Evolution of multicellularity: cheating done right

Selection, 2001

Evolutionary transitions require the organization of genetic variation at two (or more) levels of selection so that fitness heritability may emerge at the new higher level. For example, in case of the transition from single cells to multicellular organisms, single cells must, as it were, relinquish their claim to flourish and multiply in favor of the multicellular group. In this paper we consider the consequences on fitness variation and heritability of two main modes of reproduction used in multicellular organisms: vegetative reproduction, where the offspring originates from a group of cells of the adult (a propagule), and single-cell reproduction, where development starts from only one cell. Most modern organisms pass through a single-cell stage during their life-cycle, a possible explanation being that the single-cell stage increases the effectiveness of organism selection relative to cell selection, by increasing the kinship among cells within the organism. To study this hypothesis we consider simple cell colonies reproducing by fragments or propagules of differing size, with mutations occurring during colony growth. Mutations are deleterious at the colony level, but can be advantageous or deleterious at the cell level (termed "selfish" or "uniformly deleterious" mutants, respectively). In our model fragment size affects fitness in two ways, through a direct effect on group size (which in turn affects fitness) and by affecting the within and between group variances and opportunity for selection on mutations at the two levels. We show that the evolution of fragment size is determined primarily by its direct effects on group size, except when mutations are selfish. When mutations are selfish, smaller propagule size may be selected, including single-cell reproduction, even though smaller propagule size has a direct fitness cost by virtue of producing smaller groups. Using continuous distributions of mutational effects, we show that selfish mutants have an important effect on mutational load and selection on propagule size, even when selfish mutations are relatively infrequent. We then consider the role of deleterious mutation in the evolution of the germ line. Two possible ways to mediate conflict in the germ line are considered: reduction in development time (of the germ line relative to the soma) and lowered mutation rate in the germ line. The evolution of shorter development time in the germ line depends critically on whether and how the number of gametes influences fitness. If there is a direct effect of the number of gametes on fitness, it will be difficult for shorter development times in the germ line to evolve. We conclude that a lowered mutation rate in the germ line relative to the soma provides the most robust rationale for the origin of the germ line.

An evolutionary transition in individuality (ETI) is a fundamental shift in the unit of adaptation. ETIs occur through the evolution of groups of individuals into a new higher-level individual. The evolution of groups with cells specialized in somatic (viability) or reproductive functions has been proposed as a landmark of the unicellular to multicellular ETI. Several recent models of the evolution of multicellularity and cellular specialization have contributed insights on different aspects of this topic; however, these works are disconnected from each other and from the general framework of ETIs. While each of these works is valuable on its own, our interest in ETIs motivates an attempt to connect these models. We review the theory of ETIs along with these recent models with an eye towards better integrating insights from these models into the ETI framework. We consider how each model addresses key recurring topics, such as the importance of cooperation and conflict, life history trade-offs, multi-level selection, division of labor and the decoupling of fitness at the level of the group from the level of the cell. Finally, we identify a few areas in which conflicting views or unanswered questions remain, and we discuss modeling strategies that would be most suited for making further progress in understanding ETIs.

Heredity, 2001

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.

Annual Review of Ecology, Evolution, and Systematics, 2007

Biology Bulletin, 2010

The formation of morphogenetic mechanisms during emergence of multicellularity is discussed in this article.

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?

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

2014

Multicellular organisms probably originated as groups of cells formed in several ways, including cell proliferation from a group of founder cells and aggregation. Cooperation among cells benefits the group, but may be costly (altruistic) or beneficial (synergistic) to individual cooperating cells. In this paper, we study conflict mediation, the process by which genetic modifiers evolve that enhance cooperation by altering the parameters of development or rules of forma-tion of cell groups. We are particularly interested in the conditions under which these modifiers lead to a new higher-level unit of selection with increased cooperation among group members and heritable variation in fitness at the group level. By sculpting the fitness variation and opportunity for selection at the two levels, conflict modifiers create new functions at the organism level. An organism is more than a group of cooperating cells related by common descent; organisms require adaptations that regulate confli...

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.