Correction to: Evolution of multicellularity: cheating done right

Nature, 2014

Cooperation is central to the emergence of multicellular life; however, the means by which the earliest collectives (groups of cells) maintained integrity in the face of destructive cheating types is unclear. One idea posits cheats as a primitive germ line in a life cycle that facilitates collective reproduction. Here we describe an experiment in which simple cooperating lineages of bacteria were propagated under a selective regime that rewarded collective-level persistence. Collectives reproduced via life cycles that either embraced, or purged, cheating types. When embraced, the life cycle alternated between phenotypic states. Selection fostered inception of a developmental switch that underpinned the emergence of collectives whose fitness, during the course of evolution, became decoupled from the fitness of constituent cells. Such development and decoupling did not occur when groups reproduced via a cheat-purging regime. Our findings capture key events in the evolution of Darwinian individuality during the transition from single cells to multicellularity.

Annual Review of Ecology, Evolution, and Systematics, 2007

Biology & Philosophy, 2019

For decades Darwinian processes were framed in the form of the Lewontin conditions: reproduction, variation and reproductive success taken to be sufficient and necessary. Since Buss (1987) and the work of Maynard Smith and Szathmáry (1995) biologists were eager to explain the major transitions from individuals to groups forming new individuals subject to Darwinian mechanisms themselves. Explanations that seek to explain the emergence of a new level of selection, however, cannot employ properties that would already have to exist on that level for selection to take place. Hammerschmidt et al. (2014) provided an experiment corroborating much of the theoretical work Paul Rainey has done since 2003 on how new Darwinian individuals on a multicellular level can occur with a relaxed version of the Lewontin conditions. In this paper I will evaluate the significance of their results for future research and the debates surrounding multi-level selection.

Proceedings of the National Academy of Sciences, 2012

Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes. complexity | cooperation | major transitions | individuality | macro evolution T he evolution of multicellularity was transformative for life on earth (1). In addition to larger size, multicellularity increased biological complexity through the formation of new biological structures. For example, multicellular organisms have evolved sophisticated, higher-level functionality via cooperation among component cells with complementary behaviors (2, 3). However, dissolution and death of multicellular individuals occurs when cooperation breaks down, cancer being a prime example (4). There are multiple mechanisms to help ensure cooperation of component cells in most extant multicellular species (5-8), but the origin and the maintenance of multicellularity are two distinct evolutionary problems. Component cells in a nascent multicellular organism would appear to have frequent opportunities to pursue noncooperative reproductive strategies at a cost to the reproduction of the multicellular individual. How, then, does the transition to multicellularity occur?

Heredity, 2001

Journal of Theoretical Biology, 2006

The fitness of an evolutionary individual can be understood in terms of its two basic components: survival and reproduction. As embodied in current theory, trade-offs between these fitness components drive the evolution of life-history traits in extant multicellular organisms. Here, we argue that the evolution of germ-soma specialization and the emergence of individuality at a new higher level during the transition from unicellular to multicellular organisms are also consequences of trade-offs between the two components of fitnesssurvival and reproduction. The models presented here explore fitness trade-offs at both the cell and group levels during the unicellular-multicellular transition. When the two components of fitness negatively covary at the lower level there is an enhanced fitness at the group level equal to the covariance of components at the lower level. We show that the group fitness trade-offs are initially determined by the cell level trade-offs. However, as the transition proceeds to multicellularity, the group level trade-offs depart from the cell level ones, because certain fitness advantages of cell specialization may be realized only by the group. The curvature of the trade-off between fitness components is a basic issue in life-history theory and we predict that this curvature is concave in single-celled organisms but becomes increasingly convex as group size increases in multicellular organisms. We argue that the increasingly convex curvature of the trade-off function is driven by the initial cost of reproduction to survival which increases as group size increases. To illustrate the principles and conclusions of the model, we consider aspects of the biology of the volvocine green algae, which contain both unicellular and multicellular members. r (C.A. Solari), [email protected] (M. Hurand), [email protected] (A.M. Nedelcu).

American Journal of Botany, 2014

Multicellularity has evolved at least once in every major eukaryotic clade (in all ploidy levels) and numerous times among the prokaryotes. According to a standard multilevel selection (MLS) model, in each case, the evolution of multicellularity required the acquisition of cell-cell adhesion, communication, cooperation, and specialization attended by a compulsory alignment-of-fi tness phase and an export-of-fi tness phase to eliminate cell-cell confl ict and to establish a reproductively integrated phenotype. These achievements are reviewed in terms of generalized evolutionary developmental motifs (or "modules") whose overall logic constructs were mobilized and executed differently in bacteria, plants, fungi, and animals. When mapped onto a matrix of theoretically possible body plan morphologies (i.e., a morphospace), these motifs and the MLS model identify a "unicellular colonial multicellular" transformation series of body plans that mirrors trends observed in the majority of algae (i.e., a polyphyletic collection of photoautotrophic eukaryotes) and in the land plants, fungi, and animals. However, an alternative, more direct route to multicellularity theoretically exists, which may account for some aspects of fungal and algal evolution, i.e., a "siphonous multicellular" transformation series. This review of multicellularity attempts to show that natural selection typically acts on functional traits rather than on the mechanisms that generate them ("Many roads lead to Rome.") and that genome sequence homologies do not invariably translate into morphological homologies ("Rome isn't what it used to be."). This paper reviews the evolutionary origins of multicellularity and explores the developmental bio -logic constructs required for the fabrication of a multicellular body plan. A broad comparative approach is adopted because multicellularity has evolved multiple times in different ways in very different clades and because different criteria have been established to defi ne individuality in the context of multicellularity . Estimates of the exact number of times vary, depending on how multicellularity is defi ned and in what phylogenetic context. When described simply as a cellular aggregation, multicellular organisms are estimated conservatively to have evolved in at least 25 lineages , making it a "minor major" evolutionary transformation. When more stringent criteria are applied, as for example a requirement

Biology Letters, 2015

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.

2003

The basic problem in an evolutionary transition in complexity is to understand how a group of individuals becomes a new kind of individual, having heritable variation in fitness at the new level of organization. We see the formation of cooperative interactions among lower-level individuals as a necessary step in evolutionary transitions; only cooperation transfers fitness from lower levels (costs to group members) to higher levels (benefits to the group). As cooperation creates a new level of fitness, it creates the opportunity for conflict between the new level and the lower level. Fundamental to the emergence of a new higherlevel individual is the mediation of conflict among lower-level individuals in favor of the higher-level unit. We define a conflict mediator as a feature of the cell-group (the emerging multicellular organism) that restricts the opportunity for fitness variation at the lower level (cells) and/or enhances the variation in fitness at the higher level (the cell-gr...