A striking example of developmental bias in an evolutionary process: The “domestication syndrome”

The question of whether “developmental bias” can influence evolution is still controversial, despite much circumstantial evidence and a good theoretical argument. Here, I will argue that the domestication of mammalian species, which took place independently more than two dozen times, provides a particularly convincing example of developmental bias in evolution. The singular finding that underlies this claim is the repeated occurrence in domesticated mammals of a set of distinctive traits, none of which were deliberately selected. This phenomenon has been termed “the domestication syndrome”. In this article, I will: (a) describe the properties of the domestication syndrome; (b) show how it can be explained in terms of the operation of a specific genetic regulatory network, that which governs neural crest cell development; and (c) discuss Dmitry Belyaev's idea of “destabilizing selection,” which holds that selecting for a new behavior often entails neuroendocrine alterations that alter many aspects of development. Finally, I will argue for the potential general significance of such destabilizing selection, in combination with developmental bias, in animal evolution.     

Typology now: homology and developmental constraints explain evolvability

By linking the concepts of homology and morphological organization to evolvability, this paper attempts to (1) bridge the gap between developmental and phylogenetic approaches to homology and to (2) show that developmental constraints and natural selection are compatible and in fact complementary. I conceive of a homologue as a unit of morphological evolvability, i.e., as a part of an organism that can exhibit heritable phenotypic variation independently of the organism’s other homologues. An account of homology therefore consists in explaining how an organism’s developmental constitution results in different homologues/characters as units that can evolve independently of each other. The explanans of an account of homology is developmental, yet the very explanandum is an evolutionary phenomenon: evolvability in a character-by-character fashion, which manifests itself in phylogenetic patterns as recognized by phylogenetic approaches to homology. While developmental constraints and selection have often been viewed as antagonistic forces, I argue that both are complementary as they concern different parts of the evolutionary process. Developmental constraints, conceived of as the presence of the same set of homologues across phenotypic change, pertain to how heritable variation can be generated in the first place (evolvability), while natural selection operates subsequently on the produced variation.

Developmental bias in the fossil record

The role of developmental bias and plasticity in evolution is a central research interest in evolutionary biology. Studies of these concepts and related processes are usually conducted on extant systems and have seen limited investigation in the fossil record. Here, I identify plasticity‐led evolution (PLE) as a form of developmental bias accessible through scrutiny of paleontological material. I summarize the process of PLE and describe it in terms of the environmentally mediated accumulation and release of cryptic genetic variation. Given this structure, I then predict its manifestation in the fossil record, discuss its similarity to quantum evolution and punctuated equilibrium, and argue that these describe macroevolutionary patterns concordant with PLE. Finally, I suggest methods and directions towards providing evidence of PLE in the fossil record and conclude that such endeavors are likely to be highly rewarding.     

A different approach to validating screening assays for developmental toxicity

BACKGROUND: There continue to be many efforts around the world to develop assays that are shorter than the traditional embryofetal developmental toxicity assay, or use fewer or no mammals, or use less compound, or have all three attributes. Each assay developer needs to test the putative assay against a set of performance standards, which traditionally has involved testing the assays against a list of compounds that are generally recognized as “positive” or “negative” in vivo. However, developmental toxicity is highly conditional, being particularly dependent on magnitude (i.e. dose) and timing of exposure, which makes it difficult to develop lists of compounds neatly assigned as developmental toxicants or not. APPROACH: Here we offer an alternative approach for the evaluation of developmental toxicity assays based on exposures. Exposures are classified as “positive” or “negative” in a system, depending on the compound and the internal concentration. Although this linkage to “internal dose” departs from the recent approaches to validation, it fits well with widely accepted principles of developmental toxicology. CONCLUSIONS: This paper introduces this concept, discusses some of the benefits and drawbacks of such an approach, and lays out the steps we propose to implement it for the evaluation of developmental toxicity assays. Birth Defects Res (Part B) 89:526–530, 2010. © 2010 Wiley‐Liss, Inc.     

The Body Plan Concept and Its Centrality in Evo-Devo

A body plan is a suite of characters shared by a group of phylogenetically related animals at some point during their development. The concept of bauplane, or body plans, has played and continues to play a central role in the study of evolutionary developmental biology (evo-devo). Despite the importance of the body plan concept in evo-devo, many researchers may not be familiar with the progression of ideas that have led to our current understanding of body plans, and/or current research on the origin and maintenance of body plans. This lack of familiarity, as well as former ties between the body plan concept and metaphysical ideology is likely responsible for our underappreciation of the body plan concept in its own right, as well as its role in evo-devo. My aim in this review is to outline how we have arrived at our modern definition of body plan, the controversies associated with the concept, its role in evo-devo, and how current research is informing us on body plans. To this end, I integrate concepts such as the nature of phyla, the Cambrian explosion, constraint, evolvability, and results from recent research on gene regulatory networks with the much older concept of the body plan.     

Racialization: a defense of the concept

This paper defends the concept of racialization against its critics. As the concept has become increasingly popular, questions about its meaning and value have been raised, and a backlash against its use has occurred. I argue that when “racialization” is properly understood, criticisms of the concept are unsuccessful. I defend a definition of racialization and identify its companion concept, “racialized group.” Racialization is often used as a synonym for “racial formation.” I argue that this is a mistake. Racial formation theory is committed to racial ontology, but racialization is best understood as the process through which racialized – rather than racial – groups are formed. “Racialization” plays a unique role in the conceptual landscape, and it is a key concept for race eliminativists and anti-realists about race.     

Irretrievably confused? Innateness in explanatory context

The hunt for a biologically respectable definition for the folk concept of innateness is still on. I defend Ariew’s Canalization account of innateness against the criticisms of Griffiths and Machery, but highlight the remaining flaws in this proposal. I develop a new analysis based on the notion of environmental induction. A trait is innate, I argue, iff it is not environmentally induced. I augment this definition with a novel analysis of environmental induction that draws on the contrastive nature of causal explanation. Whether a trait is environmentally induced, I argue, depends on a context sensitive contrast class. I argue that a “Noninduction” analysis of innateness allows the concept an explanatory role in biology. I show how my proposal co-opts the successes of the Canalization account whilst avoiding its pitfalls, and I account for why biologists associate a range of disparate properties with innateness.     

What is a species? Essences and generation

Arguments against essentialism in biology rely strongly on a claim that modern biology abandoned Aristotle’s notion of a species as a class of necessary and sufficient properties. However, neither his theory of essentialism, nor his logical definition of species and genus (eidos and genos) play much of a role in biological research and taxonomy, including his own. The objections to natural kinds thinking by early twentieth century biologists wrestling with the new genetics overlooked the fact that species have typical developmental cycles and most have a large shared genetic component. These are the “what-it-is-to-be” members of that species. An intrinsic biological essentialism does not commit us to Aristotelian notions, nor even modern notions, of essence. There is a long-standing definition of “species” and its precursor notions that goes back to the Greeks, and which Darwin and pretty well all biologists since him share, that I call the Generative Conception of Species. It relies on there being a shared generative power that makes progeny resemble parents. The “what-it-is-to-be” a member of that species is that developmental type, mistakes in development notwithstanding. Moreover, such “essences” have always been understood to include deviations from the type. Finally, I shall examine some implications of the collapse of the narrative about essences in biology.     

Quelques apports à la théorie de l’Évolution,de la « Synthèse orthodoxe » à la « Super synthèse évo-dévo » 1970–2009 : un point de vue

Some contributions to evolutionary theory, from the “orthodox” Synthesis to the “Evo-devo Super synthesis” 1970–2009: A point of view. The “Modern Synthesis” of evolutionary biology coalesced and revitalized evolutionary theory beginning in the 1930s. It stressed the explanatory power of natural selection and gradual change to account for the processes that govern natural populations today, as well as patterns in the history of life. In the past 40 years, the synthesis has been challenged on various fronts ranging from paleontology to developmental biology, systematics, biogeography, and molecular and developmental biology. Several of its central propositions have been modified and expanded as a result. How well the synthesis continues to be effective will depend on its continued ability to test its central propositions and the efficacy of its central mechanisms, particularly on the basis of new evidence from emerging fields of study.     

Mosaic evolution,preadaptation, and the evolution of evolvability in apes

A major goal in postsynthesis evolutionary biology has been to better understand how complex interactions between traits drive movement along and facilitate the formation of distinct evolutionary pathways. I present analyses of a character matrix sampled across the haplorrhine skeleton that revealed several modules of characters displaying distinct patterns in macroevolutionary disparity. Comparison of these patterns to those in neurological development showed that early ape evolution was characterized by an intense regime of evolutionary and developmental flexibility. Shifting and reduced constraint in apes was met with episodic bursts in phenotypic innovation that built a wide array of functional diversity over a foundation of shared developmental and anatomical structure. Shifts in modularity drove dramatic evolutionary changes across the ape body plan in two distinct ways: (1) an episode of relaxed integration early in hominoid evolution coincided with bursts in evolutionary rate across multiple character suites; (2) the formation of two new trait modules along the branch leading to chimps and humans preceded rapid and dramatic evolutionary shifts in the carpus and pelvis. Changes to the structure of evolutionary mosaicism may correspond to enhanced evolvability that has a “preadaptive” effect by catalyzing later episodes of dramatic morphological remodeling.     

Phenotypic variability can promote the evolution of adaptive plasticity by reducing the stringency of natural selection

Adaptive phenotypic plasticity is a potent but not ubiquitous solution to environmental heterogeneity, driving interest in what factors promote and limit its evolution. Here, a novel computational model representing stochastic information flow in development is used to explore evolution from a constitutive phenotype to an adaptively plastic response. Results show that populations tend to evolve robustness to developmental stochasticity, but that this evolved robustness limits evolvability; specifically, robust genotypes have less ability to evolve adaptive plasticity when presented with a mix of both the ancestral environment and a new environment. Analytic calculations and computational experiments confirm that this constraint occurs when the initial mutational steps towards plasticity are pleiotropic, such that mutant fitnesses decline in the environment to which their parents are well‐adapted. Greater phenotypic variability improves evolvability in the model by lessening this decline as well as by improving the fitness of partial adaptations to the new environment. By making initial plastic mutations more palatable to natural selection, phenotypic variability can increase the evolvability of an innovative, plastic response without improving evolvability to simpler challenges such as a shifted optimum in a single environment. Populations that evolved robustness by negative feedback between the trait and its rate of change show a particularly strong constraining effect on the evolvability of plasticity, revealing another mechanism by which evolutionary history can limit later innovation. These results document a novel mechanism by which weakening selection could actually stimulate the evolution of a major innovation.     

Learning, evolvability and exploratory behaviour: extending the evolutionary reach of learning

Traditional accounts of the role of learning in evolution have concentrated upon its capacity as a source of fitness to individuals. In this paper I use a case study from invasive species biology—the role of conditioned taste aversion in mitigating the impact of cane toads on the native species of Northern Australia—to highlight a role for learning beyond this—as a source of evolvability to populations. This has two benefits. First, it highlights an otherwise under-appreciated role for learning in evolution that does not rely on social learning as an inheritance channel nor “special” evolutionary processes such as genetic accommodation (both of which many are skeptical about). Second, and more significantly, it makes clear important and interesting parallels between learning and exploratory behaviour in development. These parallels motivate the applicability of results from existing research into learning and learning evolution to our understanding the evolution of evolvability more generally.     

Extending the quasi-neutral concept

In caricature, the equilibrium paradigm of community ecology states that plant communities are stable entities consisting of competing species - and that such species coexist because each has its “niche”. This paradigm, in its extreme, has been dead for some time. Nevertheless, it has yet to be replaced by a credible “non” — equilibrium paradigm. The quasi-neutral concept of plant communities, proposed by Kristjan Zobel,Folia Geobot. 36: 3–8, 2001, possesses some of the key ingredients of a nonequilibrium theory of diversity. It recognizes that there are inescapable relationships between diversity at different scales, that similarity can influence the rate of competitive exclusion, that successional change is typically associated with changes in life form, and that rarefaction (i.e. “sampling artifacts”) can have strong effects on fine-scale diversity. However, the current formulation of the quasi-neutral concept is incomplete in that it relies on an unrealistic definition of community, it assumes that random sampling means that species richness at one scale will be linearly related to richness at finer scales, it ignores the possibility of fine-scale processes producing broader-scale patterns, and it avoids the subject of fine-scale environmental heterogeneity. But the most serious limitation of the quasi-neutral concept is that similarity of species alone is not sufficient to allow indefinite coexistence. I present the results of a simple simulation to demonstrate that: (1) identical species will eventually be lost from communities due to stochastic “drift”, (2) slight variations in reproductive rates accelerate this loss, but (3) adding a miniscule “cost of commonness” to the model allows the indefinite coexistence of species. I conclude that the quasi-neutral model cannot work without some kind of trade-off.     

Early usage and meaning of evolvability

Evolvability has become an enormously popular concept in evolutionary biology and in machine learning software architecture. While it is claimed that the term was coined in 1988 by Richard Dawkins, it was used as early as 1931 as a characteristic of life by John A. Thomson. We quote and review the earliest uses and definitions of evolvability in biological frameworks up until 1989, which are remarkably few. The meaning changed from simply the “ability to evolve” as a characteristic of life to various versions of including necessary variation to predict whether or not something could evolve to the rate and quality of that evolution. Or, meaning changed from the ability to evolve to the “quality” of the ability to evolve. Since then, evolvability has taken on many definitions as it has exploded in usage.     

THE EVOLUTION OF PHENOTYPIC CORRELATIONS AND “DEVELOPMENTAL MEMORY”

Development introduces structured correlations among traits that may constrain or bias the distribution of phenotypes produced. Moreover, when suitable heritable variation exists, natural selection may alter such constraints and correlations, affecting the phenotypic variation available to subsequent selection. However, exactly how the distribution of phenotypes produced by complex developmental systems can be shaped by past selective environments is poorly understood. Here we investigate the evolution of a network of recurrent nonlinear ontogenetic interactions, such as a gene regulation network, in various selective scenarios. We find that evolved networks of this type can exhibit several phenomena that are familiar in cognitive learning systems. These include formation of a distributed associative memory that can “store” and “recall” multiple phenotypes that have been selected in the past, recreate complete adult phenotypic patterns accurately from partial or corrupted embryonic phenotypes, and “generalize” (by exploiting evolved developmental modules) to produce new combinations of phenotypic features. We show that these surprising behaviors follow from an equivalence between the action of natural selection on phenotypic correlations and associative learning, well‐understood in the context of neural networks. This helps to explain how development facilitates the evolution of high‐fitness phenotypes and how this ability changes over evolutionary time.     

The effect of development on the direction of evolution: toward a twenty-first century consensus

Summary One of the most important questions in evolutionary biology is: what orients the evolutionary process? That is, what causes evolution to proceed toward certain developmental trajectories, and hence phenotypes, rather than others? In particular, there has been prolonged controversy over whether the direction of evolution is determined solely by external factors or whether the nature of the ontogenetic process, and the ways in which it can be altered by mutations in developmental genes, may also play a major role. Here, I examine this issue, concentrating on the following: the possible evolutionary orienting role of “developmental bias;” the question of whether selection can and/or will break bias; the extent to which bias is already incorporated in quantitative genetic studies; and ways of approaching the possible role of bias in the origin of evolutionary novelties. Finally, I suggest that developmental bias may provide a focal point for the coming together of conceptual and practical approaches to evo‐devo.     

Developmental bias,macroevolution, and the fossil record

A fuller understanding of the role of developmental bias in shaping large‐scale evolutionary patterns requires integrating bias (the probability distribution of variation accessible to an ancestral phenotype) with clade dynamics (the differential survival and production of species and evolutionary lineages). This synthesis could proceed as a two‐way exchange between the developmental data available to neontologists and the strictly phenotypic but richly historical and dynamic data available to paleontologists. Analyses starting in extant populations could aim to predict macroevolution in the fossil record from observed developmental bias, while analyses starting in the fossil record, particularly the record of extant species and lineages, could aim to predict developmental bias from macroevolutionary patterns, including the broad range of extinct phenotypes. Analyses in multivariate morphospaces are especially effective when coupled with phylogeny, theoretical and developmental models, and diversity–disparity plots. This research program will also require assessing the “heritability” of an ancestral bias across phylogeny, and the tendency for bias change in strength and orientation over evolutionary time. Such analyses will help find a set of general rules for the macroevolutionary effects of developmental bias, including its impact on and interactions with the other intrinsic and extrinsic factors governing the movement, expansion, and contraction of clades in morphospace.     

Modularity, evolvability, and adaptive radiations: a comparison of the hemi- and holometabolous insects

SUMMARY Despite recent attention given to the concept of modularity and its potential contribution to the evolvability of organisms, there has been little mention of how such a contribution may affect rates of diversification or how this would be assessed. A first key prediction is that lineages with relatively greater degrees of modularity in given traits should exhibit higher rates of diversification. Four general conditions for testing this prediction of the modular evolvability hypothesis are outlined here. The potential role of modularity as a deterministic factor in adaptive radiations is best examined by looking at historic patterns of diversification rather than just levels of extant diversity, the focus of most analyses of key innovations.
Recent developmental evidence supports the notion that phenotypes of juvenile and adult stages of insects with "complete" metamorphosis (Holometabola) are distinct developmental and evolvable modules compared to the highly correlated life stages of insects with "incomplete" metamorphosis (Hemimetabola). Family-level rates of diversification for these two groups were calculated from the fossil record. The Holometabola was found to have a significantly and characteristically higher rate of diversification compared to the less modular Hemimetabola, consistent with the idea that intrinsic differences in modularity can influence the long-term evolvability of organisms.
The modular evolvability hypothesis also makes a second key prediction: that characters in more modular clades will exhibit greater levels of variation due to their independence. This provides an independent, phenotypically based test of the hypothesis. We discuss here how this second prediction may be tested in the case of the Hemi- and Holometabola.