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Courtship Behaviour in the Drosophila Obscura Group. I: D. Pseudoobscura

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[This paper describes and analyses the courtship of Drosophila pseudoobscura, using as a basis the quantitative techniques developed by BASTOCK and MANNING for D. melanogaster. The courting male first orientates to the female, tapping her with his forelegs; he then extends one wing to 90° and vibrates it, and then jumps and attempts genital contact. He may also stand beside her with wings raised (wing-posture), or very occasionally, face her and rotate his middle legs (rowing). He may also perform the first three of these postures, together with some others (countersignalling) to other males. The courted female may run away, fend, kick or slash at the male with her legs, flutter her wings, curl her abdomen, spread her vaginal plates, or extrude her genitalia, but she only does so in response to the male's courtship - usually after some contact on his part. The male's courtship is analysed in two ways. The sequences in which the elements occur show that the usual prelude to copulation is non-courtship - orientation - vibration - jump; wing-posture is rare here, but is commonest in 3-day males courting non-receptive virgin females. The amount of time spent in courtship by the male is also analysed. Four measures are used : the length of time he spends courting a non-responsive female; Total Response Time (TRT) - the proportion of a fixed observation period spent in courtship; the average length of a courtship bout (CtBA) ; the average length of a non-courtship break (XBA). TRT and CtBA are direct measures of the intensity of the male's courtship, varying with the type of female courted; XBA varies inversely with the courtship intensity, and is unaffected by the type of female courted. On these three measures, 3-day males court at a higher intensity than 1-days ; they also court a non-responsive female for longer, and have a higher copulation success with responsive females. The effect of the female's behaviour on the male is analysed. All the female's movements except spreading inhibit the male in some way; extrusion, performed only by the fertilised females, is particularly effective, making him turn away. Spreading is performed by virgins and appears to assist genital contact after the jump, but is not a positively-stimulating "acceptance response". Unlike the Three-spined Stickleback Gasterosteus aculeatus, pseudoobscura does not depend on fresh, specific stimulation from the female to pass from one element to the next. All that is needed is for the female to provide certain very general stimuli of a non-visual nature (probably transmitted, at least in part, via the male's tapping) at the start of courtship, and to remain present thereafter, and the male will perform the complete orientation - vibration - jump chain. On the other hand, wing-posture only appears when the male has been thwarted in some way- usually by the female's inhibitory behaviour. The internal control of courtship is next analysed. BASTOCK and MANNING have postulated that the rather similar courtship of D. melanogaster is controlled by the fluctuations of a common excitation about certain thresholds, but there is no evidence of anything more than a single courtship-non-courtship threshold in pseudoobscura. It is suggested that the excitation of the 3-day males, courting at high intensity, crosses this threshold for longer at a time than that of the poorly-courting 1-days, but that, once above this threshold, both types of male court with equal frequency. The internal motivation of wing-posture is discussed in greater detail. The frequency of the posture declines in males allowed to court for long periods, while the frequency of turning away from the female increases. It is concluded that there are two tendencies present in courtship - those copulating with, and avoiding the female - and that the relative balance between the two determines whether a male will wing-posture or turn away from a female; the resultant of the two is measured by TRT and CtBA, but XBA is a measure of the copulation tendency only. It is suggested that the decline in wing-posture over long periods is largely due to a rise in the level of avoidance relative to copulation. Vibration and jump appear to be linked to the copulation tendency alone. The motivation of orientation is not clear. The lengths of vibration, and to a lesser extent orientation bouts are very constant. It is suggested that the male will begin to vibrate when he has orientated for a fixed period, and jump when he has vibrated for a fixed period, provided that the female remains constant, and that the shifts from one element to the next in this chain are controlled by feedback effects from the performance of the elements themselves. The functions of the courtship elements are discussed, with particular reference to vibration and wing-posture. The promiscuity of the males indicates that species isolation must depend on the female's choice; the variation in vibration within the obscura group suggests that she chooses on the basis of stimuli from vibration. Males whose wings have been removed and therefore cannot vibrate are less likely to copulate than are controls. The function of wing-posture is uncertain. Male-male interactions and countersignalling are briefly discussed. It is concluded that there is no evidence of a third, aggressive tendency; countersignalling can be explained in terms of modification of the normal courtship., This paper describes and analyses the courtship of Drosophila pseudoobscura, using as a basis the quantitative techniques developed by BASTOCK and MANNING for D. melanogaster. The courting male first orientates to the female, tapping her with his forelegs; he then extends one wing to 90° and vibrates it, and then jumps and attempts genital contact. He may also stand beside her with wings raised (wing-posture), or very occasionally, face her and rotate his middle legs (rowing). He may also perform the first three of these postures, together with some others (countersignalling) to other males. The courted female may run away, fend, kick or slash at the male with her legs, flutter her wings, curl her abdomen, spread her vaginal plates, or extrude her genitalia, but she only does so in response to the male's courtship - usually after some contact on his part. The male's courtship is analysed in two ways. The sequences in which the elements occur show that the usual prelude to copulation is non-courtship - orientation - vibration - jump; wing-posture is rare here, but is commonest in 3-day males courting non-receptive virgin females. The amount of time spent in courtship by the male is also analysed. Four measures are used : the length of time he spends courting a non-responsive female; Total Response Time (TRT) - the proportion of a fixed observation period spent in courtship; the average length of a courtship bout (CtBA) ; the average length of a non-courtship break (XBA). TRT and CtBA are direct measures of the intensity of the male's courtship, varying with the type of female courted; XBA varies inversely with the courtship intensity, and is unaffected by the type of female courted. On these three measures, 3-day males court at a higher intensity than 1-days ; they also court a non-responsive female for longer, and have a higher copulation success with responsive females. The effect of the female's behaviour on the male is analysed. All the female's movements except spreading inhibit the male in some way; extrusion, performed only by the fertilised females, is particularly effective, making him turn away. Spreading is performed by virgins and appears to assist genital contact after the jump, but is not a positively-stimulating "acceptance response". Unlike the Three-spined Stickleback Gasterosteus aculeatus, pseudoobscura does not depend on fresh, specific stimulation from the female to pass from one element to the next. All that is needed is for the female to provide certain very general stimuli of a non-visual nature (probably transmitted, at least in part, via the male's tapping) at the start of courtship, and to remain present thereafter, and the male will perform the complete orientation - vibration - jump chain. On the other hand, wing-posture only appears when the male has been thwarted in some way- usually by the female's inhibitory behaviour. The internal control of courtship is next analysed. BASTOCK and MANNING have postulated that the rather similar courtship of D. melanogaster is controlled by the fluctuations of a common excitation about certain thresholds, but there is no evidence of anything more than a single courtship-non-courtship threshold in pseudoobscura. It is suggested that the excitation of the 3-day males, courting at high intensity, crosses this threshold for longer at a time than that of the poorly-courting 1-days, but that, once above this threshold, both types of male court with equal frequency. The internal motivation of wing-posture is discussed in greater detail. The frequency of the posture declines in males allowed to court for long periods, while the frequency of turning away from the female increases. It is concluded that there are two tendencies present in courtship - those copulating with, and avoiding the female - and that the relative balance between the two determines whether a male will wing-posture or turn away from a female; the resultant of the two is measured by TRT and CtBA, but XBA is a measure of the copulation tendency only. It is suggested that the decline in wing-posture over long periods is largely due to a rise in the level of avoidance relative to copulation. Vibration and jump appear to be linked to the copulation tendency alone. The motivation of orientation is not clear. The lengths of vibration, and to a lesser extent orientation bouts are very constant. It is suggested that the male will begin to vibrate when he has orientated for a fixed period, and jump when he has vibrated for a fixed period, provided that the female remains constant, and that the shifts from one element to the next in this chain are controlled by feedback effects from the performance of the elements themselves. The functions of the courtship elements are discussed, with particular reference to vibration and wing-posture. The promiscuity of the males indicates that species isolation must depend on the female's choice; the variation in vibration within the obscura group suggests that she chooses on the basis of stimuli from vibration. Males whose wings have been removed and therefore cannot vibrate are less likely to copulate than are controls. The function of wing-posture is uncertain. Male-male interactions and countersignalling are briefly discussed. It is concluded that there is no evidence of a third, aggressive tendency; countersignalling can be explained in terms of modification of the normal courtship.]

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/content/journals/10.1163/156853964x00094
1964-01-01
2015-05-27

Affiliations: 1: Department of Zoology, University of Oxford

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