Z. Tierpsychol.

, 43, 304-310 (1977)

@ 1977 Verlag Paul Parey, Berlin und Hamburg ISSN 0044-3573 I ASTM-Coden: ZETIAG

Department of Zoology, University of Edinburgh, Scotland

Courtship Behaviour in Drosophila: Sexual Isolation or Sexual Selection?

By FLORIAN VON SCHILCHER and MAURICE Dow
Wi t h one figure Received: September 3,1976 Accepted: October 27, 1976

Abstract
The theory of sexual selection and isolation lays heavy emphasis on the role of the 9 as the sex with the higher parental investment - in these activities. The male investment is, however, not negligible and we hypothesize that, under certain, well defined conditions, sexual isolation will be a function of male behaviour, whereas sexual selection will always mainly be a female prerogative. We present behavioural data from observations of intra- and interspecific single pair matings of 5 sibling species of the Drosophila melanogaster group - D . melanogaster, D . simulans, D . mauritiana, D . teissieri, D. yakuba. The results are consistent with our hypothesis. 8 8 are primarily responsible for sexual isolation, whereas 99 dominate sexual selection.

- defined

Sexual isolation and sexual selection are two of the salient functions providing the selective forces which mould courtship behaviour (BASTOCK 1967; GHISELIN 1974). According to one prominent theory of speciation, two previously isolated populations, which come into contact, will evolve reproductive isolating mechanisms if their hybrids have lower fitness than offspring resulting from crosses within the populations. Initially the barriers will be mostly postmating, but as these are rather inefficient, premating isolating mechanisms will be selected for (MAYR1963). Sexual selection in the Darwinian sense within one species remains a hotly debated issue in theoretical proposed it as an evolutionary mechanism different biology since DARWIN 1972). Empirical support for the existence from natural selection (CAMPBELL of sexual selection within and sexual isolation between species comes from 1976). numerous examples of its action in diverse species of animals (WILSON However, these observations leave the problem of the justification of DARWINS distinction untouched. In the choice of a mating partner - within and between species - the 9 should generally be more critical than the 8 (BATEMAN 1948; TRIVERS 1972). In the following we report and discuss results which relate to these issues. They were obtained in intra- and interspecific matings with Drosophila melanogaster and its sibling species.

Courtship Behaviour in Drosophila: Sexual Isolation or Sexual Selection

305

The courtship behaviour of D. melanogaster and D. simulans has been 1959a). The 8 orients to the 0 , taps her with his well described (MANNING front legs, extends one wing 90' and vibrates it, licks her genitalia and attempts to copulate. Drosophila ?? can show a number of rejection movements, like kicking with their hindlegs, wingflicking and extrusion of the and COOK 1973). Among the sensory channels involved ovipositor (CONNOLLY and EWING 1967), in Drosophila courtship, auditory channels (BENNET-CLARK and BARTELL 1970) and contact chemical ones and air-borne chemical (SHOREY (MANNING 1959 b), are outstanding in their importance for successful1 copulation. The latter have been shown to function in species isolation (MANNING 1959 b), whereas airborne chemical channels play a role in intraspecific sexual 1969; AVERHOFF and RICHARDSON 1976). The function of selection (EHRMAN the auditory information given by courting 6 8 to the ?? remains an unresolved problem as far as the above discussed dichotomy is concerned (SCHILCHER 1976a). Recent experiments on the sensory basis of the rare type mating advantage in D. melanogaster have been interpreted by the authors to constitute evidence for an auditory control of this kind of intraspecific sexual selection (PETITand hTouAuD 1975). The evidence, however, rests heavily on the assumption that ?? can perceive auditory signals from wingless 8 6. There is not much support for this contention (SCHILCHER 1976b) and the results might be due to an unspecific effect of aristae amputation on female discriminatory activity. There are now 5 known sibling species of D. melanogaster - D. simulans, D. erecta, D. mauritiana, D . teissieri and D. yakuba (TSACAS pers. comm.). D. melanogaster and D. simulans are cosmopolitan (PATTERSON and STONE 1952) and are therefore sympatric with all the other species.

Materials and Methods

Stocks were cultured on standard cornmeal-molasses medium, seeded with live yeast, at 2 5 f Z O C and under 12 : 12 LD conditions. Pairs of 3 to 4 days old flies were introduced without etherization into cylindrical perspex arenas (2.5 cm in diameter, 1.1 cm high) with central partitions separating the sexes. After removal of the partition, courtship interactions were observed with a binocular microscope. We recorded the duration of the first courtship bout, the male and female sexual behaviour patterns occurring during the interaction and the sex which terminated the bout. The durations of the first bouts were dichotomized as less than c r equal to 1 s, and greater than 1 s. The start of courtship was defined as the first orientation of the 8 to the while within one bodylength of her. The bout was scored as terminated if the 8 was no longer oriented or was preening. The bout was ?-terminated if she flew away or rejected the 8 just before the end of it. The 8 ended the courtship if he turned away, did not follow the or preened, when these behaviours were not preceded by a visible female rejection. D. melanogaster and D. simulans- 88 were paired with 99 of all 6 species. As there were no significant differences between the two species of 88 in their behaviour towards conspecific the results were pooled. The results from the interspecific crosses were pooled on the same grounds.

99,

Results
As can be seen in Table 1, 86 more often terminated interspecific courtship bouts and ?? terminated more intraspecific bouts (x' = 54.95, df = 1, p < 0.001). Table 1 also shows that intraspecific courtship interactions lasted longer than interspecific ones (x' = 36.14, df = 1, p < O.OO1). Table 2 shows that the frequency of the different male behaviours depends on whether the 0 is conspecific or not (x2 = 53.6, df = 3, p < 0.001). Partitioning the chiZ. Tierpsvchol.. Bd. 43. Heft 3

20

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FLORIAN VON SCHILCHER and MAURICE Dov

Table f ; The number of courtship interactions which were terminated by each sex and their duration
terminating sex duration

intraspec ific interspecif ic

18

64

42

30 26

courtship

Behavior

0
intraspecific interspecific

T 3

v
8 1s

AC

1 19

30

27 * 4

Discussion
Since 6 6 more frequently end interspecific encounters, and as these are also much shorter than intraspecific ones, we can conclude that in the former the 8 6 are not highly motivated. As most of the interspecific courtships are terminated after the first orientation and/or tap, and as the sequence orientation-vibration-licking-attempted copulation has been interpreted as indicative of increasing male sexual excitation (BASTOCK and MANNING 1955), this is further evidence for the 6 8low state of sexual arousal in encounters with heterospecific 99.Contact - and/or airborne chemical factors will most probably be responsible for this inale discrimination of heterospecific 99. If one hypothesises that the 99 switch off the interspecific courtship by some means which we cannot readily perceive, then one has to explain why they act so conspicuously when ending intraspecific interactions. Especially since in the former the selective disadvantage conferred by a forced mating would be much more serious. In rare instances we did observe long and rather intensive interspecific interactions and as 99 do occasionally terminate these, the male displays might still be used as a fail-safe mechanism for sexual isolation; however, the selective forces maintaining this mechanism might come from the requirements of sexual selection within the species. It therefore represents a selective epiphenomenon or a preadaptation rather than a true adaptation. Our observations clearly demonstrate that the choice of a mating partner within the species is a female prerogative to a large extent at least. The theory according to which speciation is a consequence of geographic isolation, predicts that isolating mechanism will be more efficient, the earlier in the sequence of epigamic interactions between the sexes they act (MAYR 1963). The parental investment theory predicts that the 99 (the sex with the higher parental investment) should be the principal factor which maintains sexual isolation. In all cases where the 8 (the sex with the lower parental investment) initiates courtship through a physical approach to the 0 , the two

Courtship Behaviour in Drosophifa: Sexual Isolation or Sexual Selection

307

theories are somewhat discordant. According to the former, isolation should take place at the first step of the interaction, namely at the 8's approach to the 0 . According to the latter hypothesis it should only occur at the second step, because it is a prerogative of the 0 . Our results clearly favour the first argument - it is the 8 which is mainly acting in species isolation. We hypothesize, that as the need for sexual isolation arises, behavioural mechanisms which had been used solely for sexual selection within the species may gain an isolating function. The structures serving this function will rapidly be perfected in the 8, due to the selective pressures exercised by the 0 . The female sensory and neuronal discriminatory mechanisms will also be improved by selection. Simultaneously the reciprocal process will also take place, and given enough time it will win the upper hand. Fig. 1 represents a hypothetical example of this process. At time 0 the incipient species come into contact and sexual isolation becomes imperative, due to a fitness deficit of the hybrids between the two populations. The degree of isolation increases, but originally it is mainly dependent on the component from the sex with the higher parental investment. The male sex will become more and more important however, until finally its contribution replaces that of the 0 . At some point in time (time t) the courtship displays of the 8 will lose their significance for the 0 as a means for species identification because it is the 8 8 who discriminate. They take on the active part in reproductive isolation and thereby take the selective pressure off the 00. We expect that the phase in phylogeny in which the 8 is the carrier of the structures employed by the 0 for species recognition is very short in comparison to the time where the 0 carries these structures. We assume that the morphological and/or behavioural characteristics which are used for species recognition will usually be derived from those which had been used in sexual selection within the species before. Therefore when they lose their isolating function they retain their role in sexual selection. This assumption seems plausible because chemical, morphological and behavioural factors which had been involved in sexual contexts before will most conveniently be chosen, due to the fact that the sensory and neuronal mechanisms necessary for their recognition are already preexisting. Furthermore the motivational context does not have to be changed. Accepting this assumption, it follows that it will be extremely difficult to distinguish between the two kinds of structures involved in intra- and inter1

_---2 __--'\
' \

__/--

. . . . .
/ ,

/--/ / /

. . . . .

* - /-

/'
07 ' 0

, , . ,

, ,

r,

/.--. ----_-,
_xr

-- -_--.
~

---_ -----__ --- -_- -- 3

t

time

Fig. I : Schematic representation of the changing roles of the two sexes in sexual isolation, after sympatry has been initiated at time 0. 1. Degree of total sexual isolation between the incipient species. 2. Component due to the sex with the lower parental investment, which also initiates courtship by approaching the opposite sex. 3. Component due to the sex with the higher parental investment

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FLORIAN V O N SCHILCHER and MAURICE Dow

specific sexual selection respectively. The difference will be in quantity rather than in quality, and its degree depends on the phylogenetic history of the species in question. In the present case for example it is unlikely that such behaviours as wing vibration or licking play a large role in isolation, because they are almost never performed in an interspecific context. These behaviours, in particular the inter-pulse interval of the pulse song component of the male song (SCHILCHER 1976b) might however have played an important part in sexual isolation at some earlier stage of the speciation process of the D. melanogaster group of sibling species. The species specificity of the inter-pulse iiiterval (EWINGand BENNET-CLARK 1968) is clearly in favour of such a hypothesis. Indeed the species under discussion differ remarkably in their songs, both quantitatively and qualitatively (EWING1976; SCHILCHER unpublished). Our observations are also supported by SPIETH(1949, 1951, 1974) and STALKER (1942) who have shown in a more qualitative way that the 8 8 of many Drosophila species approach objects of a drosophiloid Gestalt, but after tapping for example a heterospecific 9 or some decoy, immediately turn away. If we look at other animals and the ways by which they maintain sexual isolation, we frequently find a similar picture. For example in fireflies (Photinus) the 88 of two sympatric species have similar flashing patterns. The 90 respond to the 8 8 of both species with species specific flash patterns, but the 88 are only attracted to conspecific 99 (LLOYD1968). In this case the 6 d - the sex which initiates courtship and has a lower parental investment - is mainly responsible for the maintenance of sexual isolation. The 99 and not the 8 8 are the carriers of the recognition structures, in this case flash patterns. The same holds for some moths, where the 9 emits a species specific pheromone which attracts c 3 8 (ROELOFS and COMEAU 1969). In many species of birds (LACK1968), frogs (BLAIR1974), Orthoptera, and Cicadidae (ALEXANDER 1967), the d 8 sing a species specific song and the 99 approach only conspecific 6 8. In these cases the 6 8 are not expected to decide on the species identity of their partner because they are not the initiating sex, and therefore the two theories (parental investment and the contention that isolation should take place at the first step in courtship) are not at variance with each other. There can be no question that our results support the parental investment theory as far as intraspecific sexual selection is concerned. As predicted, the 99 take on the more discriminatory part.

Summary

Intraspecific courtships within the Drosophila melanogaster species group are effectively terminated by 99,reflecting the control over sexual selection exercised by this sex. Interspecific courtships between 88 of D. melanogaster and D. simulans and 99 of D. melanogaster, D. simulans, D. erecta, D. mauritiana, D. teissieri and D. yakuba are broken off by the 8 8 who thereby control sexual isolation. These results confirm a hypothesis which states that the sex with the higher parental investment will originally, after the establishment of sympatry, be more active in sexual isolation, but that gradually this role will be taken over by the sex with the lower parental investment, if the latter also initiates courtship.

Courtship Behaviour in Drosophila : Sexual Isolation or Sexual Selection

309

Zusammenfassung Intraspezifische Paarungen werden in der Drosophila melanogasterArtengruppe, wenn uberhaupt, meist von den 99 abgebrochen. In interspezifischen Paarungskombinationen zwischen 8 8 von D. melanogaster und D. simulans und 99 dieser beiden Arten und D. erecta, D. mauritiana, D. teissieri und D. yakuba sind die d 8 haufiger fur den Abbruch der ersten Werbephase verantwortlich. Wir folgern hieraus, dai3 die 99 die sexuelle Selektion und die 8 8 die sexuelle Isolation bestimmen. Dieses Resultat ist in Obereinstimmung mit einer Hypothese, welche besagt, dai3 urspriinglich, bei der sich ergebenden Sympatrie zweier angehender Arten dasjenige Geschlecht die aktivere Rolle bei der reproduktiven Isolation spielen wird, welches ein hoheres ,,elterliches Investment" macht. Nach einer gewissen Zeit jedoch wird diese Rolle von dem anderen Geschlecht ubernommen, falls dieses das Paarungsspiel einleitet, indem es sich dem Geschlechtspartner nahert. Acknowledgements
This work was supported by scholarships from the German Academic Exchange Service to F.v.S. and from the National Research Council of Canada to M.D. We thank Prof. A . MANNING und Drs. N. P. ASHMOLE and J. M. DEAG for helpful criticism of the manuscript.

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