Inheritance of male courtship sound characteristics inDrosophila littoralis

Males ofDrosophila littoralis vibrate their wings during courtship to deliver a love song. This consists of 25- to 50-ms-long pulses with a basic frequency of about 250–400 Hz, separated by 250- to 500-ms pauses. When recording the sounds of flies from several localities in Europe, we found that males of one strain from northern Finland displayed courtship sounds with an unusally low wing beat frequency (below 250 Hz). In a genetic analysis utilizing marker stocks, the anomalous frequency was found to be caused by genes on all major autosomes, the strongest factors being on the second chromosome. Interaction between genes on chromosome 2 and on the fused chromosome 3–4 was nonadditive. In low-frequency sounds, the number of cycles in the pulse (CN) was decreased, so that the length of the sound pulse (PL) remained more or less unchanged. We suggest that the genetically and physiologically most thoroughly controlled trait in the sound ofDrosophila littoralis is the length of the pulse.     

The role of central parts of the brain in the control of sound production during courtship in Drosophila melanogaster

The question of the roles of the two main parts of the insect brain, the mushroom bodies and the central complex, in controlling motor coordination and triggering a variety of behavioral programs, including sound production, remains controversial. With the aim of improving our understanding of this question, we studied the parameters of songs used by five-day-old males during courtship for fertilized wild-type females (Canton-S, C-S) over 5-min periods at 25°C; males were of two wild-type Drosophila Melanogaster lines (Berlin and C-S). Berlin males lacking mushroom bodies because of treatment with hydroxyurea during development (chemical removal of the mushroom bodies) were used, along with two mutants with defects in the mushroom bodies (mbm ¹ and mud ¹), two mutants with defects in the central complex (ccb ^KS127 and cex ^KS181), and mutant cxb ^N71 with defects in both the mushroom bodies and the central complex. The experiments reported here showed that courtship songs in males lacking mushroom bodies were virtually identical to those of wild-type males. The main parameters of pulsatile song in mutants mbm ¹ and mud ¹ (interpulse interval and train duration) were insignificantly different from those of the songs of wild-type flies, though the stability of the pulse oscillator was the same. Flies of these lines were no different from wild-type flies in terms of courtship success (percentage of copulating pairs in 10-min tests). Conversely, the songs of mutants with defects in the central complex differed from those of wild-type males. Firstly, there was degradation of the stability of the pulse oscillator and interpulse intervals were very variable. In addition, pulses were often significantly longer and appeared multicyclic, as in the well-known cacophony mutant, while the mean train duration was significantly shorter. Males of the line cex ^KS181 usually courted very intensely, though abnormal sounds were generally emitted. Mutants cex ^KS181 and ccb ^KS127 were significantly less successful in courtship than wild-type flies. These data show that the central complex appears to play a very important role in controlling song, while the mushroom bodies are not related to this function.     

Identification of stimuli that mediate experience-dependent modification of homosexual courtship inDrosophila melanogaster

A naive, sexually matureD. melanogaster male tested with a young, sexually immature male will perform vigorous courtship, but the mature male will perform much less courtship if he is subsequently tested with a second young male. This phenomenon is called experience-dependent courtship modification (EDCM). We have shown that exposure to either or both of the two courtship-stimulating pheromones that immature males synthesize is sufficient to induce EDCM.     

Rostral midbrain lesions and copulatory behavior in male rats

Discrete electrolytic lesions were placed in the mesencephalic dorsal noradrenergic (DNE) bundle of 22 male Sprague-Dawley rats, and sham operations were performed on 14 control animals. Eight components of copulatory behavior were compared in 2 preoperative and 2 postoperative heterosexual mating tests. A significant postlesion decrease in the postejaculatory interval (PEI), number of intromissions, number of incomplete mounts and the ejaculation latency from the first intromission (ELI) occurred. Norepinephrine levels were significantly reduced in the hippocampus, amygdala and hypothalamus, but not in the preoptic area. The only statistically significant correlations between NE concentrations and behavior in the lesioned animals were negative (hippocampal NE with PEI and ELI). The results support the hypothesis that rostral midbrain lesions disinhibit some components of male rodent copulatory behavior, but suggest that a system or systems other than the DNE bundle may be responsible for this disinhibition.     

Minority mating advantage of certain eye color mutants ofDrosophila melanogaster. I. Multiple-choice and single-female tests

Alleles at the brown locus ofDrosophila melanogaster combined with homozygous scarlet provide a useful model to demonstrate minority advantage of males in mating. Heterozygotes with orange (O) eyes equal in numbers to homozygotes with red (R) eyes (1010 in both sexes) displayed no bias favoring either eye color, but each eye color was favored when males occurred in a minority ratio (218). In direct observation of single females with equal numbers of males (33) as controls,O males courted less and more slowly thanR males, but females mated with either type without bias. When unequal (41), the minority males were successful at more than twice the frequency expected. Whether successful or not, the minority males did not change their level of courtship, and thus cannot be said to compensate for their frequency in any way. The time between first courtship and mating was less for the minority males than for the majority males. We discard the hypothesis that the minority male will be accepted immediately or ahead of a majority male, because the opposite tended to occur: that if a minority male courted first he was less likely to be successful than if he waited until the majority courted. Our results then are in conformity with the hypothesis that a female samples males and their courtship cues, thus becoming habituated to the majority of the first courting male, but she accepts a male with a cue different from that which she originally detected but avoided. That male is most often the minority.This research was supported in part by National Science Foundation Grants GB-34206 to August 31, 1974, and BMS 72-02110 after that date.     

Genetic variation in the male courtship sound ofDrosophila littoralis

Drosophila littoralis males and females emit sounds during courtship by vibrating their wings. Genetic variation in the male courtship sound of this species was studied by analyzing the sounds of males of 42 fresh isofemale strains from three localities in Finland and those of several laboratory strains originating from Europe and Caucasus. Among the fresh strains, the mean number of sound cycles in a pulse varied from 12 to 17 cycles, the length of a pulse from 39 to 51 ms, the length of a sound cycle from 2.9 to 3.6 ms, and the length of an interpulse interval (ipi) from 280 to 400 ms. The sounds of the old laboratory strains differed from each other more than the sounds of the fresh strains. There was, however, no sign of geographic differentiation.This study was aided by funds from The Academy of Finland.     

Minority mating advantage of certain eye color mutants ofDrosophila melanogaster. III. Female discrimination and genetic background

A repetition of certain experiments done 2 years previously with two eye color mutants,brown andscarlet, inDrosophila melanogaster was undertaken to reconfirm results; however, initial tests revealed that strains or conditions had changed so that females were less discriminating. Testing was undertaken with changes in genetic background and certain laboratory conditions, with single females courted by equal numbers of two eye color types of males (3 red,R: 3 orange,O). These eye colors were produced as (1) mutants off the shelf, (2) recombinants from an outcross to a wild-type strain (CS), (3) mutants as in Experiment 1 but with male types stored either together or separately, and (4) recombinants from a double outcross of flies from Experiment 2 to hybrids from two additional wild strains,LS andOR. Experiment 4 producedR andO males that courted nearly equally (as in previous experiments), in contrast with about 70% courtship byR males in the other experiments. Females discriminated in favor of those second to court in G₀, G₁, and a repeat of G₀; however, with two generations of inbreeding, discrimination by this criterion lessened to become nonsignificant. In Experiments 1 and 2,O females favored second-courting males, butR females in hose experiments and all females in Experiment 3 mated more randomly. Effects of storing males either together or separately were not significant. About 20–30% of the females (low threshold) were highly receptive immediately after first courtship. Those trials plus any in which only a single type of male courted were omitted from estimations of female discrimination; a possible bias incurred by such omission against females that might have initial preferences was found to be nonsignificant. Discriminating ability was discussed as a fitness property inDrosophila populations.This research was supported in part by National Science Foundation Grant DEB 79-03259.     

Dendrites are dispensable for basic motoneuron function but essential for fine tuning of behavior

Dendrites are highly complex 3D structures that define neuronal morphology and connectivity and are the predominant sites for synaptic input. Defects in dendritic structure are highly consistent correlates of brain diseases. However, the precise consequences of dendritic structure defects for neuronal function and behavioral performance remain unknown. Here we probe dendritic function by using genetic tools to selectively abolish dendrites in identified Drosophila wing motoneurons without affecting other neuronal properties. We find that these motoneuron dendrites are unexpectedly dispensable for synaptic targeting, qualitatively normal neuronal activity patterns during behavior, and basic behavioral performance. However, significant performance deficits in sophisticated motor behaviors, such as flight altitude control and switching between discrete courtship song elements, scale with the degree of dendritic defect. To our knowledge, our observations provide the first direct evidence that complex dendrite architecture is critically required for fine-tuning and adaptability within robust, evolutionarily constrained behavioral programs that are vital for mating success and survival. We speculate that the observed scaling of performance deficits with the degree of structural defect is consistent with gradual increases in intellectual disability during continuously advancing structural deficiencies in progressive neurological disorders.Dendrites are structural ramifications of a neuron specialized for receiving and processing synaptic input (1). The estimated 100 billion neurons in the human brain (2) form approximately 100 trillion synapses onto a total of approximately 100,000 miles of dendritic cable. The functions of dendrites are proposed to range from simply providing enough surface for synaptic input (3) to highly compartmentalized units of molecular signaling and information processing (4–6). In addition to functioning as passive receivers, dendrites may be equipped with output synapses (7) and active membrane currents (8), which add tremendous computational power to a single neuron (6, 9, 10).Accordingly, dendritic abnormalities are highly consistent anatomical correlates of numerous brain disorders (11, 12), including autism spectrum disorders, Alzheimer’s disease, schizophrenia, Down syndrome, Fragile X syndrome, Rett syndrome, anxiety, and depression. However, in many cases it remains unclear whether dendritic defects are the cause or the consequence of impaired brain function. Trying to understand dendrite function poses major technical challenges because it requires selective manipulation of dendritic structure without disturbing other properties of the affected neuron, followed by quantitative analysis of neuronal function and the resulting behavioral consequences.This study uses the Drosophila genetic model system to selectively abolish dendrites from a subset of identified wing muscle motoneurons that have well-described and stereotyped dendritic morphologies (13) and firing patterns during flight (14) and courtship song (15, 16). Surprisingly, we find that motoneurons that lack 90% of their dendrites are still contacted by appropriate synaptic partners and produce qualitatively normal firing patterns and wing movements during flight and courtship song. However, normal dendritic architecture is essential for particularly challenging tasks, such as the integration of optomotor input for adequate control of flight power output, or the temporal accuracy of switching between different song elements during courtship to ensure mating success. Our data demonstrate that the vast majority of basic motor functions can be satisfactorily accomplished with motoneurons that have significant dendritic defects but normal axonal structure and membrane currents. However, a complex 3D dendritic architecture is mandatory for intricate regulation of behavioral output, which in turn imposes a positive selection pressure on the maintenance of such complex dendritic trees through evolution.