Epigenetics and the maintenance of developmental plasticity: extending the signalling theory framework

Developmental plasticity, a phenomenon of importance in both evolutionary biology and human studies of the developmental origins of health and disease (DOHaD), enables organisms to respond to their environment based on previous experience without changes to the underlying nucleotide sequence. Although such phenotypic responses should theoretically improve an organism's fitness and performance in its future environment, this is not always the case. Herein, we first discuss epigenetics as an adaptive mechanism of developmental plasticity and use signaling theory to provide an evolutionary context for DOHaD phenomena within a generation. Next, we utilize signalling theory to identify determinants of adaptive developmental plasticity, detect sources of random variability – also known as process errors that affect maintenance of an epigenetic signal (DNA methylation) over time, and discuss implications of these errors for an organism's health and fitness. Finally, we apply life‐course epidemiology conceptual models to inform study design and analytical strategies that are capable of parsing out the potential effects of process errors in the relationships among an organism's early environment, DNA methylation, and phenotype in a future environment. Ultimately, we hope to foster cross‐talk and interdisciplinary collaboration between evolutionary biology and DOHaD epidemiology, which have historically remained separate despite a shared interest in developmental plasticity.     

Russian comparative embryology takes form: a conceptual metamorphosis toward “evo‐devo”

This essay recapitulates major paths followed by the Russian tradition of what we refer to today as evolutionary developmental biology (“evo‐devo”). The article addresses several questions regarding the conceptual history of evolutionary embryological thought in its particularly Russian perspective: (1) the assertion by the St. Petersburg academician Wolff regarding the possible connections between environmental modifications during morphogenesis and the “transformation” of species, (2) the discovery of shared “principles” underlying animal development by von Baer, (3) the experimental expression of Baer's principles by Kowalevsky and Mechnikoff, (4) Severtsov's theory of phylembryogenesis, (5) Filatov's approach to the study of evolution using comparative “developmental mechanics”, and (6) Shmalgausen's concept of “stabilizing” selection as an attempt to elucidate the evolution of developmental mechanisms. The focus on comparative evolutionary embryology, which was established by Kowalevsky and Mechnikoff, still continues to be popular in present‐day “evo‐devo” research in Russia.     

Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution

The postgenomics era will bring many changes to ecology and evolution. Information about genomic sequence and function provides a new foundation for organismal biology. The crucifer Arabidopsis thaliana and its wild relatives will play an important role in this synthesis of genomics and ecology. We discuss the need for model systems in ecology, the biology and relationships of crucifers, and the molecular resources available for these experiments. The scientific potential of this model system is illustrated by several recent studies in plant–insect interactions, developmental plasticity, comparative genomics and molecular evolution.     

Is there a special conservation biology?

Conservation biology is special to the extent that it fills useful roles in the scientific and conservation fields that are not being filled by practitioners of other disciplines. The emergence of the “new conservation biology” in the late 1970's and its blossoming in the 1980's and 1990's reflect, to a large degree, a failure of traditional academic ecology and the natural resource disciplines to address modern conservation problems adequately. Yet, to be successful conservation biology, as an interdisciplinary field, must build on the strengths of other disciplines both basic and applied. The new conservation biology grew out of concern over extinction of species, although the field has expanded to include issues about management of several levels of biological organization. I examine four controversial questions of importance to conservation biologists today: 1) are there any robust principles of conservation biology? 2) Is advocacy an appropriate activity of conservation biologists? 3) Are we educating conservation biologists properly? 4) Is conservation biology distinct from other biological and resource management disciplines? I answer three of these questions with a tentative “yes” and one (3) with a regretful “in most cases, no.” I see a need for broader Training for students of conservation biology, more emphasis on collecting basic field data, compelling applications of conservation biology to real problems, increased influence on policy, and expansion of the international scope of the discipline. If all these occur, conservation biology will by truly special.     

Styles of scientific reasoning: Adolf Remane (1898–1976) and the German evolutionary synthesis

Adolf Remane is widely considered to have been one of the most influential German zoologists of the 20th Century, yet Ernst Mayr persistently characterized him as an idealistic morphologist, that is, a typologist unable to understand population genetics or indeed Darwinian theory. This stands in sharp contrast to Mayr's praise for Bernhard Rensch as one of the most important German contributors to the Modern Synthesis of evolutionary theory. Remane's style of scientific reasoning is analysed in his writings on microsystematics, ecology, comparative morphology and phylogenetics and found to be highly consistent throughout these varied fields of research, while differing fundamentally from the eminently statistical foundations of both population genetics and natural selection theory that were embraced by Mayr. A comparative analysis of Rensch's understanding of science in general, and biology in particular, shows him to share core values with Remane, both authors rooted in the Mandarin tradition of the German professoriate. Biographical and socio‐political factors appear to have influenced Mayr's contrasting perception of Remane and Rensch, one that would influence later biologists and historians of science.     

Goldilocks’ Determination of What New In Vivo Data are “Just Right” for Different Common Drug Development Scenarios,Part 1

As alternative models and scientific advancements improve the ability to predict developmental toxicity, the challenge is how to best use this information to support safe use of pharmaceuticals in humans. While in vivo experimental data are often expected, there are other important considerations that drive the impact of developmental toxicity data to human risk assessment and product labeling. These considerations include three key elements: (1) the drug's likelihood of producing off‐target toxicities, (2) risk tolerance of adverse effects based on indication and patient population, and (3) how much is known about the effects of modulating the target in pregnancy and developmental biology. For example, there is little impact or value of a study in pregnant monkeys to inform the risk assessment for a highly specific monoclonal antibody indicated for a life‐threatening indication against a target known to be critical for pregnancy maintenance and fetal survival. In contrast, a small molecule to a novel biological target for a chronic lifestyle indication would warrant more safety data than simply in vitro studies and a literature review. Rather than accounting for innumerable theoretical possibilities surrounding each potential submission's profile, we consolidated most of the typical situations into eight possible scenarios across these three elements, and present a discussion of these scenarios here. We hope that this framework will facilitate a rational approach to determining what new information is required to inform developmental toxicity risk of pharmaceuticals in context of the specific needs of each program while reducing animal use where possible.     

Stability, sensitivity, science and heurism

We examine recently proposed justifications of sensitivity analysis sensu Wheeler (1995 ), here referred to as weighted‐classes sensitivity analysis (WCSA). We refute Giribet's (2003a) claim that WCSA is the strictest possible test for a given phylogenetic hypothesis. Giribet's (2003a) classification of data exploration methods as evaluating “nodal stability” or “nodal support” is arbitrary, at odds with common usage and actually obscures the relationships between the methods he examined, all of which seek to assess the sensitivity of results to variation in analytical conditions. Stability, whether statistical or taxonomic, is not a goal of phylogenetic science. Statistical stability necessarily involves trial repetition, which is impossible in ideographic sciences like phylogenetics. Taxonomic stability can be nothing more than an unintended by‐product of scientific inquiry, i.e., the repeated failure to refute a hypothesis. Schulmeister's (2003 ) “robust‐choice” defense of WCSA does not succeed in placing non‐arbitrary bounds on parameters, and her interpretation of this approach as simultaneously verificationist and falsificationist is logically inconsistent. WCSA is neither scientific nor heuristic and therefore does not contribute to the advancement of objective knowledge claims. © The Willi Hennig Society 2005.     

The extended evolutionary synthesis: its structure,assumptions and predictions

Scientific activities take place within the structured sets of ideas and assumptions that define a field and its practices. The conceptual framework of evolutionary biology emerged with the Modern Synthesis in the early twentieth century and has since expanded into a highly successful research program to explore the processes of diversification and adaptation. Nonetheless, the ability of that framework satisfactorily to accommodate the rapid advances in developmental biology, genomics and ecology has been questioned. We review some of these arguments, focusing on literatures (evo-devo, developmental plasticity, inclusive inheritance and niche construction) whose implications for evolution can be interpreted in two ways—one that preserves the internal structure of contemporary evolutionary theory and one that points towards an alternative conceptual framework. The latter, which we label the ‘extended evolutionary synthesis'' (EES), retains the fundaments of evolutionary theory, but differs in its emphasis on the role of constructive processes in development and evolution, and reciprocal portrayals of causation. In the EES, developmental processes, operating through developmental bias, inclusive inheritance and niche construction, share responsibility for the direction and rate of evolution, the origin of character variation and organism–environment complementarity. We spell out the structure, core assumptions and novel predictions of the EES, and show how it can be deployed to stimulate and advance research in those fields that study or use evolutionary biology.     

Fifty years of invasion ecology – the legacy of Charles Elton

The publication, in 1958, of Charles Elton's book The ecology of invasions by animals and plants launched the systematic study of biological invasions. Invasion ecology has grown to become an important multi‐disciplinary subfield of ecology with growing links to many other disciplines. This paper examines the citation history of Elton's book using the Web of Science. We also examine Elton's influence in shaping the current research agenda in invasion ecology, for which we use the 28 papers in a special issue of Diversity and Distributions (Volume 14: 2) as a representative sample. After 50 years, Elton's book remains the most cited single source in the field (> 1500 citations), and is cited more often every year (> 100 times) than any other invasion‐related publication, including influential papers in journals. Most citations to Elton's book refer to particular topics/concepts covered in the book, rather than citing it as a general reference about invasions. The shift in the distribution of topics/concepts cited with reference to Elton over time follows the same trend as for biogeography and ecology in general (increasing emphasis on analytical studies, multi‐scale analyses, multi‐disciplinary studies, etc.). Some topics emphasized by Elton are still the focus of current research (dispersal and spread of invasive organisms, impact on biodiversity, role of disturbance and enemy release) but several prominent themes in modern studies were not addressed by Elton. The emergence of new themes can be attributed to a general change in approach and emphasis underpinning research questions in conservation biogeography and applied ecology over the last half century (risk analysis, multi‐scale comparisons, propagule pressure, experimental approaches) and to the recent emergence and increasing availability of large data sets on the distribution of introduced species and to the emergence of key technologies (e.g. geographic information systems, modelling techniques, including niche‐based modelling, and molecular methods). Half a century after its publication, Charles Elton's book on invasions remains influential, but massive changes in the status of invasions and other environmental issues worldwide, together with advances in technology, are reshaping the game rules and priorities of invasion ecology.     

The evolution of molecular biology into systems biology

Systems analysis has historically been performed in many areas of biology, including ecology, developmental biology and immunology. More recently, the genomics revolution has catapulted molecular biology into the realm of systems biology. In unicellular organisms and well-defined cell lines of higher organisms, systems approaches are making definitive strides toward scientific understanding and biotechnological applications. We argue here that two distinct lines of inquiry in molecular biology have converged to form contemporary systems biology.     

Darwin's Galápagos finches in modern biology

One of the classic examples of adaptive radiation under natural selection is the evolution of 15 closely related species of Darwin''s finches (Passeriformes), whose primary diversity lies in the size and shape of their beaks. Since Charles Darwin and other members of the Beagle expedition collected these birds on the Galápagos Islands in 1835 and introduced them to science, they have been the subjects of intense research. Many biology textbooks use Darwin''s finches to illustrate a variety of topics of evolutionary theory, such as speciation, natural selection and niche partitioning. Today, as this Theme Issue illustrates, Darwin''s finches continue to be a very valuable source of biological discovery. Certain advantages of studying this group allow further breakthroughs in our understanding of changes in recent island biodiversity, mechanisms of speciation and hybridization, evolution of cognitive behaviours, principles of beak/jaw biomechanics as well as the underlying developmental genetic mechanisms in generating morphological diversity. Our objective was to bring together some of the key workers in the field of ecology and evolutionary biology who study Darwin''s finches or whose studies were inspired by research on Darwin''s finches. Insights provided by papers collected in this Theme Issue will be of interest to a wide audience.     

Recreation ecology research in East Asia's protected areas: Redefining impacts?

Recreation ecology, the scientific study of visitor impacts and their effective management, has been developed largely in North America, Europe, and more recently in Australia, in response to growing impacts of visitor use to protected area resources. A body of literature has been accumulated that contributes to sustainable visitor management in protected areas. This paper traces the development of recreation ecology research in East Asia and examines the field's relevance to East Asia's protected natural areas which endure both a long history of human utilisation and contemporary recreation and tourism pressure, much of which originates from surrounding densely populated urban areas. The formative, expanding and strengthening stages of recreation ecology research in this region were identified through an extensive review of literature published in English and East Asian languages. Each of these three developmental stages was illustrated with examples and compared with the general state of research during the same period. Key challenges and opportunities for future recreation ecology research in the region are discussed in light of this review.     

Student‐led field studies of herbivory: Hands‐on experiences for remote (or in‐person) learning

Challenging students to independently design and implement experiments is a powerful way to teach the scientific method while engaging with STEM‐related course material. For ecology and organismal biology, such experiences often take the form of field work. The COVID‐19 pandemic presented formidable challenges for instructors of such courses: How can students conduct any experiments, much less ones of their own design, when they might not even have access to campus? Here we describe a student‐led field project exploring invertebrate herbivory in terrestrial plant systems. Designed to flexibly accommodate student groups working either in‐person, remotely, or both, the project would be suitable for invertebrate biology, plant biology, or general ecology courses at the college or high school level. We describe our implementation in two sections of a sophomore‐level course, provide specific advice based on our experiences, make suggestions for future improvements or adaptations, and provide all the written materials that instructors would need to implement this in their own teaching.     

Applying ecological models to communities of genetic elements: the case of neutral theory

A promising recent development in molecular biology involves viewing the genome as a mini‐ecosystem, where genetic elements are compared to organisms and the surrounding cellular and genomic structures are regarded as the local environment. Here, we critically evaluate the prospects of ecological neutral theory (ENT), a popular model in ecology, as it applies at the genomic level. This assessment requires an overview of the controversy surrounding neutral models in community ecology. In particular, we discuss the limitations of using ENT both as an explanation of community dynamics and as a null hypothesis. We then analyse a case study in which ENT has been applied to genomic data. Our central finding is that genetic elements do not conform to the requirements of ENT once its assumptions and limitations are made explicit. We further compare this genome‐level application of ENT to two other, more familiar approaches in genomics that rely on neutral mechanisms: Kimura's molecular neutral theory and Lynch's mutational‐hazard model. Interestingly, this comparison reveals that there are two distinct concepts of neutrality associated with these models, which we dub ‘fitness neutrality’ and ‘competitive neutrality’. This distinction helps to clarify the various roles for neutral models in genomics, for example in explaining the evolution of genome size.     

Identification of candidate loci for adaptive phenotypic plasticity in natural populations of spadefoot toads

Phenotypic plasticity allows organisms to alter their phenotype in direct response to changes in the environment. Despite growing recognition of plasticity's role in ecology and evolution, few studies have probed plasticity's molecular bases—especially using natural populations. We investigated the genetic basis of phenotypic plasticity in natural populations of spadefoot toads (Spea multiplicata). Spea tadpoles normally develop into an “omnivore” morph that is favored in long‐lasting, low‐density ponds. However, if tadpoles consume freshwater shrimp or other tadpoles, they can alternatively develop (via plasticity) into a “carnivore” morph that is favored in ephemeral, high‐density ponds. By combining natural variation in pond ecology and morph production with population genetic approaches, we identified candidate loci associated with each morph (carnivores vs. omnivores) and loci associated with adaptive phenotypic plasticity (adaptive vs. maladaptive morph choice). Our candidate morph loci mapped to two genes, whereas our candidate plasticity loci mapped to 14 genes. In both cases, the identified genes tended to have functions related to their putative role in spadefoot tadpole biology. Our results thereby form the basis for future studies into the molecular mechanisms that mediate plasticity in spadefoots. More generally, these results illustrate how diverse loci might mediate adaptive plasticity.     

Impacts of taxonomic inertia for the conservation of African ungulate diversity: an overview

We review the state of African ungulate taxonomy over the last 120 years, with an emphasis on the introduction of the polytypic species concept and the discipline's general neglect since the middle of the 20th century. We single out negative consequences of ‘orthodox’ taxonomy, highlighting numerous cases of neglect of threatened lineages, unsound translocations that led to lineage introgression, and cases of maladaptation to local conditions including parasitic infections. Additionally, several captive breeding programmes have been hampered by chromosome rearrangements caused by involuntary lineage mixing. We advocate that specimen‐based taxonomy should regain its keystone role in mammal research and conservation biology, with its scientific values augmented with genomic evidence. While integration with molecular biology, ecology and behaviour is needed for a full understanding of ungulate alpha diversity, we stress that morphological diversity has been neglected despite its tremendous practical importance for some groups of ‘utilizers’ such as trophy hunters, wildlife tourists and conservationists. We conclude that there is no evidence that purported ‘taxonomic inflation’ has adverse effects on ungulate conservation: rather, it is taxonomic inertia that has such adverse effects. We stress that sound science, founded on robust taxonomy, should underpin effective sustainable management (hunting, ranching, captive breeding and reintroduction programmes) of this unique African natural resource.     

Predicting ecosystem metaphenome from community metagenome: A grand challenge for environmental biology

Elucidating how an organism''s characteristics emerge from its DNA sequence has been one of the great triumphs of biology. This triumph has cumulated in sophisticated computational models that successfully predict how an organism''s detailed phenotype emerges from its specific genotype. Inspired by that effort''s vision and empowered by its methodologies, a grand challenge is described here that aims to predict the biotic characteristics of an ecosystem, its metaphenome, from nucleic acid sequences of all the species in its community, its metagenome. Meeting this challenge would integrate rapidly advancing abilities of environmental nucleic acids (eDNA and eRNA) to identify organisms, their ecological interactions, and their evolutionary relationships with advances in mechanistic models of complex ecosystems. Addressing the challenge would help integrate ecology and evolutionary biology into a more unified and successfully predictive science that can better help describe and manage ecosystems and the services they provide to humanity.     

Brief communication: A morphometric analysis of the neandertal upper second molar leuca I

The scarcity of Neandertal remains from Southern Europe hampers our understanding of Neandertal variability, and can bias interpretations about Neandertal geographic variation. To address this issue, it is often important to reassess human remains that, while discovered decades ago, remain relatively unknown to the scientific community. In this contribution, we provide a complete state‐of‐the‐art comparative morphometric analysis of Leuca I, an unworn left second upper molar (LM²) discovered in 1958 in Bambino's Cave (near Santa Maria di Leuca, Apulia, Italy) and attributed to Homo neanderthalensis. Our study includes comparisons of standard metric and nonmetric data, a 2D image analysis of the occlusal surface and measurements of both 2D and 3D enamel thickness and dental tissue proportions. Although Leuca I follows the Neandertal M²s trend in some morphometric aspects (i.e., small relative occlusal polygon area), in other cases it falls to the higher end (for 3D average enamel thickness) or even outside (for 3D‐relative enamel thickness) the Neandertal M² variability, thus increasing the known Neandertal range of variation. Am J Phys Anthropol 152:300–305, 2013. © 2013 Wiley Periodicals, Inc.     

Outside the Moral Economy? Single Female Migrants and the Changing Bangladeshi Family

Unmarried female migrants, travelling overseas for work, form a small proportion of Bangladeshi overseas migrants. Their situation is anomalous and suspect, since unmarried women should remain at home under male protection and control. The stories of Dipti, a single woman who migrated to Australia in the 1980s, and of two other single women from her native village, demonstrate clearly some of the contradictions of these women's lives. Like other single female migrants I knew, Dipti retained close links to kin in Bangladesh, contributing significantly to the income of parents and siblings back home. Indeed, her constant and generous gift‐giving can be understood as an attempt to counter her anomalous position and remain part of the moral economy of the village. However, Dipti's longing to remain part of an ‘ideal’ extended family conflicted with her relatives' desire for autonomy. This is because families in Bangladesh were themselves changing over this period, due to the intersection of the developmental cycles of domestic groups, dispositions towards the autonomy of children from their parents and each other, and through the economic pressures of contemporary Bangladeshi society, which provide a strong further impetus towards the financial autonomy of the nuclear family. These changes within the structure of their families result in alienating further these single female migrants. Thus, ultimately, both Dipti's attempts to maintain her extended family in Bangladesh and her efforts to recreate it in Australia were doomed to failure. The brief stories of the other two single women I use in the article are parallel to that of Dipti's.