The effect of bottleneck size on evolution in nested Darwinian populations.

Previous work has shown how a minimal ecological structure consisting of patchily distributed resources and recurrent dispersal between patches can scaffold Darwinian properties onto collections of cells. When the timescale of dispersal is long compared with the time to consume resources, patch fitness increases but comes at a cost to cell growth rates. This creates conditions that initiate evolutionary transitions in individuality. A key feature of the scaffold is a bottleneck created during dispersal, causing patches to be founded by single cells. The bottleneck decreases competition within patches and, hence, creates a strong hereditary link at the level of patches. Here, we construct a fully stochastic model to investigate the effect of bottleneck size on the evolutionary dynamics of both cells and collectives. We show that larger bottlenecks simply slow the dynamics, but, at some point, which depends on the parameters of the within-patch model, the direction of evolution towards the equilibrium reverses. Introduction of random fluctuations in bottleneck sizes with some positive probability of smaller sizes counteracts this, even when the probability of smaller bottlenecks is minimal.

Taming fitness: Organism-environment interdependencies preclude long-term fitness forecasting.

Fitness is a central but notoriously vexing concept in evolutionary biology. The propensity interpretation of fitness is often regarded as the least problematic account for fitness. It ties an individual's fitness to a probabilistic capacity to produce offspring. Fitness has a clear causal role in evolutionary dynamics under this account. Nevertheless, the propensity interpretation faces its share of problems. We discuss three of these. We first show that a single scalar value is an incomplete summary of a propensity. Second, we argue that the widespread method of "abstracting away" environmental idiosyncrasies by averaging over reproductive output in different environments is not a valid approach when environmental changes are irreversible. Third, we point out that expanding the range of applicability for fitness measures by averaging over more environments or longer time scales (so as to ensure environmental reversibility) reduces one's ability to distinguish selectively relevant differences among individuals because of mutation and eco-evolutionary feedbacks. This series of problems leads us to conclude that a general value of fitness that is both explanatory and predictive cannot be attained. We advocate for the use of propensity-compatible methods, such as adaptive dynamics, which can accommodate these difficulties.

When local causes are more explanatorily useful.

Madole & Harden plead for better integration of causal knowledge of different depths to understand complex human traits. Classically, local causes - a particular type of shallow causes - are considered less useful than more generalisable causes, giving a false impression that the latter causes are more useful and desirable. Using a simple example, I show that sometimes the contrary is true.

Unifying heritability in evolutionary theory.

Despite being widely used in both biology and psychology as if it were a single notion, heritability is not a unified concept. This is also true in evolutionary theory, in which the word 'heritability' has at least two technical definitions that only partly overlap. These yield two approaches to heritability: the 'variance approach' and the 'regression approach.' In this paper, I aim to unify these two approaches. After presenting them, I argue that a general notion of heritability ought to satisfy two desiderata-'general applicability' and 'separability of the causes of resemblance.' I argue that neither the variance nor the regression approach satisfies these two desiderata concomitantly. From there, I develop a general definition of heritability that relies on the distinction between intrinsic and extrinsic properties. I show that this general definition satisfies the two desiderata. I then illustrate the potential usefulness of this general definition in the context of microbiome research.

On the causal interpretation of heritability from a structural causal modeling perspective.

Heritability estimated using the analysis of variance (ANOVA) for ascribing causal responsibility to genes for a phenotype has been criticized widely. First, there are problems associated with articulating the exact causal meaning of heritability in the standard model. Second, in conditions of gene-environment interaction or covariation that violate the assumptions made by the standard model, a causal interpretation of heritability is thought to be unwarranted. This paper aims to rethink these ideas and associated disputes from a structural causal modeling (SCM) perspective. Using SCM, we show that, in the standard model, heritability reflects the causal effect of eliminating genotypic differences on the change of phenotypic variance of a population. In the presence of interaction or covariation, heritability is estimated incorrectly using ANOVA. However, SCM can provide the causal effect of genotypes on the phenotypic variance regarding particular interventions. We also show that SCM can identify different types of causal effect and answer individual-level causal questions. We conclude that SCM has the resources to provide a systematic causal interpretation that can supplement traditional heritability estimates via ANOVA and offer a more substantial causal analysis of genetic causation.

Measuring Causal Invariance Formally.

Invariance is one of several dimensions of causal relationships within the interventionist account. The more invariant a relationship between two variables, the more the relationship should be considered paradigmatically causal. In this paper, I propose two formal measures to estimate invariance, illustrated by a simple example. I then discuss the notion of invariance for causal relationships between non-nominal (i.e., ordinal and quantitative) variables, for which Information theory, and hence the formalism proposed here, is not well suited. Finally, I propose how invariance could be qualified for such variables.

Function, persistence, and selection: Generalizing the selected-effect account of function adequately.

The selected effect account is regarded by many as one of the most attractive accounts of function. This account assumes that the function of a trait is what it has been selected for. Recently, it has been generalized by Justin Garson to include cases in which selection is understood as a simple sorting process, i.e., a selection process between entities that do not reproduce. However, once extended, this generalized selected effect account seems to ascribe functions to entities for which it looks unintuitive to do so. For instance, the hardness of rocks on a beach being differentially eroded by waves would be ascribed the function of resisting erosion. Garson provides one central argument why, despite appearance, one should not ascribe functions in cases of such sorting processes. In this paper, I start by presenting his argument, which hinges on whether a collection of entities form a population. I find it wanting. I argue instead that some selection processes are evolutionarily more or less interesting and that when a selection process is regarded as evolutionarily uninteresting, it will yield an uninteresting form of function rather than a reason for withholding the concept of function altogether.

Have Causal Claims About the Gut Microbiome Been Over-Hyped?

Microbiome research attributes to whole microbiomes a causal role in the occurrence of different health outcomes. I argue, following some distinctions about causal relationships and explanations made within a philosophical account of causation, the "interventionist account," that such claims need more scrutiny.

Natural selection and the reference grain problem.

Over the last 20 years, the concept of natural selection has been highly debated in the philosophy of biology. Yet, most discussions on this topic have focused on the questions of whether natural selection is a causal process and whether it can be distinguished from drift. In this paper, I identify another sort of problem with respect to natural selection. I show that, in so far as a classical definition of fitness includes the transmission of a type between generations as part of the definition, it seems difficult to see how the fitness of an entity, following this definition, could be description independent. In fact, I show that by including type transmission as part of the definition of fitness, changing the grain at which the type of an entity is described can change the fitness of that entity. If fitness is not grain-of-description independent, this further propagates to the process of natural selection itself. I call this problem the 'reference grain problem'. I show that it can be linked to the reference class problem in probability theory. I tentatively propose two solutions to it.

Why the missing heritability might not be in the DNA.

There are four major hypotheses (H1, H2, H3, and H4) as to the source of missing heritability. We propose that estimates obtained from GWAS underestimate heritability by not taking into account non-DNA (epigenetic) sources of heritability. Taking those factors into account (H4) should result in increased heritability estimates.

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.

Generalizing Contextual Analysis.

Okasha, in Evolution and the Levels of Selection, convincingly argues that two rival statistical decompositions of covariance, namely contextual analysis and the neighbour approach, are better causal decompositions than the hierarchical Price approach. However, he claims that this result cannot be generalized in the special case of soft selection and argues that the Price approach represents in this case a better option. He provides several arguments to substantiate this claim. In this paper, I demonstrate that these arguments are flawed and argue that neither the Price equation nor the contextual and neighbour partitionings sensu Okasha are adequate causal decompositions in cases of soft selection. The Price partitioning is generally unable to detect cross-level by-products and this naturally also applies to soft selection. Both contextual and neighbour partitionings violate the fundamental principle of determinism that the same cause always produces the same effect. I argue that a fourth partitioning widely used in the contemporary social sciences, under the generic term of 'hierarchical linear model' and related to contextual analysis understood broadly, addresses the shortcomings of the three other partitionings and thus represents a better causal decomposition. I then defend this model against the argument that because it predicts that there is some organismal selection in some specific cases of segregation distortion then it should be rejected. I show that cases of segregation distortion that intuitively seem to contradict the conclusion drawn from the hierarchical linear model are in fact cases of multilevel selection 2 while the assessment of the different partitionings are restricted to multilevel selection 1.

A coarse-graining account of individuality: how the emergence of individuals represents a summary of lower-level evolutionary processes.

Explaining the emergence of individuality in the process of evolution remains a challenge; it faces the difficulty of characterizing adequately what 'emergence' amounts to. Here, I present a pragmatic account of individuality in which I take up this challenge. Following this account, individuals that emerge from an evolutionary transition in individuality are coarse-grained entities: entities that are summaries of lower-level evolutionary processes. Although this account may prima facie appear to ultimately rely on epistemic considerations, I show that it can be used to vindicate the emergence of individuals in a quasi-ontological sense. To this end, I discuss a recent account of evolutionary transitions in individuality proposed by Godfrey-Smith and Kerr (Brit J Philos Sci 64(1):205-222, 2013) where a transition occurs through several stages, each with an accompanying model. I focus on the final stage where higher-level entities are ascribed a separate fitness parameter, while they were not in the previous stages. In light of my account, I provide some justification for why such a change in parameters is necessary and cannot be dismissed as merely epistemic.

Integrating evolutionary, developmental and physiological mismatch.

Contemporary evolutionary medicine has unified the idea of 'evolutionary mismatch', derived from the older idea of 'adaptive lag' in evolution, with ideas about the mismatch in development and physiology derived from the Developmental Origins of Health and Disease (DOHaD) paradigm. A number of publications in evolutionary medicine have tried to make this theoretical framework explicit. The integrative theory of mismatch captures how organisms track environments across space and time on multiple scales in order to maintain an adaptive match to the environment, and how failures of adaptive tracking lead to disease. In this review, we try to present this complex body of theory as clearly and simply as possible with the aim of facilitating its application in new domains. We introduce terminology, which is as far as possible consistent with earlier usage, to distinguish the different forms of mismatch. Mismatch in its modern form is a productive organizing concept that can help researchers articulate how physiology, development and evolution interact with one another and with environmental change to explain health outcomes.

Tradeoff breaking as a model of evolutionary transitions in individuality and limits of the fitness-decoupling metaphor.

Evolutionary transitions in individuality (ETIs) involve the formation of Darwinian collectives from Darwinian particles. The transition from cells to multicellular life is a prime example. During an ETI, collectives become units of selection in their own right. However, the underlying processes are poorly understood. One observation used to identify the completion of an ETI is an increase in collective-level performance accompanied by a decrease in particle-level performance, for example measured by growth rate. This seemingly counterintuitive dynamic has been referred to as fitness decoupling and has been used to interpret both models and experimental data. Extending and unifying results from the literature, we show that fitness of particles and collectives can never decouple because calculations of fitness performed over appropriate and equivalent time intervals are necessarily the same provided the population reaches a stable collective size distribution. By way of solution, we draw attention to the value of mechanistic approaches that emphasise traits, and tradeoffs among traits, as opposed to fitness. This trait-based approach is sufficient to capture dynamics that underpin evolutionary transitions. In addition, drawing upon both experimental and theoretical studies, we show that while early stages of transitions might often involve tradeoffs among particle traits, later-and critical-stages are likely to involve the rupture of such tradeoffs. Thus, when observed in the context of ETIs, tradeoff-breaking events stand as a useful marker of these transitions.

Natural Selection beyond Life? A Workshop Report.

Natural selection is commonly seen not just as an explanation for adaptive evolution, but as the inevitable consequence of "heritable variation in fitness among individuals". Although it remains embedded in biological concepts, such a formalisation makes it tempting to explore whether this precondition may be met not only in life as we know it, but also in other physical systems. This would imply that these systems are subject to natural selection and may perhaps be investigated in a biological framework, where properties are typically examined in light of their putative functions. Here we relate the major questions that were debated during a three-day workshop devoted to discussing whether natural selection may take place in non-living physical systems. We start this report with a brief overview of research fields dealing with "life-like" or "proto-biotic" systems, where mimicking evolution by natural selection in test tubes stands as a major objective. We contend the challenge may be as much conceptual as technical. Taking the problem from a physical angle, we then discuss the framework of dissipative structures. Although life is viewed in this context as a particular case within a larger ensemble of physical phenomena, this approach does not provide general principles from which natural selection can be derived. Turning back to evolutionary biology, we ask to what extent the most general formulations of the necessary conditions or signatures of natural selection may be applicable beyond biology. In our view, such a cross-disciplinary jump is impeded by reliance on individuality as a central yet implicit and loosely defined concept. Overall, these discussions thus lead us to conjecture that understanding, in physico-chemical terms, how individuality emerges and how it can be recognised, will be essential in the search for instances of evolution by natural selection outside of living systems.

Ecological scaffolding and the evolution of individuality.

Evolutionary transitions in individuality are central to the emergence of biological complexity. Recent experiments provide glimpses of processes underpinning the transition from single cells to multicellular life and draw attention to the critical role of ecology. Here, we emphasize this ecological dimension and argue that its current absence from theoretical frameworks hampers development of general explanatory solutions. Using mechanistic mathematical models, we show how a minimal ecological structure comprising patchily distributed resources and between-patch dispersal can scaffold Darwinian-like properties on collectives of cells. This scaffolding causes cells to participate directly in the process of evolution by natural selection as if they were members of multicellular collectives, with collectives participating in a death-birth process arising from the interplay between the timing of dispersal events and the rate of resource use by cells. When this timescale is sufficiently long and new collectives are founded by single cells, collectives experience conditions that favour evolution of a reproductive division of labour. Together our simple model makes explicit key events in the major evolutionary transition to multicellularity. It also makes predictions concerning the life history of certain pathogens and serves as an ecological recipe for experimental realization of evolutionary transitions.

Evolutionary transitions in heritability and individuality.

With a few exceptions, the literature on evolutionary transitions in individuality (ETIs) has mostly focused on the relationships between lower-level (particle-level) and higher-level (collective-level) selection, leaving aside the question of the relationship between particle-level and collective-level inheritance. Yet, without an account of this relationship, our hope to fully understand the evolutionary mechanisms underlying ETIs is impeded. To that effect, I present a highly idealized model to study the relationship between particle-level and collective-level heritability both when a collective-level trait is a linear function and when it is a nonlinear function of a particle-level trait. I first show that when a collective trait is a linear function of a particle-level trait, collective-level heritability is a by-product of particle-level heritability. It is equal to particle-level heritability, whether the particles interact randomly or not to form collectives. Second, I show that one effect of population structure is the reduction in variance in offspring collective-level character for a given parental collective. I propose that this reduction in variance is one dimension of individuality. Third, I show that even in the simple case of a nonlinear collective-level character, collective-level heritability is not only weak but also highly dependent on the frequency of the different types of particles in the global population. Finally, I show that population structure, because one of its effects is to reduce the variance in offspring collective-level character, allows not only for an increase in collective-level character but renders it less context dependent. This in turn permits a stable collective-level response to selection. The upshot is that population structure is a driver for ETIs. These results are particularly significant in that the relationship between population structure and collective-level heritability has, to my knowledge, not been previously explored in the context of ETIs.

Multispecies individuals.

We assess the arguments for recognising functionally integrated multispecies consortia as genuine biological individuals, including cases of so-called 'holobionts'. We provide two examples in which the same core biochemical processes that sustain life are distributed across a consortium of individuals of different species. Although the same chemistry features in both examples, proponents of the holobiont as unit of evolution would recognize one of the two cases as a multispecies individual whilst they would consider the other as a compelling case of ecological dependence between separate individuals. Some widely used arguments in support of the 'holobiont' concept apply equally to both cases, suggesting that those arguments have misidentified what is at stake when seeking to identify a new level of biological individuality. One important aspect of biological individuality is evolutionary individuality. In line with other work on the evolution of individuality, we show that our cases can be distinguished by focusing on the fitness alignment between the partners of the consortia. We conclude that much of the evidence currently presented for the ubiquity and importance of multi-species individuals is simply not to the point, at least unless the issue of biological individuality is firmly divorced from the question of evolutionary individuality.

Surveillance cues enhance moral condemnation.

Humans pay close attention to the reputational consequences of their actions. Recent experiments indicate that even very subtle cues that one is being observed can affect cooperative behaviors. Expressing our opinions about the morality of certain acts is a key means of advertising our cooperative dispositions. Here, we investigated how subtle cues of being watched would affect moral judgments. We predicted that participants exposed to such cues would affirm their endorsement of prevailing moral norms by expressing greater disapproval of moral transgressions. Participants read brief accounts of two moral violations and rated the moral acceptability of each violation. Violations were more strongly condemned in a condition where participants were exposed to surveillance cues (an image of eyes interposed between the description of the violation and the associated rating scale) than in a control condition (in which the interposed image was of flowers). We discuss the role that public declarations play in the interpersonal evaluation of cooperative dispositions.