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Quantitative genetic analysis of courtship and reproduction in female Drosophila melanogaster.

Three hundred mother-daughter pairs were analyzed for seven attributes related to courtship and reproduction. Only the lag time from first courtship to copulation was significantly heritable; genetic correlations involving this attribute were not significant. The genetic correlation between fertility and lag time to first courtship was negative and significant. However, this genetic correlation is expected to have little impact on the retention of additive genetic variance or on response to selection because it involves two attributes with low heritabilities. The pattern of phenotypic covariation among traits is largely explained by environmental causes and is consistent with that found in a previous analysis of father-son pairs (Gromko, 1987).

Alleles↗

Quantitative trait loci affecting a courtship signal in Drosophila melanogaster.

Courtship plays a major role in the sexual isolation of species, yet the genetics underlying courtship behaviour are poorly understood. Here we analyse quantitative trait loci (QTL) for a major component of courtship song in recombinant inbred lines derived from two laboratory strains of Drosophila melanogaster. The total variance among lines exceeds that between parental strains, and is broadly similar to that seen among geographic strains of the Cosmopolitan form of this species. Previous studies of the quantitative genetics of fly song have implied a polygenic additive inheritance with numerous genes spread throughout the genome. We find evidence for only three significant QTLs explaining 54% of the genetic variance in total. Thus there is evidence for a few large effect genes contributing to the genetic variance among lines. Interestingly, almost all of the candidate song genes previously described for D. melanogaster do not coincide with our QTLs.

Animals↗

Courtship songs of Drosophila pseudoobscura and D. persimilis. II. Genetics of species differences.

Although male courtship songs have been repeatedly implicated in sexual isolation between numerous Drosophila species, no genetic studies have evaluated the genetic basis of differences between species beyond using quantitative genetic analyses of hybrids or surveying associations of song characters to five or fewer genetic markers. Here, we dissect the genetic basis of the difference between D. pseudoobscura and D. persimilis in two courtship song elements (interpulse interval and intrapulse frequency) using 15 molecular markers. We also evaluate the association between song elements and sexual isolation in these backcross hybrid males of these species. We find that song differences between these species are associated with at least two or three genomic regions, and the species difference in interpulse interval may be oligogenic. Courtship song differences are especially strongly associated with two inversions that differentiate these species. Further, we found that interpulse interval is strongly associated with mating success to D. pseudoobscura females, while intrapulse frequency is associated with mating success to D. persimilis females. Implications of these findings are discussed.

Animals↗

Analysis of temperature-sensitive mutants reveals new genes involved in the courtship song of Drosophila.

cacophony (cac), a mutation affecting the courtship song in Drosophila melanogaster, is revealed to cause temperature-sensitive (TS) abnormalities. When exposed to high temperatures (37 degrees), cac flies show frequent convulsions and pronounced locomotor defects. This TS phenotype seems consistent with the idea that cac is a mutation in a calcium-channel gene; it maps to the same X-chromosomal locus that encodes the polypeptide comprising the alpha-1 subunit of this membrane protein. Analysis of the courtship song of some TS physiological mutants showed that slowpoke mutations, which affect a calcium-activated potassium channel, cause severe song abnormalities. Certain additional TS mutants, in particular para(ts1) and nap(ts1), exhibit subtler song defects. The results therefore suggest that genes involved in ion-channel function are a potential source of intraspecific genetic variation for song parameters, such as the number of cycles present in "pulses" of tone or the rate at which pulses are produced by the male's courtship wing vibrations. The implications of these findings from the perspective of interspecific lovesong variations in Drosophila are discussed.

Animal Communication↗

Courtship communication and perception.

Although ethologists have detailed courtship rituals for many species, courting behavior of humans has not received extensive study from an ethological standpoint. Yet there are clearly facial expressions and gestures that are commonly labeled "flirting behaviors." These nonverbal signals have been documented recently by several investigators in field studies, but the receptivity of nonverbal courtship signals is still in question. The current research project attempted to assess the perceptual skill of naive male and female observers who were presented videotaped samples of females' nonverbal courtship and rejection behaviors and asked to rate their intensity. The results showed that overall, men rated invitational behaviors more positively than women. In contrast, signals of rejection were seen by men as sending a less potent message than that perceived by women. Evolutionary theory may offer a framework for understanding these results.

Adolescent↗

Defects in courtship and vision caused by amino acid substitutions in a putative RNA-binding protein encoded by the no-on-transient A (nonA) gene of Drosophila.

The Drosophila no-on-transient A (nonA) gene is involved in the visual behaviors and courtship song of the fly. The NONA polypeptide contains two copies of the RNA-recognition motif (RRM), a hallmark of proteins involved in RNA binding, and an adjacent conserved charged region. This 311-amino-acid region is found in four other proteins and largely overlaps the Drosophila-Behavior/Human Splicing (or DBHS) domain. The newest family member, Drosophila nAhomo, was discovered in a database search, and encodes a protein with 80% identity to NONA. In this study, three nonA mutations generated by chemical mutagenesis were sequenced and found to fall within the conserved region. Site-directed mutagenesis of the two RRMs, and within a (conserved) charged region located C-terminal to them, was performed to determine the significance of these domains with respect to whole-organismal phenotypes. Behavior and viability were assessed in transformed flies, the genetic background of which lacks the nonA locus. Point mutations of amino acid 548 in the charged region confirmed the etiology of the nonAdiss courtship-song mutation and showed that a milder substitution at this site produced intermediate singing behavior, although it failed to rescue visual defects. Mutagenesis of the RRM1 domain resulted in effects on viability, vision, and courtship song. However, amino acid substitutions in RNP-II of RRM2 led to near-normal phenotypes, and the in vivo nonA mutations located in or near RRM2 caused visual defects only. Thus, we suggest that the first RRM could be important for all functions influenced by nonA, whereas the second RRM may be required primarily for normal vision.

Amino Acid Sequence↗

Sexual dimorphism in neuromuscular junction size on a muscle used in courtship by green anole lizards.

The green anole lizard exhibits seasonal courtship behavior that is sexually dimorphic. This courtship consists of the extension of a bright red throat fan (dewlap) associated with head-bobbing display behavior. While males extend their dewlaps in aggressive encounters as well as in courtship, females use their considerably smaller dewlaps much less frequently and mainly in agonistic encounters. In parallel, a number of components of the neuromuscular system controlling dewlap extension are greater in males than in females during the breeding season, including dewlap motoneuron soma size and muscle fiber size and number. These features do not seem to change substantially in adulthood, despite a dramatic decline in dewlap use during the nonbreeding season. We explored the morphology of this neuromuscular system in more detail in the present experiment in males and females during both the breeding and nonbreeding seasons. Fiber and whole muscle length (approximately perpendicular to the fibers) were measured. Acetylcholinesterase histochemistry was used to visualize neuromuscular junctions (NMJs), and the surface area and density of NMJs were assessed for each animal. During the breeding season, NMJ size was larger in males than in females, but NMJ density along each fiber was equivalent between the sexes. In addition, whole muscle length and that of individual muscle fibers, was larger in males than in females. However, when corrected for body size, the sex difference in muscle fiber length disappeared. In the nonbreeding season, the sexual dimorphisms were maintained, suggesting that these features do not change substantially due to differences in circulating testosterone or a difference in use across seasons. Overall, these results are consistent with the idea that enhanced NMJ size is a relatively stable feature of the dewlap muscle in adulthood that either facilitates or is a consequence of using a larger muscle to extend a bigger dewlap in males compared to females.

Animals↗

Visual and song nuclei correlate with courtship skills in brown-headed cowbirds.

We assessed courtship success in 14 adult male brown-headed cowbirds, Molothrus ater. Volumes of song control nuclei and visual nuclei were measured in Nissl stained tissue. Variation in courtship success was found to be related to variation in two areas of the avian brain: the song control nucleus, area X, and the thalamic visual area, nucleus rotundus. Volume of area X was negatively correlated with song potency, as assessed by female playback, and with rate of vocalizing. Volume of nucleus rotundus was positively correlated with song potency, vocalizing to females and courtship persistence. These data are the first to implicate a visual nucleus in the use of song. The data also complement previous findings with cowbirds suggesting that song learning involves visual attention to females. Taken as a whole, these results suggest that use of song depends on integration of auditory, vocal and visual information. In that female songbirds in many species assess multimodal performance of song, these findings with cowbirds suggest that future studies of brain and behaviour include a broader view of possible behavioural and neural correlates. Copyright 1998 The Association for the Study of Animal Behaviour.

Journal Article↗

The cultural transmission of courtship patterns in cowbirds, Molothrus ater.

In this study, I tested whether the courtship behaviours that facilitate patterns of assortative pairing and mating could be culturally transmitted across generations of brown-headed cowbirds. In an earlier study, I housed a first generation of young South Dakota cowbirds in one of two cultural backgrounds: (1) with adult social models from the same population; or, (2) with adult social models from a behaviourally distinct Indiana population. During the breeding season, the first cultural generation of South Dakota cowbirds paired and mated assortatively based upon their cultural backgrounds. In the present study, I tested whether these courtship patterns could be culturally transmitted to a second generation of young South Dakota cowbirds. Serving as adult social models for birds of the second cultural generation were the first cultural generation of South Dakota birds from the previous study. During their first breeding season, the birds of the second cultural generation paired assortatively by cultural background at roughly a 3:1 ratio. In addition to the pairing data, the behavioural responses of females to the vocalizations of males indicated the influence of cultural backgrounds. This experimental demonstration of the cultural transmission of courtship patterns points to the importance of social environments as mechanisms whereby behavioural systems are inherited from one generation of animals to the next. Copyright 1998 The Association for the Study of Animal Behaviour.

Journal Article↗

Mate choice in Drosophila melanogaster and D. sechellia: criteria and their variation depending on courtship song.

Courtship song is one of the most important male signals in Drosophila mating. A female D. melanogaster copulates more readily when given a conspecific type of courtship song. Female D. melanogaster accepted winged D. sechellia more than wingless ones in a no choice test. Copulation frequencies varied between strains and were significantly correlated with male mating propensity of D. sechellia. Females from three of five strains of D. sechellia accepted winged D. melanogaster less than wingless ones in no choice tests, suggesting that D. melanogaster songs reduce mating in D. sechellia females. Multiple choice tests showed that males prefer conspecifics. In female choice tests, D. melanogaster females copulated with winged heterospecific D. sechellia males more than with wingless conspecific D. melanogaster males in the confined condition, suggesting that song differences between D. melanogaster and D. sechellia affect D. melanogaster females less than the absence of courtship song. Copyright 2000 The Association for the Study of Animal Behaviour.

Journal Article↗

Aromatase inhibition reduces specifically one display of the ring dove courtship behavior.

The courtship behavior of the male ring dove (Streptopelia risoria) combines aggressive displays (chasing, bowing) and nest-oriented displays (nest soliciting). Aggressive displays depend on circulating testosterone, whereas nest soliciting is estrogen-dependent and appears to depend on the aromatization of androgen into estrogen within the brain. The present work tested the hypothesis that aromatase specifically modulates the nest soliciting display in intact male ring doves. Males were tested for courtship behavior with receptive females before and after being implanted with micro-osmotic pumps containing Fadrozole, a nonsteroidal aromatase inhibitor, or saline. Fadrozole at the higher dose reduced estrogen-dependent nest soliciting but did not affect androgen-dependent chasing and bowing. These results support the hypothesis that aromatase modulates nest soliciting in male ring doves, and provide further evidence for separate hormonal control of different courtship displays in this species.

Androgens↗

The effects of testicular tissue and prehatching inhibition of estrogen synthesis on the development of courtship and copulatory behavior in zebra finches.

As in many mammalian and avian species, testicular androgens or their metabolites activate courtship and copulatory behaviors in adult male zebra finches. However, studies of sexual differentiation of these behaviors and related anatomical structures provide conflicting results. For example, posthatching estradiol can both masculinize courtship and the neural structures involved in song in females and inhibit the development of masculine copulation in males. These and other results have led to the hypotheses that (1) testicular androgens are converted to estradiol in the brain of developing males, and estradiol serves to masculinize the song system, whereas (2) estradiol secretion by the female ovary allows feminine rather than masculine copulatory behavior to develop. Treating embryonic zebra finches with the estrogen synthesis inhibitor fadrozole causes functional testicular tissue to develop in genetic females. The present study investigated the effects of such treatment on the development of singing and copulatory behavior as well as song system anatomy in males and females. While exogenous testosterone facilitated the display of sexual behaviors in adult males, the testicular tissue in females had no masculinizing effect on the production of audible courtship song or copulation. Their song control nuclei were also not masculinized, even in individuals lacking ovarian tissue. In contrast, embryonic inhibition of estrogen synthesis in males significantly stimulated song production. These results suggest that while manipulations of steroid hormone exposure can influence the display of sexual behaviors, gonadal secretions may not be required for normal sexual differentiation of the song system in zebra finches.

Animals↗

Castration in Gambel's and Scaled Quail: ornate plumage and dominance persist, but courtship and threat behaviors do not.

During the breeding season, testosterone in male birds is often linked to some secondary sexual ornaments, courtship behaviors, and intrasexual aggression. I examined the effect of castration on plumage expression in Gambel's Quail (Callipepla gambelii), a species in which males are highly ornate, and in Scaled Quail (C. squamata), an unornamented species. Using male pairs, each consisting of a castrate and a control, I also assessed whether castration affected (1) the behavior of males, (2) the mating decisions of females, or (3) the outcome of male-male competition. Castration did not alter the plumage of male Gambel's or Scaled Quail. In these species, and some other members of the avian order Galliformes, production of ornate plumage appears to be independent of testosterone. In contrast, castration reduced or eliminated courtship behaviors. Females almost never preferred castrated individuals. During male-male competition, castrates also exhibited lower rates of threat behaviors, which appear to be identical to those used during courtship. Castration did not, however, influence the outcome of male-male competition. Castrates of both species exhibited overt aggression (pecks, chases, displacement) and frequently won male contests. Such results suggest that certain types of aggressive behavior may be testosterone-independent. In both Gambel's and Scaled Quail, male body size correlated positively with dominant individuals.

Agonistic Behavior↗

Neuromuscular and endocrine control of an avian courtship behavior.

In many species of birds, males perform complex visual and acoustic courtship displays to attract and stimulate females. Some of these displays involve considerable use of the wings and legs, suggesting that they may be controlled by sexually dimorphic spinal motoneurons and their target muscles. Sex steroid hormones are known to organize and activate many sexually dimorphic phenotypes, so these neuromuscular systems may also be steroid sensitive. To test these ideas, we have begun studies of wild golden-collared manakins (Manacus vitellinus) in Central America. Males of this species establish a courtship arena in the forest, where they perform an elaborate dance that includes use of their wings to generate loud snapping sounds. Here we describe male golden-collared manakin courtship behavior, including the various "wingsnaps." We also review our studies, and those of others, showing sexually dimorphic properties of manakin wings, the wing musculature, and sex steroid accumulation in the spinal cord. These data suggest that manakins are useful models for evaluating steroid control of complex peripheral neuromuscular systems.

Animals↗

Artificial neural network classification of Drosophila courtship song mutants.

Courtship songs produced by Drosophila males--wild-type, plus the cacophony and dissonance behavioral mutants--were examined with the aid of newly developed strategies for adaptive acoustic analysis and classification. This system used several techniques involving artificial neural networks (a.k.a. parallel distributed processing), including learned vector quantization of signals and non-linear adaption (back-propagation) of data analysis. "Pulse" song from several individual wild-type and mutant males were first vector-quantized according to their frequency spectra. The accumulated quantized data of this kind, for a given song, were then used to "teach" or adapt a multiple-layered feedforward artificial neural network, which classified that song according to its original genotype. Results are presented on the performance of the final adapted system when faced with novel test data and on acoustic features the system decides upon for predicting the song-mutant genotype in question. The potential applications and extensions of this new system are discussed, including how it could be used to screen for courtship mutants, search novel behavior patterns or cause-and-effect relationships associated with reproduction, compress these kinds of data for digital storage, and analyze Drosophila behavior beyond the case of courtship song.

Algorithms↗

Drosophila courtship song cycles in normal and period mutant males revisited.

Courtship songs of normal males and those expressing short-period, long-period, and arrhythmic mutations at the period (per) locus of Drosophila melanogaster have been reanalyzed for rhythmic components, using spectral treatments of the fluctuating rates of tone pulse production that occur during courtship. It was concluded, as in previous studies, that such songs are strongly rhythmic, except for courtships performed by per01 males. Songs produced by males expressing this and other per alleles were compared to computer-generated "random" ones. Interpulse interval variations influenced by per01 and songs stimulated to be arrhythmic both were found to be associated with cryptic rhythmicities; several such period values, extracted by the spectral analyses, defined very short cycle durations. We discuss the implications of these findings and of some recently reported results that have challenged the existence of rhythmicity in Drosophila songs.

Animal Communication↗

Secondary courtship songs and inhibitory songs of Drosophila virilis-group males.

The males of all Drosophila virilis-group species produce primary courtship song; and the males of four of these species also provide secondary courtship song when courting a female. The amount of secondary song and the courtship phase at which it is produced vary according to the species. D. lummei males produce secondary song consisting of successive 12-ms-long sound pulses with 70-ms-long intervals between pulses. D. borealis males produce short and dense pulse trains and D. littoralis and D. flavomontana males produce single sound pulses of a long duration (80-160 ms). The males of all species produce pulse-structured inhibitory song when they are courted by another male. In the secondary and inhibitory songs of interspecific hybrids, short and dense pulse trains of parent species break into pulse song with long interpulse intervals. This suggests that songs consisting of short and dense pulse trains and pulse songs with long interpulse intervals are just different modes of the same song. Sine songs (long sound pulses) seem to be inherited independently of pulse song.

Animals↗

Courtship song and mating speed in hybrids between Drosophila melanogaster and Drosophila simulans.

Courtship song and mating speed of hybrids between Drosophila melanogaster and D. simulans were investigated. The courtship song of hybrid males is identical to that of D. simulans, suggesting that X chromosome determination, known from the cross between D. pseudoobscura and D. persimilis, is also possible here. Wingbeat frequency of hybrids is intermediate between that of the two parents, demonstrating that courtship song and wingbeat frequency are inherited independently of each other. In mating test, hybrid males cout and are accepted by D. simulans females more than hybrid females (presumably because their song is more "acceptable" to the former). D. melanogaster males readily, hybrids less readily, and D. simulans least.

Animals↗