Barrie Burnet

Courtship songs and genetic control of their acoustic characteristics in sibling species of the Drosophila melanogaster subgroup

Six sibling species of the melanogaster subgroup differ in their wing displays and in the acoustic characteristics of their courtship songs. D. melanogaster, D. simulans and D. mauritiana have distinct but similar courtship songs. D. mauritiana, which is allopatric to the others, produces, an ambivalent song with sine song frequency and intrapulse frequency like simulans and modal interpulse interval like melanogaster. These three species appear to be behaviourally more closely similar to each other than to the three African species D. yakuba, D. teissieri and D. erecta. The acoustic characteristics of the songs of interspecific hybrids, indicate that the interpulse interval and intrapulse frequency are quantitatively controlled by genes located on the autosomes. The ability to generate sine song may be controlled by one or more genes located on the X-chromosome, but an alternative possibility, of autosomal dominant inheritance, cannot be excluded.

Genetic analysis of larval feeding behaviour in Drosophila melanogaster

The larvae of Drosophila melanogaster feed continuously during their period of development. The rate of feeding activity, measured as the number of cephalopharyngeal retractions per minute, varies with the physiological age of the larva. Feeding rate responded readily to directional selection to give rise to non-overlapping populations with fast and slow feeding larvae, respectively. Realized heritabilities for the character from different selected lines varied between 11 and 21%. Crosses between the selected populations show significant dominance for fast feeding rate and appreciable non-allelic gene interaction. Larvae of the slow feeding populations showed a correlated reduction in locomotor activity but fast feeding larvae do not move about significantly faster than the unselected controls. Asymmetry of the correlated response to selection, it is argued, is due to selection in the slow feeding populations of alleles with a secondary effect in both behaviours.

Organization and patterns of inter- and intraspecific variation in the behaviour of Drosophila larvae

Abstract Larval behaviour is described in terms of a series of discrete components, the frequencies of which vary in relation to environmental factors. The rate of locomotion is high in the absence of food, and reduced when feeding occurs on a suitable food source. If larvae encounter food containing a high concentration of ethanol they show a decrease in feeding rate and an increase in locomotor activity. This may be a behavioural response to suboptimal nutritional conditions involving potential alcohol toxicity. Larvae of D. melanogaster and D. simulans exhibit both inter- and intraspecific variation in the frequency of behaviours. The organization of larval behaviour, represented in ethograms showing the patterns of transitions between elements, is comparatively stable across species, strains and environments. Functional significance of the different behaviours is discussed.

The function and processing of auditory information in the courtship behaviour of Drosophila melanogaster

The function and processing of auditory information in the courtship behaviour of Drosophila melanogaster was investigated using combination of mutant genes which cause stepwise reduction in the size of the arista. Reduction of the effective surface area of the arista lowers female sexual receptivity and the courtship success of males. Since female receptivity is known to be dependent upon accurate perception of the characteristics of male wing vibration, the results confirm that the aristae are essential for adequate auditory perception. The female, as elsewhere suggested, may compare the sound perceived to a neural representation of the parameters of the species code, which is genetically determined, and reject or accept the male depending on the outcome of the comparison. Quantitative analysis of male courtship behaviour suggests that the sound which mutant males produce is distorted as a result of imperfect auditory feedback. It is suggested that veridical feedback of the efferent signal, which may be compared to a neural representation in the same way as in the female, could be a necessary condition for production of an accurate species specific wing vibration code.

Genetic analysis of larval feeding behaviour in Drosophila melanogaster: II. Growth relations and competition between selected lines

Growth relations of lines selected for fast or slow larval feeding rate have been compared with those in the genetically heterogeneous control base population from which they were derived. Larvae of the slow strain have reduced growth rate and reach their critical weight for pupation later than unselected larvae. Larvae of the fast strain attain their critical weight at the same time as the unselected control larvae, suggesting that growth rate in the precritical period of development is already maximized in the base population and cannot be improved by increasing food intake. This constraint does not apply to the fixed period of post-critical growth however, since fast feeding larvae give rise to larger adult flies than the controls. Larval feeding rate is affected by genes located on all three major chromosomes. The small fourth chromosome has negligible effect. Selection for slow feeding rate has led to an increase in the frequency of recessive genes affecting the character. High scores of larvae selected for fast feeding rate depend upon interactions between non-homologous selected chromosomes which individually have little effect. Larval feeding rate in the control unselected population appears to be buffered, firstly by epistatic interactions against the effects of chromosomes tending to promote ‘supra-optimal’ feeding rate and, secondly, by dominance against chromosomes promoting a lowering of feeding rate. Under conditions of scramble type competition between the selected lines for limited resources, fast feeding larvae have a higher survival rate, and complete their period of larval development earlier to give larger adult flies than their slow feeding competitors. The contribution of larval feeding rate to competitive ability at different levels is discussed, and it is suggested that the effects of change in this behavioural character may be far reaching.

SELECTIVE MATING AND EYE PIGMENTATION: AN ANALYSIS OF THE VISUAL COMPONENT IN THE COURTSHIP BEHAVIOR OF DROSOPHILA MELANOGASTER

A number of investigations have shown that in competitive mating tests mutant Drosopkila are at a disadvantage when competing with wild type flies. Over long time intervals the mutant genes are either eliminated or maintained at a very low frequency in the population (Reed and Reed, 1948; Merrell and Underhill, 1956). This disadvantage has usually been attributed to a reduction in fitness on the part of the mutant when competing for the available food supply. Behavior is also a component of fitness, and there is evidence indicating that the disadvantage exhibited by many mutant genotypes is due to some impairment of their mating behavior. Reed and Reed (1950) found that males from the sex linked white eye mutation (w) of Drosophila melanogaster were at a considerable disadvantage when in competition with wild type males. Bastock (1956) demonstrated that the yellow mutant (y) of D. melanogaster gives rise to males which show a quantitative change in the wing vibration element of the courtship display. The slight reduction in mean vibration bout lengths of the mutants results in their being at a disadvantage. Petit (1959) found that wild type males had an advantage over wkite eye and Bar eyed males in a competitive situation, this she attributed to differences in the wing vibration component of the courtship display. Geer and Green (1962) were unable to confirm this effect on wing vibration in studies with vestigial mutant males. Geer and Green (loc. cit.) working with a series of eye pigment mutants obtained evidence of a relationship between the amount of eye pigmentation and mating success; the greater the pigment density the greater the mating success. This is a particularly interesting finding since it has been argued that vision plays only a minor role in the courtship of Drosophila melanogaster (Spieth and Hsu, 1950), although it has an important influence on the courtship of certain other members of the melanogaster species group (Grossfield, 1968). Geer and Green (loc. cit.) showed that the disadvantage suffered by the eye pigment mutants was no longer present when matings were allowed to take place in total darkness, indicating that vision may also be important in the courtship of Drosophila melanogaster. In none of the investigations where eye mutants have been used, has the behavior of the animals been observed, mating success being measured by progeny analysis or by the dissection of females to determine the presence or absence of sperm. Ewing and Manning (1967) in their review of behavior genetics in insects single out a difficulty in the interpretation of Geer and Greens results. They argue that although Geer and Green demonstrate a relationship between pigment density and mating success it is not possible to attribute the disadvantage shown by the eye pigment mutants solely to that sensory defect. An alternative hypothesis is that the eye pigment mutations produce some pleiotropic effect in the animals central nervous system which affects some aspect of the males sexual behavior. Since the behavior of the mutants has not been examined in detail this remains a plausible hypothesis. These two alternative explanations may be examined by using the phenocopying technique described by Burnet et al. (1968).

Courtship inDrosophila sechellia: Its structure, functional aspects, and relationship to those of other members of theDrosophila melanogaster species subgroup

The courtship behavior of Drosophila sechelliais described. Male wing displays are mainly vibration and scissoring, with low levels of rowing. As courtship proceeds the proportion of courtship spent in male wing vibration and licking increases, whereas female movement decreases. The male courtship song of sechelliacontains pulse song but no sine song. This species also shows a distinctive “copulation song” associated with mounting and copulation. The main cuticular hydrocarbon in females is 7,11-heptacosadiene. The number of copulations increased when flies were placed in the presence of food. Visual and acoustic stimuli appear to be important for mating. A multidimensional comparison was used to compare members of the melanogaster species subgroup, based upon courtship behavior, song characteristics, and cuticular hydrocarbons. A multidimensional comparison of courtship sequences in sechellia, melanogaster, simulans,and mauritianashowed differences in variability between the two island species as compared to the two cosmopolitan species. The courtship song of D. orenais described: it shows both sine and pulse song; there is also a “copulation song” in this species.

The behavioural basis of overdominance in competitive mating success at the ebony locus of Drosophila melanogaster

Male files homozygous for the gene ebony11 are partially blind, and at a disadvantage in competitive mating. The courtship of the mutant males is deficient in wing vibration stimulation, which is characterized by a low proportion of sine song and a high intra-pulse frequency. Males heterozygous for ebony have normal vision, but show an increase in courtship song, and are superior in competitive mating to wild type males. The auditory characteristics of courtship song produced by heterozygous males are indistinguishable from those of wild type, and their superiority in competitive mating success is due to overdominance involving this specific element of male courtship behaviour.

The Structure of Courtship in the Drosophila Melanogaster Species Sub-Group

[A quantitative comparison and sequence analysis of courtship behaviour of four-day old virgin flies from seven species of the Drosophila melanogaster species subgroup is described. In three species (D. melanogaster, D. simulans and D. mauritiana) courtship was observed until copulation. In four species (D. yakuba, D. teissieri, D. erecta and D. orena) courtships were truncated after a standard period. Wing rowing by the male was seen in four species (simulans, mauritiana, yakuba and teissierz). In both mauritiana and simulans the proportion of time spent in rowing tended to increase as courtship proceeded. The four species showing the greatest proportion of wing vibration in courtship (melanogaster, yakuba, erecta and orena) also showed an increase in the proportion of time spent vibrating as courtship proceeded. The amount of wing vibration and wing extension in yakuba is greater than in any other species in the subgroup. The proportion of time spent in wing extension in yakuba declined whilst vibration increased during courtship. In six species the proportion of courtship time spent licking increased during courtship. The mean lick duration was longer in yakuba than in any other species of the subgroup. When males were following actively moving females the time they spent performing courtship behaviours and the mean bout lengths were shorter than in courtship as a whole. D. simulans males expressed scissoring at a low level when courting moving females. Females of all species preened more than the males, but preening during courtship appeared to have no excitatory or inhibitory effect on the male. The behavioural sequence characteristic of the species subgroup is orientation→wing display→licking→ copulation. In five species wing vibration was the only element of wing display immediately to precede licking, but in simulans licking could also be preceded by scissoring and in yakuba by wing extension. The transition vibration→licking appears to be a characteristic of the subgroup., A quantitative comparison and sequence analysis of courtship behaviour of four-day old virgin flies from seven species of the Drosophila melanogaster species subgroup is described. In three species (D. melanogaster, D. simulans and D. mauritiana) courtship was observed until copulation. In four species (D. yakuba, D. teissieri, D. erecta and D. orena) courtships were truncated after a standard period. Wing rowing by the male was seen in four species (simulans, mauritiana, yakuba and teissierz). In both mauritiana and simulans the proportion of time spent in rowing tended to increase as courtship proceeded. The four species showing the greatest proportion of wing vibration in courtship (melanogaster, yakuba, erecta and orena) also showed an increase in the proportion of time spent vibrating as courtship proceeded. The amount of wing vibration and wing extension in yakuba is greater than in any other species in the subgroup. The proportion of time spent in wing extension in yakuba declined whilst vibration increased during courtship. In six species the proportion of courtship time spent licking increased during courtship. The mean lick duration was longer in yakuba than in any other species of the subgroup. When males were following actively moving females the time they spent performing courtship behaviours and the mean bout lengths were shorter than in courtship as a whole. D. simulans males expressed scissoring at a low level when courting moving females. Females of all species preened more than the males, but preening during courtship appeared to have no excitatory or inhibitory effect on the male. The behavioural sequence characteristic of the species subgroup is orientation→wing display→licking→ copulation. In five species wing vibration was the only element of wing display immediately to precede licking, but in simulans licking could also be preceded by scissoring and in yakuba by wing extension. The transition vibration→licking appears to be a characteristic of the subgroup.]

Effects of male paragonial gland secretion on sexual receptivity and courtship behaviour of female Drosophila melanogaster

Abstract Female Drosophila melanogaster show a switch-off in sexual receptivity and an increase in oviposition rate following impregnation. These effects are also observed in unfertilized virgin females which receive transplants of intact male paragonia into the abdominal body cavity. Virgin Amherst wildtype females show a repertoire of responses to male courtship characterized by high rates of kicking and fending and a low rate of genital extrusion. Fertilized females show low rates of kicking and fending but a high rate of genital extrusion. Virgin female hosts receiving paragonial gland implants show an altered pattern of courtship rejection with low rates of kicking and fending. Studies on these host females, and on females homozygous for the mutant allele female-sterile , suggest that the expression of genital extrusion depends, in addition to the paragonial gland substance, upon additional information input from abdominal stretch receptors or from the ovary.