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PubMed1994

Behavioral and neurobiological implications of sex-determining factors in Drosophila.

The function of the central nervous system as it controls sex-specific behaviors in Drosophila has been studied with renewed intensity, in the context of genetic factors that influence the development of sexually differentiated aspects of this insect. Three categories of genetic variations that cause anomalies in courtship and mating behaviors are discussed: (1) mutants isolated with regard to courtship defects, of which putatively courtship-specific variants such as the fruitless mutant are a subset; (2) general behavioral and neurological variants (including sensory and learning mutants), whose defects include subnormal reproductive performance; and (3) mutations of genes within the sex-determination regulatory hierarchy of Drosophila, the analysis of which has included studies of reproductive behavior. Recent studies of mutations in two of these categories have provided new insights into the control of neuronally based aspects of sex-specific behavior. The doublesex gene, the final factor acting in the sex-determination hierarchy, had been previously thought to regulate all aspects of sexual differentiation. Yet, it has been recently shown that doublesex does not control at least one neuronally-determined feature of sex-specific anatomy--a muscle in the male's abdomen, whose normal development is, however, dependent on the action of fruitless. These considerations prompted us to examine further (and in some cases re-examine) the influences exerted by sex-determination hierarchy genes on behavior. Our results--notably those obtained from assessments of doublesex mutations' effects on general reproductive actions and on a particular component of the courtship sequence (male "singing" behavior)--lead to the suggestion that there is a previously unrecognized branch within the sex-determination hierarchy, which controls the differentiation of the male- and female- specific phenotypes of Drosophila. This new branch separates from the doublesex-related one immediately before the action of that gene (just after transformer and transformer-2) and appears to control as least some aspects of neuronally determined sexual differentiation of males.

Animals↗

PubMed2004

Brief alteration in dopaminergic function during development causes deficits in adult reproductive behavior.

Our previous research revealed dramatic increases in dopaminergic function in vocal control and auditory nuclei in male zebra finches during the period of song learning. Such increases were not seen in the hypothalamic areas examined. In the current study, we manipulated dopamine receptor function during this period to determine how this might affect later singing behavior. Males were implanted with osmotic minipumps providing 0, 0.5, or 5 microg/g/day of the mixed D1/D2 dopamine receptor antagonist cis-flupenthixol from day 45 until day 57. At approximately 86 days of age, males were given subcutaneous silastic implants containing a maintenance dose of androgen, in case antagonist treatment interfered with adult androgen secretion. One week later, they began a series of three weekly tests to determine if this early treatment affected courtship singing. Males treated with the low dose of cis-flupenthixol showed profound decrements in courtship singing and copulatory behavior. Unlike saline-treated controls, low-dose males sang to females infrequently. High-intensity courtship displays in which males dance towards females while singing were most affected. Despite their decreased courtship singing, low-dose males were interested in females. They approached females as frequently as males in the other two groups, but antagonist-treated males were less likely to follow females if they moved. Low-dose males also attempted to mount females significantly less often than high-dose males. High-dose males groomed significantly less frequently than males in the other two groups. Thus, brief early treatment with cis-flupenthixol had profound and long-lasting effects on female-directed singing and on copulatory behavior, despite androgen treatment.

Androgens↗

PubMed2002

Androgen and behavior in the male three-spined stickleback, Gasterosteus aculeatus I.--changes in 11-ketotestosterone levels during the nesting cycle.

Circulating 11-ketotestosterone (11KT) levels are higher during the courtship phase than during the later parental phase in a number of male teleosts. The present study describes the temporal changes in 11KT levels and their relationships to changes in courtship behavior, after different number of spawnings, over the nesting cycle of the male three-spined stickleback, Gasterosteus aculeatus, a small teleost showing pronounced paternal behavior. Plasma 11KT levels, measured by radioimmunoassay, were approximately 34 times higher during the initial courtship phase than at the end of the following parental phase in spawned males. In addition, males that spawned with three or more females on a single day showed an earlier decline in 11KT levels and in courtship behavior compared to males that were only allowed to spawn with a single female. Plasma 11KT levels remained high in males not allowed to spawn.

Animals↗

PubMed1994

Songs produced by the females of the Drosophila virilis group of species.

Females of the Drosophila virilis group of species may vibrate their wings during courtship producing songs consisting of trains of successive sound pulses (pulse song) or sinusoidal hums (sine song). In the present study we describe these songs and study their role in courtship using a transition analysis. To find out which songs should be classified as pulse songs and which ones as sine songs, we studied the inheritance of different song types in interspecific F1 hybrids. In only a few species did the females produce large quantities of song in successful courtships. The males' reactions to female songs varied from licking and singing to stopping the courtship. Pulse trains with short and long intervals between successive pulses appeared to be different forms of the pulse song, while sine song (sinusoidal hums) was inherited independently of the pulse song.

Animals↗

PubMed1986

Males disposed to commit rape.

The hypothesis that the preferential rape pattern belongs among the courtship disorders like voyeurism, exhibitionism, and toucheurism was tested. The study consisted of two experiments. The first compared 11 rape-prone males, who were most likely afflicted with the preferential rape pattern, with 11 sexually normal controls on penile response to narratives that depicted scenes in which the individual engaged in behavior typical of voyeurs, exhibitionists, or toucheurs. Narratives depicting normal tactile interaction (short of intercourse) with a genuinely participating woman, normal intercourse, and sexually neutral scenes were also presented. The rape-prone males responded more to the voyeuristic situations than did the controls. The standing of the normal intercourse situations on the scale of erotic value, relative to the other above-mentioned situations, was lower for the rape-prone males than for the normal controls. A second experiment compared 12 rape-prone males, who most likely demonstrated the preferential rape pattern, with 12 males with (other) courtship disorders and 12 sexually normal controls. Penile response to narratives depicting the individual involved in pretactile erotic activity, in tactile sexual activity short of intercourse, or in having intercourse was compared. Each situation was presented in two modalities depicting either a genuinely participating woman or a woman fearful of the individual. The penile responses of the rape-prone males, as well as those of males with other courtship disorders, differentiated less between sexual interaction with a fearful woman and such interaction with a participating woman than did the penile responses of normal controls. There was no significant difference in this respect between the rape-prone males and males with other courtship disorders.

Adult↗

PubMed1993

Inbreeding depression and male-mating behavior in Drosophila melanogaster.

There have been relatively few studies designed to investigate the effects of inbreeding on behavioral traits. To study this phenomenon, five experimental lines of Drosophila melanogaster made isogenic for chromosome 2 were evaluated for their male-mating ability and, subsequently, male courtship behavior. All lines showed significant reductions in overall mating ability, and males from all of these lines displayed impaired mating behavior, with two lines displaying particularly aberrant courtship patterns. Line 16 displayed an inability to successfully initiate copulation following successful courtship, while line 17 displayed significant reduction in locomotor activity, resulting in virtually no successful courtship or copulatory activity. The implications of these findings for competitive mating ability in wild Drosophila populations are presented. Further, the importance of mating success as a fitness component in the management of potentially highly inbred populations of endangered species is discussed.

Animals↗

PubMed1999

Sexual behavior mutants revisited: molecular and cellular basis of Drosophila mating.

The study of Drosophila melanogaster by a combination of forward genetics with specific mutants, and reverse genetics, in which a given gene is expressed in an appropriate brain area to test its effect on behavior, provides a unique opportunity to explore the causal relationship between a particular gene, its function in the cell and the behavioral outcome at the organismic level. Enhanced male-to-male courtship has been shown to occur as a result of mutations in several different genes. For example, the Voila mutant exhibits intense GAL4 reporter expression in the tarsal gustatory sensilla, suggesting the importance of tapping by a male on the female abdomen with his forelegs. Feminization of parts of the antennal lobe and mushroom body by targeted expression of a female-determining gene transformer+ (tra+) drives the male to court other males. Mutations in the tra target gene fruitless (fru), which is expressed in the antennal lobe as well as the suboesophageal ganglion (the gustatory inputs are processed here), also induce homosexual courtship in males. These results suggest that sensory inputs mediated and/or processed by the tarsal receptors, suboesophageal ganglion, antennal lobe and mushroom body contribute to the regulation of male-female courtship. Mosaic analysis localized the neural center for male courtship behavior to the posterior dorsal brain, in which the sensory information processed by the aforementioned neural structures may be integrated. Another mosaic study mapped the neural center for female sexual behavior, as measured by her receptiveness to copulation, to the anterior dorsal brain. The issue as to how the mutations that reduce female sexual receptiveness, e.g. dissatisfaction (dsf), spinster (spin) and chaste (cht), affect the structure and/or function of this neural center deserves to be addressed urgently.

Animals↗

PubMed1983

Hormonal specificity and activation of sexual behavior in male zebra finches.

Castrated zebra finches receiving one of six hormone treatments were given three weekly tests with different females and their sexual behavior was contrasted with that of two control groups consisting of intact or castrated males given implants of cholesterol. The six hormone treatments were: two aromatizable androgens, testosterone (T) and androstenedione (AE); two nonaromatizable androgens, androsterone (AN) and dihydrotestosterone (DHT); an estrogen, estradiol (E); or a combination of E + DHT. Half the males receiving DHT received the 5 alpha-isomer, half received the 5 beta-isomer. Castration significantly reduced the proportion of males which courted females, total courtship displays, high-intensity courtship displays, beak wiping activity, and significantly increased the latencies to show these behaviors compared to intact males. Castrated males never attempted to mount a female. All of these measures of courtship and copulatory behavior were restored to normal levels only by treatments providing both estrogenic and alpha-androgenic metabolites (i.e., T, AE, E + alpha DHT). AE was clearly the most effective of these, raising behavior significantly above normal on several measures. AN treatment was more effective than alpha DHT on all measures and not significantly different from intact birds on some. Treatment with E, alpha DHT, beta DHT, or E + beta DHT was totally ineffective. Surprisingly, females only solicited males whose hormone treatments provided estrogenic metabolites. Not only did they solicit males given aromatizable androgens, which showed high rates of courtship activity, they also solicited males given E or E + beta DHT, some of which never even courted. Castration and hormone treatment also affected body and syringeal weight, but in opposite directions. Castration increased body weight while decreasing syringeal weight. Hormone treatments providing alpha-androgenic metabolites decreased body weight and increased syrinx weight. Treatments supplying estrogen as well were slightly more effective.

Androgens↗

PubMed1984

Role of the amygdala in the reproductive and aggressive behavior of the lizard, Anolis carolinensis.

Thirteen male green anole lizards were lesioned in the ventromedial nucleus (VMN) of the posterior dorsal ventricular ridge ("amygdala") and/or the paleostriatum (PS) to determine the influence of these structures on assertion and challenge displays addressed to male intruders, or courtship displays and copulatory neckgrip directed toward females. Lesions that affected both VMN and PS reduced or eliminated both challenge and courtship displays as well as the neckgrip, a crucial component in courtship. Subjects with lesions limited to VMN had assertion and challenge left unimpaired but courtship was reduced and neckgrip eliminated in most subjects. A lesion restricted to PS caused a significant deficit in challenge while other measures were unaffected. These data indicate that the VMN is involved in reproductive function in the green anole lizard.

Aggression↗

PubMed2006

Ram effect: adult rams induce a greater reproductive response in anestrous ewes than yearling rams.

The introduction of rams to previously isolated anestrous ewes ensures induction of ovulation and estrus in part of the flock, and allows for the potential to conceive. However, there is little known about the desirable characteristics of the rams used to induce these behavioral and physiological responses. Adult rams may be more effective than young rams in induction of these responses. The primary aim of the present study was to compare the response in ewes stimulated by adult or yearling rams. During the non-breeding season, two groups of 121 ewes were stimulated with adult (AR) or yearling (YR) rams. When adult rams were used, significantly more ewes had ovulations (78.5 compared with 61.1%) and came into estrus (47.9 compared with 35.5%). There were more corpora lutea per ewe exposed to rams (0.95+/-0.59 compared with 0.65+/-0.51) and per ewe that had ovulations (1.18+/-0.41 compared with 1.06+/-0.25) and a greater conception rate (58.6 compared with 20.9%) as a result. Subsequently, to determine what signals led to the greater response to adult rams, the courtship behavior of adult and yearling rams toward anestrous ewes was compared in 46 pen tests. There were no significant differences in the frequency of any of the recorded courtship behaviors (anogenital sniffing: 21.9+/-3.4 versus 25.7+/-3.2; lateral approaches: 7.1+/-1.5 compared with 9.9+/-2.9; flehmen: 2.1+/-0.4 compared with 2.2+/-0.4; mount attempts: 0.1+/-0.1 compared with 0.1+/-0.1, for AR and YR, respectively), latency to the onset of courtship behavior (13.1+/-7.0 compared with 17.3+/-6.2s) or the time engaged in courtship behavior (173.1+/-24.6 compared with 199.0+/-26.5s). The difference in the signals produced by adult and yearling rams skin glands was assessed by stimulating ewes with masks containing wool from adult (n=45) or yearling (n=48) rams. More ewes had ovulations (24/45 compared with 11/48) and came into estrus (21/45 compared with 10/48) when wool from adult rams was used. As in Experiment 1, pregnancy and conception rates were greater when adult rams were used, another trial was designed to determine if there were differences in mating and mounting frequency between adult and yearling rams. Seven adult and six yearling rams were subjected to three pen tests each with three estrual ewes. Adult rams mounted more (21.7+/-4.5 compared with 9.8+/-0.7) and tended to ejaculate more frequently (2.9+/-0.5 compared with 1.8+/-0.4) than yearling rams. It is concluded that adult rams induce a greater reproductive response in anestrous ewes than yearling rams, inducing a greater ovulation percentage and estrous response in ewes, resulting in greater ovulation numbers, pregnancy and conception rates. This greater stimulation is, in part, explained by differences in the signals provided in the wool (presumably odors) produced by adult rams. The lesser percentage of pregnancies obtained when yearling rams are used may be explained by differences in mounting behaviors and ejaculation frequency.

Age Factors↗

PubMed2006

C-fos induction in forebrain areas of two different visual pathways during consolidation of sexual imprinting in the zebra finch (Taeniopygia guttata).

Two forebrain areas in the hyperpallium apicale and in the lateral nidopallium of isolated male zebra finches are highly active (2-deoxyglucose technique) on exposure to females for the first time, that is first courtship. These areas also demonstrate enhanced neuronal plasticity when screened with c-fos immunocytochemistry. Both are areas involved in the processing of visual information conveyed by the two major visual pathways in birds, strengthening our hypothesis that courtship in the zebra finch is a visually guided behaviour. First courtship and chased birds show enhanced c-fos induction in the hyperpallial area, which could represent neuronal activity reflecting changes in the immediate environment. The enhanced expression of fos in first courtship birds in lateral nidopallial neurons indicates imminent long-lasting changes at the synaptic level that form the substrate for imprinting, a stable form of learning in birds.

Animals↗

PubMed2006

Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches.

Dopamine (DA) is produced in numerous brain areas and influences a wide variety of social behaviors, but very few data are available to establish the socially-relevant response properties of most DA populations, which comprise eight cell groups numbered A8-A15. Anatomically, these DA populations are evolutionarily conserved, and all have been identified in both birds and mammals. We now report the Fos responses of tyrosine hydroxylase-immunoreactive (TH-ir; putatively dopaminergic) neurons in the A8-A15 cell groups of male zebra finches following exposure to a control condition or one of six different social stimuli: a heterospecific male, conspecific male, fighting in a mate competition paradigm (which includes both male and female stimuli), a courtship interaction without physical contact, a courtship interaction with physical contact but no mounting, and a courtship interaction with mounting. We found that the DA cell groups exhibit distinctive profiles of responsiveness to social stimuli. Fos induction in A8, A9, A10 and midbrain A11 neurons increased significantly in response to a variety of conspecific stimuli, but not heterospecific stimuli. In contrast, Fos induction in the preoptic A14 neurons was observed specifically in response to sexual interactions, and Fos induction in hypothalamic A11 neurons appears to primarily reflect the performance of courtship singing. Infundibular A12 neurons, which may be involved in stress-related processes, showed the highest level of TH+Fos colocalization in control subjects. This colocalization decreased in response to all conspecific stimuli except fighting, and did not decrease following exposure to a heterospecific male.

Analysis of Variance↗

PubMed2000

Hormonal control of urodele reproductive behavior.

Hormonal control of expression of courtship behavior and of development of structures related to the reproductive behavior in two species of Japanese newts, Cynops pyrrhogaster and Cynops ensicauda, was described. Prolactin (PRL) and androgen were essential factors for eliciting courtship behavior. In addition, arginine vasotocin markedly enhanced the expression of courtship behavior. PRL induced migration to water, in which courtship and oviposition take place, and converted the integument from the terrestrial type to the aquatic one. PRL also stimulated the growth of the tail fin, which was blocked by estrogen. Cellular and nuclear size and number of synapses on the somata of Mauthner cells, which are involved in tail movement, were also increased by PRL and androgen. Synthesis of sodefrin, a female-attracting pheromone, in the abdominal gland as well as that of mucopolysaccharides constituting the sac of sperm in the lateral gland was enhanced by PRL and androgen. Structural development of oviducts was elicited by estrogen or PRL to a certain extent, and full oviducal development by the combination of these two hormones, PRL being indispensable for the oviducal jelly secretion.

Animals↗

PubMed2003

Mutations in raised Drosophila melanogaster affect experience-dependent aspects of sexual behavior in both sexes.

Many aspects of the reproductive behavior of Drosophila melanogaster are modified dramatically by experience and age. Males' courtship of immature males and fertilized females decreases over time. Females' receptivity to copulation, and the behaviors that females perform and elicit, are affected by their age and sexual experience. We show that mutations in a raised stock affect all of these age- and experience-dependent aspects of male and female sexual behavior. Experience has no effect on raised males' courtship of immature males and has opposite effects on raised and wild-type males' courtship of fertilized females. In comparison to controls, raised females become sexually mature at an earlier age, and sexually mature raised virgin females copulate more quickly. Following mating, raised females elicit more courtship and remate faster and more frequently than control females.

Animals↗

PubMed2001

Mating asymmetry and the direction of evolution in the Hawaiian cricket genus Laupala.

Based on studies from native Hawaiian Drosophila, a model was proposed to explain sexual isolation and mating asymmetry, from which one could potentially infer the 'direction of evolution'. We examined sexual isolation between allopatric cricket species of the genus Laupala, another endemic Hawaiian insect with an elaborate mating system, to begin to explore the nature of sexual isolation and mating asymmetry in closely related Hawaiian organisms. We studied sexual isolation and mating asymmetry in two contrasts. First, an inter-island comparison, including L. makaio from the older island of Maui and L. paranigra from the younger island of Hawaii, and second, an intra-island (Hawaii) comparison, including L. nigra from the older volcano of Mauna Kea and L. paranigra with a primary distribution on the younger volcanoes of Mauna Loa and Kilauea. We used a 'no-choice' experimental design, pairing individual males and females in homospecific or heterospecific combinations. Several behavioural aspects of courtship (proportion of male singing, latency to male singing, production of spermatophores and courtship initiation speed) were quantified as well as the success or failure of matings. We demonstrate asymmetry in sexual isolation between reciprocal combinations of L. makaio and L. paranigra. This result is examined in light of the differences in courtship behaviour manifest in the experiments with these two species. We did not find evidence of asymmetry in sexual isolation between L. nigra and L. paranigra, although differences in courtship initiation speed were evident between reciprocal combinations of these two species. In addition to the geological argument that species on older islands and older volcanoes give rise to species on younger islands and younger volcanoes, we discuss phylogenetic evidence consistent with these biogeographic hypotheses of relationships among the focal taxa. The patterns of asymmetrical sexual isolation and mating asymmetry are consistent with those found in the native Hawaiian Drosophila.

Animals↗

PubMed2003

A direct experimental test of founder-flush effects on the evolutionary potential for assortative mating.

Founder-flush speciation models propose that population bottlenecks can enhance evolutionary potential for reproductive isolation. To test this prediction, we subjected bottlenecked (three-pair founder-flush) and nonbottlenecked populations of the housefly to 18 generations of selection for assortative mating. After the selection regime, we analysed videotaped courtship bouts in these lines to identify correlated responses to the selection protocol. The realized heritabilities for assortative mating for both the bottlenecked and nonbottlenecked treatments were very low, but still significant. The founder-flush populations had thus responded to selection as well as the nonbottlenecked populations, although not significantly greater (i.e. total increases in assortative mating were 9.6 and 8.6%, respectively). Multivariate analyses on the courtship repertoires found that, although both bottlenecked and nonbottlenecked treatments attained similar levels of assortative mating, the treatments exhibited different evolutionary solutions in their correlated responses. Specifically, the bottlenecked lines demonstrated a significantly more diverse set of evolutionary trajectories (i.e. significant shifts along the second principal component for courtship). This suggests that the bottlenecked lines had greater potential for the evolution of novel phenotypes as predicted by founder-induced speciation models. Our results, however, cannot distinguish whether the more variable evolutionary responses resulted from increased heritabilities in courtship components, reduced potential to follow the convergent evolutionary trajectories noted for the nonbottlenecked lines, or some combination of both general processes in determining the resultant multivariate phenotype.

Animals↗

PubMed1981

Sexual selection in Drosophila silvestris of Hawaii.

Previous discovery that Drosophila melanogaster females tend to discriminate in mating against phenotypes of earliest courting males prompted a study of the Hawaiian species D. silvestris. Tibial bristle variation in males from opposite coasts of the island of Hawaii functions in courtship, and the possibility that females can distinguish males differing in the tibial trait is explored. Mating tests, designed to give each female and male an alternative choice between two individuals of opposite sex every 30 min, consisted of intrapopulation tests with a strain derived from an eastern (Kilauea) population and interpopulation tests between that strain and one derived from a western (Kahuku) population. Males were given initial combat tests, with "winners" then used in mating (except one test with "loser" males). Matings (52-55%) were classified into categories according to the readiness of the female to mate and sequence of courtship. Low-threshold females (accepting the first male after less than four courtship bouts) occurred at 30-35%. Among intrapopulational tests, females (with higher threshold) accepted first- and second-courting males about equally (25:36, respectively), but for male success in mating, the winning of initial intermale combats and the uniformity of courtship effort tended to be important criteria. Among interpopulation tests, homogamic matings were nearly equal (25% each), but heterogamic matings contrasted in that Kilauea females were reluctant to mate with Kahuku males (14%), while reciprocal matings occurred most frequently (34%). Females favored males second to court, particularly when a Kilauea male (with extra tibial bristles) was the second male. Thus a morphological feature likely to be influential in mating is demonstrated to be so; and sexual selection is operating via male-male combat plus discrimination in favor of particular opposite-sex individuals in this species.

Journal Article↗

PubMed1997

A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster.

Hearing is one of the last sensory modalities to be subjected to genetic analysis in Drosophila melanogaster. We describe a behavioral assay for auditory function involving courtship among groups of males triggered by the pulse component of the courtship song. In a mutagenesis screen for mutations that disrupt the auditory response, we have recovered 15 mutations that either reduce or abolish this response. Mutant audiograms indicate that seven mutants reduced the amplitude of the response at all intensities. Another seven abolished the response altogether. The other mutant, 5L3, responded only at high sound intensities, indicating that the threshold was shifted in this mutant. Six mutants were characterized in greater detail. 5L3 had a general courtship defect; courtship of females by 5L3 males also was affected strongly. 5P1 males courted females normally but had reduced success at copulation. 5P1 and 5N18 showed a significant decrement in olfactory response, indicating that the defects in these mutations are not specific to the auditory pathway. Two other mutants, 5M8 and 5N30, produced amotile sperm although in 5N30 this phenotype was genetically separable from the auditory phenotype. Finally, a new adult circling behavior phenotype, the pirouette phenotype, associated with massive neurodegeneration in the brain, was discovered in two mutants, 5G10 and 5N18. This study provides the basis for a genetic and molecular dissection of auditory mechanosensation and auditory behavior.

Animals↗