Are indirect genetic effects in behavioral ecology important? A comment on Bailey et al.

Are indirect genetic effects in behavioral ecology important? A comment on Bailey et al. The key proposal in Bailey et al. (2018) is that evolutionary processes may be misinterpreted if indirect genetic effects (IGEs) are not taken into consideration. Further, that such processes are a fundamental part of behavior and thus the genetic analysis of behavior and its evolution must take into account IGEs. The authors present a very convincing case for this proposal both from theoretical argument and empirical evidence. They suggest that an important task is to test the hypothesis that IGEs are more important in traits that involve behavior than other types of traits, as was done for the heritability of traits by Mousseau and Roff (1987). A potential difficulty I see is in categorizing traits. IGEs necessarily involve at least two traits, one in the focal individual and one in the neighbor. Both traits could be the same, as, for example, when aggression in one individual influences aggression in another or they may be quite different, as, for example, when aggression in one individual influences the hormonal status of another. Thus both traits could be 1) the same and be classified as life history, physiology, morphology or behavior; 2) different but still falling in the same category; 3) different and each falling into separate categories. The potential importance of IGEs in influencing evolutionary trajectories is illustrated using some standard quantitative genetic models. Given the assumptions of these models the results are convincing. A potential problem lies in the general assumption of a fixed genetic covariance between traits. When two traits are clearly functionally liked (e.g., two morphological traits) we might reasonably assume that the genetic covariance between the two is due to pleiotropy. However, when the two traits are very different and not functionally linked developmentally then the genetic covariance will be generated by linkage disequilibrium and be much more labile. This is well illustrated by the case of female preference for a particular male trait, where it is generally assumed that the genetic covariance between the two traits results entirely from linkage disequilibrium. Despite this, virtually all models examining the evolution of mate preference and the likelihood of Fisher’s runaway process assume a constant covariance. The present article presents precisely such a model, analyzed by Bailey and Moore (2012), to suggest that “a key determinant of whether IGEs accelerate or retard sexual selection elaboration is the sign and magnitude of the interaction coefficient ψ, which alters the influence of trait-preference genetic covariance during runaway co-evolution.” The model is based on that of Iwasa and Pomiankowski (1995) and like their model also assumes a constant covariance between female preference and the male trait. Such an assumption is necessary for present analytic models but may be quite misleading when the genetic covariance is generated by linkage disequilibrium. To circumvent this problem Roff and Fairbairn (2014) used a simulation model in which the traits were explicitly modeled by a numerical quantitative genetic model. This model thus allowed the genetic covariance to evolve as well as IGEs to occur. The correspondence between predicted runaway from the analytic model and the simulation depended critically on model components, both qualitative and quantitative. Importantly, the parameter space of permissible genetic covariances was limited by model components. As the models necessarily included IGEs it can be concluded that such effects may be important and to this degree agree with the conclusions of Bailey and Moore (2012). But the use of a constant genetic covariance to assess the importance of IGEs in cases may be unwise. I am in complete agreement with the message of this paper but urge that we more carefully consider the assumptions that are used to investigate the phenomenon. REFERENCES Bailey NW, Moore AJ. 2012. Runaway sexual selection without genetic correlations: social environments and flexible mate choice initiate and enhance the Fisher process. Evolution . 66: 2674– 2684. Google Scholar CrossRef Search ADS PubMed  Bailey NW, Marie-Orleach L, Moore A. 2018. Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution? Behav Ecol . Iwasa Y, Pomiankowski A. 1995. Continual change in mate preferences. Nature . 377: 420– 422. Google Scholar CrossRef Search ADS PubMed  Mousseau TA, Roff DA. 1987. Natural selection and the heritability of fitness components. Heredity (Edinb) . 59 (Pt 2): 181– 197. Google Scholar CrossRef Search ADS PubMed  Roff DA, Fairbairn DJ. 2014. The evolution of phenotypes and genetic parameters under preferential mating. Ecol Evol . 4: 2759– 2776. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Ecology Oxford University Press

Are indirect genetic effects in behavioral ecology important? A comment on Bailey et al.

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Oxford University Press
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© The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
ISSN
1045-2249
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1465-7279
D.O.I.
10.1093/beheco/arx163
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Abstract

The key proposal in Bailey et al. (2018) is that evolutionary processes may be misinterpreted if indirect genetic effects (IGEs) are not taken into consideration. Further, that such processes are a fundamental part of behavior and thus the genetic analysis of behavior and its evolution must take into account IGEs. The authors present a very convincing case for this proposal both from theoretical argument and empirical evidence. They suggest that an important task is to test the hypothesis that IGEs are more important in traits that involve behavior than other types of traits, as was done for the heritability of traits by Mousseau and Roff (1987). A potential difficulty I see is in categorizing traits. IGEs necessarily involve at least two traits, one in the focal individual and one in the neighbor. Both traits could be the same, as, for example, when aggression in one individual influences aggression in another or they may be quite different, as, for example, when aggression in one individual influences the hormonal status of another. Thus both traits could be 1) the same and be classified as life history, physiology, morphology or behavior; 2) different but still falling in the same category; 3) different and each falling into separate categories. The potential importance of IGEs in influencing evolutionary trajectories is illustrated using some standard quantitative genetic models. Given the assumptions of these models the results are convincing. A potential problem lies in the general assumption of a fixed genetic covariance between traits. When two traits are clearly functionally liked (e.g., two morphological traits) we might reasonably assume that the genetic covariance between the two is due to pleiotropy. However, when the two traits are very different and not functionally linked developmentally then the genetic covariance will be generated by linkage disequilibrium and be much more labile. This is well illustrated by the case of female preference for a particular male trait, where it is generally assumed that the genetic covariance between the two traits results entirely from linkage disequilibrium. Despite this, virtually all models examining the evolution of mate preference and the likelihood of Fisher’s runaway process assume a constant covariance. The present article presents precisely such a model, analyzed by Bailey and Moore (2012), to suggest that “a key determinant of whether IGEs accelerate or retard sexual selection elaboration is the sign and magnitude of the interaction coefficient ψ, which alters the influence of trait-preference genetic covariance during runaway co-evolution.” The model is based on that of Iwasa and Pomiankowski (1995) and like their model also assumes a constant covariance between female preference and the male trait. Such an assumption is necessary for present analytic models but may be quite misleading when the genetic covariance is generated by linkage disequilibrium. To circumvent this problem Roff and Fairbairn (2014) used a simulation model in which the traits were explicitly modeled by a numerical quantitative genetic model. This model thus allowed the genetic covariance to evolve as well as IGEs to occur. The correspondence between predicted runaway from the analytic model and the simulation depended critically on model components, both qualitative and quantitative. Importantly, the parameter space of permissible genetic covariances was limited by model components. As the models necessarily included IGEs it can be concluded that such effects may be important and to this degree agree with the conclusions of Bailey and Moore (2012). But the use of a constant genetic covariance to assess the importance of IGEs in cases may be unwise. I am in complete agreement with the message of this paper but urge that we more carefully consider the assumptions that are used to investigate the phenomenon. REFERENCES Bailey NW, Moore AJ. 2012. Runaway sexual selection without genetic correlations: social environments and flexible mate choice initiate and enhance the Fisher process. Evolution . 66: 2674– 2684. Google Scholar CrossRef Search ADS PubMed  Bailey NW, Marie-Orleach L, Moore A. 2018. Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution? Behav Ecol . Iwasa Y, Pomiankowski A. 1995. Continual change in mate preferences. Nature . 377: 420– 422. Google Scholar CrossRef Search ADS PubMed  Mousseau TA, Roff DA. 1987. Natural selection and the heritability of fitness components. Heredity (Edinb) . 59 (Pt 2): 181– 197. Google Scholar CrossRef Search ADS PubMed  Roff DA, Fairbairn DJ. 2014. The evolution of phenotypes and genetic parameters under preferential mating. Ecol Evol . 4: 2759– 2776. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2017. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com

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Behavioral EcologyOxford University Press

Published: Jan 1, 2018

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