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Quantitative genetic studies of behavioral evolution
BOOK
REVIEWS
Acknowledgements We thank Cliff Cunningham, and Mitchell commenting
Rod Page Leslie for reading and on the manuscript.
References Nelson, G. and Platnick, N. (1981) Systematics and Biogeography:
Cladistics and Vicariance,
Columbia University Press Darlington, P.J. (1957) Zoogeography: The Geographical Distribution ofAnimals, Wiley Wallace, A.R. (1876) The Geographical Distribution ofAnimals, Harper MacArthur, R.H. and Wilson, E.O. (1967) The
A field guide to quantitative genetics Quantitative Genetic Studies of Behavioral Evolution edited
by C.R.B. Boake
University of Chicago Press, 1994. $66.00 hbk, $26.95 pbk (416 pages) ISBN 0 226 06215 5/O 226 06216 3
To
many behaviorists, quantitative genetics must seem a cabal. It has a foreign tongue (‘pleiotropy’, ‘gene-environment interaction’), not to mention arcane symbols (some in pagan Greek). What’s all the fuss about? Chris Boake’s edited volume makes the answer clear by providing both an entree to the QC approach and explorations of its uses in several areas of behavioral biology. Arnold’s chapter on the concepts of quantitative genetics is the best introduction available to behavioral biologists. It comes as a relief to many of us who have had no place to refer students and colleagues who want to get in on the fun. (Falconer’s beloved text1 is intended more for those who study how to breed animals than those who study how animals breed.) Building on this foundation, later chapters focus on topics as diverse as mating behavior, kin effects, migration, territoriality, locomotion, cannibalism and behavioral response to environmental stress. Some behaviorists have been persuaded that optimality and game theory can replace, rather than complement, genetic approaches. But optimality and game theory describe selection alone, which is only one factor in evolution. Cheverud and Moore’s chapter states the case eloquently: ‘Selection, by itself, does not produce evolution. It is filtered through the genetic system of inheritance, which we ignore at some risk’. One situation in which the risk is great occurs whenever there are maternal effects, as when offspring learn from their parents. Theory predicts, and experiments prove, how unusual the outcome of evolution can be here. In fact, evolution can actually go in 406
Theory of island Biogeography, Princeton University Press Losos, J.B. (1994) in Lizard Ecology: Historica/ and Experimental Perspectives (Vitt, L.J. and Pianka, E.R., eds), pp. 319-333, Princeton University Press Ricklefs, R.E. and Schluter, D. (1993) in Species Divers@ in Ecological Communities: Historica/ and Geographical Perspectives (Ricklefs, R.E. and Schluter, D., eds), pp. 350-364. University
of Chicago Press Crother, B. and Guyer, C. Herpetologica (in press) Carson, H.L. and Kaneshiro, K.Y. (1976) Annu. Rev. Ecol. Syst. 7,31 l-345 Williamson, M. (1981) Island Populations,
the opposite direction to that favored by selection-hardly the picture one would get from an optimality analysis! Quantitative genetics goes beyond optimality by providing predictions for evolutionary dynamics, methods to account for forces other than selection, techniques for measuring the selection and inheritance parameters that appear in the models, and methods (such as artificial selection) for testing the predictions. Complaints are sometimes muttered that the methods are difficult to apply. But without an alternative that can do all of those things, the complaint sounds a bit like someone criticizing another’s pronunciation of a language that he himself cannot speak at all. Mating system evolution, covered from quite different perspectives by Hedrick, Heisler, Hoffman, Partridge and Travis, is another area in behavior where QC has made crucial insights that simply are not accessible to nongenetic approaches. For example, the ‘runaway’ and ‘good genes’ mechanisms for preference evolution depend entirely on genetic correlations (discussed in Heisler’s chapter). Does this mean that QG is the only path for studying sexual selection? No, as Partridge makes clear: other approaches (for example, physiological and surgical manipulations of males) are critically needed to compliment the QG results. Quantitative genetics is sometimes caricatured as an exercise in compiling boring tables of genetic correlations and heritabilities. (A digression: heritability could be expunged profitably from the evolutionary vocabulary. Far more useful are the additive genetic variance and the genetic coefficient of variationz-4.) So just what are all those parameters good for? A major use in determining what evolution regards as separate, evolvable traits. Consider the mating display rate of sailfin mollies. It varies dramatically between populations and is highly correlated with body size. Has genetic divergence in display rate occurred through selection on body size? Or the reverse? Or have both traits evolved to their individual optima? Travis’s chapter explores how QG parameters can be used to test these alternative hypotheses.
Oxford University Press 10 Haydon. D., Radtkey, R.R. and Pianka, E.R. (1993) in Species Dioersity in Ecological Communities: Historical und Geographical Perspectives (Ricklefs, R.E. and Schluter. D.,
eds), pp. 117-130, University of Chicago Press 11 Hillis, D.M.,Bull, J.J., White, M.E.,Badgett, M.R. and Molineux, 1.J.(1992) Science 255,589-592 12 Pianka, E.R. (1972) Copeia 1972, 127-145 13 McGowan, J.A. and Walker, P.W. (1993) in Species Diversity in Ecological Communities
(Ricklefs, R.E. and Schluter, D., eds), pp. 203-214, University of Chicago Press 14 Duellman, W.E. and Pianka, E.R. (1990) Annu. Rev. Eco/. Syst. 21, 57-68
A powerful tool in the QG arsenal that has been underexploited by behaviorists is artificial selection. Hoffman’s chapter discusses how it has been used to uncover unexpected conclusions about territoriality. His studies of natural phenotypic variation in Drosophila show that body size is the main factor determining the outcome of territorial disputes. This observation leads to the obvious prediction that selection for greater territoriality will cause the evolution of larger body size. Territoriality does indeed respond rapidly to artificial selection - but with no detectable change in body size. Thus, artificial selection can test hypotheses about mechanisms underlying behavioral evolution, and can reveal the pitfalls of extrapolating from phenotypic correlations to evolutionary responses. Boake has done a fine job of assembling fresh and diverse views rather than a compendium of memories from the usual tribal elders. Congratulations are also due for a contributor sex ratio that is statistically indistinguishable from even. This book is not intended as a comprehensive survey in the same way that, say, the Krebs and Davies5 volume is. Rather, it strikes a balance between review and report. There are gaps (it would be nice to see foraging represented, for example), and some of the unevenness in style and content that inevitably comes with 14 authors. But these are minor criticisms of what is an important contribution to the critical and growing interface between evolution, genetics and behavior. Mark Kirkpatrick Dept of Zoology, University of Texas, Austin, TX 78712, USA
References Falconer , D. (1989) introduction to Quantitatiue Genetics (3rd edn), Longman Charlesworth, B. (1987) in Sexua/ Se/ection: Testing the AIternatives (Bradbury, J.W. and Andersson, M.B., eds), pp. 21-40. Wiley Price, T. and Schluter, D. (1991) Evolution 45, 853-861
Houle, D. (1992) Generics 130,195-204 Krebs, J.R. and Davies, N.B. (1991) Behaoioural Eco/ogy: An Euolufionary Approach (3rd edn), Blackwell TREE uol. 9, no
IO October
1.994
REVIEWS
Acknowledgements We thank Cliff Cunningham, and Mitchell commenting
Rod Page Leslie for reading and on the manuscript.
References Nelson, G. and Platnick, N. (1981) Systematics and Biogeography:
Cladistics and Vicariance,
Columbia University Press Darlington, P.J. (1957) Zoogeography: The Geographical Distribution ofAnimals, Wiley Wallace, A.R. (1876) The Geographical Distribution ofAnimals, Harper MacArthur, R.H. and Wilson, E.O. (1967) The
A field guide to quantitative genetics Quantitative Genetic Studies of Behavioral Evolution edited
by C.R.B. Boake
University of Chicago Press, 1994. $66.00 hbk, $26.95 pbk (416 pages) ISBN 0 226 06215 5/O 226 06216 3
To
many behaviorists, quantitative genetics must seem a cabal. It has a foreign tongue (‘pleiotropy’, ‘gene-environment interaction’), not to mention arcane symbols (some in pagan Greek). What’s all the fuss about? Chris Boake’s edited volume makes the answer clear by providing both an entree to the QC approach and explorations of its uses in several areas of behavioral biology. Arnold’s chapter on the concepts of quantitative genetics is the best introduction available to behavioral biologists. It comes as a relief to many of us who have had no place to refer students and colleagues who want to get in on the fun. (Falconer’s beloved text1 is intended more for those who study how to breed animals than those who study how animals breed.) Building on this foundation, later chapters focus on topics as diverse as mating behavior, kin effects, migration, territoriality, locomotion, cannibalism and behavioral response to environmental stress. Some behaviorists have been persuaded that optimality and game theory can replace, rather than complement, genetic approaches. But optimality and game theory describe selection alone, which is only one factor in evolution. Cheverud and Moore’s chapter states the case eloquently: ‘Selection, by itself, does not produce evolution. It is filtered through the genetic system of inheritance, which we ignore at some risk’. One situation in which the risk is great occurs whenever there are maternal effects, as when offspring learn from their parents. Theory predicts, and experiments prove, how unusual the outcome of evolution can be here. In fact, evolution can actually go in 406
Theory of island Biogeography, Princeton University Press Losos, J.B. (1994) in Lizard Ecology: Historica/ and Experimental Perspectives (Vitt, L.J. and Pianka, E.R., eds), pp. 319-333, Princeton University Press Ricklefs, R.E. and Schluter, D. (1993) in Species Divers@ in Ecological Communities: Historica/ and Geographical Perspectives (Ricklefs, R.E. and Schluter, D., eds), pp. 350-364. University
of Chicago Press Crother, B. and Guyer, C. Herpetologica (in press) Carson, H.L. and Kaneshiro, K.Y. (1976) Annu. Rev. Ecol. Syst. 7,31 l-345 Williamson, M. (1981) Island Populations,
the opposite direction to that favored by selection-hardly the picture one would get from an optimality analysis! Quantitative genetics goes beyond optimality by providing predictions for evolutionary dynamics, methods to account for forces other than selection, techniques for measuring the selection and inheritance parameters that appear in the models, and methods (such as artificial selection) for testing the predictions. Complaints are sometimes muttered that the methods are difficult to apply. But without an alternative that can do all of those things, the complaint sounds a bit like someone criticizing another’s pronunciation of a language that he himself cannot speak at all. Mating system evolution, covered from quite different perspectives by Hedrick, Heisler, Hoffman, Partridge and Travis, is another area in behavior where QC has made crucial insights that simply are not accessible to nongenetic approaches. For example, the ‘runaway’ and ‘good genes’ mechanisms for preference evolution depend entirely on genetic correlations (discussed in Heisler’s chapter). Does this mean that QG is the only path for studying sexual selection? No, as Partridge makes clear: other approaches (for example, physiological and surgical manipulations of males) are critically needed to compliment the QG results. Quantitative genetics is sometimes caricatured as an exercise in compiling boring tables of genetic correlations and heritabilities. (A digression: heritability could be expunged profitably from the evolutionary vocabulary. Far more useful are the additive genetic variance and the genetic coefficient of variationz-4.) So just what are all those parameters good for? A major use in determining what evolution regards as separate, evolvable traits. Consider the mating display rate of sailfin mollies. It varies dramatically between populations and is highly correlated with body size. Has genetic divergence in display rate occurred through selection on body size? Or the reverse? Or have both traits evolved to their individual optima? Travis’s chapter explores how QG parameters can be used to test these alternative hypotheses.
Oxford University Press 10 Haydon. D., Radtkey, R.R. and Pianka, E.R. (1993) in Species Dioersity in Ecological Communities: Historical und Geographical Perspectives (Ricklefs, R.E. and Schluter. D.,
eds), pp. 117-130, University of Chicago Press 11 Hillis, D.M.,Bull, J.J., White, M.E.,Badgett, M.R. and Molineux, 1.J.(1992) Science 255,589-592 12 Pianka, E.R. (1972) Copeia 1972, 127-145 13 McGowan, J.A. and Walker, P.W. (1993) in Species Diversity in Ecological Communities
(Ricklefs, R.E. and Schluter, D., eds), pp. 203-214, University of Chicago Press 14 Duellman, W.E. and Pianka, E.R. (1990) Annu. Rev. Eco/. Syst. 21, 57-68
A powerful tool in the QG arsenal that has been underexploited by behaviorists is artificial selection. Hoffman’s chapter discusses how it has been used to uncover unexpected conclusions about territoriality. His studies of natural phenotypic variation in Drosophila show that body size is the main factor determining the outcome of territorial disputes. This observation leads to the obvious prediction that selection for greater territoriality will cause the evolution of larger body size. Territoriality does indeed respond rapidly to artificial selection - but with no detectable change in body size. Thus, artificial selection can test hypotheses about mechanisms underlying behavioral evolution, and can reveal the pitfalls of extrapolating from phenotypic correlations to evolutionary responses. Boake has done a fine job of assembling fresh and diverse views rather than a compendium of memories from the usual tribal elders. Congratulations are also due for a contributor sex ratio that is statistically indistinguishable from even. This book is not intended as a comprehensive survey in the same way that, say, the Krebs and Davies5 volume is. Rather, it strikes a balance between review and report. There are gaps (it would be nice to see foraging represented, for example), and some of the unevenness in style and content that inevitably comes with 14 authors. But these are minor criticisms of what is an important contribution to the critical and growing interface between evolution, genetics and behavior. Mark Kirkpatrick Dept of Zoology, University of Texas, Austin, TX 78712, USA
References Falconer , D. (1989) introduction to Quantitatiue Genetics (3rd edn), Longman Charlesworth, B. (1987) in Sexua/ Se/ection: Testing the AIternatives (Bradbury, J.W. and Andersson, M.B., eds), pp. 21-40. Wiley Price, T. and Schluter, D. (1991) Evolution 45, 853-861
Houle, D. (1992) Generics 130,195-204 Krebs, J.R. and Davies, N.B. (1991) Behaoioural Eco/ogy: An Euolufionary Approach (3rd edn), Blackwell TREE uol. 9, no
IO October
1.994