- Email: [email protected]
Quantitative genetics of multiple mating
406
References
Animal Behaviour, 40, 2
Quantitative Genetics of Multiple Mating
Multiple mating is widespread among animals. Brower, J. vZ. 1958a. Experimental studies of mimicry in Although it is clearly adaptive for males to insemisome North American butterflies. Part I. The monarch, nate several females, HaUiday & Arnold (1987) arDanaus plexippus, and the viceroy, Limenitis archippus gued that often there are no benefits to females who archippus. Evolution, 12, 32-47. mate multiply with different males. They proposed Brower, J. vZ. 1958b. Experimental studies of mimicry that female mating tendency may have evolved as a in some North American butterflies. Part II. Battus philenor and Papilio troilus, P. polyxenes and P. correlated genetic response to sexual selection for high mating frequencies in males. Their hypothesis glaucus. Evolution, 12, 123-136. Brower, L. P., Alcock, J. & Brower, J. vZ. 1971. Avian assumes that 'selection on mating frequency is feeding behaviour and the selective advantage of stronger in males than in females', and requires 'a incipient mimicry. In: Ecological Genetics and Evolution common, polygenic basis for mating propensity in (Ed. by E. R. Creed), pp. 261-274. Oxford: Blackwell males and females' such that 'many mutations will Scientific. have similar effects in the two sexes' (page 940). Chai, P. 1988. Wing coloration of free-flying neotropical Thus, selection on males to mate frequently is butterflies as a signal learned by a specialized avian hypothesized to drag females into copulating repredator. Biotropica, 20, 20-30. peatedly, even if multiple mating confers no benefits Codella, S. G. & Lederhouse, R. C. 1989. Inter- on females. Subsequently, Sherman & Westneat sexual comparison of mimetic protection in the black (1988) presented comparative data from various swallowtail butterfly, Papilio polyxenes: experiments with captive blue jay predators. Evolution, 43, groups of vertebrates, notably birds, to demonstrate the lack of correlation between males and females 410420. Darwin, C. 1874. The Descent of Man and Selection in in the variance in mating frequency. They also pointed out that another explanation offered by Relation to Sex. 2nd edn. London: Murray. Eltringham, H. 1916. On specific and mimetic relation- Halliday & Arnold (1987), that mechanisms underships in the genus Heliconius. Trans. R. entomol. Soc. lying mating propensity and mate choice have a Lond., 1916, 101-155. common genetic basis, was also unlikely. Sherman Gittleman, J. L., Harvey, P. H. & Greenwood, & Westneat (1988) concluded that Halliday & P. J. 1980. The evolution of conspicuous coloration: Arnold's (1987) hypothesis may not hold as a some experiments in bad taste. Anim. Behav., 28, general explanation for multiple mating by females. 897-899. In response to such criticism, Arnold & Halliday Guilford, T. 1988. The evolution of conspicuous (1988) stressed that the most critical tests for their coloration. Am. Nat. Suppl., 131, 7-21. hypothesis will have to come from studies of quanHarvey, P. H., Bull, J. J., Pemberton, M. & Paxton, R. J. 1982. The evolution of aposematic coloration in titative genetics. We submit that Halliday & distasteful prey: a family model. Am. Nat., 119, Arnold (1987) overlooked data from quantitative genetics studies, and that such data, obtained the 710-719. Johnson, J. A. & Brodie, E. D., Jr. 1975. The selective way that they stated, do not support the crucial advantage of the defensive posture of the newt, Tarieha assumption of their hypothesis, namely that mating granulosa. Am. Midl. Nat., 93, 139-148. propensities in males and females are homologous. Lederhouse, R. C., Codella, S. G. & Cowell, P. J. 1987. Divergent selection for high and low frequency Diurnal predation on roosting butterflies during in- of mating in male domestic chickens, Gallus clement weather: a substantial source of mortality domesticus, over many generations (Cook et al. in the black swallowtail, Papilio polyxenes. Jl N. Y. 1972; Cook & Siegel 1974; Dunnington & Siegel entomoL Soc., 95, 310-319. 1983) resulted in a steady increase in male mating Opler, P. A. & Krizek, G. O. 1984. Butterflies East of the frequency in the high line until generation 20, when Great Plains: an Illustrated Natural History. Baltimore, a plateau in response seemed to have occurred. ConMaryland: Johns Hopkins University Press. Silberglied, R. E. 1984. Visual communication and versely, selection for low mating frequency in males sexual selection among butterflies. In: The Biology of caused many males to pass a threshold below which Butterflies (Ed. by R. I. Vane-Wright & P. R. Ackery), they would not mate naturally (Dunnington & Siegel 1983). Siegel & Cook (1975) and Dunnington pp. 207-224. London: Academic Press. Wourms, M. K. & Wasserman, F. E. 1985. Bird predation & Siegel (1983) tested the mating responses of on Lepidoptera and the reliability of beak marks females in these lines from generations 12 to 14, and in determining predation pressure. J. Lepid. Soc., 39, generations 16 to 23, respectively, and found that 239 261. the changes in male mating frequency were not accompanied by changes in female mating frequency. Their results suggest that there is no pheno(Received 10 October 1989; initial decision typic nor genotypic correlation between male 28 November 1989;final acceptance 6 March 1990; MS. number: as-668) mating frequency and female mating frequency.
Short Communications Although selection causing changes in mating frequency in male chickens also caused changes in other male reproductive traits such as age at sexual maturity, no differences were found among lines in female age at sexual maturity, egg production or egg weights (Cook & Siegel 1972). These results further suggest that selection for high male mating frequency has no genetic effect on female reproductive traits in general. Dunnington & Siegel (1983) observed that males in the high line not only made more mating attempts, but also mated more often because they were more successful in eliciting a crouching response (receptive posture) from females (regardless of the female's genotypic background). Males from the high line were also more likely to mount the females regardless of whether the females were receptive. In rare situations where 'female mating tendency was selectively neutral' (Halliday & Arnold 1987), an increase in female mating activities could simply be a behavioural but not necessarily a genetical response to the increased activities of the males. Halliday & Arnold (1987) and Arnold & Halliday (1988) cited Manning's (1963) Drosophila experiment in support of their hypothesis. However, they failed to mention Manning's (1963) conclusion that the response by male flies to selection for male mating speed was probably affected by genes that were sex-limited in their expression. Correlated changes in female mating speed were due to differences in general activity levels, perhaps the result of inbreeding and intense selection. In natural populations, selection pressure on male mating frequencies that is so consistent and intense (such as that imposed by Manning on his flies under laboratory conditions) as to cause a significant change in general activities may not be common. Halliday & Arnold (1987) also mentioned that mechanisms underlying mating propensity and mate choice may have a common genetic basis. Divergent selection for high and low male mating frequency in Japanese quail, Coturnixjaponica, for 29 generations also resulted in changes in male mating frequency but did not alter their mate preference (Blohowiak & Siegel 1983, 1985a, b). Arnold & Halliday (1988) called for more selection experiments to test their hypothesis. In the few experiments of this type of which we are aware, the results do not support a correlated genetic response. Indeed, as Sherman & Westneat (1988) argued, such a correlation seems unlikely.
407
We thank Paul Sherman, Erica Nol, Frank McKinney and David Westneat for comments on the manuscript. KIMBERLYM. CHENG* PAUL B. SIEGEL? *Avian Genetics Laboratory, Department o f Animal Science, University o f British Columbia, Vancouver, British Columbia, V6T 2A2, Canada. ?Department o f Poultry Science, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, U.S.A.
References
Arnold, S. J. & Halliday, T. 1988. Multiple mating: natural selection is not evolution. Anim. Behav., 36, 1547-1548. Blohowiak, C. C. & Siegel, P. B. 1983. Long term selection for mating frequency in male Japanese quail. Z. Tierzucht. Ziieht Biol., 100, 338-349. Blohowiak, C. C. & Siegel, P. B. 1985a. Mate choice by males from lines of Japanese quail selected for male mating frequency. 1. Preferences among lines. Biol. Behav., 10, 87-95. Blohowiak, C. C. & Siegel, P. B. 1985b. Mate choice by males from lines of Japanese quail selected for male mating frequency. 2. Preferences among plumage colors. Biol. Behav., 10, 97-103. Cook, W. T. & Siegel, P. B. 1974. Social variables and divergent selection for mating behaviour of male chickens Gallus domesticus. Anim. Behav., 22, 390-396. Cook, W. T., Siegel, P. B. & Hinkelmann, K. 1972. Genetic analyses of male mating behavior in chickens. 2. Crosses among selected and control lines. Behav. Genet., 2, 289-300. Dunnington, E. A. & Siegel,P. B. 1983.Mating frequency in male chickens: long term selection. Theor. appl. Genet., 64, 317-323. Halliday, T. & Arnold, S. J. 1987. Multiple mating by females: a perspective from quantitative genetics. Anim. Behav., 35, 939-941. Manning, A. 1963. Selection for mating speed in Drosophila melanogaster based on the behaviour of one sex. Anita. Behav., 11, 116-120. Sherman, P. W. & Westneat, D. F. 1988.Multiple mating and quantitative genetics.Anita. Behav., 36, 1545-1547. Siegel,P. B. 1972.Genetic analyses of male mating behaviour in chickens. 1. Artificial selection. Anim. Behav., 20, 564-570. Siegel, P. B. & Cook, W. T. 1975. Sexual responses of pullets to selection for mating behaviour in male chickens. Appl. Anita. Ethol., I, 225528.
(Received 10 October 1989; initial acceptance 7 November 1989;final acceptance 18 December 1989; MS. number: AS-623)
References
Animal Behaviour, 40, 2
Quantitative Genetics of Multiple Mating
Multiple mating is widespread among animals. Brower, J. vZ. 1958a. Experimental studies of mimicry in Although it is clearly adaptive for males to insemisome North American butterflies. Part I. The monarch, nate several females, HaUiday & Arnold (1987) arDanaus plexippus, and the viceroy, Limenitis archippus gued that often there are no benefits to females who archippus. Evolution, 12, 32-47. mate multiply with different males. They proposed Brower, J. vZ. 1958b. Experimental studies of mimicry that female mating tendency may have evolved as a in some North American butterflies. Part II. Battus philenor and Papilio troilus, P. polyxenes and P. correlated genetic response to sexual selection for high mating frequencies in males. Their hypothesis glaucus. Evolution, 12, 123-136. Brower, L. P., Alcock, J. & Brower, J. vZ. 1971. Avian assumes that 'selection on mating frequency is feeding behaviour and the selective advantage of stronger in males than in females', and requires 'a incipient mimicry. In: Ecological Genetics and Evolution common, polygenic basis for mating propensity in (Ed. by E. R. Creed), pp. 261-274. Oxford: Blackwell males and females' such that 'many mutations will Scientific. have similar effects in the two sexes' (page 940). Chai, P. 1988. Wing coloration of free-flying neotropical Thus, selection on males to mate frequently is butterflies as a signal learned by a specialized avian hypothesized to drag females into copulating repredator. Biotropica, 20, 20-30. peatedly, even if multiple mating confers no benefits Codella, S. G. & Lederhouse, R. C. 1989. Inter- on females. Subsequently, Sherman & Westneat sexual comparison of mimetic protection in the black (1988) presented comparative data from various swallowtail butterfly, Papilio polyxenes: experiments with captive blue jay predators. Evolution, 43, groups of vertebrates, notably birds, to demonstrate the lack of correlation between males and females 410420. Darwin, C. 1874. The Descent of Man and Selection in in the variance in mating frequency. They also pointed out that another explanation offered by Relation to Sex. 2nd edn. London: Murray. Eltringham, H. 1916. On specific and mimetic relation- Halliday & Arnold (1987), that mechanisms underships in the genus Heliconius. Trans. R. entomol. Soc. lying mating propensity and mate choice have a Lond., 1916, 101-155. common genetic basis, was also unlikely. Sherman Gittleman, J. L., Harvey, P. H. & Greenwood, & Westneat (1988) concluded that Halliday & P. J. 1980. The evolution of conspicuous coloration: Arnold's (1987) hypothesis may not hold as a some experiments in bad taste. Anim. Behav., 28, general explanation for multiple mating by females. 897-899. In response to such criticism, Arnold & Halliday Guilford, T. 1988. The evolution of conspicuous (1988) stressed that the most critical tests for their coloration. Am. Nat. Suppl., 131, 7-21. hypothesis will have to come from studies of quanHarvey, P. H., Bull, J. J., Pemberton, M. & Paxton, R. J. 1982. The evolution of aposematic coloration in titative genetics. We submit that Halliday & distasteful prey: a family model. Am. Nat., 119, Arnold (1987) overlooked data from quantitative genetics studies, and that such data, obtained the 710-719. Johnson, J. A. & Brodie, E. D., Jr. 1975. The selective way that they stated, do not support the crucial advantage of the defensive posture of the newt, Tarieha assumption of their hypothesis, namely that mating granulosa. Am. Midl. Nat., 93, 139-148. propensities in males and females are homologous. Lederhouse, R. C., Codella, S. G. & Cowell, P. J. 1987. Divergent selection for high and low frequency Diurnal predation on roosting butterflies during in- of mating in male domestic chickens, Gallus clement weather: a substantial source of mortality domesticus, over many generations (Cook et al. in the black swallowtail, Papilio polyxenes. Jl N. Y. 1972; Cook & Siegel 1974; Dunnington & Siegel entomoL Soc., 95, 310-319. 1983) resulted in a steady increase in male mating Opler, P. A. & Krizek, G. O. 1984. Butterflies East of the frequency in the high line until generation 20, when Great Plains: an Illustrated Natural History. Baltimore, a plateau in response seemed to have occurred. ConMaryland: Johns Hopkins University Press. Silberglied, R. E. 1984. Visual communication and versely, selection for low mating frequency in males sexual selection among butterflies. In: The Biology of caused many males to pass a threshold below which Butterflies (Ed. by R. I. Vane-Wright & P. R. Ackery), they would not mate naturally (Dunnington & Siegel 1983). Siegel & Cook (1975) and Dunnington pp. 207-224. London: Academic Press. Wourms, M. K. & Wasserman, F. E. 1985. Bird predation & Siegel (1983) tested the mating responses of on Lepidoptera and the reliability of beak marks females in these lines from generations 12 to 14, and in determining predation pressure. J. Lepid. Soc., 39, generations 16 to 23, respectively, and found that 239 261. the changes in male mating frequency were not accompanied by changes in female mating frequency. Their results suggest that there is no pheno(Received 10 October 1989; initial decision typic nor genotypic correlation between male 28 November 1989;final acceptance 6 March 1990; MS. number: as-668) mating frequency and female mating frequency.
Short Communications Although selection causing changes in mating frequency in male chickens also caused changes in other male reproductive traits such as age at sexual maturity, no differences were found among lines in female age at sexual maturity, egg production or egg weights (Cook & Siegel 1972). These results further suggest that selection for high male mating frequency has no genetic effect on female reproductive traits in general. Dunnington & Siegel (1983) observed that males in the high line not only made more mating attempts, but also mated more often because they were more successful in eliciting a crouching response (receptive posture) from females (regardless of the female's genotypic background). Males from the high line were also more likely to mount the females regardless of whether the females were receptive. In rare situations where 'female mating tendency was selectively neutral' (Halliday & Arnold 1987), an increase in female mating activities could simply be a behavioural but not necessarily a genetical response to the increased activities of the males. Halliday & Arnold (1987) and Arnold & Halliday (1988) cited Manning's (1963) Drosophila experiment in support of their hypothesis. However, they failed to mention Manning's (1963) conclusion that the response by male flies to selection for male mating speed was probably affected by genes that were sex-limited in their expression. Correlated changes in female mating speed were due to differences in general activity levels, perhaps the result of inbreeding and intense selection. In natural populations, selection pressure on male mating frequencies that is so consistent and intense (such as that imposed by Manning on his flies under laboratory conditions) as to cause a significant change in general activities may not be common. Halliday & Arnold (1987) also mentioned that mechanisms underlying mating propensity and mate choice may have a common genetic basis. Divergent selection for high and low male mating frequency in Japanese quail, Coturnixjaponica, for 29 generations also resulted in changes in male mating frequency but did not alter their mate preference (Blohowiak & Siegel 1983, 1985a, b). Arnold & Halliday (1988) called for more selection experiments to test their hypothesis. In the few experiments of this type of which we are aware, the results do not support a correlated genetic response. Indeed, as Sherman & Westneat (1988) argued, such a correlation seems unlikely.
407
We thank Paul Sherman, Erica Nol, Frank McKinney and David Westneat for comments on the manuscript. KIMBERLYM. CHENG* PAUL B. SIEGEL? *Avian Genetics Laboratory, Department o f Animal Science, University o f British Columbia, Vancouver, British Columbia, V6T 2A2, Canada. ?Department o f Poultry Science, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, U.S.A.
References
Arnold, S. J. & Halliday, T. 1988. Multiple mating: natural selection is not evolution. Anim. Behav., 36, 1547-1548. Blohowiak, C. C. & Siegel, P. B. 1983. Long term selection for mating frequency in male Japanese quail. Z. Tierzucht. Ziieht Biol., 100, 338-349. Blohowiak, C. C. & Siegel, P. B. 1985a. Mate choice by males from lines of Japanese quail selected for male mating frequency. 1. Preferences among lines. Biol. Behav., 10, 87-95. Blohowiak, C. C. & Siegel, P. B. 1985b. Mate choice by males from lines of Japanese quail selected for male mating frequency. 2. Preferences among plumage colors. Biol. Behav., 10, 97-103. Cook, W. T. & Siegel, P. B. 1974. Social variables and divergent selection for mating behaviour of male chickens Gallus domesticus. Anim. Behav., 22, 390-396. Cook, W. T., Siegel, P. B. & Hinkelmann, K. 1972. Genetic analyses of male mating behavior in chickens. 2. Crosses among selected and control lines. Behav. Genet., 2, 289-300. Dunnington, E. A. & Siegel,P. B. 1983.Mating frequency in male chickens: long term selection. Theor. appl. Genet., 64, 317-323. Halliday, T. & Arnold, S. J. 1987. Multiple mating by females: a perspective from quantitative genetics. Anim. Behav., 35, 939-941. Manning, A. 1963. Selection for mating speed in Drosophila melanogaster based on the behaviour of one sex. Anita. Behav., 11, 116-120. Sherman, P. W. & Westneat, D. F. 1988.Multiple mating and quantitative genetics.Anita. Behav., 36, 1545-1547. Siegel,P. B. 1972.Genetic analyses of male mating behaviour in chickens. 1. Artificial selection. Anim. Behav., 20, 564-570. Siegel, P. B. & Cook, W. T. 1975. Sexual responses of pullets to selection for mating behaviour in male chickens. Appl. Anita. Ethol., I, 225528.
(Received 10 October 1989; initial acceptance 7 November 1989;final acceptance 18 December 1989; MS. number: AS-623)