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1.  Courtship attention in sagebrush lizards varies with male identity and female reproductive state 
Previous experiments suggest that males spend more time with the more receptive of two novel females or the one with the higher fitness potential. However, males often court individual females repeatedly over a season; for example, male lizards sequentially visit familiar females as they patrol territorial boundaries. It may benefit males to vary display intensity as they move between multiple females. In this study, we explored the factors influencing amount of male courtship to familiar females in the Sagebrush lizard, Sceloporus graciosus. We tested whether males vary the amount of courtship exhibited due to individual differences among males, female reproductive state, or female fitness potential. Each male was allowed to interact separately, but repeatedly, with two females until both females laid eggs. Male courtship behavior with each of the two females was assayed at an intermediate point, after three weeks of interaction. We found that individual differences among males were considerable. The number of male courtship displays was also positively correlated with female latency to lay eggs, with males displaying more often towards females with eggs that had not yet been fertilized. Courtship behavior was not well predicted by the number of eggs laid or by female width, both measures of female quality. Thus, male S. graciosus appear to alter courtship intensity more in response to signals of female reproductive state than in response to variation in potential female fitness.
doi:10.1093/beheco/arn072
PMCID: PMC2583109  PMID: 19458780
Sceloporus graciosus; male choice; mate choice; sexual selection; reproductive state; courtship
2.  Both male and female identity influence variation in male signalling effort 
Background
Male sexual displays play an important role in sexual selection by affecting reproductive success. However, for such displays to be useful for female mate choice, courtship should vary more among than within individual males. In this regard, a potentially important source of within male variation is adjustment of male courtship effort in response to female traits. Accordingly, we set out to dissect sources of variation in male courtship effort in a fish, the desert goby (Chlamydogobius eremius). We did so by designing an experiment that allowed simultaneous estimation of within and between male variation in courtship, while also assessing the importance of the males and females as sources of courtship variation.
Results
Although males adjusted their courtship depending on the identity of the female (a potentially important source of within-male variation), among-male differences were considerably greater. In addition, male courtship effort towards a pair of females was highly repeatable over a short time frame.
Conclusion
Despite the plasticity in male courtship effort, courtship displays had the potential to reliably convey information about the male to mate-searching females. Our experiment therefore underscores the importance of addressing the different sources contributing to variation in the expression of sexually-selected traits.
doi:10.1186/1471-2148-11-233
PMCID: PMC3163561  PMID: 21827657
3.  Food supplementation and testosterone interact to influence reproductive behavior and immune function in Sceloporous graciosus 
Hormones and behavior  2009;57(2):134.
The energetic resources in an organism’s environment are essential for executing a wide range of life history functions, including immunity and reproduction. Most energetic budgets, however, are limited, which can lead to trade-offs among competing functions. Increasing reproductive effort tends to decrease immunity in many cases; and increasing total energy via supplemental feedings can eliminate this effect. Testosterone (T), an important regulator of reproduction, and food availability are thus both potential factors regulating life-history processes, yet they are often tested in isolation of each other. In this study, we considered the effect of both food availability and elevated T on immune function and reproductive behavior in sagebrush lizards, Sceloporus graciosus, to assess how T and energy availability affect these trade-offs. We experimentally manipulated diet (via supplemental feedings) and T (via dermal patches) in males from a natural population. We determined innate immune response by calculating the bacterial killing capability of collected plasma exposed to E. coli ex vivo. We measured reproductive behavior by counting the number of courtship displays produced in a 20-min sampling period. We observed an interactive effect of food availability and T-patch on immune function, with food supplementation increasing immunity in T-patch lizards. Additionally, T increased courtship displays in control food lizards. Lizards with supplemental food had higher circulating T than controls. Collectively, this study shows that the energetic state of the animal plays a critical role in modulating the interactions among T, behavior and immunity in sagebrush lizards and likely other species.
doi:10.1016/j.yhbeh.2009.09.019
PMCID: PMC2814879  PMID: 19800885
Context-dependent; Energy allocation; Innate immunity; Life history; Resources; Sceloporus; Trade-offs
4.  Sex-specific visual performance: female lizards outperform males in motion detection 
Biology Letters  2009;5(6):732-734.
In animal communication, complex displays usually have multiple functions and, male and female receivers often differ in their utilization and response to different aspects of these displays. The perceptual variability hypothesis suggests that different aspects of complex signals differ in their ability to be detected and processed by different receivers. Here, we tested whether receiver male and female Sceloporus graciosus lizards differ in visual motion detection by measuring the latency to the visual grasp response to a motion stimulus. We demonstrate that in lizards that largely exhibit complex motions as courtship signals, female lizards are faster than males at visually detecting motion. These results highlight that differential signal utilization by the sexes may be driven by variability in the capacity to detect different display properties.
doi:10.1098/rsbl.2009.0348
PMCID: PMC2827977  PMID: 19656865
sex difference; visual performance; motion detection; complex signals; animal communication; Sceloporus graciosus
5.  Multiple male traits interact: attractive bower decorations facilitate attractive behavioural displays in satin bowerbirds. 
Sexually selected male courtship displays often involve multiple behavioural and physical traits, but little is known about the function of different traits in mate choice. Here, we examine female courtship behaviours to learn how male traits interact to influence female mating decisions. In satin bowerbirds (Ptilonorhynchus violaceus), successful males give highly aggressive, intense behavioural displays without startling females. Males do this by modulating their displays in response to female crouching, which signals the display intensity that females will tolerate without being startled. Females typically visit multiple males for multiple courtships before choosing a mate, and females show differing tolerance for intense displays during their first courtship with each male. We test three hypotheses that may explain this: (i) familiarity with the courting male; (ii) the order of the courtship in mate-searching; and (iii) the attractiveness of the courting male. We found that females are more tolerant of intense displays during first courtships with attractive males; this increased female tolerance may allow attractive males to give higher intensity courtship displays that further enhance their attractiveness. We then examined why this is so, finding evidence that females are less likely to be startled by males with better physical displays (bower decorations), and this reduced startling then contributes to male courtship success. This role of physical displays in facilitating behavioural displays suggests a novel mechanism by which multiple physical and behavioural traits may influence female choice.
doi:10.1098/rspb.2003.2530
PMCID: PMC1691511  PMID: 14667356
6.  Sex differences in the response to environmental cues regulating seasonal reproduction in birds 
Although it is axiomatic that males and females differ in relation to many aspects of reproduction related to physiology, morphology and behaviour, relatively little is known about possible sex differences in the response to cues from the environment that control the timing of seasonal breeding. This review concerns the environmental regulation of seasonal reproduction in birds and how this process might differ between males and females. From an evolutionary perspective, the sexes can be expected to differ in the cues they use to time reproduction. Female reproductive fitness typically varies more as a function of fecundity selection, while male reproductive fitness varies more as a function sexual selection. Consequently, variation in the precision of the timing of egg laying is likely to have more serious fitness consequences for females than for males, while variation in the timing of recrudescence of the male testes and accompanying territory establishment and courtship are likely to have more serious fitness consequences for males. From the proximate perspective, sex differences in the control of reproduction could be regulated via the response to photoperiod or in the relative importance and action of supplementary factors (such as temperature, food supply, nesting sites and behavioural interactions) that adjust the timing of reproduction so that it is in step with local conditions. For example, there is clear evidence in several temperate zone avian species that females require both supplementary factors and long photoperiods in order for follicles to develop, while males can attain full gonadal size based on photoperiodic stimulation alone. The neuroendocrine basis of these sex differences is not well understood, though there are many candidate mechanisms in the brain as well as throughout the entire hypothalamo–pituitary–gonadal axis that might be important.
doi:10.1098/rstb.2007.2137
PMCID: PMC2606748  PMID: 17638693
photoperiodism; circannual rhythms; sex differences; supplementary cues
7.  Male dwarf chameleons assess risk of courting large, aggressive females 
Biology Letters  2005;1(2):231-234.
Conflict between the sexes has traditionally been studied in terms of costs of mating to females and female resistance. However, courting can also be costly to males, especially when females are larger and aggressively resist copulation attempts. We examined male display intensity towards females in the Cape dwarf chameleon, Bradypodion pumilum, in which females are larger than males and very aggressive. We assessed whether aggressive female rejection imposes potential costs on males and whether males vary their display behaviour with intensity of female rejection, female size or relative size differences. Males persisted in courtship after initial female rejection in 84% of trials, and were bitten in 28% of trials. Attempted mounts were positively associated with males being bitten. Males reduced courtship with increased intensity of female rejection. Male courtship behaviour also varied with female size: males were more likely to court and approach smaller females, consistent with the hypothesis that larger females can inflict more damage. These results suggest that, in addition to assessing female willingness to mate, male dwarf chameleons may use courtship displays to assess potential costs of persistence, including costs associated with aggressive female rejection, weighed against potential reproductive pay-offs associated with forced copulation.
doi:10.1098/rsbl.2005.0299
PMCID: PMC1626215  PMID: 17148174
mating costs; sexual conflict; antagonistic coevolution; female rejection
8.  Androgen receptor expression and morphology of forebrain and neuromuscular systems in male green anoles displaying individual differences in sexual behavior 
Hormones and behavior  2007;52(2):228-236.
Investigating individual differences in sexual performance in unmanipulated males is important for understanding natural relationships between behavior and morphology, and the mechanisms regulating them. Among male green anole lizards, some court and copulate frequently (studs) and others do not (duds). To evaluate potential factors underlying differences in the level of these behaviors, morphology and androgen receptor expression in neuromuscular courtship and copulatory structures, as well as in the preoptic area and amygdala, were compared in males displaying varying degrees of sexual function. This study revealed that individual differences in behavior among unmanipulated males, in particular the extension of a throat fan (dewlap) used during courtship, were positively correlated with the size of fibers in the associated muscle and with soma size in the amygdala. The physiological response to testosterone, as indicated by the height of cells in an androgen-sensitive portion of the kidney, was also correlated with male sexual behavior, and predicted it better than plasma androgen levels. Androgen receptor expression was not related to the display of courtship or copulation in any of the tissues examined. The present data indicate that higher levels of male courtship behavior result in (or are the result of) enhanced courtship muscle and amygdala morphology, and that androgen-sensitive tissue in studs may be more responsive to testosterone than duds. However, some mechanism(s) other than androgen receptor expression likely confer this difference in responsiveness.
doi:10.1016/j.yhbeh.2007.04.009
PMCID: PMC2882099  PMID: 17531996
Testosterone; Courtship; Copulation; Reptile; Preoptic area; Amygdala
9.  Identification of Gene Expression Changes Associated With Long-Term Memory of Courtship Rejection in Drosophila Males 
G3: Genes|Genomes|Genetics  2012;2(11):1437-1445.
Long-term memory formation in Drosophila melanogaster is an important neuronal function shaping the insect’s behavioral repertoire by allowing an individual to modify behaviors on the basis of previous experiences. In conditioned courtship or courtship suppression, male flies that have been repeatedly rejected by mated females during courtship advances are less likely than naïve males to subsequently court another mated female. This long-term courtship suppression can last for several days after the initial rejection period. Although genes with known functions in many associative learning paradigms, including those that function in cyclic AMP signaling and RNA translocation, have been identified as playing critical roles in long-term conditioned courtship, it is clear that additional mechanisms also contribute. We have used RNA sequencing to identify differentially expressed genes and transcript isoforms between naïve males and males subjected to courtship-conditioning regimens that are sufficient for inducing long-term courtship suppression. Transcriptome analyses 24 hours after the training regimens revealed differentially expressed genes and transcript isoforms with predicted and known functions in nervous system development, chromatin biology, translation, cytoskeletal dynamics, and transcriptional regulation. A much larger number of differentially expressed transcript isoforms were identified, including genes previously implicated in associative memory and neuronal development, including fruitless, that may play functional roles in learning during courtship conditioning. Our results shed light on the complexity of the genetics that underlies this behavioral plasticity and reveal several new potential areas of inquiry for future studies.
doi:10.1534/g3.112.004119
PMCID: PMC3484674  PMID: 23173095
long-term memory; courtship conditioning; RNA seq; courtship behavior
10.  Assessment and decision-making in a Caribbean damselfish: nest-site quality influences prioritization of courtship and brood defence 
Biology Letters  2009;5(2):188-190.
In systems where territory quality varies, animals are expected to exhibit plasticity in behaviour in order to maximize fitness relative to their present territory quality. This requires assessment of territory quality followed by decision-making in relation to the priority of activities necessary for survival and reproduction. We examined how differences in territory quality of beaugregory damselfish (Stegastes leucostictus) influence the prioritization of courtship and egg defence by comparing behavioural responses of males defending artificial sites (high quality) with males defending natural sites (low quality) when presented with an egg predator, a conspecific female, and a simultaneous choice between both. A significant three-way interaction of territory quality, presentation type and stimulus was observed for time near stimuli. In paired presentations, males defending low-quality territories spent more time near a female and less near an egg predator; while males on high-quality territories spent more time near a predator than a female. Additionally, comparing single and paired presentations reveals that behaviours towards egg predators remain constant while behaviours towards females decrease with paired stimuli. These data suggest that territory quality and ecological context impact decision-making and the relative values of potential reproduction and/or past reproductive effort.
doi:10.1098/rsbl.2008.0698
PMCID: PMC2665824  PMID: 19158028
beaugregory damselfish; courtship; decision-making; Stegastes leucostictus; territory quality
11.  A Female-Emitted Pheromone Component Is Associated with Reduced Male Courtship in the Parasitoid Wasp Spalangia endius 
PLoS ONE  2013;8(11):e82010.
During courtship interactions, the courted individual may not always be prepared to mate. For example, mating or courtship may be detrimental to its fitness and resistance is expected under these circumstances. As such, various resistance strategies have evolved, from physically fending off courting individuals to producing behavioural signals of unreceptivity. In the parasitoid wasp Spalangia endius, females rarely re-mate and mated females are avoided by males in favour of virgin females. Further, mated females appear to advertise their mating status by the release of a pheromone component (methyl 6-methylsalicylate), but direct evidence of the nature of this release is lacking. Here we used real-time chemical analysis to track the emission of the pheromone component during courtship interactions between virgin males and either virgin or mated females. We found that females actively release methyl 6-methylsalicylate when courted and that significantly greater concentrations are released by previously mated females. Further, high concentrations of this component are associated with both the prevention and termination of courtship.
doi:10.1371/journal.pone.0082010
PMCID: PMC3835669  PMID: 24278468
12.  Eavesdropping in crabs: an agency for lady detection 
Biology Letters  2010;6(6):755-757.
Although conspicuous courtship displays are an effective way of attracting the attention of receptive females, they could provide valuable information to rival males on the location of these females. In fiddler crabs, males that see a receptive female wave their single, greatly enlarged claw in a highly conspicuous courtship display. We test whether other males use this courtship display to alert them to the presence of receptive females that they cannot directly see. We show that male fiddler crabs (Uca mjoebergi) eavesdrop on the courtship displays of nearby males to detect mate-searching females. This allows males to begin waving before a female becomes visible. Furthermore, males appear to adjust their waving according to the information available: eavesdropping males wave 12 times faster than non-courting males but only 1.7 times slower than males in full visual contact with the female.
doi:10.1098/rsbl.2010.0384
PMCID: PMC3001374  PMID: 20519196
animal communication; eavesdropping; fiddler crabs; mate attraction; Uca mjoebergi
13.  Male Choice in the Stream-Anadromous Stickleback Complex 
PLoS ONE  2012;7(6):e37951.
Studies of mating preferences and pre-mating reproductive isolation have often focused on females, but the potential importance of male preferences is increasingly appreciated. We investigated male behavior in the context of reproductive isolation between divergent anadromous and stream-resident populations of threespine stickleback, Gasterosteus aculeatus, using size-manipulated females of both ecotypes. Specifically, we asked if male courtship preferences are present, and if they are based on relative body size, non-size aspects of ecotype, or other traits. Because male behaviors were correlated with each other, we conducted a principal components analysis on the correlations and ran subsequent analyses on the principal components. The two male ecotypes differed in overall behavioral frequencies, with stream-resident males exhibiting consistently more vigorous and positive courtship than anadromous males, and an otherwise aggressive behavior playing a more positive role in anadromous than stream-resident courtship. We observed more vigorous courtship toward smaller females by (relatively small) stream-resident males and the reverse pattern for (relatively large) anadromous males. Thus size-assortative male courtship preferences may contribute to reproductive isolation in this system, although preferences are far from absolute. We found little indication of males responding preferentially to females of their own ecotype independent of body size.
doi:10.1371/journal.pone.0037951
PMCID: PMC3372497  PMID: 22701589
14.  Sound production during agonistic behavior of male Drosophila melanogaster 
Fly  2011;5(1):29-38.
Male Drosophila fruit flies acquire and defend territories in order to attract females for reproduction. Both, male-directed agonistic behavior and female-directed courtship consist of series of recurrent stereotypical components. Various studies demonstrated the importance of species-specific sound patterns generated by wing vibration as being critical for male courtship success. In this study we analyzed the patterns and importance of sound signals generated during agonistic interactions of male Drosophila melanogaster. In contrast to acoustic courtship signals that consist of sine and pulse patterns and are generated by one extended wing, agonistic signals lack sine-like components and are generally produced by simultaneous movements of both wings. Though intra-pulse oscillation frequencies (carrier frequency) are identical, inter-pulse intervals are twice as long and more variable in aggression signals than in courtship songs, where their precise temporal pattern serves species recognition. Acoustic signals accompany male agonistic interactions over their entire course but occur particularly often after tapping behavior which is a major way to identify the gender of the interaction partner. Since similar wing movements may either be silent or generate sound and wing movements with sound have a greater impact on the subsequent behavior of a receiver, sound producing wing movements seem to be generated intentionally to serve as a specific signal during fruit fly agonistic encounters.
doi:10.4161/fly.5.1.13713
PMCID: PMC3052870  PMID: 20953152
acoustic signals; temporal patterns; frequency analysis; agonistic behavior; courtship; ethogram
15.  Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster 
Theory predicts that males will benefit when they bias their mating effort towards females of higher reproductive potential, and that this discrimination will increase as males become more resource limited. We conducted a series of experiments to test these predictions in a laboratory population of the fruitfly, Drosophila melanogaster. In this species, courtship and copulation have significant costs to males, and females vary greatly in fecundity, which is positively associated with body size. When given a simultaneous choice between small and large virgin females, males preferentially mated with larger, more fecund, females. Moreover, after males had recently mated they showed a stronger preference for larger females. These results suggest that male D. melanogaster adaptively allocate their mating effort in response to variation in female quality and provide some of the first support for the theoretical prediction that male stringency in mate choice increases as resources become more limiting.
doi:10.1098/rspb.2005.3372
PMCID: PMC1560241  PMID: 16627276
male mate choice; mating costs; Drosophila melanogaster; fecundity
16.  Courtship and copulation in the adult male green anole: Effects of season, hormone and female contact on reproductive behavior and morphology 
Behavioural brain research  2006;177(2):177-185.
Interactions among reproductive season, testosterone (T) and female presence were investigated on the structure and function of forebrain and neuromuscular systems controlling courtship and copulation in the green anole lizard. Under breeding (BS) or non-breeding (NBS) environmental conditions, male green anoles were implanted with either T or blank capsules and exposed to one of three female stimulus conditions: physical, visual or no female contact. T and at least visual exposure to females increased courtship displays (extension of a throat fan, or dewlap), and these effects were greater during the BS than NBS. T also facilitated copulation, and did so to a greater extent in the BS. The hormone increased soma size in the preoptic area (POA) and amygdala (AMY), and in the AMY the effects were greater in the BS than NBS. Cross-sectional areas of copulatory organs and associated muscle fibers were enhanced by T, and more so in the BS than NBS. However, no effects on morphology of dewlap motoneurons or muscles or copulatory motoneurons were detected. Thus, (1) changes in behavior and neural and/or muscular morphology are not always parallel and (2) differences in responsiveness to T exist across seasons and among tissues.
doi:10.1016/j.bbr.2006.11.035
PMCID: PMC2892282  PMID: 17174414
Sexual behavior; Courtship; Lizard; Reptile; Forebrain; Neuromuscular
17.  Male-Male Sexual Behavior in the Parasitic Wasp Psyttalia concolor  
The role of male-male courtship in parasitic Hymenoptera is poorly known. A laboratory study was conducted to assess if Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae) male courtship can be affected by a previous experience in courting young conspecifics of both sexes. Two experiments were performed to evaluate the effect of experience in courting young wasps on both male courtship and male-male competition behavior. Results showed that a courting experience on both sexes can modify some sexual traits in a P. concolor male, without affecting its success in mating. When approaching virgin females, a P. concolor male that had a previous courtship experience with young wasps of either sex showed shorter latency times, more wing fanning, and longer courtship durations with respect to the control male. The hypothesis that a previous courting experience may allow a P. concolor male to refine its courtship behavior and to enhance courtship intensity in subsequent encounters with females was discussed.
doi:10.1673/031.013.2501
PMCID: PMC3735074  PMID: 23895402
adaptive behavior; courtship; experience; mating; Opiinae; wing fanning
18.  Sensory Integration Regulating Male Courtship Behavior in Drosophila 
PLoS ONE  2009;4(2):e4457.
The courtship behavior of Drosophila melanogaster serves as an excellent model system to study how complex innate behaviors are controlled by the nervous system. To understand how the underlying neural network controls this behavior, it is not sufficient to unravel its architecture, but also crucial to decipher its logic. By systematic analysis of how variations in sensory inputs alter the courtship behavior of a naïve male in the single-choice courtship paradigm, we derive a model describing the logic of the network that integrates the various sensory stimuli and elicits this complex innate behavior. This approach and the model derived from it distinguish (i) between initiation and maintenance of courtship, (ii) between courtship in daylight and in the dark, where the male uses a scanning strategy to retrieve the decamping female, and (iii) between courtship towards receptive virgin females and mature males. The last distinction demonstrates that sexual orientation of the courting male, in the absence of discriminatory visual cues, depends on the integration of gustatory and behavioral feedback inputs, but not on olfactory signals from the courted animal. The model will complement studies on the connectivity and intrinsic properties of the neurons forming the circuitry that regulates male courtship behavior.
doi:10.1371/journal.pone.0004457
PMCID: PMC2636894  PMID: 19214231
19.  No evidence for learned mating discrimination in male Drosophila pseudoobscura 
Background
Since females often pay a higher cost for heterospecific matings, mate discrimination and species recognition are driven primarily by female choice. In contrast, frequent indiscriminate matings are hypothesized to maximize male fitness. However, recent studies show that previously indiscriminate males (e.g., Drosophila melanogaster and Poecilia reticulata) can learn to avoid heterospecific courtship. This ability of males to discriminate against heterospecific courtship may be advantageous in populations where two species co-occur if courtship or mating is costly.
Results
Here, we tested whether Drosophila pseudoobscura males learn to discriminate against heterospecific females after being exposed to and rejected by D. persimilis females. In most of our assays, we failed to observe differences in D. pseudoobscura courtship intensity of heterospecific females by males that had previously courted heterospecific females vs. males that had been maintained in isolation.
Conclusion
We conclude that learning to avoid heterospecific courtship may not be universal, even within the genus Drosophila, and may possibly be dependent on the natural history of the species.
doi:10.1186/1471-2148-6-54
PMCID: PMC1534054  PMID: 16824212
20.  Testosterone affects reproductive success by influencing extra-pair fertilizations in male dark-eyed juncos (Aves: Junco hyemalis) 
Monogamous male birds typically allocate less effort to courtship and more to parental behaviour than males of polygynous species. The seasonal pattern of testosterone (T) secretion varies accordingly. Monogamous males exhibit a spring peak in plasma T followed by lower levels during the parental phase, while males of polygynous species continue to court females and maintain T at higher levels. To determine whether testosterone underlies the trade-off between mating and parental effort, we treated male dark-eyed juncos (Junco hyemalis) with exogenous T and compared the reproductive success (RS) of T-treated males (T-males) to that of controls. T-males had lower apparent annual RS than controls, probably because elevated T reduced parental care. Nevertheless, annual genetic RS of the treatment groups was similar because (i) T-males suffered fewer losses in genetic RS due to extra-pair fertilizations (EPFs), and (ii) T-males gained more genetic RS through their own EPFs. This is the first hormonal manipulation of an avian phenotype shown to have influenced male RS through EPFs. Together with other studies, it suggests that testosterone may have mediated the evolution of inter- and intraspecific differences in allocation of reproductive effort to mate attraction and parental care.
doi:10.1098/rspb.1997.0223
PMCID: PMC1688731
Hormones Mating Systems Testosterone Reproductive Success Dna Fingerprinting Paternity
21.  Reduction of Dopamine Level Enhances the Attractiveness of Male Drosophila to Other Males 
PLoS ONE  2009;4(2):e4574.
Dopamine is an important neuromodulator in animals and its roles in mammalian sexual behavior are extensively studied. Drosophila as a useful model system is widely used in many fields of biological studies. It has been reported that dopamine reduction can affect female receptivity in Drosophila and leave male-female courtship behavior unaffected. Here, we used genetic and pharmacological approaches to decrease the dopamine level in dopaminergic cells in Drosophila, and investigated the consequence of this manipulation on male homosexual courtship behavior. We find that reduction of dopamine level can induce Drosophila male-male courtship behavior, and that this behavior is mainly due to the increased male attractiveness or decreased aversiveness towards other males, but not to their enhanced propensity to court other males. Chemical signal input probably plays a crucial role in the male-male courtship induced by the courtees with reduction of dopamine. Our finding provides insight into the relationship between the dopamine reduction and male-male courtship behavior, and hints dopamine level is important for controlling Drosophila courtship behavior.
doi:10.1371/journal.pone.0004574
PMCID: PMC2642723  PMID: 19238209
22.  To signal or not to signal? Chemical communication by urine-borne signals mirrors sexual conflict in crayfish 
BMC Biology  2010;8:25.
Background
Sexual selection theory predicts that females, being the limiting sex, invest less in courtship signals than males. However, when chemical signals are involved it is often the female that initiates mating by producing stimuli that inform about sex and/or receptivity. This apparent contradiction has been discussed in the literature as 'the female pheromone fallacy'. Because the release of chemical stimuli may not have evolved to elicit the male's courtship response, whether these female stimuli represent signals remains an open question. Using techniques to visualise and block release of urine, we studied the role of urine signals during fighting and mating interactions of crayfish (Pacifastacus leniusculus). Test individuals were blindfolded to exclude visual disturbance from dye release and artificial urine introduction.
Results
Staged female-male pairings during the reproductive season often resulted in male mating attempts. Blocking female urine release in such pairings prevented any male courtship behaviour. Artificial introduction of female urine re-established male mating attempts. Urine visualisation showed that female urine release coincides with aggressive behaviours but not with female submissive behaviour in reproductive interactions as well as in intersexual and intrasexual fights. In reproductive interactions, females predominately released urine during precopulatory aggression; males subsequently released significantly less urine during mating than in fights.
Conclusions
Urine-blocking experiments demonstrate that female urine contains sex-specific components that elicit male mating behaviour. The coincidence of chemical signalling and aggressive behaviour in both females and males suggests that urine release has evolved as an aggressive signal in both sexes of crayfish. By limiting urine release to aggressive behaviours in reproductive interactions females challenge their potential mating partners at the same time as they trigger a sexual response. These double messages should favour stronger males that are able to overcome the resistance of the female. We conclude that the difference between the sexes in disclosing urine-borne information reflects their conflicting interests in reproduction. Males discontinue aggressive urine signalling in order to increase their chances of mating. Females resume urine signalling in connection with aggressive behaviour, potentially repelling low quality or sexually inactive males while favouring reproduction with high quality males.
doi:10.1186/1741-7007-8-25
PMCID: PMC2867775  PMID: 20353555
23.  Evolutionary Rate Covariation Identifies New Members of a Protein Network Required for Drosophila melanogaster Female Post-Mating Responses 
PLoS Genetics  2014;10(1):e1004108.
Seminal fluid proteins transferred from males to females during copulation are required for full fertility and can exert dramatic effects on female physiology and behavior. In Drosophila melanogaster, the seminal protein sex peptide (SP) affects mated females by increasing egg production and decreasing receptivity to courtship. These behavioral changes persist for several days because SP binds to sperm that are stored in the female. SP is then gradually released, allowing it to interact with its female-expressed receptor. The binding of SP to sperm requires five additional seminal proteins, which act together in a network. Hundreds of uncharacterized male and female proteins have been identified in this species, but individually screening each protein for network function would present a logistical challenge. To prioritize the screening of these proteins for involvement in the SP network, we used a comparative genomic method to identify candidate proteins whose evolutionary rates across the Drosophila phylogeny co-vary with those of the SP network proteins. Subsequent functional testing of 18 co-varying candidates by RNA interference identified three male seminal proteins and three female reproductive tract proteins that are each required for the long-term persistence of SP responses in females. Molecular genetic analysis showed the three new male proteins are required for the transfer of other network proteins to females and for SP to become bound to sperm that are stored in mated females. The three female proteins, in contrast, act downstream of SP binding and sperm storage. These findings expand the number of seminal proteins required for SP's actions in the female and show that multiple female proteins are necessary for the SP response. Furthermore, our functional analyses demonstrate that evolutionary rate covariation is a valuable predictive tool for identifying candidate members of interacting protein networks.
Author Summary
Reproduction requires more than a sperm and an egg. In animals with internal fertilization, other proteins in the seminal fluid and the female are essential for full fertility. Although hundreds of such reproductive proteins are known, our ability to understand how they interact remains limited. In this study, we investigated whether shared patterns of protein sequence evolution were predictive of functional interactions by focusing on a small network of proteins that control fertility and female post-mating behavior in the fruit fly, Drosophila melanogaster. We first showed that the six proteins already known to act in this network display correlated patterns of evolution across the Drosophila phylogeny. We then screened hundreds of otherwise uncharacterized male and female reproductive proteins and identified those with patterns of evolution most similar to those of the known network proteins. We tested each of these candidate genes and found six new network members that are each required for long-term fertility. Using molecular genetics, we also observed that the steps in the network at which these new proteins act are consistent with their strongest evolutionary correlations. Our results suggest that patterns of coevolution may be broadly useful for predicting protein interactions in a variety of biological processes.
doi:10.1371/journal.pgen.1004108
PMCID: PMC3894160  PMID: 24453993
24.  Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate 
Current biology : CB  2007;17(7):599-605.
Summary
Reproductive behavior in Drosophila has both stereotyped and plastic components that are driven by age- and sex-specific chemical cues. Males who unsuccessfully court virgin females subsequently avoid females that are of the same age as the trainer. In contrast, males trained with mature mated females associate volatile appetitive and aversive pheromonal cues and learn to suppress courtship of all females. Here we show that the volatile aversive pheromone that leads to generalized learning with mated females is (Z)-11-octadecenyl acetate (cis-vaccenyl acetate, cVA). cVA is a major component of the male cuticular hydrocarbon profile, but it is not found on virgin females. During copulation, cVA is transferred to the female in ejaculate along with sperm and peptides that decrease her sexual receptivity. When males sense cVA (either synthetic or from mated female or male extracts) in the context of female pheromone, they develop a generalized suppression of courtship. The effects of cVA on initial courtship of virgin females can be blocked by expression of tetanus toxin in Or65a, but not Or67d neurons, demonstrating that the aversive effects of this pheromone are mediated by a specific class of olfactory neuron. These findings suggest that transfer of cVA to females during mating may be part of the male’s strategy to suppress reproduction by competing males.
doi:10.1016/j.cub.2007.01.053
PMCID: PMC1913718  PMID: 17363250
Learning and memory; olfaction; Drosophila; pheromones; cis-vaccenyl acetate
25.  Eavesdropping and signal matching in visual courtship displays of spiders 
Biology Letters  2012;8(3):375-378.
Eavesdropping on communication is widespread among animals, e.g. bystanders observing male–male contests, female mate choice copying and predator detection of prey cues. Some animals also exhibit signal matching, e.g. overlapping of competitors' acoustic signals in aggressive interactions. Fewer studies have examined male eavesdropping on conspecific courtship, although males could increase mating success by attending to others' behaviour and displaying whenever courtship is detected. In this study, we show that field-experienced male Schizocosa ocreata wolf spiders exhibit eavesdropping and signal matching when exposed to video playback of courting male conspecifics. Male spiders had longer bouts of interaction with a courting male stimulus, and more bouts of courtship signalling during and after the presence of a male on the video screen. Rates of courtship (leg tapping) displayed by individual focal males were correlated with the rates of the video exemplar to which they were exposed. These findings suggest male wolf spiders might gain information by eavesdropping on conspecific courtship and adjust performance to match that of rivals. This represents a novel finding, as these behaviours have previously been seen primarily among vertebrates.
doi:10.1098/rsbl.2011.1096
PMCID: PMC3367748  PMID: 22219390
communication; eavesdropping; signal matching; spiders; Lycosidae

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