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Female preference for ‘song races’ of Ephippiger ephippiger (Orthoptera: Tettigoniidae)
Anon. Behav., 1991, 42, 518-520
Female preference for 'song races' of Ephippigerephippiger(Orthoptera: Tettigoniidae) M I C H A E L G. R I T C H I E * School of Biological Sciences, University of East Anglia, Norwich, Norfolk NR4 7TJ, U.K.
(Received 5 November 1990; initial acceptance 18 December 1990; final acceptance 25 January 1990; MS. number: sc-604)
Characters responsible for reproductive isolation between species are sometimes assumed to show little variation within a species (e.g. Paterson 1985; Ewing & Miyan 1986). Female bushcrickets find males by phonotaxis to song, therefore song can play an important role in speciation in these animals. It is produced by opening and closing movements of the tegmina. Over most of the western European range of Ephippiger ephippiger a single movement (syllable) is made per chirp. However, in the eastern Pyrenees and on the Mediterranean coast males produce polysyllabic chirps (Busnel 1963). This is a major difference in song structure (Fig. 1a) and is as great as the variation between some Ephippiger species. Duijm (1990) has shown this to occur independently of morphological variation upon which subspecies of this animal have been defined (e.g. Hartley & Warne 1984); therefore E. ephippiger from this region seems to be a single variable species, with that variation including aspects of male song. It is of interest to ask if the preferences of females also change. Busnel et al. (summarized in Dumortier 1963) carried out experiments that implied that females discriminated weakly, orienting to the 'wrong' songs in no-choice conditions, but more frequently towards their native song type when given a choice. However, aspects of these experiments are unsatisfactory, e.g, female experience was unknown and real males were used as models. These might vary in the regularity or volume with which they sing, which could influence phonotaxis. As part of a study of these 'song races', I have examined female preferences for extremes of the song types. The song models (Fig. l a) were tape loops made of four consecutive chirps each of a monosyllabic and a four-syllable male (collected at Montpellier, France and Baga, northeast Spain, respectively). Using a single model to represent each race can be criticized (Kroodsma 1989), but *Present address: Department of Genetics, University of Leicester, Leicester LE1 7RH, U.K. 0003 3472/91/090518+03503.00/0
the distributions of syllable number do not overlap, i.e. these monosyllabic races only produce monosyllabic song and males from these polysyllabic populations have a mean of four or five syllables per male, never producing monosyllabic song (personal observations of at least 50 males per race). It is therefore likely that the response of females to the models should approximate that to most males sampled from these populations. Recordings were made in a soundproofed room on a Nagra IVS recorder with A K G C451E microphone (CK8 capsule) at 38.1cm/s tape speed at 25~ The frequency profiles of the recorded songs are similar, but both will have lost some of their high frequency components during playback using the equipment available. This parameter affects female choice in tettigoniids (e.g. Latimer & Sippel 1987; Bailey et al. 1990), but higher frequencies are probably less important for Ephippiger phonotaxis (Busnel& Dumortier 1954, and see below). The dominant frequency of both songs (around 15 KHz) was reproduced faithfully. I used laboratory-reared virgin female offspring of the Montpellier (monosyllabic) population. Eleven were available for the main experiment. The first five were reared in an insectary containing singing males from their own population. All others were reared in acoustic isolation. Phonotaxis trials took place between 0900 and 1400 hours in a soundproofed room at 25 ___2~ the period of peak singing and mating activity. Playback was via a stereo amplifier with independent channel volume controls. Speakers were 1.5 m apart at a height of 0"75 m and in front of the speakers was a bamboo 'T' measuring 1.3 m across the top and 2"0 m along the approach pole, which rested on the ground. Females, placed onto the approach pole, walked up the apparatus, turning towards one of the speakers. A response was scored if she reached an arbitrary point two-thirds of the way to the speaker from the choice junction. After a trial the songs were switched
9 1991 The Association for the Study of Animal Behaviour 518
Short Communications (a)
Jmd~ ,It"Jtmr
b.2ss I-0 0.8 0.6
to
i
0.4 0.2
4s
Is
g
~'~':~ 0'60'81"0(c) 0.4 m 0.2
I
4s
/I Is
Song model
Figure 1. (a) Time-amplitude traces of a single chirp of each song model. Each syllable comprises a complete opening and closingmovement of the tegmina. (b) Overall proportion of responses to the monosyllabic (1 s) and four-syllable (4 s) song by six females reared in isolation. (c) As (b), but for fivefemalesreared in aural contact with males. See text for further details. between speakers and the test repeated. Four such trials were made with each female on one day and a result recorded only if all four were readily completed. No individual was tested on more than 4 days, giving a maximum of 16 responses per female (_~= 12). Unless otherwise stated, the volume of both models was 55 dB sound pressure level at the choice junction and equal over the apparatus (measured using a G R I F F I N sound level indicator [XER-430-V] on 'fast' setting). Of the 11 females, nine more often approached the monosyllabic song, one more often approached the four-syllable song and one approached both equally often. Thus females seem to display a fairly clear preference for their native song type (sign test: P = 0.011, Siegel 1956). Indeed, the two exceptions were amongst four females given only four individual trials. G-tests (Sokal & Rohlf 1981) were used to examine these preferences further. None of seven
519
females tested on more than one day showed significant day to day variation. Overall, there was significant heterogeneity amongst females (Gn=23"25, df= 10, P<0-01). Post hoc comparisons implied that one possible source of this variation may have been that the females reared in acoustic isolation discriminated between the song models more strongly than those reared in the presence of singing males. There was no heterogeneity amongst females within either group, and the proportion of responses females gave to the monosyllabic song were almost significantly different between the two groups despite small sample sizes (Mann-Whitney U-test: N=5,6, P=0-068). Figure lb,c compares the overall proportion of responses to each model (G = 11.50, df= 1, P < 0.001). Subsequently, a further four females became available for analysis. These were given different stimulus regimes on each of 5 days. Under no-choice conditions, the 'incorrect' four-syllable song caused phonotaxis, but in a non-directionalmanner (13 responses to the song, 19 to a silent speaker, binomial probability = 0-430, this regime being used twice). This did not happen when given the 'correct' monosyllabic song (16 responses to the song, none to the silent speaker, P < 0.001). When given monosyllabic song with a volume difference of 10 dB at the choice junction, females preferred the louder song (15 responses to 1, P < 0.001). Volume might therefore be expected to act against preference for song structure. However, these females showed a remarkable ability to track monosyllabic song when presented at 10 dB less than the four-syllable song (14 responses to 2, P--- 0.002). The variation in male song within this species is therefore matched by corresponding changes in female preference, at least to the extent that polysyllabic males would be discriminated against by females from the more common monosyllabic populations. These preferences seem relatively strong as they are expressed independently of volume preferences affecting choice within song types. This contrasts with conclusions in the literature (e.g. Walker 1957; Gwynne & Morris 1986) which are based on the work of Dumortier and colleagues. These conflicting results could be reconciled somewhat if the exposure effect suggested here is confirmed by further work. Note that further studies would also be required to confirm that syllable number is the character most responsible for discrimination as total chirp and syllable length covary. Given that my equipment will have
Animal Behaviour, 42, 3
520
attenuated the higher frequencies of the song, it seems unlikely that subtle differences in this will prove responsible. Changes in both male characters and female preferences imply these song races represent the evolution of potential premating isolation between different populations of E. ephippiger, though gene flow will currently be possible through a wide range of intermediate forms. N o sharp transitions between the song races have been found yet. Their evolution is therefore uncertain. Allopatric divergence followed by secondary contact would predict patches where several characters change, possibly linked by narrow hybrid zones (Hewitt 1988). An alternative possibility is differentiation in situ. Further studies of the origin and evolutionary significance of these song races should be rewarding. They contain much of interest to the study of behaviour and speciation. I thank Godfrey Hewitt, Matthijs Duijm, M a r k Beaumont, Winston J. Bailey, the School of Biological Sciences at U.E.A. and the Science and Engineering Research Council.
REFERENCES Bailey, W. J., Cunningham, R. J. & Lebel, L. 1990. Song power, spectral distribution and female phonotaxis in the bushcricket Requena verticalis (Tettigoniidae: Orthoptera): active female choice or passive attraction. Anita. Behav., 40, 33-42. Busnel, M.-C. 1963. Caract~risation acoustique de populations d'Ephippiger 6cologiquement voisines. Ann. Epiphyties, 14, 25-34.
Busnel, R. G. & Dumortier, B. 1954. Etude des caract+res du signal du sifflet de Galton provoquant la phonotaxie de la femelle d'Ephippiger bitterensis. C. r. s~anc. Soc. BioL, 148, 1751-1754. Duijm, M. 1990. On some song characteristics in Ephippiger (Orthoptera: Tettigoniidae) and their geographic variation. Neth. J. Zool., 40, 428-453. Dumortier, B. 1963. Ethological and physiological study of sound emissions in arthropoda. In: Acoustic Behaviour of Animals (Ed. by R.-G. Bushel), pp. 583 654. London: Elsevier. Ewing, A. W. & Miyan, J. A. 1986. Sexual selection, sexualisolation and the evolution of song in the Drosophila repleta group of species. Anon. Behav., 4, 421-429. Gwynne, D. T. & Morris, G. K. 1986. Heterospecific recognition and behavioral isolation in acoustic orthoptera (Insecta). Evol. Theor., 8, 33-38. Hartley, J. C. & Warne, A. C. 1984. Taxonomy of the Ephippiger ephippiger complex (ephippiger, cruciger and cunii) with special reference to the mechanics of copulation. Eos, 60, 43-54. Hewitt, G. M. 1988. Hybrid zones: natural laboratories for evolutionary studies. Trends Ecol. Evol., 3, 158-167. Kroodsma, D. E. 1989. Suggested experimental designs for song playbacks. Anita. Behav., 37, 600-609. Latimer, W. & Sippel, M. 1987. Acoustic cues for female choice and male competition in Tettigonia cantans. AnOn. Behav., 35, 887-900. Paterson, H. E. H. 1985. The recognition concept of species. In: Species andSpeciation (Ed. by S. Vrba), pp. 21-29. Pretoria: Transvaal Museum. Siegel, S. 1956. Nonparametric Statistics for the Behavioral Sciences. Tokyo: McGraw-Hill. Sokal, R. R. & Rohlf, F. J. 1981. Biometry. New York: W. H. Freeman and Co. Walker, T. J. 1957. Specificity in the response of female tree crickets (Orthoptera, Gryllidae, Oecanthidae) to calling songs of the males. Annls entomol. Soc. Am., 50, 626-636.
Female preference for 'song races' of Ephippigerephippiger(Orthoptera: Tettigoniidae) M I C H A E L G. R I T C H I E * School of Biological Sciences, University of East Anglia, Norwich, Norfolk NR4 7TJ, U.K.
(Received 5 November 1990; initial acceptance 18 December 1990; final acceptance 25 January 1990; MS. number: sc-604)
Characters responsible for reproductive isolation between species are sometimes assumed to show little variation within a species (e.g. Paterson 1985; Ewing & Miyan 1986). Female bushcrickets find males by phonotaxis to song, therefore song can play an important role in speciation in these animals. It is produced by opening and closing movements of the tegmina. Over most of the western European range of Ephippiger ephippiger a single movement (syllable) is made per chirp. However, in the eastern Pyrenees and on the Mediterranean coast males produce polysyllabic chirps (Busnel 1963). This is a major difference in song structure (Fig. 1a) and is as great as the variation between some Ephippiger species. Duijm (1990) has shown this to occur independently of morphological variation upon which subspecies of this animal have been defined (e.g. Hartley & Warne 1984); therefore E. ephippiger from this region seems to be a single variable species, with that variation including aspects of male song. It is of interest to ask if the preferences of females also change. Busnel et al. (summarized in Dumortier 1963) carried out experiments that implied that females discriminated weakly, orienting to the 'wrong' songs in no-choice conditions, but more frequently towards their native song type when given a choice. However, aspects of these experiments are unsatisfactory, e.g, female experience was unknown and real males were used as models. These might vary in the regularity or volume with which they sing, which could influence phonotaxis. As part of a study of these 'song races', I have examined female preferences for extremes of the song types. The song models (Fig. l a) were tape loops made of four consecutive chirps each of a monosyllabic and a four-syllable male (collected at Montpellier, France and Baga, northeast Spain, respectively). Using a single model to represent each race can be criticized (Kroodsma 1989), but *Present address: Department of Genetics, University of Leicester, Leicester LE1 7RH, U.K. 0003 3472/91/090518+03503.00/0
the distributions of syllable number do not overlap, i.e. these monosyllabic races only produce monosyllabic song and males from these polysyllabic populations have a mean of four or five syllables per male, never producing monosyllabic song (personal observations of at least 50 males per race). It is therefore likely that the response of females to the models should approximate that to most males sampled from these populations. Recordings were made in a soundproofed room on a Nagra IVS recorder with A K G C451E microphone (CK8 capsule) at 38.1cm/s tape speed at 25~ The frequency profiles of the recorded songs are similar, but both will have lost some of their high frequency components during playback using the equipment available. This parameter affects female choice in tettigoniids (e.g. Latimer & Sippel 1987; Bailey et al. 1990), but higher frequencies are probably less important for Ephippiger phonotaxis (Busnel& Dumortier 1954, and see below). The dominant frequency of both songs (around 15 KHz) was reproduced faithfully. I used laboratory-reared virgin female offspring of the Montpellier (monosyllabic) population. Eleven were available for the main experiment. The first five were reared in an insectary containing singing males from their own population. All others were reared in acoustic isolation. Phonotaxis trials took place between 0900 and 1400 hours in a soundproofed room at 25 ___2~ the period of peak singing and mating activity. Playback was via a stereo amplifier with independent channel volume controls. Speakers were 1.5 m apart at a height of 0"75 m and in front of the speakers was a bamboo 'T' measuring 1.3 m across the top and 2"0 m along the approach pole, which rested on the ground. Females, placed onto the approach pole, walked up the apparatus, turning towards one of the speakers. A response was scored if she reached an arbitrary point two-thirds of the way to the speaker from the choice junction. After a trial the songs were switched
9 1991 The Association for the Study of Animal Behaviour 518
Short Communications (a)
Jmd~ ,It"Jtmr
b.2ss I-0 0.8 0.6
to
i
0.4 0.2
4s
Is
g
~'~':~ 0'60'81"0(c) 0.4 m 0.2
I
4s
/I Is
Song model
Figure 1. (a) Time-amplitude traces of a single chirp of each song model. Each syllable comprises a complete opening and closingmovement of the tegmina. (b) Overall proportion of responses to the monosyllabic (1 s) and four-syllable (4 s) song by six females reared in isolation. (c) As (b), but for fivefemalesreared in aural contact with males. See text for further details. between speakers and the test repeated. Four such trials were made with each female on one day and a result recorded only if all four were readily completed. No individual was tested on more than 4 days, giving a maximum of 16 responses per female (_~= 12). Unless otherwise stated, the volume of both models was 55 dB sound pressure level at the choice junction and equal over the apparatus (measured using a G R I F F I N sound level indicator [XER-430-V] on 'fast' setting). Of the 11 females, nine more often approached the monosyllabic song, one more often approached the four-syllable song and one approached both equally often. Thus females seem to display a fairly clear preference for their native song type (sign test: P = 0.011, Siegel 1956). Indeed, the two exceptions were amongst four females given only four individual trials. G-tests (Sokal & Rohlf 1981) were used to examine these preferences further. None of seven
519
females tested on more than one day showed significant day to day variation. Overall, there was significant heterogeneity amongst females (Gn=23"25, df= 10, P<0-01). Post hoc comparisons implied that one possible source of this variation may have been that the females reared in acoustic isolation discriminated between the song models more strongly than those reared in the presence of singing males. There was no heterogeneity amongst females within either group, and the proportion of responses females gave to the monosyllabic song were almost significantly different between the two groups despite small sample sizes (Mann-Whitney U-test: N=5,6, P=0-068). Figure lb,c compares the overall proportion of responses to each model (G = 11.50, df= 1, P < 0.001). Subsequently, a further four females became available for analysis. These were given different stimulus regimes on each of 5 days. Under no-choice conditions, the 'incorrect' four-syllable song caused phonotaxis, but in a non-directionalmanner (13 responses to the song, 19 to a silent speaker, binomial probability = 0-430, this regime being used twice). This did not happen when given the 'correct' monosyllabic song (16 responses to the song, none to the silent speaker, P < 0.001). When given monosyllabic song with a volume difference of 10 dB at the choice junction, females preferred the louder song (15 responses to 1, P < 0.001). Volume might therefore be expected to act against preference for song structure. However, these females showed a remarkable ability to track monosyllabic song when presented at 10 dB less than the four-syllable song (14 responses to 2, P--- 0.002). The variation in male song within this species is therefore matched by corresponding changes in female preference, at least to the extent that polysyllabic males would be discriminated against by females from the more common monosyllabic populations. These preferences seem relatively strong as they are expressed independently of volume preferences affecting choice within song types. This contrasts with conclusions in the literature (e.g. Walker 1957; Gwynne & Morris 1986) which are based on the work of Dumortier and colleagues. These conflicting results could be reconciled somewhat if the exposure effect suggested here is confirmed by further work. Note that further studies would also be required to confirm that syllable number is the character most responsible for discrimination as total chirp and syllable length covary. Given that my equipment will have
Animal Behaviour, 42, 3
520
attenuated the higher frequencies of the song, it seems unlikely that subtle differences in this will prove responsible. Changes in both male characters and female preferences imply these song races represent the evolution of potential premating isolation between different populations of E. ephippiger, though gene flow will currently be possible through a wide range of intermediate forms. N o sharp transitions between the song races have been found yet. Their evolution is therefore uncertain. Allopatric divergence followed by secondary contact would predict patches where several characters change, possibly linked by narrow hybrid zones (Hewitt 1988). An alternative possibility is differentiation in situ. Further studies of the origin and evolutionary significance of these song races should be rewarding. They contain much of interest to the study of behaviour and speciation. I thank Godfrey Hewitt, Matthijs Duijm, M a r k Beaumont, Winston J. Bailey, the School of Biological Sciences at U.E.A. and the Science and Engineering Research Council.
REFERENCES Bailey, W. J., Cunningham, R. J. & Lebel, L. 1990. Song power, spectral distribution and female phonotaxis in the bushcricket Requena verticalis (Tettigoniidae: Orthoptera): active female choice or passive attraction. Anita. Behav., 40, 33-42. Busnel, M.-C. 1963. Caract~risation acoustique de populations d'Ephippiger 6cologiquement voisines. Ann. Epiphyties, 14, 25-34.
Busnel, R. G. & Dumortier, B. 1954. Etude des caract+res du signal du sifflet de Galton provoquant la phonotaxie de la femelle d'Ephippiger bitterensis. C. r. s~anc. Soc. BioL, 148, 1751-1754. Duijm, M. 1990. On some song characteristics in Ephippiger (Orthoptera: Tettigoniidae) and their geographic variation. Neth. J. Zool., 40, 428-453. Dumortier, B. 1963. Ethological and physiological study of sound emissions in arthropoda. In: Acoustic Behaviour of Animals (Ed. by R.-G. Bushel), pp. 583 654. London: Elsevier. Ewing, A. W. & Miyan, J. A. 1986. Sexual selection, sexualisolation and the evolution of song in the Drosophila repleta group of species. Anon. Behav., 4, 421-429. Gwynne, D. T. & Morris, G. K. 1986. Heterospecific recognition and behavioral isolation in acoustic orthoptera (Insecta). Evol. Theor., 8, 33-38. Hartley, J. C. & Warne, A. C. 1984. Taxonomy of the Ephippiger ephippiger complex (ephippiger, cruciger and cunii) with special reference to the mechanics of copulation. Eos, 60, 43-54. Hewitt, G. M. 1988. Hybrid zones: natural laboratories for evolutionary studies. Trends Ecol. Evol., 3, 158-167. Kroodsma, D. E. 1989. Suggested experimental designs for song playbacks. Anita. Behav., 37, 600-609. Latimer, W. & Sippel, M. 1987. Acoustic cues for female choice and male competition in Tettigonia cantans. AnOn. Behav., 35, 887-900. Paterson, H. E. H. 1985. The recognition concept of species. In: Species andSpeciation (Ed. by S. Vrba), pp. 21-29. Pretoria: Transvaal Museum. Siegel, S. 1956. Nonparametric Statistics for the Behavioral Sciences. Tokyo: McGraw-Hill. Sokal, R. R. & Rohlf, F. J. 1981. Biometry. New York: W. H. Freeman and Co. Walker, T. J. 1957. Specificity in the response of female tree crickets (Orthoptera, Gryllidae, Oecanthidae) to calling songs of the males. Annls entomol. Soc. Am., 50, 626-636.