In 1961, Ernst Mayr published a highly influential article on the nature of causation in biology, in which he distinguished between proximate and ultimate causes. Mayr argued that proximate causes (e.g. physiological factors) and ultimate causes (e.g. natural selection) addressed distinct ‘how’ and ‘why’ questions and were not competing alternatives. That distinction retains explanatory value today. However, the adoption of Mayr’s heuristic led to the widespread belief that ontogenetic processes are irrelevant to evolutionary questions, a belief that has (1) hindered (...) progress within evolutionary biology, (2) forged divisions between evolutionary biology and adjacent disciplines and (3) obstructed several contemporary debates in biology. Here we expand on our earlier (Laland et al. in Science 334:1512–1516, 2011) argument that Mayr’s dichotomous formulation has now run its useful course, and that evolutionary biology would be better served by a concept of reciprocal causation, in which causation is perceived to cycle through biological systems recursively. We further suggest that a newer evolutionary synthesis is unlikely to emerge without this change in thinking about causation. (shrink)

The theoretical status of ‘niche construction’ in evolution is intensely debated. Here we substantiate the reasons for different interpretations. We consider two concepts of niche construction brought to bear on evolutionary theory; one that emphasizes how niche construction contributes to selection and another that emphasizes how it contributes to development and inheritance. We explain the rationale for claims that selective and developmental niche construction motivate conceptual change in evolutionary biology and the logic of those who reject these claims. Our analysis (...) shows how the contention arises from alternative assumptions regarding the causal independence of the processes that generate variation, differential fitness and inheritance. (shrink)

A comprehensive treatment of the concept of causation in evolutionary biology that makes clear its central role in both historical and contemporary debates. Most scientific explanations are causal. This is certainly the case in evolutionary biology, which seeks to explain the diversity of life and the adaptive fit between organisms and their surroundings. The nature of causation in evolutionary biology, however, is contentious. How causation is understood shapes the structure of evolutionary theory, and historical and contemporary debates in evolutionary biology (...) have revolved around the nature of causation. Despite its centrality, and differing views on the subject, the major conceptual issues regarding the nature of causation in evolutionary biology are rarely addressed. This volume fills the gap, bringing together biologists and philosophers to offer a comprehensive, interdisciplinary treatment of evolutionary causation. Contributors first address biological motivations for rethinking evolutionary causation, considering the ways in which development, extra-genetic inheritance, and niche construction challenge notions of cause and process in evolution, and describing how alternative representations of evolutionary causation can shed light on a range of evolutionary problems. Contributors then analyze evolutionary causation from a philosophical perspective, considering such topics as causal entanglement, the commingling of organism and environment, and the relationship between causation and information. Contributors John A. Baker, Lynn Chiu, David I. Dayan, Renée A. Duckworth, Marcus W Feldman, Susan A. Foster, Melissa A. Graham, Heikki Helanterä, Kevin N. Laland, Armin P. Moczek, John Odling-Smee, Jun Otsuka, Massimo Pigliucci, Arnaud Pocheville, Arlin Stoltzfus, Karola Stotz, Sonia E. Sultan, Christoph Thies, Tobias Uller, Denis M. Walsh, Richard A. Watson. (shrink)

We are grateful to the commentators for taking the time to respond to our article. Too many interesting and important points have been raised for us to tackle them all in this response, and so in the below we have sought to draw out the major themes. These include problems with both the term ‘ultimate causation’ and the proximate-ultimate causation dichotomy more generally, clarification of the meaning of reciprocal causation, discussion of issues related to the nature of development and phenotypic (...) plasticity and their roles in evolution, and consideration of the need for an extended evolutionary synthesis. (shrink)

Evolutionary biology is paying increasing attention to the mechanisms that enable phenotypic plasticity, evolvability, and extra‐genetic inheritance. Yet, there is a concern that these phenomena remain insufficiently integrated within evolutionary theory. Understanding their evolutionary implications would require focusing on phenotypes and their variation, but this does not always fit well with the prevalent genetic representation of evolution that screens off developmental mechanisms. Here, we instead use development as a starting point, and represent it in a way that allows genetic, environmental (...) and epigenetic sources of phenotypic variation to be independent. We show why this representation helps to understand the evolutionary consequences of both genetic and non‐genetic phenotype determinants, and discuss how this approach can instigate future areas of empirical and theoretical research. (shrink)

Biologists rely on theories, apply models and construct explanations, but rarely reflect on their nature and structure. This book introduces key topics in philosophy of science to provide the required philosophical background for this kind of reflection, which is an important part of all aspects of research and communication in biology. It concisely and accessibly addresses fundamental questions such as: Why should biologists care about philosophy of science? How do concepts contribute to scientific advancement? What is the nature of scientific (...) controversies in the biological sciences? Chapters draw on contemporary examples and case studies from across biology, making the discussion relevant and insightful. Written for researchers and advanced undergraduate and graduate students across the life sciences, its aim is to encourage readers to become more philosophically minded and informed to enable better scientific practice. It is also an interesting and pertinent read for philosophers of science. (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)

The presence of various mechanisms of non-genetic inheritance is one of the main problems for current evolutionary theory according to several critics. Sufficient empirical and conceptual reasons exist to take this claim seriously, but there is little consensus on the implications of multiple inheritance systems for evolutionary processes. Here we use the Price Equation as a starting point for a discussion of the differences between four recently proposed categories of inheritance systems; genetic, epigenetic, behavioral and symbolic. Specifically, we address how (...) the components of the Price Equation encompass different non-genetic systems of inheritance in an attempt to clarify how the different systems are conceptually related. We conclude that the four classes of inheritance systems do not form distinct clusters with respect to their effect on the rate and direction of phenotypic change from one generation to the next in the absence or presence of selection. Instead, our analyses suggest that different inheritance systems can share features that are conceptually very similar, but that their implications for adaptive evolution nevertheless differ substantially as a result of differences in their ability to couple selection and inheritance. (shrink)

Parents influence the development of their offspring in many ways beyond the transmission of DNA. This includes transfer of epigenetic states, nutrients, antibodies and hormones, and behavioural interactions after birth. While the evolutionary consequences of such nongenetic inheritance are increasingly well understood, less is known about how inheritance mechanisms evolve. Here, we present a simple but versatile model to explore the adaptive evolution of non-genetic inheritance. Our model is based on a switch mechanism that produces alternative phenotypes in response to (...) different inputs, including genes and non-genetic factors transmitted from parents and the environment experienced during development. This framework shows how genetic and non-genetic inheritance mechanisms and environmental conditions can act as cues by carrying correlational information about future selective conditions. Differential use of these cues is manifested as different degrees of genetic, parental or environmental morph determination. We use this framework to evaluate the conditions favouring non-genetic inheritance, as opposed to genetic determination of phenotype or within-generation plasticity, by applying it to two putative examples of adaptive non-genetic inheritance: maternal effects on seed germination in plants and transgenerational phase shift in desert locusts. Our simulation models show how the adaptive value of non-genetic inheritance depends on its mechanism, the pace of environmental change, and life history characteristics. (shrink)

Individuals are often restricted to indirect cues when assessing the mate value of a potential partner. Females of some species have been shown to copy each other’s choice; in other words, the probability of a female choosing a particular male increases if he has already been chosen by other females. Recently it has been suggested that mate-choice copying could be an important aspect of human mate choice as well. We tested one of the hypotheses, the so-called wedding ring effect—that women (...) would prefer men who are already engaged or married—in a series of live interactions between men and women. The results show that women do not find men signaling engagement, or being perceived as having a partner, more attractive or higher in socioeconomic status. Furthermore, signs of engagement did not influence the women’s reported willingness to engage in short-term or long-term relationships with the men. Thus, this study casts doubt on some simplified theories of human mate-choice copying, and alternative, more complex scenarios are outlined and discussed. (shrink)