Multilevel selection analysis of a microbial social trait

The study of microbial communities often leads to arguments for the evolution of cooperation due to group benefits. However, multilevel selection models caution against the uncritical assumption that group benefits will lead to the evolution of cooperation. We analyze a microbial social trait to precisely define the conditions favoring cooperation. We combine the multilevel partition of the Price equation with a laboratory model system: swarming in Pseudomonas aeruginosa. We parameterize a population dynamics model using competition experiments where we manipulate expression, and therefore the cost‐to‐benefit ratio of swarming cooperation. Our analysis shows that multilevel selection can favor costly swarming cooperation because it causes population expansion. However, due to high costs and diminishing returns constitutive cooperation can only be favored by natural selection when relatedness is high. Regulated expression of cooperative genes is a more robust strategy because it provides the benefits of swarming expansion without the high cost or the diminishing returns. Our analysis supports the key prediction that strong group selection does not necessarily mean that microbial cooperation will always emerge.     

Natural Selection and Drift as Individual-Level Causes of Evolution

In this paper I critically evaluate Reisman and Forber’s (Philos Sci 72(5):1113–1123, 2005) arguments that drift and natural selection are population-level causes of evolution based on what they call the manipulation condition. Although I agree that this condition is an important step for identifying causes for evolutionary change, it is insufficient. Following Woodward, I argue that the invariance of a relationship is another crucial parameter to take into consideration for causal explanations. Starting from Reisman and Forber’s example on drift and after having briefly presented the criterion of invariance, I show that once both the manipulation condition and the criterion of invariance are taken into account, drift, in this example, should better be understood as an individual-level rather than a population-level cause. Later, I concede that it is legitimate to interpret natural selection and drift as population-level causes when they rely on genuinely indeterministic events and some cases of frequency-dependent selection.     

THE CAUSES OF NATURAL SELECTION

We discuss the necessary and sufficient conditions for identifying the cause of natural selection on a phenotypic trait. We reexamine the observational methods recently proposed for measuring selection in natural populations and illustrate why the multivariate analysis of selection is insufficient for identifying the causal agents of selection. We discuss how the observational approach of multivariate selection analysis can be complemented by experimental manipulations of the phenotypic distribution and the environment to identify not only how selection is operating on the phenotypic distribution but also why it operates in the observed manner. A significant point of departure of our work from recent discussions is in regard to the role of the environment in the study of natural selection. Instead of viewing the environment as a source of unwanted variation that obscures the relationship between phenotype and fitness, we view fitness as arising from the interaction of the phenotype with the environment. The biotic and abiotic environment is the context that gives rise to the relationship between phenotype and fitness (selection). The analysis of the causes of selection is in essence a problem in ecology. The experimental study of the association between selection gradients and environmental characteristics is necessary to identify the agents of natural selection. We recommend research methods for identifying the agency of selection that depend upon a reciprocity between the observational approach of multivariate selection analysis and the manipulative approach of field experiments in evolutionary ecology.     

Explanatory unification and natural selection explanations

The debate between the dynamical and the statistical interpretations of natural selection is centred on the question of whether all explanations that employ the concepts of natural selection and drift are reducible to causal explanations. The proponents of the statistical interpretation answer negatively, but insist on the fact that selection/drift arguments are explanatory. However, they remain unclear on where the explanatory power comes from. The proponents of the dynamical interpretation answer positively and try to reduce selection/drift arguments to some of the most prominent accounts of causal explanation. In turn, they face the criticism raised by statisticalists that current accounts of causation have to be violated in some of their core conditions or otherwise used in a very loose manner in order to account for selection/drift explanations. We propose a reconciliation of both interpretations by conveying evolutionary explanations within the unificationist model of scientific explanation. Therefore, we argue that the explanatory power in natural selection arguments is a result of successful unification of individual- and population-level facts. A short case study based on research on sympatric speciation will be presented as an example of how population- and individual-level facts are unified to explain the morphological mosaic of bill shape in island scrub jays (Aphelocoma insularis).     

On Reciprocal Causation in the Evolutionary Process

Recent calls for a revision of standard evolutionary theory (SET) are based partly on arguments about the reciprocal causation. Reciprocal causation means that cause–effect relationships are bi-directional, as a cause could later become an effect and vice versa. Such dynamic cause-effect relationships raise questions about the distinction between proximate and ultimate causes, as originally formulated by Ernst Mayr. They have also motivated some biologists and philosophers to argue for an Extended Evolutionary Synthesis (EES). The EES will supposedly expand the scope of the Modern Synthesis (MS) and SET, which has been characterized as gene-centred, relying primarily on natural selection and largely neglecting reciprocal causation. Here, I critically examine these claims, with a special focus on the last conjecture. I conclude that reciprocal causation has long been recognized as important by naturalists, ecologists and evolutionary biologists working in the in the MS tradition, although it it could be explored even further. Numerous empirical examples of reciprocal causation in the form of positive and negative feedback are now well known from both natural and laboratory systems. Reciprocal causation have also been explicitly incorporated in mathematical models of coevolutionary arms races, frequency-dependent selection, eco-evolutionary dynamics and sexual selection. Such dynamic feedback were already recognized by Richard Levins and Richard Lewontin in their bok The Dialectical Biologist. Reciprocal causation and dynamic feedback might also be one of the few contributions of dialectical thinking and Marxist philosophy in evolutionary theory. I discuss some promising empirical and analytical tools to study reciprocal causation and the implications for the EES. Finally, I briefly discuss how quantitative genetics can be adapated to studies of reciprocal causation, constructive inheritance and phenotypic plasticity and suggest that the flexibility of this approach might have been underestimated by critics of contemporary evolutionary biology.     

Probabilistic causation and the explanatory role of natural selection

The explanatory role of natural selection is one of the long-term debates in evolutionary biology. Nevertheless, the consensus has been slippery because conceptual confusions and the absence of a unified, formal causal model that integrates different explanatory scopes of natural selection. In this study we attempt to examine two questions: (i) What can the theory of natural selection explain? and (ii) Is there a causal or explanatory model that integrates all natural selection explananda? For the first question, we argue that five explananda have been assigned to the theory of natural selection and that four of them may be actually considered explananda of natural selection. For the second question, we claim that a probabilistic conception of causality and the statistical relevance concept of explanation are both good models for understanding the explanatory role of natural selection. We review the biological and philosophical disputes about the explanatory role of natural selection and formalize some explananda in probabilistic terms using classical results from population genetics. Most of these explananda have been discussed in philosophical terms but some of them have been mixed up and confused. We analyze and set the limits of these problems.     

Quantifying the causal pathways contributing to natural selection

The consequences of natural selection can be understood from a purely statistical perspective. In contrast, an explicitly causal approach is required to understand why trait values covary with fitness. In particular, key evolutionary constructs, such as sexual selection, fecundity selection, and so on, are best understood as selection via particular fitness components. To formalize and operationalize these concepts, we must disentangle the various causal pathways contributing to selection. Such decompositions are currently only known for linear models, where they are sometimes referred to as “Wright's rules.” Here, we provide a general framework, based on path analysis, for partitioning selection among its contributing causal pathways. We show how the extended selection gradient—which represents selection arising from a trait's causal effects on fitness—can be decomposed into path-specific selection gradients, which correspond to distinct causal mechanisms of selection. This framework allows for nonlinear effects and nonadditive interactions among variables, which may be estimated using standard statistical methods (e.g., generalized linear [mixed] models or generalized additive models). We thus provide a generalization of Wright's path rules that accommodates the nonlinear and nonadditive mechanisms by which natural selection commonly arises.     

The causal pie model: an epidemiological method applied to evolutionary biology and ecology

A general concept for thinking about causality facilitates swift comprehension of results, and the vocabulary that belongs to the concept is instrumental in cross‐disciplinary communication. The causal pie model has fulfilled this role in epidemiology and could be of similar value in evolutionary biology and ecology. In the causal pie model, outcomes result from sufficient causes. Each sufficient cause is made up of a “causal pie” of “component causes”. Several different causal pies may exist for the same outcome. If and only if all component causes of a sufficient cause are present, that is, a causal pie is complete, does the outcome occur. The effect of a component cause hence depends on the presence of the other component causes that constitute some causal pie. Because all component causes are equally and fully causative for the outcome, the sum of causes for some outcome exceeds 100%. The causal pie model provides a way of thinking that maps into a number of recurrent themes in evolutionary biology and ecology: It charts when component causes have an effect and are subject to natural selection, and how component causes affect selection on other component causes; which partitions of outcomes with respect to causes are feasible and useful; and how to view the composition of a(n apparently homogeneous) population. The diversity of specific results that is directly understood from the causal pie model is a test for both the validity and the applicability of the model. The causal pie model provides a common language in which results across disciplines can be communicated and serves as a template along which future causal analyses can be made.     

Hidden evolution: progress and limitations in detecting multifarious natural selection

From illustrative examples of research on the best-studied group of species to date, Drosophila melanogaster and its closest relatives, we argue that selection is multifarious, but often hidden. Selective fixation of new, highly advantageous alleles is the most parsimonious explanation for a typical pattern of molecular variation observed in genomic regions characterized by very low recombination: drastically reduced DNA sequence variation within species and typical levels of sequence divergence among species. At the same time, the identity of the gene (or genes) influenced by selection is not just difficult to discern; it may be impossible. Studies of the genetic basis of reproductive isolation demonstrate that, although the D. melanogaster complex species appear virtually identical, dozens of currently unidentified genes contribute to hybrid sterility. We argue that these findings are best explained by selectively-driven functional divergence and demonstrate the multifarious nature of selection. Although multifarious selection certainly occurs, the exact characters responsible for differences in survival and reproductive success are unknown. We do not see these inherent limits as a cause for despair or a problem for evolutionary biology. Instead, we hope to raise awareness of these complexities of evolution by highlighting both the progress and the limitations of characterizing multifarious natural selection.     

Darwin, Herschel, and the role of analogy in Darwin’s origin

In what follows, I consider the role of analogy in the first edition of Darwin’s Origin. I argue that Darwin follows Herschel’s methodology and hence exploits an analogy between artificial and natural selection that allows him generalize selection as a cause of evolutionary change. This argument strategy is not equivalent to an argument from analogy. Reading Darwin’s argument as conforming to Herschel’s two-step methodology of causal analysis followed by generalization allows us to understand the role and placement of Darwin’s discussion of artificial selection in the Origin, without making the mistake of portraying Darwin’s argument for the existence and character of natural selection as an analogical argument.     

Natural selection. VII. History and interpretation of kin selection theory

Kin selection theory is a kind of causal analysis. The initial form of kin selection ascribed cause to costs, benefits and genetic relatedness. The theory then slowly developed a deeper and more sophisticated approach to partitioning the causes of social evolution. Controversy followed because causal analysis inevitably attracts opposing views. It is always possible to separate total effects into different component causes. Alternative causal schemes emphasize different aspects of a problem, reflecting the distinct goals, interests and biases of different perspectives. For example, group selection is a particular causal scheme with certain advantages and significant limitations. Ultimately, to use kin selection theory to analyse natural patterns and to understand the history of debates over different approaches, one must follow the underlying history of causal analysis. This article describes the history of kin selection theory, with emphasis on how the causal perspective improved through the study of key patterns of natural history, such as dispersal and sex ratio, and through a unified approach to demographic and social processes. Independent historical developments in the multivariate analysis of quantitative traits merged with the causal analysis of social evolution by kin selection.     

Experimental studies of group selection: what do they tell us about group selection in nature?

The study of group selection has developed along two autonomous lines. One approach, which we refer to as the adaptationist school, seeks to understand the evolution of existing traits by examining plausible mechanisms for their evolution and persistence. The other approach, which we refer to as the genetic school, seeks to examine how currently acting artificial or natural selection changes traits within populations and focuses on current evolutionary change. The levels of selection debate lies mainly within the adaptationist school, whereas the experimental studies of group selection lie within the genetic school. Because of the very different traditions and goals of these two schools, the experimental studies of group selection have not had a major impact on the group selection debate. We review the experimental results of the genetic school in the context of the group selection controversy and address the following questions: Under what conditions is group selection effective? What is the genetic basis of a response to group selection? How common is group selection in nature?     

Space,sympatry and speciation

Sympatric speciation remains controversial. ‘Sympatry’ originally meant “in the same geographical area”. Recently, evolutionists have redefined ‘sympatric speciation’ non‐spatially to require panmixia (m = 0.5) between a pair of demes before onset of reproductive isolation. Although panmixia is a suitable starting point in models of speciation, it is not a useful definition of sympatry in natural populations, because it becomes virtually impossible to find or demonstrate sympatry in nature. The newer, non‐spatial definition fails to address the classical debate about whether natural selection within a geographic overlap regularly causes speciation in nature, or whether complete geographic isolation is usually required. We therefore propose a more precise spatial definition by incorporating the population genetics of dispersal (or ‘cruising range’). Sympatric speciation is considerably more likely under this spatial definition than under the demic definition, because distance itself has a powerful structuring effect, even over small spatial scales comparable to dispersal. Ecological adaptation in two‐dimensional space often acts as a ‘magic trait’ that causes pleiotropic reductions of gene flow. We provide examples from our own research.     

The uniqueness of biological self-organization: challenging the Darwinian paradigm

Here we discuss the challenge posed by self-organization to the Darwinian conception of evolution. As we point out, natural selection can only be the major creative agency in evolution if all or most of the adaptive complexity manifest in living organisms is built up over many generations by the cumulative selection of naturally occurring small, random mutations or variants, i.e., additive, incremental steps over an extended period of time. Biological self-organization—witnessed classically in the folding of a protein, or in the formation of the cell membrane—is a fundamentally different means of generating complexity. We agree that self-organizing systems may be fine-tuned by selection and that self-organization may be therefore considered a complementary mechanism to natural selection as a causal agency in the evolution of life. But we argue that if self-organization proves to be a common mechanism for the generation of adaptive order from the molecular to the organismic level, then this will greatly undermine the Darwinian claim that natural selection is the major creative agency in evolution. We also point out that although complex self-organizing systems are easy to create in the electronic realm of cellular automata, to date translating in silico simulations into real material structures that self-organize into complex forms from local interactions between their constituents has not proved easy. This suggests that self-organizing systems analogous to those utilized by biological systems are at least rare and may indeed represent, as pre-Darwinists believed, a unique ascending hierarchy of natural forms. Such a unique adaptive hierarchy would pose another major challenge to the current Darwinian view of evolution, as it would mean the basic forms of life are necessary features of the order of nature and that the major pathways of evolution are determined by physical law, or more specifically by the self-organizing properties of biomatter, rather than natural selection.     

Junk or functional DNA? ENCODE and the function controversy

In its last round of publications in September 2012, the Encyclopedia Of DNA Elements (ENCODE) assigned a biochemical function to most of the human genome, which was taken up by the media as meaning the end of ‘Junk DNA’. This provoked a heated reaction from evolutionary biologists, who among other things claimed that ENCODE adopted a wrong and much too inclusive notion of function, making its dismissal of junk DNA merely rhetorical. We argue that this criticism rests on misunderstandings concerning the nature of the ENCODE project, the relevant notion of function and the claim that most of our genome is junk. We argue that evolutionary accounts of function presuppose functions as ‘causal roles’, and that selection is but a useful proxy for relevant functions, which might well be unsuitable to biomedical research. Taking a closer look at the discovery process in which ENCODE participates, we argue that ENCODE’s strategy of biochemical signatures successfully identified activities of DNA elements with an eye towards causal roles of interest to biomedical research. We argue that ENCODE’s controversial claim of functionality should be interpreted as saying that 80 % of the genome is engaging in relevant biochemical activities and is very likely to have a causal role in phenomena deemed relevant to biomedical research. Finally, we discuss ambiguities in the meaning of junk DNA and in one of the main arguments raised for its prevalence, and we evaluate the impact of ENCODE’s results on the claim that most of our genome is junk.     

Evidence of ecological niche shift in Rhododendron ponticum (L.) in Britain: Hybridization as a possible cause of rapid niche expansion

Biological invasions threaten global biodiversity and natural resources. Anticipating future invasions is central to strategies for combating the spread of invasive species. Ecological niche models are thus increasingly used to predict potential distribution of invasive species. In this study, we compare ecological niches of Rhododendron ponticum in its native (Iberian Peninsula) and invasive (Britain) ranges. Here, we test the conservation of ecological niche between invasive and native populations of R. ponticum using principal component analysis, niche dynamics analysis, and MaxEnt‐based reciprocal niche modeling. We show that niche overlap between native and invasive populations is very low, leading us to the conclusion that the two niches are not equivalent and are dissimilar. We conclude that R. ponticum occupies novel environmental conditions in Britain. However, the evidence of niche shift presented in this study should be treated with caution because of nonanalogue climatic conditions between native and invasive ranges and a small population size in the native range. We then frame our results in the context of contradicting genetic evidence on possible hybridization of this invasive species in Britain. We argue that the existing contradictory studies on whether hybridization caused niche shift in R. ponticum are not sufficient to prove or disprove this hypothesis. However, we present a series of theoretical arguments which indicate that hybridization is a likely cause of the observed niche expansion of R. ponticum in Britain.     

Speciation by natural and sexual selection: models and experiments

A large number of mathematical models have been developed that show how natural and sexual selection can cause prezygotic isolation to evolve. This article attempts to unify this literature by identifying five major elements that determine the outcome of speciation caused by selection: a form of disruptive selection, a form of isolating mechanism (assortment or a mating preference), a way to transmit the force of disruptive selection to the isolating mechanism (direct selection or indirect selection), a genetic basis for increased isolation (a one- or two-allele mechanism), and an initial condition (high or low initial divergence). We show that the geographical context of speciation (allopatry vs. sympatry) can be viewed as a form of assortative mating. These five elements appear to operate largely independently of each other and can be used to make generalizations about when speciation is most likely to happen. This provides a framework for interpreting results from laboratory experiments, which are found to agree generally with theoretical predictions about conditions that are favorable to the evolution of prezygotic isolation.     

Using path analysis to measure natural selection

We expand current methods for calculating selection coefficients using path analysis and demonstrate how to analyse nonlinear selection. While this incorporation is a straightforward extension of current procedures, the rules for combining these traits to calculate selection coefficients can be complex. We demonstrate our method with an analysis of selection in an experimental population of Arabidopsis thaliana consisting of 289 individuals. Multiple regression analyses found positive directional selection and positive nonlinear selection only for inflorescence height. In contrast, the path analyses also revealed positive directional selection for number of rosette leaves and positive nonlinear selection for leaf number and time of inflorescence initiation. These changes in conclusions came about because indirect selection was converted into direct selection with the change in causal structure. Path analysis has great promise for improving our understanding of natural selection but must be used with caution since coefficient estimates depend on the assumed causal structure.