This paper evaluates and criticises the developmental systems conception of evolution and develops instead an extension of the gene's eye conception of evolution. We argue (i) Dawkin's attempt to segregate developmental and evolutionary issues about genes is unsatisfactory. On plausible views of development it is arbitrary to single out genes as the units of selection. (ii) The genotype does not carry information about the phenotype in any way that distinguishes the role of the genes in development from that other factors. (...) (iii) There is no simple and general causal criterion which distinguishes the role of genes in development and evolution. (iv) There is, however, an important sense in which genes but not every other developmental factor represent the phenotype. (v) The idea that genes represent features of the phenotype forces us to recognise that genes are not the only, or almost the only, replicators. Many mechanisms of replication are involved in both development and evolution. (vi) A conception of evolutionary history which recognises both genetic and non-genetic replicators, lineages of replicators and interactors has advantages over both the radical rejection of the replicator/interactor distinction and the conservative restriction of replication to genetic replication. (shrink)

There is increasing evidence for epigenetically mediated transgenerational inheritance across taxa. However, the evolutionary implications of such alternative mechanisms of inheritance remain unclear. Herein, we show that epigenetic mechanisms can serve two fundamentally different functions in transgenerational inheritance: (i) selection-based effects, which carry adaptive information in virtue of selection over many generations of reliable transmission; and (ii) detection-based effects, which are a transgenerational form of adaptive phenotypic plasticity. The two functions interact differently with a third form of epigenetic information transmission, (...) namely information about cell state transmitted for somatic cell heredity in multicellular organisms. Selection-based epigenetic information is more likely to conflict with somatic cell inheritance than is detection-based epigenetic information. Consequently, the evolutionary implications of epigenetic mechanisms are different for unicellular and multicellular organisms, which underscores the conceptual and empirical importance of distinguishing between these two different forms of transgenerational epigenetic effect. (shrink)

What role does non-genetic inheritance play in evolution? In recent work we have independently and collectively argued that the existence and scope of non-genetic inheritance systems, including epigenetic inheritance, niche construction/ecological inheritance, and cultural inheritance—alongside certain other theory revisions—necessitates an extension to the neo-Darwinian Modern Synthesis (MS) in the form of an Extended Evolutionary Synthesis (EES). However, this argument has been challenged on the grounds that non-genetic inheritance systems are exclusively proximate mechanisms that serve the ultimate function of calibrating organisms (...) to stochastic environments. In this paper we defend our claims, pointing out that critics of the EES (1) conflate non-genetic inheritance with early 20th-century notions of soft inheritance; (2) misunderstand the nature of the EES in relation to the MS; (3) confuse individual phenotypic plasticity with trans-generational non-genetic inheritance; (4) fail to address the extensive theoretical and empirical literature which shows that non-genetic inheritance can generate novel targets for selection, create new genetic equilibria that would not exist in the absence of non-genetic inheritance, and generate phenotypic variation that is independent of genetic variation; (5) artificially limit ultimate explanations for traits to gene-based selection, which is unsatisfactory for phenotypic traits that originate and spread via non-genetic inheritance systems; and (6) fail to provide an explanation for biological organization. We conclude by noting ways in which we feel that an overly gene-centric theory of evolution is hindering progress in biology and other sciences. (shrink)

Since the discovery of the double helical structure of DNA, the standard account of the inheritance of features has been in terms of DNA-copying and DNA-transmission. This theory is just a version of the old theory according to which the inheritance of features is explained by the transfer at conception of some developmentally privileged material from parents to offspring. This paper does the following things: (1) it explains what the inheritance of features is; (2) it explains how the DNA-centric theory (...) emerged; (3) it clarifies the relation between the DNA-centric theory and the ‘unfolding’ theory of development; (4) it argues that (given what we now know about developmental processes and genetic activity) the DNA-centric theory should be abandoned in favour of a pluralistic (but not holistic) theory of the inheritance of features. According to this pluralistic theory, the reliable reoccurrence of phenotypes must be explained by appealing not only to processes responsible for the reliable reoccurrence of genetic developmental factors but also to processes responsible for the reliable reoccurrence (or persistence) of nongenetic developmental factors. (shrink)

According to the received view of evolution, only genes are inherited. From this view it follows that only genetically-caused phenotypic variation is selectable and, thereby, that all selection is at bottom genetic selection. This paper argues that the received view is wrong. In many species, there are intergenerationally-stable phenotypic differences due to environmental differences. Natural selection can act on these nongenetically-caused phenotypic differences in the same way it acts on genetically-caused phenotypic differences. Some selection is at bottom nongenetic selection. The (...) argument against the received view involves a reformulation of the concepts of inheritance and heritability. Inherited factors are all those developmental factors responsible for parent–offspring similarity; some inherited factors are genetic and some are not. Heritable variation is intergenerationally-stable phenotypic variation; some such variation is genetically-caused and some is not. The received view and its critics The possibility of nongenetic selection (the lucky butterfly) The reality of nongenetic selection 3.1 Imprinting mechanisms 3.2 Other learning mechanisms 3.3 Other nongenetic mechanisms Genetic and nongenetic inheritance mechanisms Genetic and nongenetic inherited factors Genetic and nongenetic heritability Conclusions + Current address: Dr Matteo Mameli, Research Fellow, King's College, Cambridge, CB2 1ST, United Kingdom, matteo.mameli{at}kings.cam.ac.uk' + u + '@' + d + ''//-->. (shrink)

Developmental systems theory (DST) expands the unit of replication from genes to whole systems of developmental resources, which DST interprets in terms of cycling developmental processes. Expansion seems required by DST's argument against privileging genes in evolutionary and developmental explanations of organic traits. DST and the expanded replicator brook no distinction between biological and cultural evolution. However, by endorsing a single expanded unit of inheritance and leaving the classical molecular notion of gene intact, DST achieves only a nominal reunification of (...) heredity and development. I argue that an alternative conceptualization of inheritance denies the classical opposition of genetics and development while avoiding the singularity inherent in the replicator concept. It also yields a new unit--the reproducer--which genuinely integrates genetic and developmental perspectives. The reproducer concept articulates the non-separability of "genetic" and "developmental" roles in units of heredity, development, and evolution. DST reformulated in terms of reproducers rather than replicators preserves an empirically interesting distinction between cultural and biological evolution. (shrink)

Laland and colleagues have sought to challenge the proximate–ultimate distinction claiming that it imposes a unidirectional model of causation, is limited in its capacity to account for complex biological phenomena, and hinders progress in biology. In this article the core of their argument is critically analyzed. It is claimed that contrary to their claims Laland et al. rely upon the proximate–ultimate distinction to make their points and that their alternative conception of reciprocal causation refers to phenomena that were already accounted (...) for by standard theory. (shrink)

In the six decades since the publication of Julian Huxley's Evolution: The Modern Synthesis, spectacular empirical advances in the biological sciences have been accompanied by equally significant developments within the core theoretical framework of the discipline. As a result, evolutionary theory today includes concepts and even entire new fields that were not part of the foundational structure of the Modern Synthesis. In this volume, sixteen leading evolutionary biologists and philosophers of science survey the conceptual changes that have emerged since Huxley's (...) landmark publication, not only in such traditional domains of evolutionary biology as quantitative genetics and paleontology but also in such new fields of research as genomics and EvoDevo. Most of the contributors to Evolution—The Extended Synthesis accept many of the tenets of the classical framework but want to relax some of its assumptions and introduce significant conceptual augmentations of the basic Modern Synthesis structure—just as the architects of the Modern Synthesis themselves expanded and modulated previous versions of Darwinism. This continuing revision of a theoretical edifice the foundations of which were laid in the middle of the nineteenth century—the reexamination of old ideas, proposals of new ones, and the synthesis of the most suitable—shows us how science works, and how scientists have painstakingly built a solid set of explanations for what Darwin called the "grandeur" of life. (shrink)

Human, cognition, interaction, and culture are thoroughly intertwined. Without cognition and interaction, there would be no culture. Without culture, cognition and interaction would be very different affairs, as they are among other social species. The effect of culture on mental life has always been a main concern of the social sciences and, after a long period of almost total neglect, it is more and more taken into consideration in cognitive psychology. The effect of cognition, and in particular of the ability (...) to attribute mental states to others, on interaction has become a important topic of investigation in developmental and social psychology. Little attention, on the other hand, is paid to the effect of cognition on culture. All would agree, of course that the human mind is what makes human culture possible. Quite generally, however, the mind is seen as a mere enabler of culture, a pure opportunity with no constraints attached, nothing that might contribute to shaping, or at least to biasing cultural contents. Against this neglect of cognition, I will argue that understanding the mind is doubly important to the study of culture. Psychological considerations are crucial both to a proper characterization of what is cultural and to a proper explanation of cultural phenomena. Most anthropologists may be too savvy to still talk of the mind as a “blank slate”, but they too often meet any discussion of psychological factors in culture with a blank stare. Most evolutionary theorists who see cultural evolution as an analogue of biological evolution by natural selection postulate rather than investigate the few particulars of the human mind.. (shrink)

To properly understand behavior, we must obtain both ultimate and proximate explanations. Put briefly, ultimate explanations are concerned with why a behavior exists, and proximate explanations are concerned with how it works. These two types of explanation are complementary and the distinction is critical to evolutionary explanation. We are concerned that they have become conflated in some areas of the evolutionary literature on human behavior. This article brings attention to these issues. We focus on three specific areas: the evolution of (...) cooperation, transmitted culture, and epigenetics. We do this to avoid confusion and wasted effort—dangers that are particularly acute in interdisciplinary research. Throughout this article, we suggest ways in which misunderstanding may be avoided in the future. (shrink)