How does courtship behavior aid survival

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Trends Ecol Evol 7 : 30 Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide.

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Volume Article Contents Abstract. Courtship displays and coloration as indicators of safety rather than of male quality : the safety assurance hyposthesis. Warner , Robert R. Address correspondence to R. E-mail : warner lifesci. Oxford Academic. Google Scholar. Cite Cite Robert R. Select Format Select format. Permissions Icon Permissions. Abstract Male courtship displays and bright coloration are usually assumed to provide information to females about some aspect of the male's value as a mate.

Figure 1. Open in new tab Download slide. Table 1 Two-factor analysis of variance of the effect of total flank patch width and percentage white area in the flank patch on visibility distance.

SS, sum of squares ; MS, mean square. Observations were made on 5 different days. Patch width A 2 0. Open in new tab. Overall, the physiological roles of the GPCR-mediated actions of steroids and the underlying molecular mechanisms remain poorly understood, and sometimes controversial, in spite of their importance. In particular, it is unknown how this non-canonical steroid mechanism influences neural functions and complex behaviors Ishimoto, Drosophila genetics has been extensively used to study the roles and mechanisms of action of steroid hormones in vivo.

The major steroid hormone in Drosophila is the molting hormone hydroxy-ecdysone 20E , which orchestrates a wide array of developmental events, including embryogenesis, larval molting and metamorphosis. In general, the functions of 20E during development and adulthood are thought to be executed by ecdysone receptors EcRs , members of the evolutionarily conserved nuclear hormone receptor family Ishimoto, In situ hybridization and microarray data revealed that DopEcR transcripts are preferentially expressed in the nervous system.

In heterologous cell culture systems, DopEcR is localized to the plasma membrane and responds to dopamine as well as ecdysteroids ecdysone and 20E , modulating multiple, intracellular signaling cascades Srivastava, Furthermore, Inagaki recently detected DopEcR expression in the sugar-sensing gustatory neurons of adult flies, and showed that DopEcR-mediated dopaminergic signaling enhances the proboscis extension reflex during starvation.

Nonetheless, little is known about whether DopEcR functions as a steroid receptor in vivo , and about how it drives responses in the central nervous system CNS to modulate complex behaviors. This study reports that DopEcR mediates non-genomic ecdysone signaling in the adult brain, and that it is critical for memory processing.

It was also shown that, during memory processing, DopEcR transmits information via novel steroid signals that interact with the cAMP pathway, a signaling cascade that is universally important for neuronal and behavioral plasticity. This genetic study thus uncovers underappreciated GPCR-mediated functions and mechanisms of action that employ non-canonical steroid signaling to regulate the adult nervous system and, thereby, behavior Ishimoto, This study used genetic, pharmacological, and behavioral approaches in Drosophila to demonstrate that the steroid hormone 20E rapidly regulates behavioral plasticity via a non-genomic mechanism that is mediated by the GPCR-family protein DopEcR.

This non-canonical steroid signaling pathway was found to have strong functional interactions with the classical 'memory genes' rut and dnc , which encode the central components of the cAMP pathway. The identification of 20E as an important modulator of cAMP signaling in the adult Drosophila brain reveals an unprecedented opportunity - that of taking advantage of fly genetics to dissect the molecular and cellular mechanisms responsible for the non-genomic steroid signaling that underlies neuronal and behavioral plasticity Ishimoto, Electrophysiological analyses revealed that the adult giant-fiber GF pathway of DopEcR mutant flies is more resistant to habituation than that of control flies.

Direct excitation of GF or its downstream elements would lead to a short-latency response of the dorsal longitudinal flight muscle DLM , which could follow high-frequency stimuli up to several hundred Hz. In contrast, the afferent input to the GF leads to a long-latency response that is labile and fails to follow repetitive stimulation well below Hz and displays habituation even at Hz. Although there is the possibility that DopEcR-positive thoracic neurons may modulate thoracic motor outputs and contribute to certain parameters of the habituation process not characterized in this study, the more effective modulation would occur in the more labile element afferent to the GF circuit rather than the robust GF-PSI-DLMn downstream pathway PSI referring to peripherally synapsing interneuron , which is responsible for the reliability of the escape reflex.

Thus, the mutant phenotype in habituation indicates that DopEcR positively controls activity-dependent suppression of neuronal circuits afferent to the GF neurons in the brain Ishimoto, Moreover, the finding that DopEcR and rut mutants have a similar GF habituation phenotype raises the possibility that DopEcR positively regulates cAMP levels in the relevant neurons following repetitive brain stimulation.

Besides GF habituation, Drosophila displays olfactory habituation, which is mediated by the neural circuit in the antennal lobe. Interestingly, Das found that olfactory habituation is induced by enhancement of inhibitory GABAergic transmission, and that rut function is required for this neuronal modulation.

Several studies already suggested that 20E has rapid, EcR-independent effects in Drosophila and other invertebrate species. For example, 20E was shown to reduce the amplitude of excitatory junction potentials at the dissected Drosophila larval neuromuscular junction NMJ , and to do so within minutes of direct application Ruffner, Whereas treatment with 20E did not change the size and shape of the synaptic currents generated by spontaneous release, it led to a reduction in the number of synaptic vesicles released by the motor nerve terminals following electrical stimulation.

A similar effect of 20E was observed in crayfish, and it was suggested that the suppression of synaptic transmission by 20E may account for the quiescent behavior of molting insects and crustaceans.

These observations suggested that 20E suppresses synaptic efficacy under certain conditions by modulating presynaptic physiology through a non-genomic mechanism. It is possible that such actions of 20E are mediated by DopEcR. To detail the mechanisms underlying DopEcR-dependent neural plasticity, it will be worthwhile to determine if and how DopEcR contributes to 20E-induced, rapid synaptic suppression at the physiologically accessible larval NMJ, and to determine the extent to which non-genomic mechanisms of steroid actions are shared between the larval NMJ and the adult brain Ishimoto, One surprising finding made in this study is that ecdysone signaling can modify the phenotypes associated with mutations in the classic 'memory genes', namely rut and dnc , through the actions of DopEcR.

This assumption is supported by the finding that loss-of-function dnc mutants restore courtship memory when DopEcR activity is suppressed. A similar restoration of the dnc memory phenotype also occurs in a dnc and rut double mutant, again supporting the idea that DopEcR positively regulates cAMP production Ishimoto, The results of rescue and phenocopy experiments indicate that the MB is critical for the DopEcR-dependent processing of courtship memory.

Surprisingly, enhancement of DopEcR-mediated ecdysone signaling restored courtship memory in flies harboring a strong hypomorphic allele of rut rut A similar result was obtained even in mutants harboring a presumptive rut null allele rut 1. These results suggest that, upon stimulation by 20E, DopEcR may be able to signal via another adenylyl cyclase that can compensate for the lack of Rut.

This interesting possibility requires further investigation Ishimoto, This study has focused on the roles and mechanisms of action of DopEcR-mediated, non-genomic ecdysone signaling. Since it has been found that 20E levels rise in the head during courtship conditioning Ishimoto, , the data presented in this study suggest that DopEcR is activated by 20E during conditioning, triggers a rise in cAMP levels and induces physiological changes that subsequently suppress courtship behavior.

Previous cell-culture studies suggested that DopEcR also responds to dopamine to modulate intracellular signaling Srivastava, It is therefore necessary to consider whether dopamine is directly involved in the processing of courtship memory through DopEcR. This possibility is thought unlikely because even when courtship memory is disrupted by pharmacological suppression of dopamine synthesis, 20E feeding can compensate for decreased dopamine and allow restoration of memory.

Although dopamine plays a significant role in courtship memory, the results suggest that DopEcR does not act as the major dopamine receptor in this particular learning paradigm. The possibility is thus favored that dopamine contributes to courtship memory in parallel with, or upstream of, DopEcR-mediated ecdysone signaling. Ecdysone signaling through nuclear EcRs is necessary for forming long-term courtship memory that lasts at least 5 days, but appears not to have a significant effect on short-term courtship memory Ishimoto, In contrast, we found that DopEcR-mediated ecdysone signaling is critical for habituation and minute courtship memory.

These findings suggest that DopEcR and EcRs control distinct physiological responses to courtship conditioning, and that the former regulates short-term memory, while the latter regulates long-term memory.

Although non-genomic actions of steroid hormones have been implicated in vertebrate learning and memory, such actions have been attributed mainly to the classical nuclear hormone receptors that function outside of the nucleus and exert roles distinct from those of steroid-activated transcription factors. Although recent evidence has shown that membrane-bound receptors independent of the classical estrogen receptors are involved in estradiol-induced consolidation of hippocampal memory, the molecular identities of these proteins have not been established.

The current findings in this study provide a novel framework for dissecting GPCR-mediated steroid signaling at the molecular and cellular levels. Furthermore, future analysis of the functional interplay between genomic and non-genomic steroid signaling pathways is expected to reveal novel mechanisms through which steroid hormones regulate plasticity of the nervous system and other biological phenomena Ishimoto, In fly courtship, the female decides whether or not to mate and is thought to display receptivity by slowing down to accept the male.

Very little is known on the neuronal brain circuitry controlling female receptivity. This study used genetic manipulation and behavioural studies to identify a novel set of neurons in the brain that controls sexual receptivity in the female without triggering the postmating response. These neurons, defined by the expression of the transcription factor Apterous , affect the modulation of female walking speed during courtship.

Interestingly, it was found that the Apterous neurons required for female receptivity are neither Doublesex nor Fruitless positive suggesting that Apterous neurons are not specified by the sex-determination cascade. Overall, these findings identify a neuronal substrate underlying female response to courtship and highlight the central role of walking speed in the receptivity behaviour Aranha, Reproductive behaviours are essential for the survival and fitness of the species.

In Drosophila melanogaster , as in many other species, the decision of whether or not to mate is made by the female. However, understanding about the behaviour displayed by the virgin female and the neuronal circuits underlying it is still poor. This study set out to identify neurons involved in the response of virgin females to courting males.

Female virgins with compromised activity in apterous neurons in the brain display a substantial reduction in copulation. What is specifically changed in the premating behaviour of apterous -silenced females? Ovipositor extrusion is a display that occurs exclusively in the context of courtship. A caveat of this work is the large number of neurons that are affected by this manipulation. Is the low copulation rate a result of an issue created by silencing large numbers of neurons?

The capacity to recognize the male partner does not seem to be affected and the phenotypes that were observed are revealed only in the context of courtship, which strongly suggests that parts of the natural receptivity circuit were specifically affected Aranha, How can changes in activity of apterous neurons affect female velocity during courtship?

The best understood cue from the male that shapes female velocity is the song. It is unlikely though that apterous -silenced females have impaired hearing. Third order auditory neurons innervate the ventral lateral protocerebrum VLP. The VLP neurons and a few other neurons that express apterous were silenced, and no receptivity phenotype was observed. Moreover, flies with impaired hearing do not copulate within the time of the analysis. Most likely apterous neurons are involved in integrating sensory cues provided by the male that would lead to a receptive state of the female and over time result in a decrease of female velocity.

Aranha, This study also uncovered a role for apterous neurons in controlling egg laying, another critical aspect of reproductive behaviour. Females that have mated and then have their apterous neurons in the brain inhibited lay very few eggs, unlike control females.

Classic gynandromorph studies pointed to an egg laying suppression focus in the brain, but this study seems to have identified a focus that promotes egg laying when active. A recent study implicates the doublesex -positive and female-specific PMN2 descending neurons in oviposition behaviou. In conclusion, these findings contribute to understanding female receptivity and highlight the central role of female speed modulation during courtship.

It will be interesting to elucidate in the future the role of the different apterous clusters and reveal how they interact with the sexual specification circuits Aranha, Insulin signaling in the peripheral and central nervous system regulates female sexual receptivity during starvation in Drosophila Many animals adjust their reproductive behavior according to nutritional state and food availability.

Drosophila females for instance decrease their sexual receptivity following starvation. Insulin signaling, which regulates many aspects of insect physiology and behavior, also affects reproduction in females. This study shows that insulin signaling is involved in the starvation-induced reduction in female receptivity. More specifically, females mutant for the insulin-like peptide dilp5 were less affected by starvation compared to the other dilp mutants and wild-type flies.

Knocking-down the insulin receptor, either in all fruitless-positive neurons or a subset of these neurons dedicated to the perception of a male aphrodisiac pheromone, decreased the effect of starvation on female receptivity. Disrupting insulin signaling in some parts of the brain, including the mushroom bodies even abolished the effect of starvation.

In addition, Fruitless-positive neurons in the dorso-lateral protocerebrum and in the mushroom bodies co-expressing the insulin receptor were identified.

Together, these results suggest that the interaction of insulin peptides determines the tuning of female sexual behavior, either by acting on pheromone perception or directly in the central nervous system Lebreton, a. Drosophila females need nutrients to produce eggs and a nutrient rich substrate to lay their eggs.

When food is scarce it would therefore be beneficial for flies to decrease their sexual behavior and to focus on food searching instead. On the other hand, female flies can store sperm and use it several days later when conditions are suitable.

It could therefore be optimal for females to remain receptive for short periods of food deprivation. Several insulin peptides produced in specific spatiotemporal patterns acting through one single receptor enables a fine-scale regulation of behaviors in response to changes in physiology. The expression of the different dilps is differentially affected by food quality or food deprivation. For instance, both starvation and dietary restriction reduce the expression of dilp5 but increase the expression of dilp6 , while the expression of dilp2 is not affected by either condition.

The results suggest that DILP5 might be involved in the decrease of receptivity during non-feeding stages. Indeed, dilp5 mutant females were less affected by starvation than other dilp mutants. Although, background mutation effects cannot be completely ruled out, this suggests that DILP5 might interact with other DILPs to finely tune female sexual receptivity Lebreton, a. Insulin is known to act on the olfactory system to modulate odor sensitivity after feeding.

Moreover, normal InR expression in Or67d-expressing Fruitless-positive OSNs is necessary for fed females to be attracted to a blend of food odors and cVA, a pheromone promoting sexual receptivity. The results suggest that insulin signaling in Fruitless-positive neurons, and more specifically in Or67d OSNs may decrease sexual receptivity during starvation Lebreton, a.

Fruitless-positive cells other than pheromone-sensing neurons can also be involved. Different Fruitless-positive cells in the protocerebrum were found that strongly express InR. First of all, a large number of Kenyon cells in the calyx of the mushroom bodies express both Fruitless and the insulin receptor.

Additionally, one pair of neurons was found with somata located in the anterior dorso-lateral protocerebrum. It was not possible to trace any processes from these somata, and thus it is not known what neuropils they innervate. However, the fact that InR immunostaining was observed in Fruitless neurons, most of which were Kenyon cells, corroborate the behavioral results.

Indeed, the sexual receptivity of females in which insulin signaling was knocked down in the mushroom bodies was not affected by starvation. Interestingly, the mushroom bodies are not required for virgin females to be receptive, suggesting that these structures may regulate the activity of neuronal networks inducing sexual receptivity. However, this result must be take with caution, given the fact that the Gal4 line that were used to target the mushroom bodies also drive expression to some extent in other brain tissues.

Further experiments will be necessary to confirm that the mushroom bodies are indeed responsible for this effect Lebreton, a. Insulin signaling not only modulates neuronal activity in adults but also shapes neuronal networks during development. The effects observed in this study may therefore be the consequence of a developmental defect of specific neuronal circuitry rather than a direct effect of insulin on these neurons during starvation.

However, Fruitless-positive neurons being required for females to be receptive, fed females would be expected to be unreceptive if the disruption of insulin signaling had altered the connectivity of these neurons during development, which was not the case.

This suggests that insulin acts on these neurons during adult stage to modulate sexual receptivity. This is different for the mushroom bodies, which are not necessary for females to be receptive. Knocking down InR specifically during development or specifically in adults will be necessary to disentangle these two possible modes of action of insulin Lebreton, a. In contrast with Fruitless neurons and the mushroom bodies, no effect was observed of the corpora allata in the insulin-dependent control of sexual receptivity, whereas these structures have been linked to the development of receptivity in virgin females.

This result should however be taken with caution, considering the behavioral variability displayed by the different transgenic lines, which would have prevented observing of subtle changes. Nonetheless, the results suggest that the structures that generate behaviors such as the corpora allata and those modulating these behaviors for example the mushroom bodies can be different and the underlying mechanisms uncoupled Lebreton, a.

Taken together, Drosophila flies adjust their sexual behavior to match their nutritional state. Together with other hormonal pathways, insulin regulates some aspects of sexual activity, both after food intake and after a period of starvation. The results suggest that specific insulin peptides regulate female receptivity, possibly by acting on pheromone perception at the periphery or directly in the central nervous system. Indeed, the mushroom bodies probably play a major role in the insulin-dependent effect of starvation on female sexual receptivity.

The next step will be to untangle the specific neuronal circuitry involved Lebreton, a. A male's seminal fluid increases later competitors' productivity Polyandrous females allow for sexual selection to persist after mating. In the event that females successfully mate with more than one male, sperm competition can occur. Seminal fluid proteins can indirectly affect a male's success in sperm competition through reducing the remating behaviour of females, and can directly influence sperm competition through directly displacing competitor sperm or inducing females to eject it.

These direct effects on competitor sperm are thought to contribute to the 'second male advantage', whereby the second male to mate sires the majority of offspring. This study shows an additional mechanism where seminal proteins already present within a mated female appear to enhance offspring production of later competitor males, and contribute to second male advantage.

Counter to expectation, increased offspring production was not due to a priming effect of greater early female productivity, nor was it through a general and consistent increase in offspring production.

Instead, enhanced productivity was solely through lengthening the time that offspring are sired by the second male, indicating that seminal proteins from the first male to mate may enhance second male advantage through a presumably unintended protective effect on subsequent competitor sperm Nguyen, The Drosophila post-mating response: Gene expression and behavioral changes reveal perdurance and variation in cross-tissue interactions Examining cross-tissue interactions is important for understanding physiology and homeostasis.

In animals, the female gonad produces signaling molecules that act distally. This study examined gene expression in Drosophila melanogaster female head tissues in 1 virgins without a germline compared to virgins with a germline, 2 post-mated females with and without a germline compared to virgins, and 3 post-mated females mated to males with and without a germline compared to virgins.

In virgins, the absence of a female germline results in expression changes in genes with known roles in nutrient homeostasis. At one- and three-days post-mating, genes that change expression are enriched with those that function in metabolic pathways, in all conditions. Female post-mating impacts were systematically examined on sleep, food preference and re-mating, in the strains and time points used for gene expression analyses and compare to published studies.

Post-mating, gene expression changes vary by strain, prompting an examination of variation in female re-mating. Together, these data reveal how gene expression and behavior in females are influenced by cross-tissue interactions, by examining the impact of mating, fertility, and genotype Newell, Structural variation in Drosophila melanogaster spermathecal ducts and its association with sperm competition dynamics The ability of female insects to retain and use sperm for days, months, or even years after mating requires specialized storage organs in the reproductive tract.

In most orders, these organs include a pair of sclerotized capsules known as spermathecae. In recent years, evidence that copulatory and post-copulatory events play an important role in determining the outcome of fertilization and reproduction has been increasing. Post-copulatory selection refers to the events that occur during and after mating.

Post-copulatory male-male competition is known as sperm competition a term coined by Parker who recognized that when females mate with multiple males, their ejaculates compete inside the female reproductive tract for access to eggs.

Post-copulatory female choice refers to the ability of females to affect the likelihood that sperm from a particular male fertilizes their eggs, and their decision to invest in offspring based on the identity of the male with whom they mate. Females exert this choice via morphological, chemical and behavioral adaptations.

This type of selection is called cryptic choice because it occurs inside the female reproductive tract and cannot be detected from behavioral studies alone Eberhard Although both sexes are seeking to optimize their reproductive success, their genetic interests are not aligned, resulting in sexual conflict Parker Traits that allow a male to increase his reproductive success at the expense of the female will be positively selected if the female mates with multiple males.

These traits will be genetically transmitted and spread in the population, despite their negative effects on female reproductive success, if the reproductive success of these males is higher than that of males lacking such traits Parker Sexual conflict can often result in an evolutionary arms race, whereby the evolution of a trait that imposes harm on one sex will result in evolution of a counter-trait to mitigate the harm on the affected sex, with subsequent escalation in both Chapman et al.

Examples of sexual conflict include traumatic insemination in bed bugs, copulatory grasping and anti-grasping structures in waterstriders, and genital coevolution in waterfowl. Birkhead, T. Sperm Competition and Sexual Selection. Calhim, S. Testes size in birds: quality versus quantity — assumptions, errors and estimates.

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What are the five main groups of arthropods. Which characteristics do scientists use to group species. Hypothalamus produces hormones secreted by which gland. Q: How does courtship behavior aid survival? Write your answer Related questions. How does instinctive coutship behavior aid survival? How does a panda's behavior aid survival? What is the function in courtship behavior for an animal?

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