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Female choice and genetic correlations
CORRESPONDENCE
Female choice and genetic correlations Pomiankowski and Sheridan assert in their TREE article1 that recent studies of guppies, sticklebacks and stalk-eyed flies provide compelling evidence for strong genetic correlations between male ornamentation and female preferences for such traits. Such covariance is a critical assumption of indirect models for the evolution of female preference. We agree that such correlations are likely to arise from assortative mating and that good-genes models of female preference are plausible. However, the studies discussed by Pomiankowski and Sheridan, as well as other studies, do not, in our opinion, constitute unequivocal evidence for strong genetic correlations arising from linkage disequilibria. The two selection experiments in guppies provrde little evidence for a correlation between attractive male coloration and female preference for this coloration. Houde’s study2 showed a correlated response in female preference for orange coloration, following selection on orange coloration tn males in only two of four replicates. This highlights an important weakness inherent in selection experiments: each selected line, although representing a considerable amount of effort, represents only one independent datum. Additionally, the significant response in the two replicates was not present after the third generation of selection. In Breden and Hornaday’s study3. four replicates selected for either high or low overall male coloration showed no correlated change in female preference for overall coloration. Pomrankowski and Sheridan1 correctly point out that the breeding design of this study limrts its power to detect a genetic correlation arising from assortative mating: however, they also argue that the lack of the correlation could be real given the ecology of the stock population. Moreover, the two positive results in Houde’s experiments also could have been generated by uncontrolled assortative mating leading to unintended selection as discussed by Butlir?, who also cites other failures to demonstrate genetic correlations in experiments in which mating patterns were properly controlled. Bakker’s study5 on sticklebacks found a strong correlation between male Intensity of red and female preference. However, the study examined only six independent familres, and Bakker5 himself suggested the possibility that the strong correlation arose from recent mixing of genetically differentiated populations. Wilkinson and Reillo’s study6 of stalk-eyed flies showed that females from the short (S) line preferred short males, but preferences of females from the long (L) line were no different than those of unselected females. The latter result IS puzzling because Wilkinson7 demonstrated strong symmetrical responses to bi-directional selection in the male trait. Selection in the L line should have generated at least some exaggeration of the preference for long males If there was a strong correlation between the preference and the male trait. Another study, not cited by Pomiankowski and SheridanI, had equivocal results. In the planthopper Ribautodelphis imjtans, females produce a vibratory courtship signal to which males respond. De Winter+ found a very strong
effect of selection on interpulse interval in the signals of females, and there was evidence for between-line assortative mating. However, males did not prefer interpulse intervals in simulated calls that were typical of the females in the same coselected line, suggesting that other factors contributed to assortative mating instead of, or in addition to, the selected trait. In summary, studies of only two species, sticklebacks and flies, have demonstrated genetic correlations, and the correlation in sticklebacks could have resulted from mixing genetically dissimilar populations. Results from guppies and planthoppers provide only weak evidence for genetic correlations arising from linkage disequilibria. We think it is premature to draw the general conclusion that such correlations, which have been the subject of much debate, are widespread and well-documented. Additional studies, including attempts to estimate the magnitudes of genetic correlations, are badly needed, especially if runaway models of indirect selection are to be tested.
Felix Breden Dept of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A lS6 H. Carl Gerhardt Division of Biological Sciences, University of Missouri, Columbia, MO 65211, USA Roger K. Butlin Dept of Genetics, University Leeds, UK LS2 9JT
of Leeds,
References 1 Pomiankowski, A. and Sheridan, L. (1994) Trends Ecol Eva/. 9, 241-244 2 Houde, A. Proc. R. Sot. London Ser. 6 (in press) 3 Breden, F. and Hornaday, K. Heredity(in press) 4 Butlin, R.K. (1993) Anim. Behav. 45403-404 5 Bakker, T.C.M. (1993) Nature 363, 255-257 6 Wilkinson, G.S. and Reillo, P.R. (1994) Proc. R. Sot. London Ser. B 255,1-6 7 Wilkinson, G.S. (1993) Genet. Res. 62,213-222 8 De Winter, A.J. (1992) J. Evol. Biol. 5, 249-265
Reply from A. Pomiankowski and L. Sheridan Biologists have finally got around to accepting that females choose their mates. But given half a chance many still deny that preferences have evolved, are adaptive, or are genetically variable. Breden et a/. extend this pessimistic view to recent experimental work documenting genetic correlations between mating preference and sexual ornamentation. Though there is always room for scepticism, the criticisms raised do not amount to much and can be answered easily. Overall there is strong evidence for genetic
correlations, which are most likely created by nonrandom mating. Breden et al. raise doubts about all three studies mentioned in our TREENews & Commentl. The main criticism of Houde’sz experiment selecting for orange area in guppies is that only two of four selection lines showed a correlated response in female preference. This is picking at one statistic and ignoring the rest. Overall there was stronger female preference in high lines in seven out of seven tests (first generation) and seven out of eight tests (second generation). This pattern IS inconsistent with expectations of random genetic drift. There was no difference between high and low lines in the third generation suggesting that the genetic correlations are caused by linkage disequilibrium: a 50% reduction in linkage disequilibrium is expected per generation for unlinked genes. A further point-that ‘assortative mating’ was not controlled in Houde’s study - is no criticism at all. This is the supposed mechanism for the generation of genetic correlations. The case for guppies stands. Wilkinson and Reillo’s similar experiment3 on stalk-eyed flies is attacked because preference rn the long line did not differ from the unselected control. This again is a remark out of context. The central result is that selection influenced female mate choice. Wilkinson and Reillo discuss a number of reasons for the lack of a detectable difference between control and long lines. The most likely explanation is that the experimental assessment of preference was too insensitive. There is no reason to suppose a genetic correlation does not exist. The case for stalk-eyed flies stands. Breden et al. also cast doubt on genetic correlations found in sticklebacks4 and claim these are because of ‘recent mixing of genetically distinct stocks’. In fact, the last recorded ‘recent mixrng’ occurred in 1872, over 120 years ago. Why should genetic correlatrons be maintained over such an extended period? Maybe there have been subsequent unrecorded introductions. But what is the value of such a vague and unsubstantiated possibility. Could it even in principle explain the large genetic correlation observed? The case for sticklebacks stands. Finally, Breden et al. suggest we missed out other studies with more equivocal results. But they only cite one other study and there are many more. Most show evidence for genetic correlatrons and we are currently preparing a review. It is time to wake up to the facts. The general case for genetic correlatrons between mating preference and sexual ornamentation stands.
Andrew Pomiankowski Letitia Sheridan Dept of Genetics and Biometry, University College London, 4 Stephenson Way, London, UK NW1 2HE References 1 Pomiankowski. A. and Sheridan..” L. (1994) Trends Ecol. Evol. 9, 242-244 2 Houde, A.E. Proc. R. Sot. London Ser. B(in press) 3 WIlkInson, G.S. and Reillo. P.R. (1994) Proc. R. Sot. London Ser. B 255, I-6 4 Bakker. T.C.M. (1993) Nature 363, 255-257
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Female choice and genetic correlations Pomiankowski and Sheridan assert in their TREE article1 that recent studies of guppies, sticklebacks and stalk-eyed flies provide compelling evidence for strong genetic correlations between male ornamentation and female preferences for such traits. Such covariance is a critical assumption of indirect models for the evolution of female preference. We agree that such correlations are likely to arise from assortative mating and that good-genes models of female preference are plausible. However, the studies discussed by Pomiankowski and Sheridan, as well as other studies, do not, in our opinion, constitute unequivocal evidence for strong genetic correlations arising from linkage disequilibria. The two selection experiments in guppies provrde little evidence for a correlation between attractive male coloration and female preference for this coloration. Houde’s study2 showed a correlated response in female preference for orange coloration, following selection on orange coloration tn males in only two of four replicates. This highlights an important weakness inherent in selection experiments: each selected line, although representing a considerable amount of effort, represents only one independent datum. Additionally, the significant response in the two replicates was not present after the third generation of selection. In Breden and Hornaday’s study3. four replicates selected for either high or low overall male coloration showed no correlated change in female preference for overall coloration. Pomrankowski and Sheridan1 correctly point out that the breeding design of this study limrts its power to detect a genetic correlation arising from assortative mating: however, they also argue that the lack of the correlation could be real given the ecology of the stock population. Moreover, the two positive results in Houde’s experiments also could have been generated by uncontrolled assortative mating leading to unintended selection as discussed by Butlir?, who also cites other failures to demonstrate genetic correlations in experiments in which mating patterns were properly controlled. Bakker’s study5 on sticklebacks found a strong correlation between male Intensity of red and female preference. However, the study examined only six independent familres, and Bakker5 himself suggested the possibility that the strong correlation arose from recent mixing of genetically differentiated populations. Wilkinson and Reillo’s study6 of stalk-eyed flies showed that females from the short (S) line preferred short males, but preferences of females from the long (L) line were no different than those of unselected females. The latter result IS puzzling because Wilkinson7 demonstrated strong symmetrical responses to bi-directional selection in the male trait. Selection in the L line should have generated at least some exaggeration of the preference for long males If there was a strong correlation between the preference and the male trait. Another study, not cited by Pomiankowski and SheridanI, had equivocal results. In the planthopper Ribautodelphis imjtans, females produce a vibratory courtship signal to which males respond. De Winter+ found a very strong
effect of selection on interpulse interval in the signals of females, and there was evidence for between-line assortative mating. However, males did not prefer interpulse intervals in simulated calls that were typical of the females in the same coselected line, suggesting that other factors contributed to assortative mating instead of, or in addition to, the selected trait. In summary, studies of only two species, sticklebacks and flies, have demonstrated genetic correlations, and the correlation in sticklebacks could have resulted from mixing genetically dissimilar populations. Results from guppies and planthoppers provide only weak evidence for genetic correlations arising from linkage disequilibria. We think it is premature to draw the general conclusion that such correlations, which have been the subject of much debate, are widespread and well-documented. Additional studies, including attempts to estimate the magnitudes of genetic correlations, are badly needed, especially if runaway models of indirect selection are to be tested.
Felix Breden Dept of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada V5A lS6 H. Carl Gerhardt Division of Biological Sciences, University of Missouri, Columbia, MO 65211, USA Roger K. Butlin Dept of Genetics, University Leeds, UK LS2 9JT
of Leeds,
References 1 Pomiankowski, A. and Sheridan, L. (1994) Trends Ecol Eva/. 9, 241-244 2 Houde, A. Proc. R. Sot. London Ser. 6 (in press) 3 Breden, F. and Hornaday, K. Heredity(in press) 4 Butlin, R.K. (1993) Anim. Behav. 45403-404 5 Bakker, T.C.M. (1993) Nature 363, 255-257 6 Wilkinson, G.S. and Reillo, P.R. (1994) Proc. R. Sot. London Ser. B 255,1-6 7 Wilkinson, G.S. (1993) Genet. Res. 62,213-222 8 De Winter, A.J. (1992) J. Evol. Biol. 5, 249-265
Reply from A. Pomiankowski and L. Sheridan Biologists have finally got around to accepting that females choose their mates. But given half a chance many still deny that preferences have evolved, are adaptive, or are genetically variable. Breden et a/. extend this pessimistic view to recent experimental work documenting genetic correlations between mating preference and sexual ornamentation. Though there is always room for scepticism, the criticisms raised do not amount to much and can be answered easily. Overall there is strong evidence for genetic
correlations, which are most likely created by nonrandom mating. Breden et al. raise doubts about all three studies mentioned in our TREENews & Commentl. The main criticism of Houde’sz experiment selecting for orange area in guppies is that only two of four selection lines showed a correlated response in female preference. This is picking at one statistic and ignoring the rest. Overall there was stronger female preference in high lines in seven out of seven tests (first generation) and seven out of eight tests (second generation). This pattern IS inconsistent with expectations of random genetic drift. There was no difference between high and low lines in the third generation suggesting that the genetic correlations are caused by linkage disequilibrium: a 50% reduction in linkage disequilibrium is expected per generation for unlinked genes. A further point-that ‘assortative mating’ was not controlled in Houde’s study - is no criticism at all. This is the supposed mechanism for the generation of genetic correlations. The case for guppies stands. Wilkinson and Reillo’s similar experiment3 on stalk-eyed flies is attacked because preference rn the long line did not differ from the unselected control. This again is a remark out of context. The central result is that selection influenced female mate choice. Wilkinson and Reillo discuss a number of reasons for the lack of a detectable difference between control and long lines. The most likely explanation is that the experimental assessment of preference was too insensitive. There is no reason to suppose a genetic correlation does not exist. The case for stalk-eyed flies stands. Breden et al. also cast doubt on genetic correlations found in sticklebacks4 and claim these are because of ‘recent mixing of genetically distinct stocks’. In fact, the last recorded ‘recent mixrng’ occurred in 1872, over 120 years ago. Why should genetic correlatrons be maintained over such an extended period? Maybe there have been subsequent unrecorded introductions. But what is the value of such a vague and unsubstantiated possibility. Could it even in principle explain the large genetic correlation observed? The case for sticklebacks stands. Finally, Breden et al. suggest we missed out other studies with more equivocal results. But they only cite one other study and there are many more. Most show evidence for genetic correlatrons and we are currently preparing a review. It is time to wake up to the facts. The general case for genetic correlatrons between mating preference and sexual ornamentation stands.
Andrew Pomiankowski Letitia Sheridan Dept of Genetics and Biometry, University College London, 4 Stephenson Way, London, UK NW1 2HE References 1 Pomiankowski. A. and Sheridan..” L. (1994) Trends Ecol. Evol. 9, 242-244 2 Houde, A.E. Proc. R. Sot. London Ser. B(in press) 3 WIlkInson, G.S. and Reillo. P.R. (1994) Proc. R. Sot. London Ser. B 255, I-6 4 Bakker. T.C.M. (1993) Nature 363, 255-257
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