EVOLUTIONARY BIOLOGY IN BIODIVERSITY SCIENCE,CONSERVATION, AND POLICY: A CALL TO ACTION

Evolutionary biologists have long endeavored to document how many species exist on Earth, to understand the processes by which biodiversity waxes and wanes, to document and interpret spatial patterns of biodiversity, and to infer evolutionary relationships. Despite the great potential of this knowledge to improve biodiversity science, conservation, and policy, evolutionary biologists have generally devoted limited attention to these broader implications. Likewise, many workers in biodiversity science have underappreciated the fundamental relevance of evolutionary biology. The aim of this article is to summarize and illustrate some ways in which evolutionary biology is directly relevant. We do so in the context of four broad areas: (1) discovering and documenting biodiversity, (2) understanding the causes of diversification, (3) evaluating evolutionary responses to human disturbances, and (4) implications for ecological communities, ecosystems, and humans. We also introduce bioGENESIS, a new project within DIVERSITAS launched to explore the potential practical contributions of evolutionary biology. In addition to fostering the integration of evolutionary thinking into biodiversity science, bioGENESIS provides practical recommendations to policy makers for incorporating evolutionary perspectives into biodiversity agendas and conservation. We solicit your involvement in developing innovative ways of using evolutionary biology to better comprehend and stem the loss of biodiversity.     

Concluding overview: looking back, looking forward

The gamma-herpesviruses are a group of related agents which share the same broad strategy for infection of and persistence within the lymphoid tissues of their hosts. Yet in evolutionary terms these agents are sufficiently diverse to display multiple different molecular mechanisms whereby that strategy can be achieved. Attempts are made to relate the different in vitro growth transforming capacities of the gamma1-herpesviruses, the T-lymphotropic gamma2-herpesviruses and the B-lymphotropic gamma2-herpesviruses to what is known about the biology of these virus infections in their natural or in experimental hosts. The review then summarizes the evidence linking gamma-herpesviruses with oncogenesis and proposes that the diverse spectrum of Epstein-Barr virus and human herpesvirus 8-associated human tumours falls into three pathogenetically distinct categories. Many questions remain unanswered in the areas of gamma-herpesvirus biology and disease pathogenesis: resolving these questions will require a broadening of our experimental approaches and a willingness to relinquish 'single-model' panaceas.     

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.     

Accepting evolution

Poor public perceptions and understanding of evolution are not unique to the developed and more industrialized nations of the world. International resistance to the science of evolutionary biology appears to be driven by both proponents of intelligent design and perceived incompatibilities between evolution and a diversity of religious faiths. We assessed the success of a first-year evolution course at the University of Cape Town and discovered no statistically significant change in the views of students before the evolution course and thereafter, for questions that challenged religious ideologies about creation, biodiversity, and intelligent design. Given that students only appreciably changed their views when presented with "facts," we suggest that teaching approaches that focus on providing examples of experimental evolutionary studies, and a strong emphasis on the scientific method of inquiry, are likely to achieve greater success. This study also reiterates the importance of engaging with students' prior conceptions, and makes suggestions for improving an understanding and appreciation of evolutionary biology in countries such as South Africa with an inadequate secondary science education system, and a dire lack of public engagement with issues in science.     

Chance, explanation, and causation in evolutionary theory

Chance comes into plays at many levels of the explanation of the evolutionary process; but the unity of sense of this category is problematic. The purpose of this talk is to clarify the meaning of chance at various levels in evolutionary theory: mutations, genetic drift, genetic revolutions, ecosystems, macroevolution. Three main concepts of chance are found at these various levels: luck (popular concept), randomness (probabilistic concept), and contingency relative to a given theoretical system (epistemological concept). After identifying which concept(s) of chance fit(s) with these levels, the question is raised whether these concepts can be reduced to a smaller number, and whether chance in evolutionary theory has a subjective or an objective sense.     

Theory and speciation

The study of speciation has become one of the most active areas of evolutionary biology, and substantial progress has been made in documenting and understanding phenomena ranging from sympatric speciation and reinforcement to the evolutionary genetics of postzygotic isolation. This progress has been driven largely by empirical results, and most useful theoretical work has concentrated on making sense of empirical patterns. Given the complexity of speciation, mathematical theory is subordinate to verbal theory and generalizations about data. Nevertheless, mathematical theory can provide a useful classification of verbal theories; can help determine the biological plausibility of verbal theories; can determine whether alternative mechanisms of speciation are consistent with empirical patterns; and can occasionally provide predictions that go beyond empirical generalizations. We discuss recent examples of progress in each of these areas.     

Evolution of phenotypic plasticity: where are we going now?

The study of phenotypic plasticity has progressed significantly over the past few decades. We have moved from variation for plasticity being considered as a nuisance in evolutionary studies to it being the primary target of investigations that use an array of methods, including quantitative and molecular genetics, as well as of several approaches that model the evolution of plastic responses. Here, I consider some of the major aspects of research on phenotypic plasticity, assessing where progress has been made and where additional effort is required. I suggest that some areas of research, such the study of the quantitative genetic underpinning of plasticity, have been either settled in broad outline or superseded by new approaches and questions. Other issues, such as the costs of plasticity are currently at the forefront of research in this field, and are likely to be areas of major future development.     

Understanding the diversity of foliar endophytic fungi: progress,challenges, and frontiers

Fungal endophytes, a diverse group of primarily ascomycetous fungi defined functionally by their occurrence within asymptomatic photosynthetic tissues of plants, occur in all major lineages of land plants and in natural and anthropogenic communities ranging from the arctic to the tropics. Because of the tremendous diversity they encompass, ecological questions regarding the interactions of endophytes with the plants in which they live - and with other organisms that in turn interact with endophyte-plants symbiota – are difficalt to address. The goals of this review are to highlight progress, challenges, and frontiers in the study of foliar endophyte diversity, with the ultimate goal of encouraging research that both bridges the gap between, and advances, research in alpha taxonomy and ecology. I focus on four themes that are reflected in the recent and rapidly expanding literature regarding endophyte biology: (1) the taxonomic and ecological distinctiveness of endophytes relative to other nonpathogenic plant-associated fungi; (2) the insights that can be gained from studies that consider genotypes as the relevant unit of biological organization, especially in the context of traditional species-level taxonomy and robust phylogenetic methods that tie these genotypes and species together in an explicit evolutionary context; (3) the context-dependency of endophyte communities, highlighting the importance of both the identify of host plants and the geographic location in which plants occur; and (4) the complexity of the endophyte-pathogen-saprotroph continuum, and the challeges and exciting frontiers that lie in understanding the evolutionary relationships and ecological lability of fungi that exhibit these ecological modes. I argue that never before has the study of endophytic fungi been more exciting or more tractable, and that the potential for endophyte researchers to inform diverse areas of biology has never been greater.     

Ecology and evolution of plant�Cpollinator interactions

Background

Some of the most exciting advances in pollination biology have resulted from interdisciplinary research combining ecological and evolutionary perspectives. For example, these two approaches have been essential for understanding the functional ecology of floral traits, the dynamics of pollen transport, competition for pollinator services, and patterns of specialization and generalization in plant–pollinator interactions. However, as research in these and other areas has progressed, many pollination biologists have become more specialized in their research interests, focusing their attention on either evolutionary or ecological questions. We believe that the continuing vigour of a synthetic and interdisciplinary field like pollination biology depends on renewed connections between ecological and evolutionary approaches.

Scope

In this Viewpoint paper we highlight the application of ecological and evolutionary approaches to two themes in pollination biology: (1) links between pollinator behaviour and plant mating systems, and (2) generalization and specialization in pollination systems. We also describe how mathematical models and synthetic analyses have broadened our understanding of pollination biology, especially in human-modified landscapes. We conclude with several suggestions that we hope will stimulate future research. This Viewpoint also serves as the introduction to this Special Issue on the Ecology and Evolution of Plant–Pollinator Interactions. These papers provide inspiring examples of the synergy between evolutionary and ecological approaches, and offer glimpses of great accomplishments yet to come.Key words: Floral traits, generalization and specialization, global change, male fitness, mating systems, multiple paternity, plant–pollinator networks, pollen and gene dispersal, pollinator behaviour, pollination syndromes, pollination webs, self-fertilization     

The risk of flawed inference in evolutionary studies when detectability is less than one

Addressing evolutionary questions in the wild remains a challenge. It is best done by monitoring organisms from birth to death, which is very difficult in part because individuals may or may not be resighted or recaptured. Although the issue of uncertain detection has long been acknowledged in ecology and conservation biology, in evolutionary studies of wild populations it is often assumed that detectability is perfect. We argue that this assumption may lead to flawed inference. We demonstrate that the form of natural selection acting on body mass of sociable weavers is altered and that the rate of senescence of roe deer is underestimated when not accounting for a value of detectability that is less than one. Because mark-recapture models provide an explicit way to integrate and reliably model the detection process, we strongly recommend their use to address questions in evolutionary biology.     

Fungal evolution: cellular,genomic and metabolic complexity

The question of how phenotypic and genomic complexity are inter‐related and how they are shaped through evolution is a central question in biology that historically has been approached from the perspective of animals and plants. In recent years, however, fungi have emerged as a promising alternative system to address such questions. Key to their ecological success, fungi present a broad and diverse range of phenotypic traits. Fungal cells can adopt many different shapes, often within a single species, providing them with great adaptive potential. Fungal cellular organizations span from unicellular forms to complex, macroscopic multicellularity, with multiple transitions to higher or lower levels of cellular complexity occurring throughout the evolutionary history of fungi. Similarly, fungal genomes are very diverse in their architecture. Deep changes in genome organization can occur very quickly, and these phenomena are known to mediate rapid adaptations to environmental changes. Finally, the biochemical complexity of fungi is huge, particularly with regard to their secondary metabolites, chemical products that mediate many aspects of fungal biology, including ecological interactions. Herein, we explore how the interplay of these cellular, genomic and metabolic traits mediates the emergence of complex phenotypes, and how this complexity is shaped throughout the evolutionary history of Fungi.     

Ella Thea Smith and the Lost History of American High School Biology Textbooks

Two influential articles published in the 1970s suggested that pressure from Christian fundamentalists, subsequent to the Scopes trial of 1925, forced American high school biology textbook authors and publishers to significantly limit discussion of the topic of evolution. The conclusions reached by these studies have become foundational for historians examining the interplay between science and religion in the United States in the twentieth century. However, a reexamination of key twentieth century biology textbooks suggests that the narrative that the treatment of the theory of evolution was held hostage to anti-rational cultural forces is largely a myth, created first as part of a public relations effort by the Biological Sciences Curriculum Study (BSCS) to differentiate, defend, and promote its work, and later as part of an attempt by scholars to sound a warning concerning the rise of the religious right. A focus on this narrative has not only allowed biologists to sidestep uncomfortable questions regarding the race-biased and class-biased assumptions embedded within the concept of evolutionary progress, it has also limited reliance on the texts in question as reliable reflections of the cultural assumptions of educators and scientists. A reexamination of the most popular American biology textbooks from 1907 to 1963, particularly the work of Ella Thea Smith, provides evidence in support of these contentions.     

Maladaptation and natural selection

The transformations George Williams initiated in evolutionary biology seem so blindingly obvious in retrospect that they spur the question of why he saw what no one else did. While most humans are prone to see only what theory predicts, Williams sees in bold relief whatever does not fit. Not an adaptationist or an anti-adaptationist, Williams is better described as a maladaptionist. The challenge of finding evolutionary explanations for apparent maladaptations has been overlooked with casualness akin to that once typical for group selection. Suboptimal traits tend to be dismissed as illustrations of the weakness and stochastic nature of selection compared with mutation and drift. A closer look suggests that such constraints are only one of six possible kinds of explanations for apparently suboptimal designs: mismatch, coevolution, tradeoffs, constraints, reproductive advantage at the expense of the individual, and defenses that are aversive but useful Medicine has asked proximate questions at every possible level but has only begun to ask evolutionary questions about why bodies are vulnerable to disease. Considering all six possible evolutionary reasons for apparently suboptimal traits will spur progress not only in medicine but also more generally in biology. 'Williams Vision" may not yield a net benefit to the possessor, but it is invaluable for the species.     

Kowalevsky, comparative evolutionary embryology, and the intellectual lineage of evo-devo

Alexander Kowalevsky was one of the most significant 19th century biologists working at the intersection of evolution and embryology. The reinstatement of the Alexander Kowalevsky Medal by the St. Petersburg Society of Naturalists for outstanding contributions to understanding evolutionary relationships in the animal kingdom, evolutionary developmental biology, and comparative zoology is timely now that Evo-devo has emerged as a major research discipline in contemporary biology. Consideration of the intellectual lineage of comparative evolutionary embryology explicitly forces a reconsideration of some current conceptions of the modern emergence of Evo-devo, which has tended to exist in the shadow of experimental embryology throughout the 20th century, especially with respect to the recent success of developmental biology and developmental genetics. In particular we advocate a sharper distinction between the heritage of problems and the heritage of tools for contemporary Evo-devo. We provide brief overviews of the work of N. J. Berrill and D. T. Anderson to illustrate comparative evolutionary embryology in the 20th century, which provides an appropriate contextualization for a conceptual review of our research on the sea urchin genus Heliocidaris over the past two decades. We conclude that keeping research questions rather than experimental capabilities at the forefront of Evo-devo may be an antidote to any repeat of the stagnation experienced by the first group of evolutionary developmental biologists over one hundred years ago and acknowledges Kowalevsky's legacy in evolutionary embryology.     

Fungal evolution and speciation

Molecular-genetic methods are making possible a revolution in the the study of fungal evolutionary biology. To date, substantial progress has been made toward the goal of determining phylogenetic relationships, This is particularly true for higher taxonomic levels, where small-subunit rRNA sequences have proved valuable. The tremendous range of life-cycle diversity exhibited among fungi makes them excellent candidates for exploring areas of evolutionary biology that are as yet poorly investigated, particularly in terms of population biology, reproductive strategies and speciation. This argument is supported by the results of recent studies.     

Bridging the regeneration gap: genetic insights from diverse animal models

Significant progress has recently been made in our understanding of animal regenerative biology, spurred on by the use of a wider range of model organisms and an increasing ability to use genetic tools in traditional models of regeneration. This progress has begun to delineate differences and similarities in the regenerative capabilities and mechanisms among diverse animal species, and to address some of the key questions about the molecular and cell biology of regeneration. Our expanding knowledge in these areas not only provides insights into animal biology in general, but also has important implications for regenerative medicine and stem-cell biology.     

The 1999 Crafoord Prize lectures. Neo-Lamarckian experimentalism in America: origins and consequences

The 1890s and the first decades of the twentieth century saw a vigorous debate about the mechanisms of evolutionary change. On one side, August Weismann defended the selectionist hypothesis; on the other, Herbert Spencer defended neo-Lamarckian theory. Supporters of Spencer, notably the American paleontologist and evolutionary theorist Henry Fairfield Osborn, recognized that the questions raised by Weismann and Spencer could only be settled experimentally. They called for the application of experimental methods, and the establishment of a new institution for the purpose of confirming the inheritance of acquired characters. To a great extent, the experimental program championed by Osborn and others was implemented and, although it failed to reveal soft inheritance and was soon eclipsed by Mendelian and chromosomal genetics, it did make significant and lasting contributions to evolutionary biology. Thus the importance of methodological and institutional innovation and theoretical pluralism to the progress of science is illustrated and underscored.     

LOST IN THE MAP

Organismal development and evolution are complex, multifaceted processes that depend intimately on context. They are subject to environmental influences, chance appearance and fixation of mutations, and numerous other idiosyncrasies. Genomics is detailing the molecular signature of effects of these mechanisms on phenotypes, but because numerous distinct evolutionary explanations can produce a given genomic pattern, the molecular details, rather than elucidating process, typically distract from explanatory insight and contribute little to predictive capability. While genomic research has burgeoned, direct study of evolutionary and developmental processes has lagged. We advocate for reinvigoration of direct study of process, along with refocusing of attention on questions of broad biological import, as more productive of urgently needed insights, which genomic approaches are not providing.     

What is speciation and how should we study it?

To understand speciation, we first need to know what species are. Yet debates over species concepts have seemed endless, with little obvious relevance to the study of speciation. Recently, there has been progress in resolving these debates, favoring a lineage-based, evolutionary species concept. This progress calls for reconsideration of the study of speciation. Traditional speciation research based on the biological species concept has led to great advances in understanding how nonallopatric speciation occurs and how species diverge and remain separate from each other. However, this research has neglected the question of how new species arise in the first place for the most common geographic mode (allopatric). A new and very different research program is needed to understand the ecological and evolutionary processes that split an ancestral species into new allopatric lineages. This research program will connect speciation to many other fundamental questions in evolutionary biology, ecology, biogeography, and conservation biology.     

Developing the genotype-to-phenotype relationship in evolutionary theory: A primer of developmental features

For decades, there have been repeated calls for more integration across evolutionary and developmental biology. However, critiques in the literature and recent funding initiatives suggest this integration remains incomplete. We suggest one way forward is to consider how we elaborate the most basic concept of development, the relationship between genotype and phenotype, in traditional models of evolutionary processes. For some questions, when more complex features of development are accounted for, predictions of evolutionary processes shift. We present a primer on concepts of development to clarify confusion in the literature and fuel new questions and approaches. The basic features of development involve expanding a base model of genotype-to-phenotype to include the genome, space, and time. A layer of complexity is added by incorporating developmental systems, including signal-response systems and networks of interactions. The developmental emergence of function, which captures developmental feedbacks and phenotypic performance, offers further model elaborations that explicitly link fitness with developmental systems. Finally, developmental features such as plasticity and developmental niche construction conceptualize the link between a developing phenotype and the external environment, allowing for a fuller inclusion of ecology in evolutionary models. Incorporating aspects of developmental complexity into evolutionary models also accommodates a more pluralistic focus on the causal importance of developmental systems, individual organisms, or agents in generating evolutionary patterns. Thus, by laying out existing concepts of development, and considering how they are used across different fields, we can gain clarity in existing debates around the extended evolutionary synthesis and pursue new directions in evolutionary developmental biology. Finally, we consider how nesting developmental features in traditional models of evolution can highlight areas of evolutionary biology that need more theoretical attention.