Discussion: Three Ways to Misunderstand Developmental Systems Theory

Developmental systems theory (DST) is a general theoretical perspective on development, heredity and evolution. It is intended to facilitate the study of interactions between the many factors that influence development without reviving `dichotomous' debates over nature or nurture, gene or environment, biology or culture. Several recent papers have addressed the relationship between DST and the thriving new discipline of evolutionary developmental biology (EDB). The contributions to this literature by evolutionary developmental biologists contain three important misunderstandings of DST.     

Evolutionary Psychology: The Burdens of Proof

I discuss two types of evidential problems with the most widely touted experiments in evolutionary psychology, those performed by Leda Cosmides and interpreted by Cosmides and John Tooby. First, and despite Cosmides and Tooby's claims to the contrary, these experiments don't fulfil the standards of evidence of evolutionary biology. Second Cosmides and Tooby claim to have performed a crucial experiment, and to have eliminated rival approaches. Though they claim that their results are consistent with their theory but contradictory to the leading non-evolutionary alternative, Pragmatic Reasoning Schemas theory, I argue that this claim is unsupported. In addition, some of Cosmides and Tooby's interpretations arise from misguided and simplistic understandings of evolutionary biology. While I endorse the incorporation of evolutionary approaches into psychology, I reject the claims of Cosmides and Tooby that a modular approach is the only one supported by evolutionary biology. Lewontin's critical examinations of the applications of adaptationist thinking provide a background of evidentiary standards against which to view the currently fashionable claims of evolutionary psychology.     

Integrating the Multiple Biological Causes of Human Behavior

I introduce a range of examples of different causal hypotheses about human mate selection. The hypotheses I focus on come from evolutionary psychology, fluctuating asymmetry research and chemical signaling research. I argue that a major obstacle facing an integrated biology of human behavior is the lack of a causal framework that shows how multiple proximate causal mechanisms can act together to produce components of our behavior.     

Agency in Reproduction

While niche construction theory and developmental approaches to evolution have brought to the front the active role of organisms as ecological and developmental agents, respectively, the role of agents in reproduction has been widely neglected by organismal perspectives of evolution. This paper addresses this problem by proposing an agential view of reproduction and shows that such a perspective has implications for the explanation of the origin of modes of reproduction, the evolvability of reproductive modes, and the coevolution between reproduction and social behavior. After introducing the two prevalent views of agency in evolutionary biology, namely those of organismal agency and selective agency, I contrast these two perspectives as applied to the evolution of animal reproduction. Taking eutherian pregnancy as a case study, I wonder whether organismal approaches to agency forged in the frame of niche construction and developmental plasticity theories can account for the goal-directed activities involved in reproductive processes. I conclude that the agential role of organisms in reproduction is irreducible to developmental and ecological agency, and that reproductive goals need to be included into our definitions of organismal agency. I then explore the evolutionary consequences of endorsing an agential approach to reproduction, showing how such an approach might illuminate our understanding of the evolutionary origination and developmental evolvability of reproductive modes. Finally, I analyze recent studies on the coevolution between viviparity and social behavior in vertebrates to suggest that an agential notion of reproduction can provide unforeseen links between developmental and ecological agency.     

Promises and limits of an agency perspective in evolutionary developmental biology

An agent-based perspective in the study of complex systems is well established in diverse disciplines, yet is only beginning to be applied to evolutionary developmental biology. In this essay, we begin by defining agency and associated terminology formally. We then explore the assumptions and predictions of an agency perspective, apply these to select processes and key concept areas relevant to practitioners of evolutionary developmental biology, and consider the potential epistemic roles that an agency perspective might play in evo devo. Throughout, we discuss evidence supportive of agential dynamics in biological systems relevant to evo devo and explore where agency thinking may enrich the explanatory reach of research efforts in evolutionary developmental biology.     

Agential autonomy and biological individuality

What is a biological individual? How are biological individuals individuated? How can we tell how many individuals there are in a given assemblage of biological entities? The individuation and differentiation of biological individuals are central to the scientific understanding of living beings. I propose a novel criterion of biological individuality according to which biological individuals are autonomous agents. First, I articulate an ecological–dynamical account of natural agency according to which, agency is the gross dynamical capacity of a goal-directed system to bias its repertoire to respond to its conditions as affordances. Then, I argue that agents or agential dynamical systems can be agentially dependent on, or agentially autonomous from, other agents and that this agential dependence/autonomy can be symmetrical or asymmetrical, strong or weak. Biological individuals, I propose, are all and only those agential dynamical systems that are strongly agentially autonomous. So, to determine how many individuals there are in a given multiagent aggregate, such as multicellular organism, a colony, symbiosis, or a swarm, we first have to identify how many agential dynamical systems there are, and then what their relations of agential dependence/autonomy are. I argue that this criterion is adequate to the extent that it vindicates the paradigmatic cases, and explains why the paradigmatic cases are paradigmatic, and why the problematic cases are problematic. Finally, I argue for the importance of distinguishing between agential and causal dependence and show the relevance of agential autonomy for understanding the explanatory structure of evolutionary developmental biology.     

Bridging the gap between developmental systems theory and evolutionary developmental biology

Many scientists and philosophers of science are troubled by the relative isolation of developmental from evolutionary biology. Reconciling the science of development with the science of heredity preoccupied a minority of biologists for much of the twentieth century, but these efforts were not corporately successful. Mainly in the past fifteen years, however, these previously dispersed integrating programmes have been themselves synthesized and so reinvigorated. Two of these more recent synthesizing endeavours are evolutionary developmental biology (EDB, or "evo-devo") and developmental systems theory (DST). While the former is a bourgeoning and scientifically well-respected biological discipline, the same cannot be said of DST, which is virtually unknown among biologists. In this review, we provide overviews of DST and EDB, summarize their key tenets, examine how they relate to one another and to the study of epigenetics, and survey the impact that DST and EDB have had (and in future should have) on biological theory and practice.     

Mouse models and the evolutionary developmental biology of the skull

Understanding development is relevant to understanding evolutionbecause developmental processes structure the expression ofphenotypic variation upon which natural selection acts. Advancesin developmental biology are fueling a new synthesis of developmentaland evolutionary biology, but it remains unclear how to usedevelopmental information that largely derives from a few modelorganisms to test hypotheses about the evolutionary developmentalbiology of taxa such as humans and other primates that havenot been or are not amenable to direct study through experimentaldevelopmental biology. In this article, we discuss how and whenmodel organisms like mice are useful for studying the evolutionarydevelopmental biology of even rather distantly related and morphologicallydifferent groups like primates. A productive approach is tofocus on processes that are likely to play key roles in producingevolutionarily significant phenotypic variation across a largephylogenetic range. We illustrate this approach by applyingthe analysis of craniofacial variation in mouse mutant modelsto primate and human evolution.     

Synthetic Biology and the Moral Significance of Artificial Life: A Reply to Douglas,Powell and Savulescu

I discuss the moral significance of artificial life within synthetic biology via a discussion of Douglas, Powell and Savulescu's paper 'Is the creation of artificial life morally significant’. I argue that the definitions of 'artificial life’ and of 'moral significance’ are too narrow. Douglas, Powell and Savulescu's definition of artificial life does not capture all core projects of synthetic biology or the ethical concerns that have been voiced, and their definition of moral significance fails to take into account the possibility that creating artificial life is conditionally acceptable. Finally, I show how several important objections to synthetic biology are plausibly understood as arguing that creating artificial life in a wide sense is only conditionally acceptable.     

Developmental objections to evolutionary modularity

Evolutionary psychologists argue that selective pressures in our ancestral environment yield a highly specialized set of modular cognitive capacities. However, recent papers in developmental psychology and neuroscience claim that evolutionary accounts of modularity are incompatible with the flexibility and plasticity of the developing brain. Instead, they propose cortical and neuronal brain structures are fixed through interactions with our developmental environment. Buller and Gray Hardcastle contend that evolutionary accounts of cognitive development are unacceptably rigid in light of evidence of cortical plasticity. The developing structure of the brain is both too random and too sensitive to external stimuli to be the product of a fixed genetic mechanism. They also claim that the complexity of the human brain cannot be explained in terms of our meager genetic endowment. There simply are not enough genes to program the intricate neuronal structures that are essential to cognition. I argue that neither of these arguments are persuasive. Small numbers of genes can function to determine diverse phenotypical outcomes through evolutionarily selected developmental systems. Similarly, theories of modularity do not rule out the possibility that innate cognitive systems exploit environmental regularities to guide the developing structure of the brain. Consequently, the anti-adaptionist consequences of these positions should be rejected.     

THE SUBSTANCE VIEW: A CRITIQUE

According to the theory of intrinsic value and moral standing called the ‘substance view,’ what makes it prima facie seriously wrong to kill adult human beings, human infants, and even human fetuses is the possession of the essential property of the basic capacity for rational moral agency – a capacity for rational moral agency in root form and thereby not remotely exercisable. In this critique, I cover three distinct reductio charges directed at the substance view's conclusion that human fetuses have the same intrinsic value and moral standing as adult human beings. After giving consideration to defenders of the substance view's replies to these charges, I then critique each of them, ultimately concluding that none is successful. Of course, in order to understand all of these things – the reductio charges, defenders of the substance view's replies to them, and my criticisms of their replies – one must have a better understanding of the substance view (in particular, its understanding of rational moral agency) as well as its defense. Accordingly, I address the substance view's understanding of rational moral agency as well as present its defense.     

Cellular hyperproliferation and cancer as evolutionary variables

Technological advances in biology have begun to dramatically change the way we think about evolution, development, health and disease. The ability to sequence the genomes of many individuals within a population, and across multiple species, has opened the door to the possibility of answering some long-standing and perplexing questions about our own genetic heritage. One such question revolves around the nature of cellular hyperproliferation. This cellular behavior is used to effect wound healing in most animals, as well as, in some animals, the regeneration of lost body parts. Yet at the same time, cellular hyperproliferation is the fundamental pathological condition responsible for cancers in humans. Here, I will discuss why microevolution, macroevolution and developmental biology all have to be taken into consideration when interpreting studies of both normal and malignant hyperproliferation. I will also illustrate how a synthesis of evolutionary sciences and developmental biology through the study of diverse model organisms can inform our understanding of both health and disease.     

The positive value of moral distress

Moral distress in healthcare has been an increasingly prevalent topic of discussion. Most authors characterize it as a negative phenomenon, while few have considered its potentially positive value. In this essay, I argue that moral distress can reveal and affirm some of our most important concerns as moral agents. Indeed, the experience of it under some circumstances appears to be partly constitutive of an honorable character and can allow for crucial moral maturation. The potentially positive value, then, is twofold; moral distress carries both aretaic and instrumental value. Granted, this position is not without its caveats, but by making these clear, I provide a novel framework for policy recommendations regarding when, if ever, we should work to reduce moral distress.     

EvoDevo and niche construction: building bridges

Evolutionary developmental biology and niche-construction theory have much in common, despite independent intellectual origins. Both place emphasis on the role of ontogenetic processes in evolution. The same historical events shaped them, and similar philosophical and sociological barriers hindered their respective advances. Both perspectives maintain that neo-Darwinism needs a theory of macroevolutionary variation and that such a theory can now be adduced from developmental biology. Some proponents of both EvoDevo and niche construction propose additional evolutionary mechanisms, and specify a key role for stable extra-genetic forms of inheritance. Similarly, proponents of each lay emphasis on "reciprocal causation" in the relationship between organism and environment. We illustrate here how EvoDevo and niche construction could gain "added value" from each other, and demonstrate how the niche-construction perspective potentially provides a useful conduit to integrate evolutionary and developmental biology.     

Snail shell coiling (re-)evolution and the evo-devo revolution

During the last two decades evolutionary developmental biology has become a major research programme whose findings put into question some concepts lying at the core of the 'Synthetic Theory'. However, some authors are waiting for a 'revolution' in biology, one in which the existing genetic determinism will give way to a new conceptual understanding of the complexity of living organisms. This 'revolution' should necessarily pass through the elaboration of an appropriate theoretical framework integrating the non-linear dynamics of development as its fundamental basis. This objective implies a drastic shift in the way causality is generally understood as well as a purge of numerous convenient but misleading metaphors such as genetic or developmental programmes. Although most authors do not take these metaphors too literally, some persist in employing such 'instructionist' notions in a more literal perspective, and, in doing so, deny some concepts at the core of evolutionary developmental biology. We critically review two recent studies suggesting that shell coiling has re-evolved in a family of limpets (Calyptraeidae, Gastropoda). We stress that this putative re-evolution of snail shell coiling results only from an arbitrary scoring procedure leading us to consider shell coiling as a binary discrete character. We show that the way in which these authors connect this case study to evolutionary theories stems from the unwarranted premise of a linear mapping of genes onto phenotypes where particulate inheritance of morphological characters seems implicitly assumed. We illustrate how the persisting unclear role of genes in morphogenesis allows the maintenance of the adaptationist programme.     

Developmental capacitance, genetic accommodation, and adaptive evolution

The concept of genetic accommodation remains controversial, in part because it remains unclear whether evolution by genetic accommodation forces a revolution, or merely a shift in emphasis, in our understanding of how evolution produces adaptive new traits. Here I outline a perspective that largely favors the latter view. I argue that evolution by genetic accommodation can easily be integrated into traditional evolutionary concepts. At the same time, evolution by genetic accommodation invites novel empirical and theoretical approaches that may allow biologists to push the boundaries of our current understanding of the process of evolution and to solve some long-standing controversies. Specifically, I discuss the role of developmental mechanisms as natural, and likely ubiquitous, capacitors of cryptic genetic variation, and the role of environmental perturbations as mechanisms by which such variation can become visible to selection on an individual to population-wide scale. I argue that in combination, developmental capacitance and large-scale environmental perturbations have the potential to facilitate rapid evolution including the origin of novel adaptive features while circumventing otherwise powerful genetic and population-biological constraints on adaptive evolution. I end by highlighting several promising avenues for future empirical research to explore the mechanisms and significance of evolution by genetic accommodation.     

Michael Akam and the rise of evolutionary developmental biology

Michael Akam has been awarded the 2007 Kowalevsky medal for his many research accomplishments in the area of evolutionary developmental biology. We highlight three tributaries of Michael’s contribution to evolutionary developmental biology. First, he has made major contributions to our understanding of development of the fruit fly, Drosophila melanogaster. Second, he has maintained a consistent focus on several key problems in evolutionary developmental biology, including the evolving role of Hox genes in arthropods and, more recently, the evolution of segmentation mechanisms. Third, Michael has written a series of influential reviews that have integrated progress in developmental biology into an evolutionary perspective. Michael has also made a large impact on the field through his effective mentorship style, his selfless promotion of younger colleagues, and his leadership of the University Museum of Zoology at Cambridge and the European community of evolutionary developmental biologist.     

The Epistemology of Moral Bioenhancement

Moral bioenhancement is the potential practice of manipulating individuals’ moral behaviors by biological means in order to help resolve pressing moral issues such as climate change and terrorism. This practice has obvious ethical implications, and these implications have been and continue to be discussed in the bioethics literature. What have not been discussed are the epistemological implications of moral bioenhancement. This article details some of these implications of engaging in moral bioenhancement. The argument begins by making the distinction between moral bioenhancement that manipulates the contents of mental states (e.g. beliefs) and that which manipulates other, non‐representational states (e.g. motivations). Either way, I argue, the enhanced moral psychology will fail to conform to epistemic norms, and the only way to resolve this failure and allow the moral bioenhancement to be effective in addressing the targeted moral issues is to make the moral bioenhancement covert.     

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems

A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype and the nature of the selective environment, and how organisms in turn affect the environment through eco evo and eco devo feedbacks. To illustrate the usefulness of an integrated eco evo devo perspective, we connect it with the theory of resource polymorphism (i.e. the phenotypic and genetic diversification that occurs in response to variation in available resources). In so doing, we highlight fishes from recently glaciated freshwater systems as exceptionally well‐suited model systems for testing predictions of an eco evo devo framework in studies of diversification. Studies on these fishes show that intraspecific diversity can evolve rapidly, and that this process is jointly facilitated by (i) the availability of diverse environments promoting divergent natural selection; (ii) dynamic developmental processes sensitive to environmental and genetic signals; and (iii) eco evo and eco devo feedbacks influencing the selective and developmental environments of the phenotype. We highlight empirical examples and present a conceptual model for the generation of resource polymorphism – emphasizing eco evo devo, and identify current gaps in knowledge.