Evolutionary transitions in individuality (ETIs) underlie the watershed events in the history of life on Earth, including the origins of cells, eukaryotes, plants, animals, and fungi. Each of these events constitutes an increase in the level of complexity, as groups of individuals become individuals in their own right. Among the best-studied ETIs is the origin of multicellularity in the green alga Volvox, a model system for the evolution of multicellularity and cellular differentiation. Since its divergence from unicellular ancestors, Volvox has evolved into a highly integrated multicellular organism with cellular specialization, a complex developmental program, and a high degree of coordination among cells. Remarkably, all of these changes were previously thought to have occurred in the last 50 -75 million years. Here we estimate divergence times using a multigene data set with multiple fossil calibrations and use these estimates to infer the times of developmental changes relevant to the evolution of multicellularity. Our results show that Volvox diverged from unicellular ancestors at least 200 million years ago. Two key innovations resulting from an early cycle of cooperation, conflict and conflict mediation led to a rapid integration and radiation of multicellular forms in this group. This is the only ETI for which a detailed timeline has been established, but multilevel selection theory predicts that similar changes must have occurred during other ETIs.evolution ͉ multicellularity ͉ multilevel selection ͉ transitions in individuality ͉ Volvox T he history of life on Earth has involved a number of evolutionary transitions in individuality (ETIs), in which groups of once-autonomous individuals became new individuals. Through the transfer of fitness from the individuals making up the group to the group itself, a new entity was formed with a single fitness and a single evolutionary fate. In this way, groups of interacting molecular replicators became single-celled organisms, prokaryotic cells became a primitive eukaryote, groups of single-celled organisms became multicellular organisms, and groups of multicellular organisms became social individuals (as in the social insects). In many cases such transitions have opened up entire new adaptive landscapes leading to vast radiations as completely new ways of being alive became available (e.g., cellular life, eukaryotes, plants, and animals). Understanding how and why groups of individuals become new kinds of individuals is a major challenge in explaining the history of life.The transition from unicellular to multicellular life is the paradigm case of the integration of lower-level individuals (cells) into a new higher-level individual-the multicellular organism. This transition has occurred dozens of times independently, for example in the red algae, brown algae, land plants, animals, and fungi (reviewed in ref. 1). Among the best-studied ETIs is the origin of multicellularity in the green alga Volvox and its relatives (the volvocine algae), which have been develop...
A second cycle, in which the defection of somatic cells must be prevented, may still be in progress.
Individuality is a complex trait, yet a series of stages each advantageous in itself can be shown to exist allowing evolution to get from unicellular individuals to multicellular individuals. We consider several of the key stages involved in this transition: the initial advantage of group formation, the origin of reproductive altruism within the group, and the further specialization of cell types as groups increase in size. How do groups become individuals? This is the central question we address. Our hypothesis is that fitness tradeoffs drive the transition of a cell group into a multicellular individual through the evolution of cells specialized at reproductive and vegetative functions of the group. We have modeled this hypothesis and have tested our models in two ways. We have studied the origin of the genetic basis for reproductive altruism (somatic cells specialized at vegetative functions) in the multicellular Volvox carteri by showing how an altruistic gene may have originated through cooption of a life-history tradeoff gene present in a unicellular ancestor. Second, we ask why reproductive altruism and individuality arise only in the larger members of the volvocine group (recognizing that high levels of kinship are present in all volvocine algae groups). Our answer is that the selective pressures leading to reproductive altruism stem from the increasing cost of reproduction with increasing group size. Concepts from population genetics and evolutionary biology appear to be sufficient to explain complexity, at least as it relates to the problem of the major transitions between the different kinds of evolutionary individuals.evolutionary transitions ͉ multicellularity ͉ Volvox
No abstract
The transition to multicellularity has occurred numerous times in all domains of life, yet its initial steps are poorly understood. The volvocine green algae are a tractable system for understanding the genetic basis of multicellularity including the initial formation of cooperative cell groups. Here we report the genome sequence of the undifferentiated colonial alga, Gonium pectorale, where group formation evolved by co-option of the retinoblastoma cell cycle regulatory pathway. Significantly, expression of the Gonium retinoblastoma cell cycle regulator in unicellular Chlamydomonas causes it to become colonial. The presence of these changes in undifferentiated Gonium indicates extensive group-level adaptation during the initial step in the evolution of multicellularity. These results emphasize an early and formative step in the evolution of multicellularity, the evolution of cell cycle regulation, one that may shed light on the evolutionary history of other multicellular innovations and evolutionary transitions.
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 formation 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 conflict within. Otherwise their continued evolution is frustrated by the creation of within‐organism variation and conflict between levels of selection. The evolution of conflict modifiers is a necessary prerequisite to the emergence of individuality and the continued well being of the organism. Conflict leads — through the evolution of adaptations that reduce it — to greater individuality and harmony for the organism.
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