copulatory courtship in drosophila birchii and d. serrata, species recognition and sexual selection

P1: FDR/lwe P2: FDR/fok QC: FhN

Journal of Insect Behavior [joib] PJ002-795 April 13, 2000 19:8 Style file version Feb 08, 2000

Journal of Insect Behavior, Vol. 13, No. 3, 2000

Copulatory Courtship in Drosophila birchii andD. serrata, Species Recognition and Sexual Selection

Anneli Hoikkala,1,3 Stella Crossley,2 and Claudia Castillo-Melendez2

Accepted December 3, 1999; revised December 29, 1999

Two endemic Australian Drosophila species, D. birchii and D. serrata, havea copulatory courtship, i.e., the males court the female mainly during copula-tion. In the present study we found the males of both species to mount theirprospective mating partners selectively, exhibiting both sex and species recog-nition. The males began to sing after mounting the female, and they often ex-hibited also postcopulatory displays typical to copulatory courtship. D. birchiiand D. serrata females discriminated against males which did not sing duringmounting/copulation, which suggests that the females utilize cryptic femalechoice. Our findings raise the question of how widespread a phenomenoncryptic female choice is in Drosophila species.

KEY WORDS: Drosophila; copulatory courtship; mate choice; cryptic female choice.

INTRODUCTION

The primitive courtship pattern in Diptera is mating in flight (Downes, 1969).In most species of this order, however, the mating occurs on the substrateand is usually preceded by elaborate courtship rituals. These rituals havebeen studied most thoroughly in the species of the genus Drosophila, wherecourtship displays and signals emitted by the courting flies can be fascinating

1Department of Biology, University of Oulu, Finland.2Department of Psychology, Monash University, Clayton, Victoria, Australia.3To whom correspondence should be addressed at Department of Biology, University of Oulu,P.O. Box 3000, 90401 Oulu, Finland; e-mail: [email protected].

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362 Hoikkala, Crossley, and Castillo-Melendez

(Spieth, 1974). Complex courtship behavior of the males enables the femalesto exercise mate choice before mating (Ewing, 1983).

In many insect species the males begin to court the female only aftermounting her, and they may go on courting her even after the copulation isover (Eberhard, 1991). In these “copulatory courtships” the females’ abilityto exercise selection before mounting/copulation is limited. Eberhard (1991)has suggested that copulatory courtships may evolve only if the females exer-cise “cryptic choice,” i.e., if the females are able to influence male’s chances offathering offspring even after the male has achieved intromission. Eberhard(1991) further suggested that as copulatory courtships are widespread amonginsect species, sexual selection by cryptic female choice may have been animportant factor in the evolution of insect species.

In our earlier study (Hoikkala and Crossley, n.d.), we found the males oftwo Australian Drosophila species, D. birchii and D. serrata, to court the fe-male actively during copulation. These species are thus potential candidatesfor species exhibiting cryptic female choice. D. birchii and D. serrata forman interesting species pair also in other respects. They are partly sympatricin New Guinea and northern Australia (Dobzhansky and Mather, 1961).The species look alike, but external male genitalia separates them unequiv-ocally (Bock, 1976). Sexual isolation between the species, and in some casesalso between conspecific populations, is very strong (Ayala, 1965), but inthe laboratory the species produce viable and fertile interspecific hybridsof both sexes. D. birchii and D. serrata belong to the montium subgroup ofDrosophila, which is the largest subgroup of the melanogaster group (Bock,1980). In this subgroup a few other species have also been found to exhibitcourtship during copulation (Tomaru and Oguma, 1994), although to a lesserextent than D. birchii and D. serrata.

In the present study we confirm that the courtships of D. birchii andD. serrata can be classified as copulatory courtship. We also study sex andspecies recognition exercised by the males and mate choice exercised by thefemales of these species. Here our main questions are: Do the males exerciseselection on their prospective mating partners before mounting and do thefemales discriminate against males which are not able to produce song duringcopulation?

METHODS

Flies

We used flies of D. serrata and D. birchii isofemale stocks established byAry Hoffman (LaTrobe University) about 1 year ago. The D. birchii stock



Mate Choice in Drosophila 363

originated from Barraine (Queensland) and the D. serrata stock from Eugella(Queensland). Fly stocks were maintained on potato/sugar medium in stan-dard culture bottles in 12:12 light–dark cycle at 25◦C. Males and females weresexed within 6 h of eclosion under light carbon dioxide anesthesia. At thesame time the wings of half of the males for the female-choice experimentwere removed. The flies were held in food vials and used in the experimentsat the age of 3–10 days. Each fly was used in the experiments once.

Sex and Species Recognition

We videotaped for both D. birchii and D. serrata 20 single-pair courtshipsbetween the following fly pairs: (1) D. birchii male with D. birchii female,(2) D. birchii male with D. serrata female, (3) two D. birchii males, (4) D. ser-rata male with D. serrata female, (5) D. serrata male with D. birchii female,and (6) two D. serrata males. The flies were introduced, without anaesthesia,into small Perspex chambers (height 0.4 cm, width 1.5 cm), which were cov-ered with a glass coverslip. Each chamber had a small hole in its side throughwhich the flies were introduced. During the videorecordings these holes wereplugged with a moistened cotton stopper. The six chambers, having differentcombinations of flies, were placed on white paper and videotaped for 3 hwith the camera held vertically above the chambers. Recordings were madeusing a Panasonic NV-S99A videocamera and a Panasonic NV-FS1 videorecorder. One set of each of the six different kinds of pairings was run oneach day between 0900 and 1200 hours. Light was daylight and ambient tem-perature, 21–26◦C. The method gave 3 h of continuous videorecordings ofthe six chambers at each setup.

Videotapes were analyzed by observing interactions between the flies ineach chamber. Behaviors observed are listed in Table I. Individual behaviors,

Table I. Male Behaviors Observed

Orientation Male orientates toward the female (or male) or follows her/him; occasionallythe male can also touch his partner or circle around her/him

Wing vibration Male repeatedly extends one wing 30◦–70◦ and vibrates it in that position;these wing vibrations occurred during mounting (in which case the malewing vibration was not classified separately), immediately afterdismounting, and, occasionally, when the male followed his partner closely

Mounting Male lunges onto the back of the female; at the beginning of the mountingbout the males always vibrated their wings; mountings where the malesucceeded to remain in a copulation posture for at least 1 min areclassified as successful mountings (see text for explanation)

Fighting Fighting includes aggressive interactions between flies: rapid wing extensions(one or both wings) and quick attacks where the flies touch each otherwith their front legs




separated from each other by a change in male’s behavior (most often bya break in courtship), are called behavior bouts. To analyze the data, wecounted the frequencies of different behavior bouts exhibited by the maleand measured the durations of these bouts in each courtship. In successfulcourtships this was done both before and after mounting/copulation.

Mate Choice Exercised by the Females

To study mate choice exercised by the females, we observed 100 single-pair courtships for each species, half of them with normal and half withwingless males. In many Drosophila species the females have been found todiscriminate against wingless males because these are not able to produceaudible courtship songs (Ewing, 1983). Comparison of copulations with andwithout male songs gave us an opportunity to study whether D. birchii andD. serrata females discriminated against males which did not sing duringcopulation.

The flies were transferred, with an aspirator, into empty glass vials(height 10 cm, width 2.5 cm), and the vials were stoppered by a moistenedcotton plug. The vials were set in a horizontal position on white paper. Ineach 30-min session we observed the behavior of 10 fly pairs: 5 females withnormal males and 5 females with wingless males, each pair in its own vial. Allobservations were made between 0900 and 1200 h. To study progeny produc-tion of the females mated with normal and wingless males, we transferredthe females which had copulated during the observation period individuallyinto fresh food vials and left them to lay eggs for 1 week. During the next2 weeks we counted the number of progeny emerging from the vials.

While observing the flies, we made notes on the behavior of the malesduring mounting: How quickly did the male achieve copulation posture aftermounting the female? How long did he vibrate his wings before and afterthe copulation had taken place? How long did the copulation last?

RESULTS

Sex and Species Recognition

Both D. birchii and D. serrata males behaved differently when courting amale or a female of their own species or a female of an alien species. Table IIshows the summary of male behavioral acts in chambers with different flycombinations during the 3-h videorecording period. Division into unsuccess-ful mounting attempts and successful mountings was based on the lengths of




Tabl

eII

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ians

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(s)

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edia

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ange

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the

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gths

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dual

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tsof

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ehav

iors

(Sec

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D.b

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tion

175

(14–

1049

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–237

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)12

2(5

–140

0)53

.0(5

–415

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8(1

9–55

4)24

.4(7

–91)

9.50

(5–2

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–26)

22.0

(5–9

7)17

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(5–4

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10N=

15N=

20N=

15N=

19W

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27.0

(10–

53)

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12N=

2M

ount

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11.0

(1–1

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17.0

(7–2

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Table III. The Durations (Medians and Ranges) of Male Behaviors During Mounting inCourtships for Normal and Wingless D. birchii and D. serrata Malesa

Time from mounting Copulation Wing vibrationMale N to copulation (s) length (s) during mounting (s)

D. birchii 31 5.00 (1–25) 207 (123–407) 28 (5–142)normal

D. birchii 5 11 (2–15) 341 (86–668)wingless

D. serrata 31 3.0 (2–5) 240 (157–472) 9.0 (4–22)normal

D. serrata 14 4.5 (2–8) 245 (107–489)wingless

aN refers to the number of males which succeeded in copulating with the female for at least1 min.

the mounting bouts. In D. birchii short mountings lasted for 1 to 59 s (median10 s) and longer mountings for 136 to 436 s (median 258 s). In D. serrata therespective lengths were 2–27 s (median 5.6 s) and 182–500 s (median 332 s).As the flies copulated within a few seconds after mounting (Table III), and asthe shortest copulation leading to progeny production was 123 s in D. birchiiand 157 s in D. serrata (see below), short mountings of both species couldsafely be classified as unsuccessful mounting attempts. Consequently, mount-ings where the male succeeded to remain in copulation posture for at least1 min were classified as successful mountings.

The males were most active in chambers with conspecific females. Inthese chambers both D. birchii and D. serrata males spent most of their ac-tive courtship time in orientating toward the female (D. birchii, 37%, andD. serrata, 22%, of active courtship time) and, in successful courtships, inmounting (D. birchii, 54%, and D. serrata, 61%, of active courtship time).D. serrata males frequently orientated also toward D. birchii females and con-specific males. Other interesting observations are that D. serrata males foughtwith each other quite frequently and that they made unsuccessful mountingattempts in nearly all intraspecific homo- and heterosexual courtships.

Medians for the total durations of different behaviors as well as medianlengths of individual bouts of these behaviors are given for the courtshipswhere these behaviors occurred. The total durations of different behaviorspresented in Table II are not directly comparable between chambers with oneand two courting males. For this reason we have compared only the lengthsof individual behavioral bouts between different fly groups (see Table II).The lengths of the orientation bouts of D. birchii males varied significantlydepending on whether the male was courting a D. birchii female or male ora D. serrata female (Kruskal–Wallis analysis of variance, χ2= 13.432, df =2, P= 0.001). As the males always vibrated their wings while mounting the




female, only wing vibration occurring before or after (not during) mountingwas registered separately (see Table I). Both in D. birchii and D. serrata, thewing vibration bouts occurring before or after mounting were significantlylonger in intraspecific heterosexual courtships than in homosexual court-ships (Mann–Whitney U-test, D. birchii: U= 2.500, P= 0.006; D. serrata:U= 0.500, P= 0.036). This may partly be due to fact that in heterosexualcourtships the males vibrated their wings only during or after mounting(except one D. birchii male, which vibrated his wings before mounting thefemale), while in homosexual courtships the males vibrated their wings forshorter periods ‘any time.’

Intraspecific, heterosexual courtship led to copulation in 12 of the20 chambers both in D. birchii and in D. serrata. Figure 1 shows the timespent by the male in active courtship and/or copulation before, during, andafter mounting in these courtships. The males of both species spent lesstime in courting the female before than after mounting, but the differencewas statistically significant only in D. serrata (Wilcoxon signed ranks test,Z= −2.919, P= 0.004). In six courtships of D. birchii and D. serrata wherethe male courted the female both before and after a successful mount-ing, copulation changed males’ behavior quite dramatically (Fig. 2). Be-fore mounting, the males spent nearly all of their active courtship time inorientating toward the female, while after copulation, they began to vi-brate their wings and make further mounting attempts. Only the increase inD. serrata wing vibration was statistically significant (Wilcoxon signed rankstest, Z= −2.023, N = 6, P< 0.05).

Mate Choice Exercised by the Females

When studying the mate choice exercised by the females we observedthe behavior of the flies in glass vials. This enabled us to observe more thor-oughly male behavior during mounting, e.g., how quickly the male achievedcopulation posture after mounting the female and how long he vibrated hiswings during mounting/copulation.

The behavior of D. birchii and D. serrata males during mounting hadsome species-specific characters. Normal D. serrata males achieved copu-lation posture within three seconds (medium) after mounting the female,while for normal D. birchii males this took about five seconds (Table III).The difference between the normal males of the two species was significant(Mann–Whitney U-test, U = 239.5, P = 0.001). The males of both speciesvibrated their wings while mounting the female. D. birchii males vibratedlonger than D. serrata males (Mann–Whitney U-test: U = 88, P < 0.0001).The males of the first-mentioned species produced about 71% of their song




Fig. 1. Medians, quartiles, and maximum and minimum values of the duration ofthe time the males spent in active courtship/copulation before, during, and after asuccessful mounting in intraspecific successful courtships. Number of courtshipsin both species is 12.




Fig. 2. Medians, quartiles, and maximum and minimum values of the durationsof male behaviors (orientation, wing vibration, and mounting attempts) as aproportion of active courtship time before (1) and after (2) a successful mountingin D. birchii and D. serrata. In both species the values are given for six intraspecificcourtships where the male courted the female both before and after a successfulmounting.




and the males of the last-mentioned species about 61% of their song afterthe male had reached the copulation posture. Copulations lasted for 3–4 minin both species.

The importance of male wing vibration for the mounted female was stud-ied by observing whether the females discriminated against wingless maleswhich were not able to sing during copulation. Both normal and winglessmales courted the female actively, even though wingless D. birchii maleshad some difficulties in mounting the female. In this species 35 of 50 nor-mal males (70%) and 18 of 50 wingless males (36%) mounted the femaleat least once during the 30-min observation period. The difference betweenthe two male types was significant (χ2-test: χ2= 11.60, df= 1, P< 0.001). InD. serrata, 64% of normal and 48% of wingless males made at least onemounting attempt during the observation period. In this species the frequen-cies of mounting males did not differ between normal and wingless males(χ2-test: χ2= 2.60, df= 1, P= 0.107, NS).

Normal males succeeded to copulate with the female during their mount-ing bouts more often than the wingless males. Copulation length was usuallydetermined by the female, which forcibly dislodged the male after a shorter ora longer mounting period. In D. birchii, 89% of normal and 22% of winglessmales which mounted the female during the observation period succeededto stay in copulation posture for at least 1 min. In D. serrata the respec-tive numbers were 97% and 54%. In both species normal males were moresuccessful in staying in copulation than wingless males (χ2-tests: D. birchiiχ2= 29.34, df= 1, P< 0.0001; D. serrata χ2= 11.68, df= 1, P< 0.001).

The females were transferred in food vials after the experiment tostudy how long the flies had to copulate for a successful sperm transfer.Shortest copulation producing progeny was 123 s in D. birchii and 157 s inD. serrata. The number of progeny which the females produced during the1 week following copulation did not correlate with the copulation lengthin either species (Spearman’s rank correlation for normal D. birchii males:rs = −0.130, N = 31, NS; for normal D. serrata males: rs = −0.133, N = 27,NS; and for wingless D. serrata males: rs = −0.138, N = 14, NS [one-tailedtests]).

DISCUSSION

Courtships of D. birchii and D. serrata can definitely be classified as cop-ulatory courtship. Typical of these courtships is that they occur mainly afterintromission and that the males also court the female after the copulationhas finished (Eberhard, 1991). In our previous paper (Hoikkala and Crossley,




n.d.), we showed that D. birchii and D. serrata males court the females dur-ing mounting. In the present paper we also showed that the males of thesespecies mount their prospective mates selectively and also exhibit postcopu-latory displays. Females discriminated against wingless (mute) males duringmounting both before and after the onset of copulation, which suggests thatfemale mate choice is at least partly cryptic.

In primitive courtships typical to Acalypteratae, the males lunge ontoany suitable individual, grasp her/him with their forelegs, and attempt toachieve intromission (Spieth, 1974). This is not the case in D. birchii andD. serrata. Even though the males of these species usually mount the femaleswithout first courting them, they clearly exercise choice on their prospectivemating partners. In the present study both D. birchii and D. serrata malesdirected most of their orientation bouts and mounting attempts toward con-specific flies, mainly the females. Also, the lengths of the male behaviorbouts varied depending on the sex and species of the courtship object. Blowsand Allan (1998) have shown that cuticular hydrocarbons of D. birchii andD. serrata separate in three levels of organization: species, sex, and sex withinthe species. By perfuming individuals of one species with the smell of indi-viduals of the same sex from the other species, Blows and Allan were ableto increase the frequency of hybridization between the two species. Thissuggests that pheromones play an important role in enabling D. birchii andD. serrata males to recognize the females of their own species.

Even though sexual isolation would largely be maintained by males,sexual selection within the species will always mainly be a female prerogative(von Schilcher and Dow, 1977). In general, the females may exercise choice ontheir prospective mates before, during, and/or after mating (Thornhill, 1983).In cryptic female choice, selection occurs during the last two mentionedstages. In our study, both D. birchii and D. serrata females were found todiscriminate against wingless males (i.e., males which were not able to sing)during mounting. The females could exercise choice before copulation bypreventing the males from achieving intromission, and during copulation byforcibly dislodging the male after a shorter or a longer copulation period. Inour previous paper (Hoikkala and Crossley, n.d.) we show that D. birchii andD. serrata females have evolved various methods to dislodge the copulatingmale.

Eberhard (1991) showed that copulatory courtships are quite commonin insect species. Based on a sample of 230 published papers, he estimatedthat this kind of courtship occurs in 36% of 302 species in 34% of 231 gen-era, and 43% of 102 families in 13 different orders. He suggests that cop-ulatory courtship behavior diverges relatively rapidly, as it often differs incongeneric species. Copulatory courtship was earlier reported in only one




Drosophila species, D. pegasa (Wasserman et al., 1971). The males of thisspecies forcibly mount the female and ride her for hours while attemptingmultiple intromissions. Some features of copulatory courtship are, however,apparent in several Drosophila species. Males of some species of D. virilisgroup (Hoikkala et al., 1982), D. bipectinata complex (ananassae subgroup,melanogaster group; Crossley, 1986), auraria complex (montium subgroup,melanogaster group; Tomaru and Oguma, 1994), and of D. phalerata (quinariagroup; Neems et al., 1997) have been reported to vibrate their wings produc-ing song and also to rub the female abdomen during copulation. Courtshipduring copulation has also been reported in Zaprionus species (Bennet-Clarket al., 1980), which are close relatives of Drosophila.

D. birchii and D. serrata males exhibited also postinsemination displayswhich are typical to copulatory courtship. The males of both species often vi-brated their wings immediately after dismounting the female or when follow-ing the female at a close range after dismounting. They (especially D. serratamales) also made several mounting attempts after copulation. According toAlcock and Buchmann (1985), this kind of display may keep the female unre-ceptive preventing further matings and sperm displacement. Courtship aftercopulation was earlier reported in some species of D. virilis group (Hoikkalaet al., 1982), auraria complex (Oguma et al., 1987), eremophila complex (re-pleta group; Alonso-Pimentel, 1995), and in Zaprionus (Bennet-Clark et al.,1980).

Eberhard (1991) suggested that cryptic female choice is a prerequisitefor the evolution of copulatory courtship. In species with cryptic femalechoice, the males will be selected to induce the females to perform crucialpostintromission processes, and this may lead to the evolution of courtship af-ter intromission has begun. In the present paper we found that both D. birchiiand D. serrata males selectively mounted their prospective mating partners,and that copulations occurred only between conspecific flies. We also foundthat the females of these species discriminated against males which werenot able to produce courtship song during copulation. Our findings raisethe question of how widespread a phenomenon cryptic female choice is inDrosophila species in general.

ACKNOWLEDGMENTS

We are grateful to Ary Hoffman and Mark Kellett for providing flies forthe study. We also thank the Department of Psychology, Monash University,for excellent working facilities. This work was supported by grants from theDepartment of Psychology, Monash University, and the Academy of Finlandto A.H.




REFERENCES

Alcock, J., and Buchmann, S. L. (1985). The significance of post-insemination display by malesof Centris pallida (Hymenoptera: Anthophoridae). Z. Tierpsychol. 68: 231–243.

Alonso-Pimentel, H. (1995). Courtship sounds and behavior of the two saguaro-breedingDrosophila and their relatives. Anim. Behav. 50: 1031–1039.

Ayala, F. J. (1965). Sibling species of the Drosophila serrata group. Evolution 19: 538–545.Bennet-Clark, H. C., Leroy, Y., and Tsacas, L. (1980). Species and sex-specific songs and

courtship behavior in the genus Zaprionus (Diptera, Drosophilidae). Anim. Behav. 28:230–255.

Blows, M. W., and Allan, R. A. (1998). Levels of mate recognition within and between theDrosophila species and their hybrids. Am. Nat. 152: 826–837.

Bock, I. R. (1976). Drosophilidae of Australia 1. Drosophila (Insecta: Diptera). AustralianJournal of Zoology Supplementary Series No. 40.

Bock, I. R. (1980). Current status of the Drosophila melanogaster species-group (Diptera). Syst.Entomol. 5: 341–356.

Crossley, S. A. (1986). Courtship sounds and behavior in the four species of the Drosophilabipectinata complex. Anim. Behav. 34: 1146–1159.

Dobzhansky, Th., and Mather, W. B. (1961). The evolutionary status of Drosophila serrata.Evolution 15: 461–467.

Downes, J. A. (1969). The swarming and mating flight in Diptera. Annu. Rev. Entomol. 14:271–298.

Eberhard, W. G. (1991). Copulatory courtship and cryptic female choice in insects. Biol. Rev.66: 1–31.

Ewing, A. W. (1983). Functional aspects of Drosophila courtship. Biol. Rev. 58: 275–292.Hoikkala, A., and Crossley, S. (n.d.). Copulatory courtship in Drosophila: Behavior and songs

of D. birchii and D. serrata. J. Insect Behav., in press.Hoikkala, A., Lakovaara, S., and Romppainen, E. (1982). Mating behavior and male courtship

sounds in the Drosophila virilis group. In: Lakovaara, S. (ed.), Advances in Genetics, De-velopment and Evolution of Drosophila, Plenum Press, New York, pp. 407–421.

Neems, R. M., Dooher, K., Butlin, R., and Shorrocks, B. (1997). Differences in male courtshipsong among the species of the quinaria group of Drosophila. J. Insect Behav. 10: 237–246.

Oguma, Y., Kurokawa, H., Akai, S. M., Tamaki, H., and Kajita, J. (1987). Interspecific differencesin some courtship behavioral properties among the four species belonging to the Drosophilaauraria complex. Zool. Sci. 4: 889–896.

Spieth, H. T. (1974). Courtship behavior in Drosophila. Annu. Rev. Entomol. 19: 385–405.Thornhill, R. (1983). Cryptic female choice and its implications in the scorpionfly Harpobittacus

nigriceps. Am. Nat. 122: 765–788.Tomaru, M., and Oguma, Y. (1994). Differences in courtship song in the species of the Drosophila

auraria complex. Anim. Behav. 47: 133–140.von Schilcher, F., and Dow, M. (1977). Courtship behavior in Drosophila: Sexual isolation or

sexual selection. Z. Tierpsychol. 43: 304–310.Wasserman, M. J., Heller, J., and Zombek, J. (1971). Male determined sexual discrimination in

the species Drosophila pegasa. Am. Midl. Nat. 86: 231–235.

copulatory courtship in drosophila birchii and d. serrata, species recognition and sexual selection

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