The broader evolutionary lessons to be learned from a comparative and phylogenetic analysis of primate muscle morphology

The present publication reviews the broader evolutionary implications of our long‐term study of primate musculature. It summarizes the implications of the study for our understanding of the use of myological characters for phylogenetic reconstruction, for assessing the importance of homoplasy and reversions in evolution, and for our understanding of Dollo's law, the notion of ‘direction’ in evolution, the common myth of human complexity, the tempo and mode of primate and human evolutionary history, adaptive radiations, the notion that ‘common’ equals ‘primitive’ and the influence of morphogenesis on the variability of head, neck, pectoral and upper limb muscles. Among other results our study shows that myological characters are useful for phylogenetic reconstruction. The results also stress the importance of homoplasy and of evolutionary reversions in morphological evolution, and they provide examples of reversions that violate Dollo's law due to the retention of ancestral developmental pathways. They also show that contrary to the idea of a ‘general molecular slow‐down of hominoids’ the rates of muscle evolution at the nodes leading to and within the hominoid clade are higher than those in most other primate clades. However, there is no evidence of a general trend or ‘directionality’ towards an increasing complexity during the evolutionary history of hominoids and of modern humans in particular, at least regarding the number of muscles or of muscle bundles. The rates of muscle evolution at the major euarchontan and primate nodes are different, but within each major primate clade (Strepsirrhini, Platyrrhini, Cercopithecidae and Hominoidea) the rates at the various nodes, and particularly at the nodes leading to the higher groups (i.e. those including more than one genus) are strikingly similar. Our results also support, in general terms, the assumption that ‘common is primitive’ and they lend some support for the ‘vertebrate‐specific model’ in the sense that during the divergent events that resulted in these four major primate clades there was more emphasis on postcranial changes than on cranial changes. Our study of primates does not, however, support suggestions that the distal structures of the upper limb are more prone to variation than the proximal ones, or that the topological origins of the upper limb muscles are more prone to evolutionary change than their insertions.     

Eco‐evolutionary feedbacks between private and public goods: evidence from toxic algal blooms

The importance of ‘eco‐evolutionary feedbacks’ in natural systems is currently unclear. Here, we advance a general hypothesis for a particular class of eco‐evolutionary feedbacks with potentially large, long‐lasting impacts in complex ecosystems. These eco‐evolutionary feedbacks involve traits that mediate important interactions with abiotic and biotic features of the environment and a self‐driven reversal of selection as the ecological impact of the trait varies between private (small scale) and public (large scale). Toxic algal blooms may involve such eco‐evolutionary feedbacks due to the emergence of public goods. We review evidence that toxin production by microalgae may yield ‘privatised’ benefits for individual cells or colonies under pre‐ and early‐bloom conditions; however, the large‐scale, ecosystem‐level effects of toxicity associated with bloom states yield benefits that are necessarily ‘public’. Theory predicts that the replacement of private with public goods may reverse selection for toxicity in the absence of higher level selection. Indeed, blooms often harbor significant genetic and functional diversity: bloom populations may undergo genetic differentiation over a scale of days, and even genetically similar lineages may vary widely in toxic potential. Intriguingly, these observations find parallels in terrestrial communities, suggesting that toxic blooms may serve as useful models for eco‐evolutionary dynamics in nature. Eco‐evolutionary feedbacks involving the emergence of a public good may shed new light on the potential for interactions between ecology and evolution to influence the structure and function of entire ecosystems.     

A levels-of-selection approach to evolutionary individuality

What changes when an evolutionary transition in individuality takes place? Many different answers have been given, in respect of different cases of actual transition, but some have suggested a general answer: that a major transition is a change in the extent to which selection acts at one hierarchical level rather than another. The current paper evaluates some different ways to develop this general answer as a way to characterise the property ‘evolutionary individuality’; and offers a justification of the option taken in Clarke (J Philos 110(8):413–435, 2013)—to define evolutionary individuality in terms of an object’s capacity to undergo selection at its own level. In addition, I suggest a method by which the property can be measured and argue that a problem which is often considered to be fatal to that method—the problem of ‘cross-level by-products’—can be avoided.     

Methodological and contextual factors in the Dawkins/Gould dispute over evolutionary progress

Biologists Richard Dawkins and Stephen Jay Gould have recently extended their decades-old disagreements about evolution to the issue of the nature and reality of evolutionary progress. According to Gould, ‘progress’ is a noxious notion that deserves to be expunged from evolutionary biology. In Dawkins' view, on the other hand, progress is one of the most important, pervasive and inevitable aspects of evolution. Simple appeals to ‘the evidence’ are clearly insufficient to resolve this disagreement, since it is precisely the interpretation of the evidence that is in dispute. Scientific controversies in general, and the Dawkins/Gould dispute over evolutionary progress in particular, are worth examining in some detail because doing so sheds light on the interconnected roles of methodological and contextual factors in the formation, articulation and defense of scientific claims. My aim in this paper is to clarify the structure of the Dawkins/Gould dispute by analyzing it in terms of a tri-level model of scientific controversies, involving ‘top-level’ substantive disagreements, ‘middle-level’ methodological differences, and ‘bottom-level’ differences in historical and social factors. This simple three-tiered model is sufficiently abstract to have more general applicability to other scientific controversies.     

The evolutionary significance of wing dimorphism in carabid beetles (Coleoptera: Carabidae)

A review of data on the background of wing dimorphism in carabid beetles (Coleoptera: Carabidae) and especially of the closely relatedCalathus cinctus andC. melanocephalus is given. In bothCalathus species wing dimorphism is inherited in a simple Mendelian fashion with the brachypterous condition dominant, but inC. melanocephalus the expression of the long winged genotype is under environmental control as well. The development of long winged phenotypes in the latter species is favoured by relatively favourable environmental conditions, such as high temperatures and a high food-supply. The higher fecundity of the larger and heavier long winged females of both species may compensate for losses of long winged phenotypes by flight activities. The evolutionary significance of both types of inheritance is discussed in relation to dispersal. The ‘fixed type’ as found inC. cinctus is considered an opportunistic short term ‘between sites strategy’, whereas the ‘dynamic type’ ofC. melanocephalus represents a flexible long term ‘within sites strategy’.     

More on how and why: cause and effect in biology revisited

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.     

The genomic basis of eco‐evolutionary dynamics

Recent recognition that ecological and evolutionary processes can operate on similar timescales has led to a rapid increase in theoretical and empirical studies on eco‐evolutionary dynamics. Progress in the fields of evolutionary biology, genomics and ecology is greatly enhancing our understanding of rapid adaptive processes, the predictability of adaptation and the genetics of ecologically important traits. However, progress in these fields has proceeded largely independently of one another. In an attempt to better integrate these fields, the centre for ‘Adaptation to a Changing Environment’ organized a conference entitled ‘The genomic basis of eco‐evolutionary change’ and brought together experts in ecological genomics and eco‐evolutionary dynamics. In this review, we use the work of the invited speakers to summarize eco‐evolutionary dynamics and discuss how they are relevant for understanding and predicting responses to contemporary environmental change. Then, we show how recent advances in genomics are contributing to our understanding of eco‐evolutionary dynamics. Finally, we highlight the gaps in our understanding of eco‐evolutionary dynamics and recommend future avenues of research in eco‐evolutionary dynamics.     

The evolutionary history of the ‘alba’ polymorphism in the butterfly subfamily Coliadinae (Lepidoptera: Pieridae)

Polymorphisms are common in the natural world and have played an important role in our understanding of how selection maintains multiple phenotypes within extant populations. Studying the evolutionary history of polymorphisms has revealed important features of this widespread form of phenotypic diversity, including its role in speciation, niche breadth, and range size. In the present study, we examined the evolutionary history of a ubiquitous colour polymorphism in the sulphur butterflies (subfamily: Coliadinae) termed the ‘alba’ polymorphism. We investigated the origin and stability of the ‘alba’ polymorphism using ancestral state reconstruction analysis. Our results indicate that the ancestor of the Coliadinae was polymorphic and that this polymorphism has undergone repeated transitions to monomorphism. Repeated loss of polymorphism suggests that the ‘alba’ polymorphism may be relatively unstable over evolutionary time. These results provide a framework for future studies on the origin and maintenance of the ‘alba’ polymorphism and guide the direction of future hypotheses. We discuss these results in light of current understandings of how the ‘alba’ polymorphism is maintained in extant populations.     

Accidental experiments: ecological and evolutionary insights and opportunities derived from global change

Humans are the dominant ecological and evolutionary force on the planet today, transforming habitats, polluting environments, changing climates, introducing new species, and causing other species to decline in number or go extinct. These worrying anthropogenic impacts, collectively termed global change, are often viewed as a confounding factor to minimize in basic studies and a problem to resolve or quantify in applied studies. However, these ‘accidental experiments’ also represent opportunities to gain fundamental insight into ecological and evolutionary processes, especially when they result in perturbations that are large or long in duration and difficult or unethical to impose experimentally. We demonstrate this by describing important fundamental insights already gained from studies which utilize global change factors as accidental experiments. In doing so, we highlight why accidental experiments are sometimes more likely to yield insights than traditional approaches. Next, we argue that emerging environmental problems can provide even more opportunities for scientific discovery in the future, and provide both examples and guidelines for moving forward. We recommend 1) a greater flow of information between basic and applied subfields of ecology and evolution to identify emerging opportunities; 2) considering the advantages of the ‘accidental experiment’ approach relative to more traditional approaches; and 3) planning for the challenges inherent to uncontrolled accidental experiments. We emphasize that we do not view the accidental experiments provided by global change as replacements for scientific studies quantifying the magnitude of anthropogenic impacts or outlining strategies for mitigating impacts. Instead, we believe that accidental experiments are uniquely situated to provide insights into evolutionary and ecological processes that ultimately allow us to better predict and manage change on our human‐dominated planet. Synthesis Humans have an increasingly large impact on the planet. In response, ecologists and evolutionary biologists are dedicating increasing scientific attention to global change, largely with studies documenting biological effects and testing strategies to avoid or reverse negative impacts. In this article, we analyze global change from a different perspective, and suggest that human impacts on the environment also serve as valuable ‘accidental experiments’ that can provide fundamental scientific insight. We highlight and synthesize examples of studies taking this approach, and give guidance for gaining future insights from these unfortunate ‘accidental experiments’.     

Editorial policy and Notes for authors

Modern accounts of evolutionary mechanism pay little attention to the pattern and logic of Darwin's explanation, but recognition of the logic of Darwin's explanation has significance for our understanding of evolution and for our appreciation of the extent to which Darwin's concept of evolutionary mechanism accords with modern evolutionary thought. Also, Darwin's explanation exemplifies the concept of a scientific ‘law’ and thus is of considerable value in helping learners to understand the nature of scientific explanation.     

The cambrian evolutionary ‘explosion’ recalibrated

The sudden appearance in the fossil record of the major animal phyla apparently records a phase of unparalleled, rapid evolution at the base of the Cambrian period, 545 Myr ago. This has become known as the Cambrian evolutionary ‘explosion’, and has fuelled speculation about unique evolutionary processes operating at that time. The acceptance of the palaeontological evidence as a true reflection of the evolutionary narrative has been criticised in two ways: from a reappraisal of the phylogenetic relationships of the early fossils, and from predicitions of molecular divergence times, based on six appropriate metazoan genes. Phylogenetic analysis of the arthropods implies an earlier, Precambrian history for most clades, and hence an extensive period of cladogenesis unrecorded by fossils. A similar argument can be applied to molluscs, lophophorates and deuterostomes. Molecular evidence implies divergence between clades to at least 1000 Myr ago. The apparent paradox between the sudden appearance of recognisable metazoans and their extended evolutionary history might be explained by a sudden Cambrian increase in body size, which was accompanied by skeletisation. A new paradigm suggests that the ‘explosion’ in the record may have been decoupled from the evolutionary innovation.     

Models of parent-offspring conflict. IV. Suppression: Evolutionary retaliation by the parent

We have earlier analysed ESSs for the amount of parental investment (PI) that offspring are expected to solicit from their parents, given that parents acquiesce to offspring demands. The present paper considers evolutionary retaliation by the parent for species where only one parent provides PI. Two genetic loci are envisaged: one (the ‘conflictor’ locus) determines the extent of offspring solicitation; the other (the ‘suppressor’ locus) determines how parents retaliate. Solicitation is assumed to carry a cost which may affect a particular offspring uniquely if time and energy are the major costs, or may affect all offspring in a brood equally if the main cost is predation risk. Two kinds of parental retaliation are possible. Parents may supply PI in proportion to offspring demands, or may ignore solicitation altogether and give a fixed PI. Analytical models of conflict in which the parent supplies PI in proportion to solicitation yield pure ESSs with PI at a compromise level between parent and offspring interests. These are termed ‘pro rata’ ESSs. Where solicitation costs are high, an ‘offspring wins’ ESS (offspring get all they ‘want’) is possible especially for forms of conflict that affect future sibs, and a ‘parent wins’ ESS (parent supplies its optimum) is possible especially for conflict that affects contemporary sibs. When parental retaliation takes the form of ignoring offspring solicitation, this can lead to a ‘parent wins’ ESS if costs of ignoring solicitation are negligible, but where parental insensitivity carries costs, the result is an unresolvable evolutionary chase with cycling frequencies of alleles coding for parent and offspring strategies. ‘Pro rata’ ESSs cannot be invaded by ‘ignore solicitation’ mutants but ‘pro rata’ mutants can often invade at certain stages in ‘ignore solicitation’ limit cycles. We therefore conclude that the probable evolutionary end product for most species will be the ‘pro rata’ ESS in which the parent supplies more PI than would be optimal in the absence of conflict, but less PI than would be an ESS for the offspring in the absence of parental retaliation. Such ESSs will be characterized by solicitation costs; offspring will ‘ask’ for more PI than they get. In nature, under similar conditions, highest conflict will occur when both parents sustain equally the effects of conflict, or when conflict affects contemporary rather than future sibs.     

Origins of evolutionary transitions

An ‘evolutionary transition in individuality’ or ‘major transition’ is a transformation in the hierarchical level at which natural selection operates on a population. In this article I give an abstract (i.e. level-neutral and substrate-neutral) articulation of the transition process in order to precisely understand how such processes can happen, especially how they can get started.     

‘The Miserablest People in the World’: Race,Humanism and the Australian Aborigine

This paper considers how an idea of the Australian Aborigine impacted upon the development of racial thinking throughout the nineteenth century. We distinguish three phases of this development. Against the background of what was considered to be a distinctly human capacity to rise above nature, our central argument however is that the extreme and irremediable savagery attributed to the Aborigine led to the mid‐nineteenth shift to a polygenist, or an innatist, idea of race. The first part of our discussion, covering the early 1800s, elicits a specifically humanist puzzlement at the unimproved condition of the Aborigines. But, as we will show in the central part of our discussion, it was not only the Aborigines' inclination but their capacity for ‘improvement’ that came to be doubted. Challenging the very basis upon which ‘the human’ had been defined, and the unity of humankind assumed, the Aborigine could not be accommodated within a prevailing conception of racial difference as a mere variety of the human. The elaboration of polygenism may therefore be understood as arising out of this humanist incomprehension: as an attempt to account for the ontologically inexplicable difference of the Australian Aborigine. In the final part of our discussion, we trace the legacy of the Aborigine's place within polygenism through the evolutionary thought of the late nineteenth century. Despite an explicit return to monogenism, here the Aborigine is invoked to support the claim that race constitutes a more or less permanent difference and, for certain races, a more or less permanent deficiency. And as, in these terms, the anomalous Aborigine became an anachronism, so Australia's indigenous peoples came to embody the most devastating conclusion of evolutionary thought: that in the human struggle for existence certain races were destined not even to survive.     

Divergent evolutionary processes associated with colonization of offshore islands

Oceanic islands have been a test ground for evolutionary theory, but here, we focus on the possibilities for evolutionary study created by offshore islands. These can be colonized through various means and by a wide range of species, including those with low dispersal capabilities. We use morphology, modern and ancient sequences of cytochrome b (cytb) and microsatellite genotypes to examine colonization history and evolutionary change associated with occupation of the Orkney archipelago by the common vole (Microtus arvalis), a species found in continental Europe but not in Britain. Among possible colonization scenarios, our results are most consistent with human introduction at least 5100 bp (confirmed by radiocarbon dating). We used approximate Bayesian computation of population history to infer the coast of Belgium as the possible source and estimated the evolutionary timescale using a Bayesian coalescent approach. We showed substantial morphological divergence of the island populations, including a size increase presumably driven by selection and reduced microsatellite variation likely reflecting founder events and genetic drift. More surprisingly, our results suggest that a recent and widespread cytb replacement event in the continental source area purged cytb variation there, whereas the ancestral diversity is largely retained in the colonized islands as a genetic ‘ark’. The replacement event in the continental M. arvalis was probably triggered by anthropogenic causes (land‐use change). Our studies illustrate that small offshore islands can act as field laboratories for studying various evolutionary processes over relatively short timescales, informing about the mainland source area as well as the island.     

Development of evolutionary biomedicine as a novel direction of biological science

This review analyzes the data obtained for the last decade on invertebrate animals (insects, round worms, molluscs) as models of various human diseases. As illustration, there are considered advances in studying of the invertebrate system of insulin-like peptides and signaling mechanisms of their action—evolutionary conservative homologues of the mammalian insulin/IGF-1 system. Results are presented of studies on the nematode Caenorhabditis elegans, Drosophila Drosophila melanogaster, and mollusks, which “model” individual aspects of some human diseases—diabetes, neurodegenerative dysfunction, carcinogenesis, as well as aging. A conclusion is made about the development of a new, synthetic direction combining evolutionary science and molecular biology and medicine, which we call evolutionary biomedicine. The roots of the appearance of this synthetic direction are to be searched for in L.A. Orbeli’s evolutionary ideas, methods, and scientific predictions.     

Pyrogeography,historical ecology,and the human dimensions of fire regimes

In our 2011 synthesis (Bowman et al., Journal of Biogeography, 2011, 38 , 2223–2236), we argued for a holistic approach to human issues in fire science that we term ‘pyrogeography’. Coughlan & Petty (Journal of Biogeography, 2013, 40 , 1010–1012) critiqued our paper on the grounds that our ‘pyric phase’ model was built on outdated views of cultural development, claiming we developed it to be the unifying explanatory framework for all human–fire sciences. Rather, they suggest that ‘historical ecology’ could provide such a framework. We used the ‘pyric transition’ for multiple purposes but did not offer it as an exclusive explanatory framework for pyrogeography. Although ‘historical ecology’ is one of many useful approaches to studying human–fire relationships, scholars should also look to political and evolutionary ecology, ecosystems and complexity theories, as well as empirical generalizations to build an interdisciplinary fire science that incorporates human, ecological and biophysical dimensions of fire regimes.     

A conceptual framework of evolutionary novelty and innovation

Since 1990 the recognition of deep homologies among metazoan developmental processes and the spread of more mechanistic approaches to developmental biology have led to a resurgence of interest in evolutionary novelty and innovation. Other evolutionary biologists have proposed central roles for behaviour and phenotypic plasticity in generating the conditions for the construction of novel morphologies, or invoked the accessibility of new regions of vast sequence spaces. These approaches contrast with more traditional emphasis on the exploitation of ecological opportunities as the primary source of novelty. This definitional cornucopia reflects differing stress placed on three attributes of novelties: their radical nature, the generation of new taxa, and ecological and evolutionary impact. Such different emphasis has led to conflating four distinct issues: the origin of novel attributes (genes, developmental processes, phenotypic characters), new functions, higher clades and the ecological impact of new structures and functions. Here I distinguish novelty (the origin of new characters, deep character transformations, or new combinations) from innovation, the ecological and evolutionary success of clades. Evidence from the fossil record of macroevolutionary lags between the origin of a novelty and its ecological success demonstrates that novelty may be decoupled from innovation, and only definitions of novelty based on radicality (rather than generativity or consequentiality) can be assessed without reference to the subsequent history of the clade to which a novelty belongs. These considerations suggest a conceptual framework for novelty and innovation, involving: (i) generation of the potential for novelty; (ii) the formation of novel attributes; (iii) refinement of novelties through adaptation; (iv) exploitation of novelties by a clade, which may coincide with a new round of ecological or environmental potentiation; followed by (v) the establishment of innovations through ecological processes. This framework recognizes that there is little empirical support for either the dominance of ecological opportunity, nor abrupt discontinuities (often caricatured as ‘hopeful monsters’). This general framework may be extended to aspects of cultural and social innovation.     

Urban evolutionary ecology brings exaptation back into focus

The contribution of pre-existing phenotypic variation to evolution in novel environments has long been appreciated. Nevertheless, evolutionary ecologists have struggled with communicating these aspects of the adaptive process. In 1982, Gould and Vrba proposed terminology to distinguish character states shaped via natural selection for the roles they currently serve (‘adaptations’) from those shaped under preceding selective regimes (‘exaptations’), with the intention of replacing the inaccurate ‘preadaptation’. Forty years later, we revisit Gould and Vrba’s ideas which, while often controversial, continue to be widely debated and highly cited. We use the recent emergence of urban evolutionary ecology as a timely opportunity to reintroduce the ideas of Gould and Vrba as an integrated framework to understand contemporary evolution in novel environments.