Group and individual selection during evolutionary transitions in individuality: meanings and partitions.

The Price equation embodies the 'conditions approach' to evolution in which the Darwinian conditions of heritable variation in fitness are represented in equation form. The equation can be applied recursively, leading to a partition of selection at the group and individual levels. After reviewing the well-known issues with the Price partition, as well as issues with a partition based on contextual analysis, we summarize a partition of group and individual selection based on counterfactual fitness, the fitness that grouped cells would have were they solitary. To understand 'group selection' in multi-level selection models, we assume that only group selection can make cells suboptimal when they are removed from the group. Our analyses suggest that there are at least three kinds of selection that can be occurring at the same time: group-specific selection along with two kinds of individual selection, within-group selection and global individual selection. Analyses based on counterfactual fitness allow us to specify how close a group is to being a pseudo-group, and this can be a basis for quantifying progression through an evolutionary transition in individuality (ETI). During an ETI, fitnesses at the two levels, group and individual, become decoupled, in the sense that fitness in a group may be quite high, even as counterfactual fitness goes to zero. This article is part of the theme issue 'Fifty years of the Price equation'.

Generation time and fitness tradeoffs during the evolution of multicellularity.

The evolution of multicellular organisms from their unicellular ancestors is an example of an evolutionary transition in individuality (ETI), i.e. a change in the units of selection and adaptation. The theory of ETIs poses particular challenges because, by definition, key theoretical constructs such as fitness are shifting during an ETI. Past work emphasized the importance of life history tradeoffs during ETIs in which lower level units form groups and become individuals at a higher level. In particular, it has been hypothesized that the convexity of the lower-level tradeoff between viability and fecundity changes with group size and determines the optimality of lower-level specialization in the fitness components of the group. This is important because lower-level specialization is a key indicator of higher-level individuality. Here we show that increasing generation time can increase the convexity of the lower-level viability-fecundity tradeoff. This effect is a novel hypothesis for the positive association between cell-group size and cellular specialization in a major model system for ETIs, the volvocine algae. The pattern in this clade is thought to be an example of a more general size-complexity rule. Our hypothesis is that larger groups have longer generation times and longer generation times lead to more convex lower-level viability-fecundity tradeoffs, which could account for specialization being optimal only in larger cell groups (colonies). We discuss the robustness of this effect to various changes in the assumptions of our model. Our work is important for the study of ETIs in general because viability and fecundity are fundamental components of fitness in all systems and because generation time is expected to be changing during many ETIs.

Models of cell division initiation in Chlamydomonas: A challenge to the consensus view.

We develop and compare two models for division initiation in cells of the unicellular green alga Chlamydomonas reinhardtii, a topic that has remained controversial in spite of years of empirical work. Achieving a better understanding of C. reinhardtii cell cycle regulation is important because this species is used in studies of fundamental eukaryotic cell features and in studies of the evolution of multicellularity. C. reinhardtii proliferates asexually by multiple fission, interspersing rapid rounds of symmetric division with prolonged periods of growth. Our Model 1 reflects major elements of the current consensus view on C. reinhardtii division initiation, with cells first growing to a specific size, then waiting for a particular time prior to division initiation. In Model 2, our proposed alternative, growing cells divide when they have reached a growth-rate-dependent target size. The two models imply a number of different empirical patterns. We highlight these differences alongside published data, which currently fall short of unequivocally distinguishing these differences in predicted cell behavior. Nevertheless, several lines of evidence are suggestive of more Model 2-like behavior than Model 1-like behavior. Our specification of these models adds rigor to issues that have too often been worked out in relation to loose, verbal models and is directly relevant to future development of informative experiments.

A model for the origin of group reproduction during the evolutionary transition to multicellularity.

During the evolution of multicellular organisms, the unit of selection and adaptation, the individual, changes from the single cell to the multicellular group. To become individuals, groups must evolve a group life cycle in which groups reproduce other groups. Investigations into the origin of group reproduction have faced a chicken-and-egg problem: traits related to reproduction at the group level often appear both to be a result of and a prerequisite for natural selection at the group level. With a focus on volvocine algae, we model the basic elements of the cell cycle and show how group reproduction can emerge through the coevolution of a life-history trait with a trait underpinning cell cycle change. Our model explains how events in the cell cycle become reordered to create a group life cycle through continuous change in the cell cycle trait, but only if the cell cycle trait can coevolve with the life-history trait. Explaining the origin of group reproduction helps us understand one of life's most familiar, yet fundamental, aspects-its hierarchical structure.

A Darwinian approach to the origin of life cycles with group properties.

A selective explanation for the evolution of multicellular organisms from unicellular ones requires knowledge of both selective pressures and factors affecting the response to selection. Understanding the response to selection is particularly challenging in the case of evolutionary transitions in individuality, because these transitions involve a shift in the very units of selection. We develop a conceptual framework in which three fundamental processes (growth, division, and splitting) are the scaffold for unicellular and multicellular life cycles alike. We (i) enumerate the possible ways in which these processes can be linked to create more complex life cycles, (ii) introduce three genes based on growth, division and splitting that, acting in concert, determine the architecture of the life cycles, and finally, (iii) study the evolution of the simplest five life cycles using a heuristic model of coupled ordinary differential equations in which mutations are allowed in the three genes. We demonstrate how changes in the regulation of three fundamental aspects of colonial form (cell size, colony size, and colony cell number) could lead unicellular life cycles to evolve into primitive multicellular life cycles with group properties. One interesting prediction of the model is that selection generally favors cycles with group level properties when intermediate body size is associated with lowest mortality. That is, a universal requirement for the evolution of group cycles in the model is that the size-mortality curve be U-shaped. Furthermore, growth must decelerate with size.

Cellular differentiation and individuality in the 'minor' multicellular taxa.

Biology needs a concept of individuality in order to distinguish organisms from parts of organisms and from groups of organisms, to count individuals and compare traits across taxa, and to distinguish growth from reproduction. Most of the proposed criteria for individuality were designed for 'unitary' or 'paradigm' organisms: contiguous, functionally and physiologically integrated, obligately sexually reproducing multicellular organisms with a germ line sequestered early in development. However, the vast majority of the diversity of life on Earth does not conform to all of these criteria. We consider the issue of individuality in the 'minor' multicellular taxa, which collectively span a large portion of the eukaryotic tree of life, reviewing their general features and focusing on a model species for each group. When the criteria designed for unitary organisms are applied to other groups, they often give conflicting answers or no answer at all to the question of whether or not a given unit is an individual. Complex life cycles, intimate bacterial symbioses, aggregative development, and strange genetic features complicate the picture. The great age of some of the groups considered shows that 'intermediate' forms, those with some but not all of the traits traditionally associated with individuality, cannot reasonably be considered ephemeral or assumed transitional. We discuss a handful of recent attempts to reconcile the many proposed criteria for individuality and to provide criteria that can be applied across all the domains of life. Finally, we argue that individuality should be defined without reference to any particular taxon and that understanding the emergence of new kinds of individuals requires recognizing individuality as a matter of degree.

Distributions of reproductive and somatic cell numbers in diverse Volvox (Chlorophyta) species.

BACKGROUND: Volvox (Chlorophyta) asexual colonies consist of two kinds of cells: a large number of small somatic cells and a few large reproductive cells. The numbers of reproductive and somatic cells correspond directly to the major components of fitness - fecundity and viability, respectively. Volvox species display diverse patterns of development that give rise to the two cell types. QUESTIONS: For Volvox species under fixed conditions, do species differ with respect to the distribution of somatic and reproductive cell numbers in a population of asexual clones? Specifically, do they differ with respect to the dispersion of the distribution, i.e. with respect to their intrinsic variability? If so, are these differences related to major among-species developmental differences? DATA DESCRIPTION: For each of five Volvox species, we estimate the number of somatic and reproductive cells for 40 colonies and the number of reproductive cells for an additional 200 colonies. We sampled all colonies from growing, low-density, asexual populations under standard conditions. SEARCH METHOD: We compare the distribution of reproductive cell numbers to a Poisson distribution. We also compare the overall dispersion of reproductive cell number among species by calculating the coefficient of variation (CV). We compare the bivariate (reproductive and somatic cell) dataset to simulated datasets produced from a simple model of cell-type specification with intrinsic variability and colony size variation. This allows us to roughly estimate the level of intrinsic variability that is most consistent with our observed bivariate data (given an unknown level of size variation). CONCLUSIONS: The overall variability (CV) in reproductive cell number is high in Volvox compared with more complex organisms. Volvox species show differences in reproductive cell number CV that were not clearly related to development, as currently understood. If we used the bivariate data and tried to account for the effects of colony size variation, we found that the species that have fast embryonic divisions and asymmetric divisions have substantially higher intrinsic variability than the species that have slow divisions and no asymmetric divisions. Under our culture conditions, the Poisson distribution is a good description of intrinsic variability in reproductive cell number for some but not all Volvox species.