vector: how learning may influence mate choice and fecundity in Diaphorina citri

AbstractIn some arthropods, females learn in the context of reproduction to refine their mate choices and avoid males displaying traits associated with impotency. Previous studies have shown that males of the Asian citrus psyllid, Diaphorina citriKuwayama (Hemiptera: Psyllidae), associate female odor with copulatory rewards. However, it is unclear whether females similarly learn about male traits. We compared mate choice in females previously mated to either blue or orange males and found that females may associate male color with reproductive success, and avoided blue males after previous experience. Orange males mated more frequently than blue males and appeared to be more sexually aggressive in their mating attempts. In addition, females mated to orange males laid approximately twice as many eggs as those mated to blue males. We dissected male psyllids and measured the size of their reproductive organs to determine whether abdominal color was associated with reproductive development. Our morphometric analysis indicated that blue males may not be physiologically immature compared with orange males. Rather, blue males displayed larger testes and seminal vesicles than orange males, suggesting that differences in reproductive output may be behavioral in nature. Based on our data, we suggest that females learn about the appearance and mating behaviors of blue and orange males from early mating experiences, and subsequently avoid blue males in future matings. Although the roles of blue males within a population are unclear, it is possible that blue morphs may specialize in other functions such as dispersal.

Integrating Neural Circuits Controlling Female Sexual Behavior.

The hypothalamus is most often associated with innate behaviors such as is hunger, thirst and sex. While the expression of these behaviors important for survival of the individual or the species is nested within the hypothalamus, the desire (i.e., motivation) for them is centered within the mesolimbic reward circuitry. In this review, we will use female sexual behavior as a model to examine the interaction of these circuits. We will examine the evidence for a hypothalamic circuit that regulates consummatory aspects of reproductive behavior, i.e., lordosis behavior, a measure of sexual receptivity that involves estradiol membrane-initiated signaling in the arcuate nucleus (ARH), activating β-endorphin projections to the medial preoptic nucleus (MPN), which in turn modulate ventromedial hypothalamic nucleus (VMH) activity—the common output from the hypothalamus. Estradiol modulates not only a series of neuropeptides, transmitters and receptors but induces dendritic spines that are for estrogenic induction of lordosis behavior. Simultaneously, in the nucleus accumbens of the mesolimbic system, the mating experience produces long term changes in dopamine signaling and structure. Sexual experience sensitizes the response of nucleus accumbens neurons to dopamine signaling through the induction of a long lasting early immediate gene. While estrogen alone increases spines in the ARH, sexual experience increases dendritic spine density in the nucleus accumbens. These two circuits appear to converge onto the medial preoptic area where there is a reciprocal influence of motivational circuits on consummatory behavior and vice versa. While it has not been formally demonstrated in the human, such circuitry is generally highly conserved and thus, understanding the anatomy, neurochemistry and physiology can provide useful insight into the motivation for sexual behavior and other innate behaviors in humans.