Mutation and evolution: Conceptual possibilities.

Although random mutation is central to models of evolutionary change, a lack of clarity remains regarding the conceptual possibilities for thinking about the nature and role of mutation in evolution. We distinguish several claims at the intersection of mutation, evolution, and directionality and then characterize a previously unrecognized category: complex conditioned mutation. Empirical evidence in support of this category suggests that the historically famous fluctuation test should be revisited, and new experiments should be undertaken with emerging experimental techniques to facilitate detecting mutation rates within specific loci at an ultra-high, individual base pair resolution.

Reframing research on evolutionary novelty and co-option: Character identity mechanisms versus deep homology.

A central topic in research at the intersection of development and evolution is the origin of novel traits. Despite progress on understanding how developmental mechanisms underlie patterns of diversity in the history of life, the problem of novelty continues to challenge researchers. Here we argue that research on evolutionary novelty and the closely associated phenomenon of co-option can be reframed fruitfully by: (1) specifying a conceptual model of mechanisms that underwrite character identity, (2) providing a richer and more empirically precise notion of co-option that goes beyond common appeals to "deep homology", and (3) attending to the nature of experimental interventions that can determine whether and how the co-option of identity mechanisms can help to explain novel character origins. This reframing has the potential to channel future investigation to make substantive progress on the problem of evolutionary novelty. To illustrate this potential, we apply our reframing to two case studies: treehopper helmets and beetle horns.

The Paradox of Predictability Provides a Bridge Between Micro- and Macroevolution.

The relationship between the evolutionary dynamics observed in contemporary populations (microevolution) and evolution on timescales of millions of years (macroevolution) has been a topic of considerable debate. Historically, this debate centers on inconsistencies between microevolutionary processes and macroevolutionary patterns. Here, we characterize a striking exception: emerging evidence indicates that standing variation in contemporary populations and macroevolutionary rates of phenotypic divergence are often positively correlated. This apparent consistency between micro- and macroevolution is paradoxical because it contradicts our previous understanding of phenotypic evolution and is so far unexplained. Here, we explore the prospects for bridging evolutionary timescales through an examination of this "paradox of predictability." We begin by explaining why the divergence-variance correlation is a paradox, followed by data analysis to show that the correlation is a general phenomenon across a broad range of temporal scales, from a few generations to tens of millions of years. Then we review complementary approaches from quantitative-genetics, comparative morphology, evo-devo, and paleontology to argue that they can help to address the paradox from the shared vantage point of recent work on evolvability. In conclusion, we recommend a methodological orientation that combines different kinds of short-term and long-term data using multiple analytical frameworks in an interdisciplinary research program. Such a program will increase our general understanding about how evolution works within and across timescales.

Corrigendum: Organizing Interdisciplinary Research on Purpose.

[This corrects the article DOI: 10.1093/biosci/biab128.].

Characterizing scientific failure: Putting the replication crisis in context.

A better understanding of the nature and causes of failure in research could inform policies to improve the reproducibility of biomedical research.

Stress-Induced Evolutionary Innovation: A Mechanism for the Origin of Cell Types.

Understanding the evolutionary role of environmentally induced phenotypic variation (i.e., plasticity) is an important issue in developmental evolution. A major physiological response to environmental change is cellular stress, which is counteracted by generic stress reactions detoxifying the cell. A model, stress-induced evolutionary innovation (SIEI), whereby ancestral stress reactions and their corresponding pathways can be transformed into novel structural components of body plans, such as new cell types, is described. Previous findings suggest that the cell differentiation cascade of a cell type critical to pregnancy in humans, the decidual stromal cell, evolved from a cellular stress reaction. It is hypothesized that the stress reaction in these cells was elicited ancestrally via inflammation caused by embryo attachment. The present study proposes that SIEI is a distinct form of plasticity-based evolutionary change leading to the origin of novel structures rather than adaptive transformation of pre-existing characters.

Evolution evolving? Reflections on big questions.

John Bonner managed a long and productive career that balanced specialized inquiry into cellular slime molds with general investigations of big questions in evolutionary biology, such as the origins of multicellular development and the evolution of complexity. This commentary engages with his final paper ("The evolution of evolution"), which argues that the evolutionary process has changed through the history of life. In particular, Bonner emphasizes the possibility that natural selection plays different roles at different size scales. I identify some underlying assumptions in his argument and evaluate its cogency to both foster future discussion and emulate the intellectual example set by Bonner over a lifetime. This endeavor is important beyond Bonner's own theoretical disposition because similar issues are visible in controversies about the possibility of an extended evolutionary synthesis.

John Tyler Bonner: Remembering a scientific pioneer.

Throughout his life, John Tyler Bonner contributed to major transformations in the fields of developmental and evolutionary biology. He pondered the evolution of complexity and the significance of randomness in evolution, and was instrumental in the formation of evolutionary developmental biology. His contributions were vast, ranging from highly technical scientific articles to numerous books written for a broad audience. This historical vignette gathers reflections by several prominent researchers on the greatness of John Bonner and the implications of his work.

Free Will, Determinism, and Intuitive Judgments About the Heritability of Behavior.

The fact that genes and environment contribute differentially to variation in human behaviors, traits and attitudes is central to the field of behavior genetics. Perceptions about these differential contributions may affect ideas about human agency. We surveyed two independent samples (N = 301 and N = 740) to assess beliefs about free will, determinism, political orientation, and the relative contribution of genes and environment to 21 human traits. We find that lay estimates of genetic influence on these traits cluster into four distinct groups, which differentially predict beliefs about human agency, political orientation, and religiosity. Despite apparent ideological associations with these beliefs, the correspondence between mean lay estimates and published heritability estimates for the surveyed traits is large (r = .77). Belief in genetic determinism emerges as a modest predictor of accuracy in these lay estimates. Additionally, educated mothers with multiple children emerge as particularly accurate in their estimates of the genetic contribution to these traits.

Rethinking Living Fossils.

Biologists would be mistaken if they relegated living fossils to paleontological inquiry or assumed that the concept is dead. It is now used to describe entities ranging from viruses to higher taxa, despite recent warnings of misleading inferences. Current work on character evolution illustrates how analyzing living fossils and stasis in terms of parts (characters) and wholes (e.g., organisms and lineages) advances our understanding of prolonged stasis at many hierarchical levels. Instead of viewing the concept's task as categorizing living fossils, we show how its primary role is to mark out what is in need of explanation, accounting for the persistence of both molecular and morphological traits. Rethinking different conceptions of living fossils as specific hypotheses reveals novel avenues for research that integrate phylogenetics, ecological and evolutionary modeling, and evo-devo to produce a more unified theoretical outlook.

Corrigendum: Rethinking Living Fossils.

[This corrects the article DOI: 10.1093/biosci/biy084.].

The significance and scope of evolutionary developmental biology: a vision for the 21st century.

Evolutionary developmental biology (evo-devo) has undergone dramatic transformations since its emergence as a distinct discipline. This paper aims to highlight the scope, power, and future promise of evo-devo to transform and unify diverse aspects of biology. We articulate key questions at the core of eleven biological disciplines-from Evolution, Development, Paleontology, and Neurobiology to Cellular and Molecular Biology, Quantitative Genetics, Human Diseases, Ecology, Agriculture and Science Education, and lastly, Evolutionary Developmental Biology itself-and discuss why evo-devo is uniquely situated to substantially improve our ability to find meaningful answers to these fundamental questions. We posit that the tools, concepts, and ways of thinking developed by evo-devo have profound potential to advance, integrate, and unify biological sciences as well as inform policy decisions and illuminate science education. We look to the next generation of evolutionary developmental biologists to help shape this process as we confront the scientific challenges of the 21st century.

Collaborative explanation, explanatory roles, and scientific explaining in practice.

Scientific explanation is a perennial topic in philosophy of science, but the literature has fragmented into specialized discussions in different scientific disciplines. An increasing attention to scientific practice by philosophers is (in part) responsible for this fragmentation and has put pressure on criteria of adequacy for philosophical accounts of explanation, usually demanding some form of pluralism. This commentary examines the arguments offered by Fagan and Woody with respect to explanation and understanding in scientific practice. I begin by scrutinizing Fagan's concept of collaborative explanation, highlighting its distinctive advantages and expressing concern about several of its assumptions. Then I analyze Woody's attempt to reorient discussions of scientific explanation around functional considerations, elaborating on the wider implications of this methodological recommendation. I conclude with reflections on synergies and tensions that emerge when the two papers are juxtaposed and how these draw attention to critical issues that confront ongoing philosophical analyses of scientific explanation.

Dimensions of integration in interdisciplinary explanations of the origin of evolutionary novelty.

Many philosophers of biology have embraced a version of pluralism in response to the failure of theory reduction but overlook how concepts, methods, and explanatory resources are in fact coordinated, such as in interdisciplinary research where the aim is to integrate different strands into an articulated whole. This is observable for the origin of evolutionary novelty-a complex problem that requires a synthesis of intellectual resources from different fields to arrive at robust answers to multiple allied questions. It is an apt locus for exploring new dimensions of explanatory integration because it necessitates coordination among historical and experimental disciplines (e.g., geology and molecular biology). These coordination issues are widespread for the origin of novel morphologies observed in the Cambrian Explosion. Despite an explicit commitment to an integrated, interdisciplinary explanation, some potential disciplinary contributors are excluded. Notable among these exclusions is the physics of ontogeny. We argue that two different dimensions of integration-data and standards-have been insufficiently distinguished. This distinction accounts for why physics-based explanatory contributions to the origin of novelty have been resisted: they do not integrate certain types of data and differ in how they conceptualize the standard of uniformitarianism in historical, causal explanations. Our analysis of these different dimensions of integration contributes to the development of more adequate and integrated explanatory frameworks.

Teleonomy: Revisiting a Proposed Conceptual Replacement for Teleology.

The concept of teleonomy has been attracting renewed attention recently. This is based on the idea that teleonomy provides a useful conceptual replacement for teleology, and even that it constitutes an indispensable resource for thinking biologically about purposes. However, both these claims are open to question. We review the history of teleological thinking from Greek antiquity to the modern period to illuminate the tensions and ambiguities that emerged when forms of teleological reasoning interacted with major developments in biological thought. This sets the stage for an examination of Pittendrigh's (Adaptation, natural selection, and behavior. In: Roe A, Simpson GG (eds) Behavior and evolution. Yale University Press, New Haven, pp 390-416, 1958) introduction of "teleonomy" and its early uptake in the work of prominent biologists. We then explore why teleonomy subsequently foundered and consider whether the term may yet have significance for discussions of goal-directedness in evolutionary biology and philosophy of science. This involves clarifying the relationship between teleonomy and teleological explanation, as well as asking how the concept of teleonomy impinges on research at the frontiers of evolutionary theory.

The hierarchical basis of serial homology and evolutionary novelty.

Given the pervasiveness of gene sharing in evolution and the extent of homology across the tree of life, why is everything not homologous with everything else? The continuity and overlapping genetic contributions to diverse traits across lineages seem to imply that no discrete determination of homology is possible. Although some argue that the widespread overlap in parts and processes should be acknowledged as "partial" homology, this threatens a broad base of presumed comparative morphological knowledge accepted by most biologists. Following a long scientific tradition, we advocate a strategy of "theoretical articulation" that introduces further distinctions to existing concepts to produce increased contrastive resolution among the labels used to represent biological phenomena. We pursue this strategy by drawing on successful patterns of reasoning from serial homology at the level of gene sequences to generate an enriched characterization of serial homology as a hierarchical, phylogenetic concept. Specifically, we propose that the concept of serial homology should be applied primarily to repeated but developmentally individualized body parts, such as cell types, differentiated body segments, or epidermal appendages. For these characters, a phylogenetic history can be reconstructed, similar to families of paralogous genes, endowing the notion of serial homology with a hierarchical, phylogenetic interpretation. On this basis, we propose a five-fold theoretical classification that permits a more fine-grained mapping of diverse trait-types. This facilitates answering the question of why everything is not homologous with everything else, as well as how novelty is possible given that any new character possesses evolutionary precursors. We illustrate the fecundity of our account by reference to debates over insect wing serial homologs and vertebrate paired appendages.

Conceptualizing evolutionary novelty: moving beyond definitional debates.

According to many biologists, explaining the evolution of morphological novelty and behavioral innovation are central endeavors in contemporary evolutionary biology. These endeavors are inherently multidisciplinary but also have involved a high degree of controversy. One key source of controversy is the definitional diversity associated with the concept of evolutionary novelty, which can lead to contradictory claims (a novel trait according to one definition is not a novel trait according to another). We argue that this diversity should be interpreted in light of a different epistemic role played by the concept of evolutionary novelty-the structuring of a problem space or setting of an explanatory agenda-rather than the concept's capacity to categorize traits as novel. This distinctive role is consistent with the definitional diversity and shows that the concept of novelty benefits ongoing investigation by focusing attention on answering different questions related to comprehending the origins of novelty. A review of recent theoretical and empirical work on evolutionary novelty confirms this interpretation.

Co-option of stress mechanisms in the origin of evolutionary novelties.

It is widely accepted that stressful conditions can facilitate evolutionary change. The mechanisms elucidated thus far accomplish this with a generic increase in heritable variation that facilitates more rapid adaptive evolution, often via plastic modifications of existing characters. Through scrutiny of different meanings of stress in biological research, and an explicit recognition that stressors must be characterized relative to their effect on capacities for maintaining functional integrity, we distinguish between: (1) previously identified stress-responsive mechanisms that facilitate evolution by maintaining an adaptive fit with the environment, and (2) the co-option of stress-responsive mechanisms that are specific to stressors leading to the origin of novelties via compensation. Unlike standard accounts of gene co-option that identify component sources of evolutionary change, our model documents the cost-benefit trade-offs and thereby explains how one mechanism-an immediate response to acute stress-is transformed evolutionarily into another-routine protection from recurring stressors. We illustrate our argument with examples from cell type origination as well as processes and structures at higher levels of organization. These examples suggest a general principle of evolutionary origination based on the capacity to switch between regulatory states related to reproduction and proliferation versus survival and differentiation.