@ Masson, Paris, 1978

Biology of Behaviour, 1978, 3, 187-190

Courte note

Sexual Experience and Courtship Behaviour in Drosophila melanogaster

Maurice A. Dow
Depaltment oi Zoology, Unzversity o f Ediilbuugh, Edz~iht~rghH 9 3JT (Scotland) E Key words: Mating Behaviour, licking rate, sexual experience.

KESUME
Experience sexuelle et parade nuptiale chez Drosophila meln~zogasleu. I1 a et6 montrd que l'expkrience sexuelle du m5le de Drosophila rnelanogaster a un effet sur son comportemcnt sexuel. La quantite de cour exigte pour qu'un msle expkrimente s'accouple avec une femelle vierge s'accroit a rnesure qu'augmente le nombre des accouplements accomplis par le rniile. La frequence B laquelle le mSle lkche I'extrCmitC de l'abdomen de la femelle diminue entre le premier accouplement du miile et les suivants. Cette reponse n'est pas adaptative du point de vue du miile puisque cela rend plus difficile des accouplements ultdrieurs avec d'autres femelles. Cependant puisque la quantitC des spermatozoi'des du msle diminue aprks chaque copulation, cette rkponse due 2 I'experience est adaptative pour la femelle ; elle augmente la probabilitk pour la femelle de s'accoupler avec un msle vierge qui a une quantitk maximale de spermatozoi'des disponibles.

Mozs cles: Paradc nuptiale, frequence du lecher, experience sexuelle.

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SUMMARY

Linley and Mook (1975) have recently reported that sexual experience in Culicoides melleus males affects their courtship behaviour and decreases their mating success and that this response is adaptive from the female's point of view and not the male's. Since it has also been show that previous mating experiences affect mating success in Drosophila pseudoobscura (Pruzan and Ehrman, 1974), I have examined whether experience affects the courtship behaviour of male Drosophila melanogaster and whether the effect is adaptive.

R e ~ ule : 3-1-77 ; Accept6 le : 27-5-77. Tire's a part: Maurice A. Dow, adresse ci-dessus.

A recently collected (France, Sept., 1974) wild type strain of

D. melanogaster was mass bred on standard medium at 2O C. All flies 5

where collected as virgins within 15 min. from eclosion without anaesthetization and kept singly until 4 days old. Each pair of flies was introduced into a perspex arena (13 mm diameter, 7 mm high) without anaesthetization and the sexes separated by a sliding partition. After a 5 min. period to settle the flies, the partition was removed and the courtship behaviour was observed with a binocular microscope.

mating time- defined as the time from the start of courtship to the time that copulation started, and licking rate-defined as the total number of times that the male licked the female's genitalia, divided by the mating time. Licking rate was chosen as a measure of the intensity of courtship since it is highly correlated with most other aspects of courtship behaviour and is easily scored (Manning, 1961). After the first copulation had ended the female was removed and the male was given a 20 min. rest. A second female was introduced then and the procedure was repeated. After the third such mating the male was returned to his vial. Twenty four hours later a fourth courtship was observed. Figure 1 shows that there was a significant increase in mating time with the number of courtships completed by the male A = 0.53, t = 2.75, P < 0.05). The increase in mating time between the first courtship and all later ones was highly significant (t = 3.92, P < 0.001). The amount of recovery after 24 hours was not significant. The correlation between licking rate and the number of completed courtships (fig. 2) was not significant (F A = -0.34, t = 1.76, P > 0.1). However, there was a significant decrease in licking rate between the first and later courtship (t = 3.32, P <0.01). Again, the amount of recovery after 24 hours was not significant. Combining these two relationships, one finds that mating time and licking rate were highly correlated (r A = - 0.76, t = 7.0, P < 0.001). Since neither mating time nor licking rate showed significant recovery after 24 hours of rest, it is unlikely that physical fatigue was solely responsible for the effects shown in the two figures ; after three courtships the males had spent a maximum of 15 min. in active courtship and 50 min. in copula. Males of D. mela~logasterare capable of successfully inseminating up to eight females per 12 hour mating period (Kvelland, 1965) and since the number of females a male inseminates is negatively correlated with his mating time (Fulker, 1966), an experiential response which increases his mating time (fig. 1) is maladaptive.

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Fig. 1: T h e relationship between m e a n mating t i m e (2 S E ) and the number of courtships p e r f o r n ~ e db y the male. Mating times were normalised by logarithmic transformation. Each mean is based on nine or ten observations. Fig. 1: La connexton enlre la dure'e moycnne de parade tzuptiale (2 l ' i c ~ r t lype d e Zn mo,enne) et Z n o m b r e des e cottrs que le male n exicutee. Les durCes de parade nuptiale ont CtC normalis6 avec la transforn~ation logarithm. Chaquc moyenne est basie sur neut ou dix observations.

Fig. 2 : Therelationship between t h e m e a n licking rate ( 4 S E ) and t h e nuntber o/ courfships p e r f o t n ~ e d b y t h e male. Fig. : La connexion entre la frkquence moyenne d e lecher e t le nombre des collrs q u e Ic mdle U exiclitke.

Also, it should be noted that in natural, unconfined conditions, an increase in mating time would result in a number of aborted courtships due to the female flying or running away before copulation or due to the distraction of the courting male by neighbouring flies. However, such an increase is adaptive from the female's point of view. It has been shown that for sexually mature (3 day old) males, the first copulation produces more progeny (i.e. more sperm available) than any later copulation and that there is a trend toward the production of fewer offspring per mating with increasing number of consecutive copulation~ (Kvelland, 1965). Both egg production and hatchability vary with female age, reaching a maximum between days 6-10 and declining thereafter (McMillan et aL, 1970). Egg hatchability also depends upon the number of sperm present in the female (Kaufmann and Demerec, 1942) and as females tend not to remate until they have exhausted their previous sperm supply (Manning, 19621, it is advantageous for a female to have the maximum amount of sperm possible during the optimum productive period. The response shown in figure l will tend to insure that this is the case.

This is analogous to the response found in sexually experienced Ctllicoides m e l l e ~ l s(Linley and Mook, 1975) where its adaptiveness was also attributed to the female's sperm requirement. The response of male Drosoplzila melalzogaster to sexual experience would increase the fecundity of females that remate, as such females would be more likely to mate with the males with the most sperm, and thus the response could evolve through individual selection acting on the female. I t could also evolve through lrin selection acting on the female's relatives (e.g. sisters) for the sanie reason. For such altruistic behaviour to work, sisters would have to be more common than unrelated females in the local population at the time of mating (Hamilton, 1964). Linley and Mook (1975) ascribed the change in mating success to male sensitization by the female's defensive grooming (kicking) during a previous copulation. Since D. ~~zelanogaster females also exhibit kicking and defensive grooming during copulation (Spieth, 1974, and personal observations), the causal basis for the increase in mating time in D. ~ ~ z e l rzugaster may be the same type of male sensitization. Detailed observations are required to determine whether this is so.
Acknowledgments : Research supported by the National Research Council of Canada. I thank Mr. J. Wrigl~tfor translating the French summary, and Dr. A.W. Ewing and Mr. R. Wright for their comments o n the manuscript.

REFERENCES Fulker D.W., 1966. Mating speed in male Drosophila inelanogaster : A psychogenetic analysis. Science, 153, 203-205. Hamilton W.D., 1964. The genetical evolution of social behaviour. J. Theoret. Biol., 7, 1-16. Kaufmann B.P. and Demerec M., 1942. Utilization of sperm by the female Drosophila melanogaster.. Arner. Natur., 76, 445-460. Kvelland I., 1965. Some observations on the mating activity and fertility o DrosoE phila melanogaster males. Hereditas, 53, 281-306. Liiiley J.R. and Mook MS., 1975. Behavioural interaction between sexually experienced C~ilicoidesmelleus (Coquillet) (Diptera : Ceratopogonidae). Behaviour, 54, 97-110. Manning A., 1961. The effects of artificial selection for mating speed in Drosophila nzelanogaster. Anim. Behav., 9, 83-92. Manning A., 1962. A sperm factor affecting the receptivity of Drosophila melanogaster females. Nature, 194, 252-253. McMillan I., Fitz-Earle M,, Butler L. and Robson D.S., 1970. Quantitative genetics of fertility. 11. Lifetime egg production of Drosophila melanogaster-Experimental. Getfetics, 65, 355-369. Pruzan A. and Ehrman L., 1974. Age, experience and rare male mating advantages in Drosophila pseudoobscura. Belzav. Genet., 4, 159-164. Spieth H.T., 1974. Courtship behaviour in Drosophila. Ann. Rev. Entomol., 19, 385-405.