A revolution has been taking place in the biological sciences regarding how to conceptualize genes, development, inheritance, and evolution. This revolution has contributed to the rapid growth of areas such as epigenetics, evolutionary developmental biology, and systems biology. In an extension of this ongoing revolution, Charney has presented a detailed and comprehensive critique of the genomic model underlying contemporary behavior genetics. I was impressed with the range of topics covered and the clear and appropriately detailed presentation of the implications of recent findings across the life sciences for how we think about heritability, gene expression, the use of twin studies, and gene association studies. Although his detailed examples of the remarkably fluid nature of the genome will likely challenge many non-biologists, these examples provide a solid and necessary empirical basis for the “postgenomic” paradigm shift outlined by Charney in his target article.
I entirely agree with Charney that the traditional genomic model promoted for much of the twentieth century across the life sciences is no longer viable. The idea of a fixed genome that is the sole source of heritable traits is simply not plausible, given advances over the last several decades in genetics, molecular biology, and the like. The mind-boggling combinatorial complexity of the bidirectional traffic inherent in the process of development, a key point of Charney's arguments against old-fashioned behavior genetics, blurs the boundary between genes and environment and highlights the dynamic fusion of biology and ecology that is proving key to our understanding of both development and evolution.
A key point of Charney's argument is that genes do not stand outside the developmental system (of which they are a part), acting as independent causes of traits or characters. Their expression, whether they are active or inactive, is determined by an array of influences from other levels of the system. This idea of distributed control, that direction for the emergence and development of traits resides in the nature of the relationships between internal genetic and non-genetic factors and external environmental variables, is a key principle of a developmental point of view. This point of view is in sharp contrast to the concept of the additivity of genes and environment, a key assumption of traditional heritability analysis. A developmental point of view shifts the focus from population statistics to the study of individual development, because it is only through the study of the process of development that we can understand the dynamics of developmental (and evolutionary) change. In this light, it important to emphasize that there is no direct connection between genetic activity and behavior. All genetic effects on behavior are mediated through the cell membrane and subsequent coactions among cells and neural networks (Johnston & Edwards Reference Johnston and Edwards2002).
Documenting the bidirectional relations from gene action to the external environment and their effects on behavior over the life course, including the prenatal period, remains a major conceptual, empirical, and analytical challenge for developmental science. Charney has provided a useful and instructive snapshot of where we are in meeting this challenge. His review of the wide range of factors that are participants in gene activity and expression, in some cases well beyond the timescale of individual development, supports the view that the organism–environment system is the fundamental level of analysis in our efforts to understand the links among development, heredity, and evolution (Lickliter Reference Lickliter2009). An organism and its environment are fundamentally connected, and the epigenetic research considered by Charney is providing powerful evidence that they cannot be functionally separated.
One implication of this insight for behavior genetics seems clear – linking genotypes to behavioral outcomes requires developmental investigation. As pointed out by Gottlieb (Reference Gottlieb1995; Reference Gottlieb2003) some years ago, the population view of behavioral genetics is not developmental. It is based on the assumption that a quantitative analysis of the genetic and environmental contributions to individual differences can contribute to an understanding of the developmental process of individuals. However, it is clear that individual development is the result of organism–environment relationships in which the quantitative contribution of either cannot be specified. Charney has provided a scholarly and integrative review of why this is the case, and I applaud his accomplishment.
Further, Charney's review demonstrates that because of the variability of relevant resources across different environments and because only a portion of the genome is expressed in any individual, what is actually realized during the course of individual development is only one of many possibilities. This is a core tenet of probabilistic epigenesis (Gottlieb Reference Gottlieb2007), the view of development and evolution that emphasizes that because of the multiplicity of levels, factors, and interactions involved and because of its history-dependent and situated nature, neither physical nor behavioral development can have a predetermined outcome. To understand the origin, maintenance, or transformation of any phenotypic trait, it is necessary to study its development. This is the challenge now facing behavior genetics, and we will have to see if the field is up to the task of achieving a science grounded in developmental processes.
My lone reservation regarding Charney's exposure of the shortcomings of the basic assumptions of behavior genetics is that he has not gone far enough in exploring the implications of what this means for the future of behavior genetics, as well as biology and psychology more generally. I have emphasized the need for assuming a developmental point of view, but there are a number of other concerns that remain, including whether it will be possible for the field to reinvent itself in light of the range of molecular findings that appear to be undermining its conceptual foundation, a foundation rooted in the assumptions of Mendelian genetics. More broadly, Charney hints at but does not directly address the possibility that given that phenotypic development is a multidetermined phenomenon involving systemic complexity over time, the number of variables, interactions, and contingencies involved from fertilized egg to functional adult may well put its full understanding beyond human comprehension. Explanatory and predictive power are hard to come by when dealing with complex systems.
A revolution has been taking place in the biological sciences regarding how to conceptualize genes, development, inheritance, and evolution. This revolution has contributed to the rapid growth of areas such as epigenetics, evolutionary developmental biology, and systems biology. In an extension of this ongoing revolution, Charney has presented a detailed and comprehensive critique of the genomic model underlying contemporary behavior genetics. I was impressed with the range of topics covered and the clear and appropriately detailed presentation of the implications of recent findings across the life sciences for how we think about heritability, gene expression, the use of twin studies, and gene association studies. Although his detailed examples of the remarkably fluid nature of the genome will likely challenge many non-biologists, these examples provide a solid and necessary empirical basis for the “postgenomic” paradigm shift outlined by Charney in his target article.
I entirely agree with Charney that the traditional genomic model promoted for much of the twentieth century across the life sciences is no longer viable. The idea of a fixed genome that is the sole source of heritable traits is simply not plausible, given advances over the last several decades in genetics, molecular biology, and the like. The mind-boggling combinatorial complexity of the bidirectional traffic inherent in the process of development, a key point of Charney's arguments against old-fashioned behavior genetics, blurs the boundary between genes and environment and highlights the dynamic fusion of biology and ecology that is proving key to our understanding of both development and evolution.
A key point of Charney's argument is that genes do not stand outside the developmental system (of which they are a part), acting as independent causes of traits or characters. Their expression, whether they are active or inactive, is determined by an array of influences from other levels of the system. This idea of distributed control, that direction for the emergence and development of traits resides in the nature of the relationships between internal genetic and non-genetic factors and external environmental variables, is a key principle of a developmental point of view. This point of view is in sharp contrast to the concept of the additivity of genes and environment, a key assumption of traditional heritability analysis. A developmental point of view shifts the focus from population statistics to the study of individual development, because it is only through the study of the process of development that we can understand the dynamics of developmental (and evolutionary) change. In this light, it important to emphasize that there is no direct connection between genetic activity and behavior. All genetic effects on behavior are mediated through the cell membrane and subsequent coactions among cells and neural networks (Johnston & Edwards Reference Johnston and Edwards2002).
Documenting the bidirectional relations from gene action to the external environment and their effects on behavior over the life course, including the prenatal period, remains a major conceptual, empirical, and analytical challenge for developmental science. Charney has provided a useful and instructive snapshot of where we are in meeting this challenge. His review of the wide range of factors that are participants in gene activity and expression, in some cases well beyond the timescale of individual development, supports the view that the organism–environment system is the fundamental level of analysis in our efforts to understand the links among development, heredity, and evolution (Lickliter Reference Lickliter2009). An organism and its environment are fundamentally connected, and the epigenetic research considered by Charney is providing powerful evidence that they cannot be functionally separated.
One implication of this insight for behavior genetics seems clear – linking genotypes to behavioral outcomes requires developmental investigation. As pointed out by Gottlieb (Reference Gottlieb1995; Reference Gottlieb2003) some years ago, the population view of behavioral genetics is not developmental. It is based on the assumption that a quantitative analysis of the genetic and environmental contributions to individual differences can contribute to an understanding of the developmental process of individuals. However, it is clear that individual development is the result of organism–environment relationships in which the quantitative contribution of either cannot be specified. Charney has provided a scholarly and integrative review of why this is the case, and I applaud his accomplishment.
Further, Charney's review demonstrates that because of the variability of relevant resources across different environments and because only a portion of the genome is expressed in any individual, what is actually realized during the course of individual development is only one of many possibilities. This is a core tenet of probabilistic epigenesis (Gottlieb Reference Gottlieb2007), the view of development and evolution that emphasizes that because of the multiplicity of levels, factors, and interactions involved and because of its history-dependent and situated nature, neither physical nor behavioral development can have a predetermined outcome. To understand the origin, maintenance, or transformation of any phenotypic trait, it is necessary to study its development. This is the challenge now facing behavior genetics, and we will have to see if the field is up to the task of achieving a science grounded in developmental processes.
My lone reservation regarding Charney's exposure of the shortcomings of the basic assumptions of behavior genetics is that he has not gone far enough in exploring the implications of what this means for the future of behavior genetics, as well as biology and psychology more generally. I have emphasized the need for assuming a developmental point of view, but there are a number of other concerns that remain, including whether it will be possible for the field to reinvent itself in light of the range of molecular findings that appear to be undermining its conceptual foundation, a foundation rooted in the assumptions of Mendelian genetics. More broadly, Charney hints at but does not directly address the possibility that given that phenotypic development is a multidetermined phenomenon involving systemic complexity over time, the number of variables, interactions, and contingencies involved from fertilized egg to functional adult may well put its full understanding beyond human comprehension. Explanatory and predictive power are hard to come by when dealing with complex systems.