Visual signals in the courtship of Drosophila melanogaster: Mutant analysis

J. Insect fhysiol.

Vol. 31, No. 12, Printed in Great Britain. All rights

pp. 899-907, reserved

1985 Copyright

VISUAL SIGNALS

IN THE COURTSHIP

DROSOPHILA

0

0022-1910/85 $3.00 + 0.00 1985 Pergamon Press Ltd

OF

MELANOGASTER:

MUTANT

ANALYSIS

F. SCH~~FFELand R. WILLMUND Institut fiir Biologie III, 7800 Freiburg. F.R.G. (Received 19 November 1984; revised 4 Februarv 1985)

Abstract-Visual cues are necessary for optimal mating success in Drosophila melanoguster. The male’s most important visually guided behaviour is tracking. It is shown here that tracking requires intact visual receptor cells RI-6 and the presence of screening pigments in the eye. Thus flies carrying the mutation ebony as well as wild type flies affected in receptor cell RI-6 are unable to use visual cues when they track females. A similar defect was obseved in white-eyed flies lacking screening pigments. Female receptivity depends on visual signals provided by the male flies. Most important cues are the light reflection from and the shape of the male’s eyes. No influence of the light reflected from the thorax could be seen. Absence of eyes in the male, however, does not depress female receptivity as much as white eyes. Some evidence is provided that male courtship behaviour is evaluated visually by the female. Key Word Index: Female vision, mutant analysis

INTRODUCTION

Many experiments have been carried out showing that mutant males are at a disadvantage in competition with wildtype males (Merrell, 1949; Rendel, 1951; Petit, 1959). This could be due to changes in their behaviour patterns (Bastock, 1956; Kyriacou et al., 1978) causing them to provide suboptimal courtship, to reduced activity generally or to changes in their visual appearance or odour, so that females reject them more frequently than wildtype males. No light dependent effect on mating success can be seen in experiments conducted over several hours of observation. Mating occurs equally in light or darkness. However, more detailed observations have demonstrated greater success of wildtype flies in the light. This has been proposed to result from increased activity in the light (Rendel, 1951; Bastock, 1956). In addition it has been shown by means of competition experiments that there is a correlation between mating success and eye pigmentation in males in the light. In the dark, mating is random. Pleiotropic effects of the mutations affecting eye pigmentation, which change light dependent activity of the different mutants were proposed to explain the correlation (Ewing and Manning, 1967). In order to eliminate the possibility of pleiotropic effects, screening pigments were restored by phenocopying techniques (Connolly er al., 1969) and similar results were again found. Observations of single pair mating demonstrated the inability of males with less pigmented eyes to establish and maintain visual contact with females. Pertinently, mutations affecting the density of the screening pigments present in the eye reduce visual acuity (Kalmus, 1943; GGtz, 1964). Many detailed descriptions of courtship behaviour in Drosophila melanogaster are available (Bastock and Manning, 1955; Manning, 1965; Spieth, 1974). The most important visually guided component of the behaviour ,P 31,12--A

displayed by the males is tracking the female (Cook 1979; Cook, 1980). The effects listed above are therefore hardly surprising. Comparison of the mating success of mutants in the light with that in the dark may provide evidence that visual perception of females is also involved. For instance white-eyed males show increased mating success in the dark with wildtype females (Reed and Reed, 1960; Oakeshott and Haymann, 1979; Willmund and Ewing, 1982). This could be due to increased activity of the white-eyed males in the dark which provides more stimulating courtship (Kyriacou et al., 1978; Kyriacou, 1981) an idea that contradicts the earlier conclusion of Bastock (1956). Nonetheless, the difference in some white-eyed mutants is too large to be explained as an effect of the male’s poor visual acuity alone. Therefore the removal under cover of darkness of aversive visual stimuli provided by the mutant males was proposed to be one reason for the greater success (Willmund and Ewing, 1982). Usually female behaviour is observed in single pair matings. If white-eyed males are offered, changes in the pattern of rejection responses by the female has been found. White-eyed males elicit from wildtype females a higher proportion of extrusion relative to wing flicking and kicking, than is the case for wildtype males (Willmund and Ewing, 1982). All three behaviours indicate unwillingness to mate, but extrusion of the ovipositor is a more extreme behaviour in that it makes copulation impossible and may also have an inhibitory effect on male courtship (Bastock and Manning, 1955; Connolly and Cook, 1972). Similarly, mutant females defective in visual-informationprocessing show reduced receptivity in the light with wildtype males. These observations have been taken to indicate that the female’s visual perception is also involved. The question arises: what kind of visual cues provided by the males are important for the female’s response? Her visual evaluation could relate 899

900

F.

SCHAFFELand

to the male’s appearance or his changed behaviour induced by the mutation. Both possibilities have to be taken into account. We have used different eye and body colour mutants to study this question and report here an analysis of certain male specific visual cues which affect female receptivity. MATERIAL AND METHODS

Stocks

The wildtype stock used was Berlin. Mutants were crossed back to the wildtype strain for at least 3 generations to provide a more homogeneous genetic background. The experimental procedure selects for visual signals. For example, differences in activity resulting from different genetic backgrounds will scarcely affect the results, because only lightdependent differences were taken into account. Mutants used se (sepia); bw (brownish-white); wa (white-apricot); cn (cinnabar); MI(white, laboratory stock Freiburg); ~28 (white, laboratory stock Edinburgh); so (sine oculi); e (ebony); B (bar); He (half-eyed); rdg B (Rl-6 degenerated).

All eye colours were combined with wildtype (+) and ebony (e) body colour. One mutant (e;cn) showed extremely low mating success; therefore it was not used. Additionally, mutants without eyes and ocelli (so and e;so), and two eye shape mutants (Bar, having a small disc of ommatidia in the posterior part of the eye and He, possessing the upper part of the eye only) were used. The latter mutation was induced by ethyl methanesulphonate (EMS) on the third chromosome (Campos-Ortega, personal communication).

R.

WILLMUND

receptors was achieved as described by Willmund (1979) by preadaption with intense blue light (2.5 Wm-2) for 30min. The visual pigment is converted to stable metarhodopsin inducing a prolonged depolarisation in the receptors (Cosens and Briscoe 1972; Stark, 1972; Minke et al., 1975; Broda and Wright, 1978) which effectively inactivates the visual subsystem Rl-6 for more than 1 h. Immediate recovery of function is possible by application of an intense yellow light for a few seconds (10 Wme2). Therefore, to prevent the reversion of the photopigment, experiments have to be done in blue light. Light reflected by the eye and thorax under different wavelengths was measured by taking black and white photographs of etherised flies (Fig. 1). Diffuse light was used to illuminate flies while they were photographed, thereby eliminating shine from the surface of the flies and allowing determination of light remission by pigments. The film was used in the linear region of sensitivity. Negative films were anlysed by photometric measurements. The following comparisons were made for five different wavelengths: Thorax-background. Eye-background. Eye-thorax. Means were calculated from independent measurements of 6 individual flies. For calculating correlations between behavioural data and light reflection the Spearman rank correlation coefficient was used (Snedecor and Cochran, 1968). Finally, as shown by Dow (Ph.D. Thesis, Edinburgh 1978) mating success differs with time. Therefore, experiments and corresponding controls were done simultaneously. In addition, flies were maintained in the same room as they were tested. RESULTS

EXPERIMENTAL PROCEDURES

Twenty-five male and 25 virgin female flies were selected after eclosion. They were mass mated as described by Manning (1961), in a conical flask (250ml) during the morning of the third day after emergence. Diffuse illumination was provided by a 60 W bulb at a distance of 40 cm from the closed end. The flask was screened by translucent paper to eliminate an accumulation of flies at one end of the flask due to positive phototaxis. Copulating pairs were counted every 2 min in the dark using dim red light (665 nm), conditions under which flies show no phototactic responses. Means of 6-10 replicates were plotted against time. Because it has been shown that olfactory signals are important (Shorey and Bartell, 1970; Averhoff and Richardson, 1976; Tompkins et al., 1980; Tompkins and Hall, 198la) the influence of different olfactory cues of the mutants which may affect mating success was reduced by using the same flask during all experiments. To assess influence of the visual subsystem Rl-6 [which is impaired in all ebony mutants (Hotta and Benzer, 1969; Heisenberg, 1972a)], mass matings were carried out with populations containing 10 pairs only, since disturbed tracking can be seen better under these conditions. Selective inactivation of these

Wildtype flies were used to test affects of the visual subsystem Rl-6. If the subsystem is inactivated by previous blue-adaptation, mating success is depressed to the same level as found for blind males (so) and photoreceptor degeneration mutant rdg B (Fig. 2). Mating success can be increased immediately to almost the control level by application of intense yellow light, which restores function of Rl-6. For detailed analysis, observations were carried out on single pairs. The importance of visual cues in tracking behaviour is indicated by the duration of the tracking bouts, since mean bout duration increases considerably when visual cues are being used (Willmund and Ewing, 1982). Therefore, the time of 6 bouts was taken in 10 independent experiments (Table 1). Preadaptation procedure was carried out in the same manner as described above. It has been shown also for mutant ora (outer retinula cells Rl-6 absent), that mating success is depressed and the importance of Rl-6 has been discussed elsewhere (Markow and Manning, 1980). In contrast, lack of input via the central retinula cell R7 does not affect visual tracking ability (Willmund and Ewing, 1982). Mass matings with wildtype flies exhibit significantly better success in the light than in the dark (Bastock, 1956; Willmund and Ewing, 1982)

573 nm

478 nm

Fig. 1. Light reflection from the mutant e;wa. The difference in reflection of monochromatic wavelengths 478 and 573 nm from the thorax and the eye is demonstrated.

901

light of

Visual signals ”

903 n

IO

5 1

e

k&s+=+-: I

0

10

20

t[minl

Fig. 2. Effects of inactivation of retina cells RI-6 in male flies. In blue-adapted wildtype flies (0) mating success was depressed to the same level as was found in blind so males (A) and receptor degeneration mutant rdg B (m). A short pulse (10 s) of yellow light (10 Wrn-‘) when applied (see arrow) restored function of RI-6 in wildtype males and

increased mating success rapidly (+). Control yellow adapted wildtype flies (a). Numbers of pairs copulating (n) are plotted against time (t). SEM’s of 610 independent experiments are indicated.

indicating that visual input generally increases success in wildtype flies (Fig. 3). On the other hand several mutants displayed greater success in the dark, especially white-eyed males (Fig. 3). In comparing mating success in wildtype and white-eyed flies it can be seen that it is the behaviour in light that is dissimilar implying that a femalespecific effect is operating. This can be tested by using blind females (e;so) as described above. Results of control experiments are shown below (Fig. 4). Better success in the light indicates the importance of visual tracking and/or increased activity in the light, as seen in wildtype males (Fig. 4). Comparing Fig. 3 and Fig. 4, however, indicates that white-eyed males are more successful with blind females again, implying that they are not rejected. Here the low success compared with wildtype males may relate to poor visual acuity. In addition, white-eyed males exhibit no difference in the light and dark if offered to blind females. To compare the figures the following criterion was used: after a lag-phase occurring within the first 2 min an almost linear increase in the number of pairs copulating is observed for at least 6min. Therefore mating speed between 2 and 8 min (c) which was determined by c=

0)

- 42)

t Cmlnl

Fig. 3. Light dependent difference in mating success in wildtype flies and in the mutant w. In wildtype flies (0) mating success was increased in the light (L). In contrast, if white-eyed males were offered to wildtype females (0) lower success was observed in the light than in the dark (D). All differences are highly significant (Student’s r-test). Plot as in Fig. 2.

and this variable was used for characterisation. Using this criterion, the success of the wildtype males was underestimated because the linear region was abbreviated due to the high mating speed resulting in a deficiency of unmated flies (if only the linear region is used wildtype flies are much more successful than all mutants as indicated in Fig. 7). The difference in mating speed of wildtype flies in the light and in the dark. (A:) is the result of visual components acting in male as well as in female flies. In contrast the light/dark difference found when using blind females (e;so) results from visual components in the male response alone (Ac’:~“). (e;so females were used instead of so, because in pretests wild-type males were more successful). Therefore the total difference (AC,,, = A: - A:;““) should contain a visual evaluation of the wildtype female and also general light dependent variations in receptivity. The latter can be eliminated by comparing the success of all mutants. Visual components which were taken into account are listed in Table 2. Using the criterion described to compare all the

“I

20

15 0 L.D

10

6 5

Table 1. Tracking bout duration of mutant male flies, and blue or vellow adauted wildtvoe male flies

Strain

+

yellow yellow

rdg B usine

+ + _

Mean bout duration (s). SEM’s indicated

Preadaptation before experiment

mu/i

yellow

blue blue-yellow

..

. .

txperlments were carned out m blue light

23.8 + 0.1 1.4kO.1 1.4 + 0.05 1.3 f 0.02 19.6 + 0.7

0

5

10

15

t ImInI Fig. 4. Using blind females (e ;so) which removes any visual cues derived from the male, the wildtype male courtship behaviour was either more stimulating in the light or they were able to follow females more successfully (a). In contrast, no light/dark difference was found when whiteeyed males (w) were offered to blind (e;so) females (0) implying that male vision may not be important. Plot as in Fia - -0. 2 -

904

F. SCH~~FFEL and R. WILLMUND Table 2. Tracking Light dependent

actiwy

Evaluation of the male Light dependent activity

Tracking Light dependent activity (Evaluation of the fern&) (Ealuation

of rhe female)

Evaluation of the male Light dependent activity

Light/dark differences in mating success in mass mating experiments with wildtype females (AC+) and blind females (AC’.“) represent visual components as listed above. AC,,, indicates the light-dependent evaluation of the male by the wildtype female as most of the visual components of male behaviour are eliminated (AC,,,= AC+- Ac’.~). Light dependent differences in activity of the wildtype females will be eliminated by comparing the success of all the mutants.

(Fig. S), it can be seen, that visually guided tracking ability is correlated with eye pigmentation. These results are in agreement with the data of Connolly et al. (1969). The inability of all ebony mutants to use visual cues for tracking females was shown by Crossley and Zuill (1970). Furthermore it can be seen that greater success in the dark is not an effect of the male’s behaviour alone: if all mutants are compared after elimination of the male’s visual components (calculating Ac,,J. the correlation between eye pigmentation and success with wildtype females remains high (Fig. 6). By comparing the success of the mutants differing in body colour but not in eye colour no advantage of wildtype body coloured males was observed. Furthermore flies without eyes were not discriminated against, regardless of body colour (Fig. 7). If light reflection from the thorax is plotted against the degree of visual assessment by wildtype females no correlation can be seen. More evidence can be provided that the male’s eye is an important cue for the female’s assessment by using eye shape mutants. One mutant with changed eye shape (He) was strongly rejected in spite of its good vision (Fig. 8a. Sb). mutants

Fig. 6. After elimination of male visuaf components, mating success still correlates with male eye colour indicating that wildtype female receptivity also depends on male eye colour (0) males with wildtype body colour. (m) males with ebany body colour.

se

bw

wa

w

‘1

so

W28

Fig. 5. Using the criterion described in the text, the importance of visual cues is compared in the mutant males. Tracking ability is inversely correlated with the reflection of 573 nm light by the eye pigmentation in all male flies with wildtype body colour (a). In contrast all males carrying the mutation ebony (m) were unable to use visual cues. Error bars are calculated from the SEM’s measured in the mass mating experiments.

Fig. 7. Comparison of female visual assessment of the mutant males. The same eye colour was offered on wildtype (white column) and ebony (hatched column) body-colour background. No significant difference in female visual as sessment is observed if male vision is impaired (bw, wa, w, ~28, so). Using the criterion described in text, wildtype male mating success is underestimated. A more appropriate evaluation is indicated (dashed fine). For details see text.

Visual signals

visual subsystem Rl-6 is necessary for females to recognize the eye shape of the male (Fig. 9). Because mating success was different in all mutants when compared in the dark (no visual components), songs of the mutants were tested. However, no specific differences were found in parameters which are known to be important (Bennet-Clark and Ewing, 1969).

zo-

15 i

WD

J/--L

104

F

DISCUSSION

10 t

15

Male eye pigmentation

Cmin 1

(a) 25 t

t Cmlnl (b)

Fig. 8a. He 3.x + $. Fig. 8b. He 6x e;so 0. Mutant males with changed eye shape were strongly rejected in spite of their good vision: If blind females were offered (Fig. 8b) it can be seen that mating success was higher in the light than in the dark, indicating that visual cues were important for the males. On the other hand, if wildtype females were used lower mating success was observed in the light (Fig. 8a). Thereby it is shown that wildtype females reject males with changed eye shape in the light. Plot as in Fig. 2. Compare with Fig. 3 and Fig. 4.

Although blue-adaption of females depressed receptivity of a male’s courtship, it was found rejection of males with changed eye shape decreased-males were more successful implying

their that also that

n

t

15 1

influences mating success in

Drosophila melanogaster in a complex way. Firstly,

n /

20

905

YD

male visual acuity depends on the eye pigmentation. Secondly, female receptivity affecting male mating success varies with male eye colour. Therefore care has to be taken that effects of male vision are eliminated if the visual components of female behaviour are to be measured. Experiments using females with defective vision indicated that normal vision is necessary for them to be maximally receptive (Willmund and Ewing, 1982) and could explain the generally depressed receptivity displayed by blind females (e;so) used as controls. The generally depressed mating success could also account for the decrease in the difference found in light/dark comparisons. One cannot be sure that a male’s visual components are indeed eliminated when experiments with blind females and wildtype females are compared. Therefore simple subtraction of AC+ and A:+’ may not be sufficient. For this reason the following calculation was carried out correcting the data of blind females to the level observed in wildtype females:

Correlations between the eye absorption in male and female receptivity of the male courtship are still high (Table 3). Two additonal questions arise: (a) What reference is used by the female flies? This could be the thorax of the male and/or the background. (b) Does the female just assess contrasts, or is eye colour important as well? Correlations were made using the thorax as the reference for the difference in reflected light from it and the eye. At all wavelengths used the correlations were higher to thorax than to background (see Table 3). This could indicate that evaluation of the eye-thorax contrast takes place. It cannot be decided whether wavelengthdependent variation of correlation coefficient repreTable 3. Rank correlation

t [minl

Fig. 9. He dx + 9. Visual subsystem RI-6 in females is necessary for detection of male changed eye shape. If the subsystem Rl-6 was inactivated (PDA, a), mating success was increased. Female receptivity is depressed in the dark if they have been previously blue adapted. Control wildtype females, not blue adapted (0). Experiments were carried out in blue light. Compare with Fig. 8.

.___

Eye-background

i (nm)

rl

rl (corr.)

426 478 516 543 573

0.635 0.629 0.689 0.676 0.758

0.473 0.580 0.566 0.632 0.808

Levels of significance: r-test).

a = 0.05:0.553;

coefficients Eye-thorax __--.-___ rl (corr.) rl __ .___ 0.725 0.x02 0.824 0.841 0.871 0.846 0.857 0.797 0.808 O.Yl8 OL= 0.01:0.684.

(Student’s

906

F. SCH~FFEL and R. WILLMUND

sents the ability of the female to see the eye colour (Hernandez de Spatz 1983). Neither does the experimental procedure eliminate the possibility of higher level visual interactions by male and female flies. Indeed, some evidence can be provided that these visually cued interactions occur: for example (Fig. 7). two males differing in body colour but with the same eye colour do not differ in mating success if their vision is also impaired. However, if the male with wildtype body colour can see well it is comparatively more successful, being more favourably assessed by the female (+/e and se/e;se). Since this favourable assessment is not based on body colour, it could be based on the visual assessment of the male’s courtship behaviour. Secondly, the higher level interaction of the vision of male and female fly can be explained in terms of visually stimulated courtship behaviour in the male. For example, if the male can see well it may respond to visual cues provided by the female. This response might be evaluated visually by the female and result in a more favourable assessment by her. Single matings with wildtype males and red-eyed and white-eyed females were carried out in order to determine whether the male is stimulated by the red eye of the female. In agreement with results of Willmund and Ewing (1982) courtship latency of the males was significantly reduced if red-eyed females (43.6 _+8 s) were compared with white-eyed ones (75.7 +_16.5 s). In control experiments with blind males there were no significant differences (red-eyed females: 131.8 _+24.5 s; white-eyed females: 128.8 _t 14.5 s). Thus the different latencies observed are the result of visual cues. Whether it is the difference in female appearance with respect to eye colour or a difference in the behaviour of the red-eyed and white-eyed females that provide the visual cue for the male cannot be determined. Indeed a combination of both factors may operate. Light dependent pleiotropic effects of the gene locus under consideration or of closely linked background genes on which coselection took place can cause differences of mating success in the light/dark comparison (Oakeshott and Haymann, 1979). Therefore only by comparing several mutants is it possible to decide which criteria are important for the female visual assessment of the males: white eyes along with wrong eye shape provide the aversive stimuli; combination of both aversive stimuli (He;w) causes rejection comparable to white eyes alone; males without eyes are not rejected to the same extent; males with few ommatidia (B) at the posterior part of the eye are treated as having no eyes; greatest success is observed in males having strongly pigmented eyes; no evaluation of body colour could be observed. Under normal laboratory culture conditions (many individuals kept together in a small space) no longterm effects of variations of female receptivity as a consequence of these visual cues will be detectable. However, under natural conditions such visual signals could influence mating success. Acknowledgements-We wish to thank Dr A. W. Ewing for reading an earlier version of the manuscript, for his helpful advice and for providing the opportunity to measure the songs of the mutants, Professor Dr H.-Ch. Spatz for helpful discussions, Professor Dr J. Campos-Ortega for making

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