Does frequency-dependent selection optimize fitness?

In evolutionary biology, the axiom that natural selection tends ideally to maximize inclusive fitness of the individual or some other suitable quantity is often advanced (Cody, 1974; Maynard Smith, 1978; Krebs & McCleery, 1984; Houston et al., 1988). Moreover, the evolutionists generally distinguish two situations (Dawkins, 1980; Maynard Smith, 1982): one in which fitness is independent of the frequency of the phenotypes present in the population (frequency-independent selection), and one in which it does depend on this frequency (frequency-dependent selection). This led some authors such as Parker (1984), and more recently Parker & Maynard Smith (1990), to consider "a 2-speed optimization": frequency-independent selection should lead to a "simple optimum" at the end of the selective process, since all the individuals should have the same strategy and the mean fitness of the population should be maximized; frequency-dependent selection, formulated in terms of the theory of games, should lead to a "competitive optimum" even though the "evolutionary stable strategy" (or "ESS"; Maynard Smith & Price, 1973) characterizing the equilibrium "is not the strategy that maximizes fitness in a population sense" (Parker & Maynard Smith, 1990: 30). Our aim in this short communication is to criticize the concept of "competitive optimum" by Parker & Maynard Smith, as well as the general ability of natural selection to "maximize fitness", even in "phenotypic models" (Lloyd, 1977). These models, devoid of genetic constraints since each strategist is assumed to reproduce its own kind, are especially suitable for examining the ideal effect of natural selection.     

Reducing ambiguity in describing plant–insect interactions: "preference", "acceptability" and "electivity"

Ecologists and evolutionary biologists have a common interest in plant–insect interactions. Ecologists develop terminology describing patterns of association between plants and insects, while evolutionary biologists use the same words to denote potentially heritable traits of individuals. Use of the same terms to describe both traits of the interaction and traits of the organisms hinders communication. An example is "preference", often used by ecologists to denote properties of the plant–insect interaction and by behavioural or evolutionary biologists to denote insect traits. The existing term "electivity" could be incorporated into the lexicon of plant–insect interactions to supplant the ecological use of "preference". The term "preference" would then denote a behavioural trait of the insect. The mirror-image trait of the plant would be "acceptability". This could be a step towards a common terminology that would be usable by both ecologists and evolutionists.     

Ecological aspects of the evolutionary processes

Darwin in his On the Origin of species made it clear that evolutionary change depends on the combined action of two different causes, the first being the origin of genetically based phenotypic variation in the individual organisms comprising the population and the second being the action of selective agents of the external environment placing demands on the individual organisms. For over a century following Darwin, most evolutionists focused on the origin of inherited variation and its transmission; many workers continue to regard genetics to be the core of evolutionary theory. Far less attention has been given to the exact nature of the selective agents with most evolutionists still treating this cause imprecisely to the detriment of our understanding of both nomological and historical evolutionary theory. Darwin was vague in the meaning of his new concept of "Natural Selection," using it interchangeably as one of the causes for evolutionary change and as the final outcome (= evolutionary change). In 1930, natural selection was defined clearly as "non-random, differential reproduction of genes" by R. Fisher and J.B.S. Haldane which is a statement of the outcome of evolutionary process and which omits mention of the causes bringing about this change. Evolutionists quickly accepted this outcome definition of natural selection, and have used interchangeably selection both as a cause and as the result of evolutionary change, causing great confusion. Herein, the details will be discussed of how the external environment (i.e., the environment-phenotype interaction) serves as selective agents and exerts demands on the phenotypic organisms. Included are the concepts of fitness and of the components of fitness (= adaptations) which are respectively (a) survival, (b) direct reproductive and (c) indirect reproductive features. Finally, it will be argued that historical-narrative analyses of organisms, including classification and phylogenetic history, are possible only with a full understanding of nomological evolutionary theory and with functional/adaptive studies of the employed taxonomic features in addition to the standard comparative investigations.     

Are There Laws of Genome Evolution?

Research in quantitative evolutionary genomics and systems biology led to the discovery of several universal regularities connecting genomic and molecular phenomic variables. These universals include the log-normal distribution of the evolutionary rates of orthologous genes; the power law-like distributions of paralogous family size and node degree in various biological networks; the negative correlation between a gene's sequence evolution rate and expression level; and differential scaling of functional classes of genes with genome size. The universals of genome evolution can be accounted for by simple mathematical models similar to those used in statistical physics, such as the birth-death-innovation model. These models do not explicitly incorporate selection; therefore, the observed universal regularities do not appear to be shaped by selection but rather are emergent properties of gene ensembles. Although a complete physical theory of evolutionary biology is inconceivable, the universals of genome evolution might qualify as "laws of evolutionary genomics" in the same sense "law" is understood in modern physics.     

The units ofselection

The individual has long been considered by evolutionists to be the only level at which selection acts. Recent advances in molecular biology have forced them to accept at least one other, the molecular level. This paves the way for a broadening of perspective in evolutionary thought, but renders it more necessary to clarify the debate about the level at which the process of evolution occurs. This debate cannot be resolved without clarifying the premises on which the argument is based. To this end, it is helpful to distinguish between that which is transmitted and that which transmits. The discrimination of genetic information from its material support (avatar) can be most useful, particularly when placed in the context of the hierarchical organization of biological systems. The utility of this approach is exemplified by its application to the case of the evolution of sex.     

Homology and the hierarchy of biological systems

Homology is the similarity between organisms due to common ancestry. Introduced by Richard Owen in 1843 in a paper entitled "Lectures on comparative anatomy and physiology of the invertebrate animals", the concept of homology predates Darwin's "Origin of Species" and has been very influential throughout the history of evolutionary biology. Although homology is the central concept of all comparative biology and provides a logical basis for it, the definition of the term and the criteria of its application remain controversial. Here, I will discuss homology in the context of the hierarchy of biological organization. I will provide insights gained from an exemplary case study in evolutionary developmental biology that indicates the uncoupling of homology at different levels of biological organization. I argue that continuity and hierarchy are separate but equally important issues of homology.     

The structure of microbial evolutionary theory

The study of microbial phylogeny and evolution has emerged as an interdisciplinary synthesis, divergent in both methods and concepts from the classical evolutionary biology. The deployment of macromolecular sequencing in microbial classification has provided a deep evolutionary taxonomy hitherto deemed impossible. Microbial phylogenetics has greatly transformed the landscape of evolutionary biology, not only in revitalizing the field in the pursuit of life's history over billions of years, but also in transcending the structure of thought that has shaped evolutionary theory since the time of Darwin. A trio of primary phylogenetic lineages, along with the recognition of symbiosis and lateral gene transfer as fundamental processes of evolutionary innovation, are core principles of microbial evolutionary biology today. Their scope and significance remain contentious among evolutionists.     

Red queen for a day: models of symmetry and selection in paleoecology

The Unified Theory of Biodiversity (UNTB), the Red Queen’s Hypothesis (RQH), and the Cascading Extinctions on Graphs hypothesis (CEG) are explored as members of a spectrum describing the ecological partitioning of species richness. All are models of historical biodiversity, but fare differently in explaining observed features of Phanerozoic biodiversity. The models treat species as symmetric, asymmetric, or partially symmetric respectively. Symmetry in the UNTB is broken by the generation and selection of variation of ecological performance, while the robustness and hence longevity of RQ communities are subject to selection. The CEG model reconciles some of the differences, demonstrating the importance of functional partitioning to both species evolution and selection at the community level. It is concluded that the UNTB explains communities partially on the shortest of evolutionary time scales, while RQ communities would be, at best, geologically ephemeral yet conditionally important.     

The fall and rise of Dr Pangloss: adaptationism and the Spandrels paper 20 years later

Twenty years have passed since Gould and Lewontin published their critique of 'the adaptationist program' - the tendency of some evolutionary biologists to assume, rather than demonstrate, the operation of natural selection. After the 'Spandrels paper', evolutionists were more careful about producing just-so stories based on selection, and paid more attention to a panoply of other processes. Then came reactions against the excesses of the anti-adaptationist movement, which ranged from a complete dismissal of Gould and Lewontin's contribution to a positive call to overcome the problems. We now have an excellent opportunity for finally affirming a more balanced and pluralistic approach to the study of evolutionary biology.     

What will result from the interaction between functional and evolutionary biology?

The modern synthesis has been considered to be wrongly called a "synthesis", since it had completely excluded embryology, and many other disciplines. The recent developments of Evo-Devo have been seen as a step in the right direction, as complementing the modern synthesis, and probably leading to a "new synthesis". My argument is that the absence of embryology from the modern synthesis was the visible sign of a more profound lack: the absence of functional biology in the evolutionary synthesis. I will consider the reasons for this absence, as well as the recent transformations which favoured a closer interaction between these two branches of biology. Then I will describe two examples of recent work in which functional and evolutionary questioning were tightly linked. The most significant part of the paper will be devoted to the transformation of evolutionary theory that can be expected from this encounter: a deep transformation, or simply an experimental confirmation of this theory? I will not choose between these two different possibilities, but will discuss some of the difficulties which make the choice problematic.     

Species of thought: A comment on evolutionary epistemology

The primary outcome of natural selection is adaptation to an environment. The primary concern of epistemology is the acquistion of knowledge. Evolutionary epistemology must therefore draw a fundamental connection between adaptation and knowledge. Existing frameworks in evolutionary epistemology do this in two ways; (a) by treating adaptation as a form of knowledge, and (b) by treating the ability to acquire knowledge as a biologically evolved adaptation. I criticize both frameworks for failing to appreciate that mental representations can motivate behaviors that are adaptive in the real world without themselves directly corresponding to the real world. I suggest a third framework in which mental representations are to reality as species are to ecosystems. This is a many-to-one relationship that predicts a diversity of adaptive representations in the minds of interacting people. As “species of thought”, mental representations share a number of properties with biological species, including isolating mechanisms that prevent them from blending with other representations. Species of thought also are amenable to the empirical methods that evolutionists use to study adaptation in biological species. Empirical studies of mental representations in everyday life might even be necessary for science to succeed as a normative “truth-seeking” discipline.     

Reinventing Molecular Weismannism: Information in Evolution

Molecular Weismannism is the claim that: In the development of an individual, DNA causes the production both of DNA (genetic material) and of protein (somatic material). The reverse process never occurs. Protein is never a cause of DNA. This principle underpins both the idea that genes are the objects upon which natural selection operates and the idea that traits can be divided into those that are genetic and those that are not. Recent work in developmental biology and in philosophy of biology argues that an acceptance of Molecular Weismannism requires the tacit assumption that genetic causes are different in kind from other developmental causes. They argue that if this assumption proves to be unwarranted then we should abandon, not just gene selectionism and gene centred functional solutions to the units of selection problem, but also the very notion that there is any such thing as a genetic trait. A group of possible causal distinctions (proximity, ultimacy and specificity) are explored and found wanting. It is argued that an extended version of information theory, while not strong enough to support Molecular Weismannism, will support both the claim that traits can be divided into those that are genetic and those that are not as well as the claim that there is good reason to privilege genetic causes within evolutionary and developmental explanations. The outcome of this for the units of selection debate is explored.     

Bridging the gap between molecular epidemiologists and evolutionists

Molecular epidemiology designates the various molecular methods that aim to identify the relevant units of analysis of pathogens involved in transmissible diseases: species, subspecies, strains, clones and genes of interest. It is frequently based on an empirical approach. I advocate that evolutionary concepts enrich this discipline considerably and should be considered as an integral part. In turn, the experience and questioning of field experts are crucial to evolutionists who use transmissible diseases as models. A molecular epidemiology aim gives evolutionary studies a practical goal, putting a stop to approaches that are overly speculative.     

Function without purpose

Philosophers of evolutionary biology favor the so-called etiological concept of function according to which the function of a trait is its evolutionary purpose, defined as the effect for which that trait was favored by natural selection. We term this the selected effect (SE) analysis of function. An alternative account of function was introduced by Robert Cummins in a non-evolutionary and non-purposive context. Cummins's account has received attention but little support from philosophers of biology. This paper will show that a similar non-purposive concept of function, which we term causal role (CR) function, is crucial to certain research programs in evolutionary biology, and that philosophical criticisms of Cummins's concept are ineffective in this scientific context. Specifically, we demonstrate that CR functions are a vital and ineliminable part of research in comparative and functional anatomy, and that biological categories used by anatomists are not defined by the application of SE functional analysis. Causal role functions are non-historically defined, but may themselves be used in an historical analysis. Furthermore, we show that a philosophical insistence on the primary of SE functions places practicing biologists in an untenable position, as such functions can rarely be demonstrated (in contrast to CR functions). Biologists who study the form and function of organismal design recognize that it is virtually impossible to identify the past action of selection on any particular structure retrospectively, a requirement for recognizing SE functions.     

Organisms in evolution

Organisms constitute one of the most remarkable features of our living world. However, they have not yet received any accepted characterization within the framework of the evolutionary theory. The reasons for this contrast between the saliency of organisms in the biological landscape and their theoretical status are multiple and they are analyzed in the first part of this paper. Starting from this contrast, I argue for a theoretically grounded concept of organism within the framework of evolutionary theory itself. To this effect I argue that the theory of major transitions in evolution (Maynard Smith and Szathmáry 1995; Michod 1999) provides us with the theoretical basis for an understanding of the individuality of organisms and I propose a first characterization of organisms as evolutionary units structured by a division of reproductive labor among their parts. I also discuss one of the most important implications of this definition, namely that some colonial entities are to be counted as superorganisms. Finally, I show that though theoretically satisfying, this definition does not suffice in order fully to individuate the organisms and superorganisms in practice. To this end, physiology is needed, because it offers us some criteria for their individuation in ecological space. These criteria, however, are not immune to errors through misidentification and their shortcomings are discussed in the last section. In conclusion, I emphasize the positive implications of these criteria concerning the ecological significance of organisms.     

The cell theory--history, present state and prospects (on the 150th anniversary of the development of the cell theory)

The main stages of history of this most important biological conception are presented and the state of the modern cell theory and its future prospects are considered. Since 1839, when T. Schwann expounded his conception of the cell, a long pathway in cognition of the cell function and organization has been covered. From the original picture of the complex organism as a "cellular state", made up of relatively independent "elementary organisms", i.e. cells the modern biology has come to the idea of the cell as an integral system either being a part of a complex organism, or living free in the nature (protists). The cell represents certain qualitatively peculiar level in a complex evolutionary established hierarchy of biological systems. Some particular tight relations, existing between cytology, as a fundamental biological science and molecular biology, genetics, ecology and other biological disciplines are considered. The importance of the cell conception is ascertained for practical aims, especially in medicine.     

The risk‐return trade‐off between solitary and eusocial reproduction

Social insect colonies can be seen as a distinct form of biological organisation because they function as superorganisms. Understanding how natural selection acts on the emergence and maintenance of these colonies remains a major question in evolutionary biology and ecology. Here, we explore this by using multi‐type branching processes to calculate the basic reproductive ratios and the extinction probabilities for solitary vs. eusocial reproductive strategies. We find that eusociality, albeit being hugely successful once established, is generally less stable than solitary reproduction unless large demographic advantages of eusociality arise for small colony sizes. We also demonstrate how such demographic constraints can be overcome by the presence of ecological niches that strongly favour eusociality. Our results characterise the risk‐return trade‐offs between solitary and eusocial reproduction, and help to explain why eusociality is taxonomically rare: eusociality is a high‐risk, high‐reward strategy, whereas solitary reproduction is more conservative.     

Waiting for Sequences: Morris Goodman,Immunodiffusion Experiments,and the Origins of Molecular Anthropology

During the early 1960s, Morris Goodman used a variety of immunological tests to demonstrate the very close genetic relationships among humans, chimpanzees, and gorillas. Molecular anthropologists often point to this early research as a critical step in establishing their new specialty. Based on his molecular results, Goodman challenged the widely accepted taxonomic classification that separated humans from chimpanzees and gorillas in two separate families. His claim that chimpanzees and gorillas should join humans in family Hominidae sparked a well-known conflict with George Gaylord Simpson, Ernst Mayr, and other prominent evolutionary biologists. Less well known, but equally significant, were a series of disagreements between Goodman and other prominent molecular evolutionists concerning both methodological and theoretical issues. These included qualitative versus quantitative data, the role of natural selection, rates of evolution, and the reality of molecular clocks. These controversies continued throughout Goodman’s career, even as he moved from immunological techniques to protein and DNA sequence analysis. This episode highlights the diversity of methods used by molecular evolutionists and the conflicting conclusions drawn from the data that these methods generated.     

Animal models and conserved processes

Background

The concept of conserved processes presents unique opportunities for using nonhuman animal models in biomedical research. However, the concept must be examined in the context that humans and nonhuman animals are evolved, complex, adaptive systems. Given that nonhuman animals are examples of living systems that are differently complex from humans, what does the existence of a conserved gene or process imply for inter-species extrapolation?

Methods

We surveyed the literature including philosophy of science, biological complexity, conserved processes, evolutionary biology, comparative medicine, anti-neoplastic agents, inhalational anesthetics, and drug development journals in order to determine the value of nonhuman animal models when studying conserved processes.

Results

Evolution through natural selection has employed components and processes both to produce the same outcomes among species but also to generate different functions and traits. Many genes and processes are conserved, but new combinations of these processes or different regulation of the genes involved in these processes have resulted in unique organisms. Further, there is a hierarchy of organization in complex living systems. At some levels, the components are simple systems that can be analyzed by mathematics or the physical sciences, while at other levels the system cannot be fully analyzed by reducing it to a physical system. The study of complex living systems must alternate between focusing on the parts and examining the intact whole organism while taking into account the connections between the two. Systems biology aims for this holism. We examined the actions of inhalational anesthetic agents and anti-neoplastic agents in order to address what the characteristics of complex living systems imply for inter-species extrapolation of traits and responses related to conserved processes.

Conclusion

We conclude that even the presence of conserved processes is insufficient for inter-species extrapolation when the trait or response being studied is located at higher levels of organization, is in a different module, or is influenced by other modules. However, when the examination of the conserved process occurs at the same level of organization or in the same module, and hence is subject to study solely by reductionism, then extrapolation is possible.