“Why” and “How” behavior evolves: a comment on Bailey et al.

“Why” and “How” behavior evolves: a comment on Bailey et al. Now that we are living in the Age of the Genome, it is all too easy to regard fields of biological research that analyze the phenotype as quaint, old-fashioned, and incapable of deep insight. But before we rush to condemn research in Behavioral Ecology in this way, it is worth remembering the immense intellectual heft of the theoreticians that established this field and the rigor and clarity of thought behind the first wave of empirical research in this area. There is more to Behavioral Ecology than the “optimality” way of thinking portrayed by Bailey et al. (2018). Behavioral Ecology is about understanding adaptations. It explains why selection favors the evolution of some traits and not others, and why selection varies under different ecological and social conditions. With its key insights on kin selection (Hamilton 1964), social adaptations (Williams 1966), contests (Maynard Smith and Price 1973), parent–offspring conflict (reviewed in Keller 1999), sexual conflict (reviewed in Keller 1999), and intraspecific arms races (Dawkins and Krebs 1979), this field has been particularly ground-breaking in explaining why social interactions act to change the fitness of other individuals. “Social selection” was thus well-characterized by Behavioral Ecology long before the inception of Indirect Genetic Effects. Furthermore, now that Hamilton’s (1964) insights about kin selection have revolutionized our understanding of social evolution, students of Behavioral Ecology are routinely trained as undergraduates to take the “genes-eye” view of social behavior (see Keller 1999 or Davies et al. 2012, for example). Any student alert to these twin triumphs of Behavioral Ecology, namely the contribution of social interactions to fitness and the importance of taking the “genes-eye” perspective when quantifying fitness, is unlikely to be as naive as the second column in Table 1 of Bailey et al.’s review suggests. They will also be able to derive the interpretations presented in the third column of this table without knowing anything about Indirect Genetic Effects. Table 1 Complementary questions about the evolution of a trait, for example body size   Phenotypic Gambit  Quantitative Genetics (including IGEs)  Asks:  How is body size adaptive, through its net contribution to fitness?  How evolvable is body size, and how rapidly can body size evolve in response to selection?  Quantifies:  Fitness costs and benefits of a given body size, for self and via kin  Relative contribution of genes and the environment (including the social environment, and the genes within it) to body size  Deduces:  How selection optimizes fitness derived from body size, in different ecological and social environments  Pace and direction of evolutionary change in body size, in response to selection  Can’t:  Describe pace and direction of future evolutionary change in body size, because it ignores underlying genetic mechanisms  Say whether evolutionary change in body size is adaptive because the source of selection is not specified in the model    Phenotypic Gambit  Quantitative Genetics (including IGEs)  Asks:  How is body size adaptive, through its net contribution to fitness?  How evolvable is body size, and how rapidly can body size evolve in response to selection?  Quantifies:  Fitness costs and benefits of a given body size, for self and via kin  Relative contribution of genes and the environment (including the social environment, and the genes within it) to body size  Deduces:  How selection optimizes fitness derived from body size, in different ecological and social environments  Pace and direction of evolutionary change in body size, in response to selection  Can’t:  Describe pace and direction of future evolutionary change in body size, because it ignores underlying genetic mechanisms  Say whether evolutionary change in body size is adaptive because the source of selection is not specified in the model  View Large What research in Behavioral Ecology cannot do, however, is explain how traits change in response to selection, including social selection. The phenotypic gambit taken by models in Behavioral Ecology is that it is possible to analyze the evolution of adaptations by focusing on the phenotype alone. The approach is to focus on the fitness costs and benefits associated with any given trait, and to ignore the trait’s underlying genetic architecture (Table 1). The phenotypic gambit has paid off in the sense that it can account for existence of both adaptive and seemingly nonadaptive traits (e.g., Davies et al. 2012). However, it can say nothing specific about the pace or trajectory of future evolutionary change in those traits (see Table 1), nor the traits they affect, including why they might not change at all in response to selection. This is where quantitative genetics, including Indirect Genetic Effects, is important (see Table 1). As Bailey et al. (2018) explain, the Indirect Genetic Effects models describe quantitative trait change by considering the contribution of genes in the social partner to that trait as well as an individual’s own genes. New insights can then be gained into the possible pace and direction of future evolutionary trait change in the focal individual. As Bailey et al. (2018) point out, this modeling approach has proven highly successful in predicting the effects of artificial selection on traits of economic significance in agricultural plants and animals, including why these traits sometimes fail to respond to selection at all. The approaches taken by the phenotypic gambit and quantitative genetics therefore offer complementary perspectives on the evolution of any trait, including animal behavior (Table 1; and as has been argued before by others, e.g., Moore et al. 1997). Behavioral Ecology offers a reason for selection. Quantitative genetics tells us the extent to which traits then evolve in response to selection. In a recent paper (Jarrett et al. 2017), we combined these complementary approaches to consider how social behaviors, as they are defined in Behavioral Ecology, contribute to evolutionary change. The general logic was to map social behavior onto the interaction coefficient ψ specified by models of Indirect Genetics Effects. We think this simple approach could be taken in future work on other species. We were specifically interested in understanding the effects of reciprocal interactions between parents and offspring on the evolution of body size in burying beetles. Here, greater levels of parental care increase offspring body size, and better-nourished offspring mature into better parents. Thus the interaction coefficient ψ is positive in each direction of this reciprocal interaction. Since larger adults and better parents also have higher fitness, the interaction is also cooperative. Models of Indirect Genetics Effects predict that when ψ is positive for reciprocally interacting traits, then the pace of evolutionary change is accelerated (Moore et al. 1997). Therefore, we should expect cooperative interactions to enhance the response to selection on body size in burying beetles. We tested this idea by imposing selection for increased body size on laboratory populations of burying beetles. In some populations, larvae received parental care but in others they never received any care from their parents. We discovered that larger bodies evolved in response to selection but only when larvae received parental care. Thus, cooperation between parents and offspring facilitated an evolutionary increase in body size (Jarrett et al. 2017). In summary, we wholeheartedly agree with Bailey et al.’s general proposition that merging the predictions gained by using the phenotypic gambit with those from models of Indirect Genetic Effects is likely be fruitful. The combined approach can explain why different types of social behavior exist, and how they can contribute to any further evolutionary change. REFERENCES Bailey N, Marie-Orleach L, Moore AJ. 2018. Indirect genetic effects in behavioral ecology: does behaviour play a special role in evolution? Behavioral Ecology  Davies NB, Krebs JR, West SA. 2012. An Introduction to Behavioural Ecology . 3rd ed. Chichester (UK): Wiley Blackwell. Dawkins R, Krebs JR. 1979. Arms races between and within species. Proc R Soc B. 205: 489– 511. Hamilton WD. 1964. The genetical evolution of social behaviour. J Theor Biol . 7: 1– 52. CrossRef Search ADS PubMed  Jarrett BJ, Schrader M, Rebar D, Houslay TM, Kilner RM. 2017. Cooperative interactions within the family enhance the capacity for evolutionary change in body size. Nat Ecol Evol . 1: 0178. Google Scholar CrossRef Search ADS PubMed  Keller L. 1999 (editor). Levels of Selection in Evolution . Princeton (NJ): Princeton University Press. Maynard Smith J, Price GR. 1973. The logic of animal conflict. Nature . 246: 15– 18. Google Scholar CrossRef Search ADS   Moore AJ, BrodieIII ED, Wolf JB. 1997. Interacting phenotypes and the evolutionary process I: direct and indirect genetic effects of social interactions. Evolution . 51: 1352– 1362. Google Scholar CrossRef Search ADS PubMed  Williams GC. 1966. Adaptation and Natural Selection. Princeton, NJ: Princeton University Press. © 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

“Why” and “How” behavior evolves: a comment on Bailey et al.

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Abstract

Now that we are living in the Age of the Genome, it is all too easy to regard fields of biological research that analyze the phenotype as quaint, old-fashioned, and incapable of deep insight. But before we rush to condemn research in Behavioral Ecology in this way, it is worth remembering the immense intellectual heft of the theoreticians that established this field and the rigor and clarity of thought behind the first wave of empirical research in this area. There is more to Behavioral Ecology than the “optimality” way of thinking portrayed by Bailey et al. (2018). Behavioral Ecology is about understanding adaptations. It explains why selection favors the evolution of some traits and not others, and why selection varies under different ecological and social conditions. With its key insights on kin selection (Hamilton 1964), social adaptations (Williams 1966), contests (Maynard Smith and Price 1973), parent–offspring conflict (reviewed in Keller 1999), sexual conflict (reviewed in Keller 1999), and intraspecific arms races (Dawkins and Krebs 1979), this field has been particularly ground-breaking in explaining why social interactions act to change the fitness of other individuals. “Social selection” was thus well-characterized by Behavioral Ecology long before the inception of Indirect Genetic Effects. Furthermore, now that Hamilton’s (1964) insights about kin selection have revolutionized our understanding of social evolution, students of Behavioral Ecology are routinely trained as undergraduates to take the “genes-eye” view of social behavior (see Keller 1999 or Davies et al. 2012, for example). Any student alert to these twin triumphs of Behavioral Ecology, namely the contribution of social interactions to fitness and the importance of taking the “genes-eye” perspective when quantifying fitness, is unlikely to be as naive as the second column in Table 1 of Bailey et al.’s review suggests. They will also be able to derive the interpretations presented in the third column of this table without knowing anything about Indirect Genetic Effects. Table 1 Complementary questions about the evolution of a trait, for example body size   Phenotypic Gambit  Quantitative Genetics (including IGEs)  Asks:  How is body size adaptive, through its net contribution to fitness?  How evolvable is body size, and how rapidly can body size evolve in response to selection?  Quantifies:  Fitness costs and benefits of a given body size, for self and via kin  Relative contribution of genes and the environment (including the social environment, and the genes within it) to body size  Deduces:  How selection optimizes fitness derived from body size, in different ecological and social environments  Pace and direction of evolutionary change in body size, in response to selection  Can’t:  Describe pace and direction of future evolutionary change in body size, because it ignores underlying genetic mechanisms  Say whether evolutionary change in body size is adaptive because the source of selection is not specified in the model    Phenotypic Gambit  Quantitative Genetics (including IGEs)  Asks:  How is body size adaptive, through its net contribution to fitness?  How evolvable is body size, and how rapidly can body size evolve in response to selection?  Quantifies:  Fitness costs and benefits of a given body size, for self and via kin  Relative contribution of genes and the environment (including the social environment, and the genes within it) to body size  Deduces:  How selection optimizes fitness derived from body size, in different ecological and social environments  Pace and direction of evolutionary change in body size, in response to selection  Can’t:  Describe pace and direction of future evolutionary change in body size, because it ignores underlying genetic mechanisms  Say whether evolutionary change in body size is adaptive because the source of selection is not specified in the model  View Large What research in Behavioral Ecology cannot do, however, is explain how traits change in response to selection, including social selection. The phenotypic gambit taken by models in Behavioral Ecology is that it is possible to analyze the evolution of adaptations by focusing on the phenotype alone. The approach is to focus on the fitness costs and benefits associated with any given trait, and to ignore the trait’s underlying genetic architecture (Table 1). The phenotypic gambit has paid off in the sense that it can account for existence of both adaptive and seemingly nonadaptive traits (e.g., Davies et al. 2012). However, it can say nothing specific about the pace or trajectory of future evolutionary change in those traits (see Table 1), nor the traits they affect, including why they might not change at all in response to selection. This is where quantitative genetics, including Indirect Genetic Effects, is important (see Table 1). As Bailey et al. (2018) explain, the Indirect Genetic Effects models describe quantitative trait change by considering the contribution of genes in the social partner to that trait as well as an individual’s own genes. New insights can then be gained into the possible pace and direction of future evolutionary trait change in the focal individual. As Bailey et al. (2018) point out, this modeling approach has proven highly successful in predicting the effects of artificial selection on traits of economic significance in agricultural plants and animals, including why these traits sometimes fail to respond to selection at all. The approaches taken by the phenotypic gambit and quantitative genetics therefore offer complementary perspectives on the evolution of any trait, including animal behavior (Table 1; and as has been argued before by others, e.g., Moore et al. 1997). Behavioral Ecology offers a reason for selection. Quantitative genetics tells us the extent to which traits then evolve in response to selection. In a recent paper (Jarrett et al. 2017), we combined these complementary approaches to consider how social behaviors, as they are defined in Behavioral Ecology, contribute to evolutionary change. The general logic was to map social behavior onto the interaction coefficient ψ specified by models of Indirect Genetics Effects. We think this simple approach could be taken in future work on other species. We were specifically interested in understanding the effects of reciprocal interactions between parents and offspring on the evolution of body size in burying beetles. Here, greater levels of parental care increase offspring body size, and better-nourished offspring mature into better parents. Thus the interaction coefficient ψ is positive in each direction of this reciprocal interaction. Since larger adults and better parents also have higher fitness, the interaction is also cooperative. Models of Indirect Genetics Effects predict that when ψ is positive for reciprocally interacting traits, then the pace of evolutionary change is accelerated (Moore et al. 1997). Therefore, we should expect cooperative interactions to enhance the response to selection on body size in burying beetles. We tested this idea by imposing selection for increased body size on laboratory populations of burying beetles. In some populations, larvae received parental care but in others they never received any care from their parents. We discovered that larger bodies evolved in response to selection but only when larvae received parental care. Thus, cooperation between parents and offspring facilitated an evolutionary increase in body size (Jarrett et al. 2017). In summary, we wholeheartedly agree with Bailey et al.’s general proposition that merging the predictions gained by using the phenotypic gambit with those from models of Indirect Genetic Effects is likely be fruitful. The combined approach can explain why different types of social behavior exist, and how they can contribute to any further evolutionary change. REFERENCES Bailey N, Marie-Orleach L, Moore AJ. 2018. Indirect genetic effects in behavioral ecology: does behaviour play a special role in evolution? Behavioral Ecology  Davies NB, Krebs JR, West SA. 2012. An Introduction to Behavioural Ecology . 3rd ed. Chichester (UK): Wiley Blackwell. Dawkins R, Krebs JR. 1979. Arms races between and within species. Proc R Soc B. 205: 489– 511. Hamilton WD. 1964. The genetical evolution of social behaviour. J Theor Biol . 7: 1– 52. CrossRef Search ADS PubMed  Jarrett BJ, Schrader M, Rebar D, Houslay TM, Kilner RM. 2017. Cooperative interactions within the family enhance the capacity for evolutionary change in body size. Nat Ecol Evol . 1: 0178. Google Scholar CrossRef Search ADS PubMed  Keller L. 1999 (editor). Levels of Selection in Evolution . Princeton (NJ): Princeton University Press. Maynard Smith J, Price GR. 1973. The logic of animal conflict. Nature . 246: 15– 18. Google Scholar CrossRef Search ADS   Moore AJ, BrodieIII ED, Wolf JB. 1997. Interacting phenotypes and the evolutionary process I: direct and indirect genetic effects of social interactions. Evolution . 51: 1352– 1362. Google Scholar CrossRef Search ADS PubMed  Williams GC. 1966. Adaptation and Natural Selection. Princeton, NJ: Princeton University Press. © 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

Journal

Behavioral EcologyOxford University Press

Published: Jan 1, 2018

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