Evolution of individuality during the transition from unicellular to multicellular life

Abstract

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.

Fig. 1.

Examples of volvocine species varying in cell number, colony volume, degree of specialization, and proportion of somatic cells. (A) C. reinhardtii, a unicell. (B) Gonium pectorale, a flat or curved sheet of 8–32 undifferentiated cells. (C) Eudorina elegans, a spherical colony of 16–64 undifferentiated cells. (D) Pleodorina californica, a spherical colony with 30–50% somatic cells. (E) V. carteri. (F) Volvox aureus. Where two cell types are present (D–F), the smaller cells are somatic cells and the larger cells are reproductive cells. Photos were taken by C. Solari (University of Arizona).

Fig. 2.

Change in expression of a life-history gene in space and in time. Expression of genes is indicated by the thick arrows. The effect on fitness when the gene is on is in green, and the effect on fitness when the gene is off is in red. (A) In a unicellular individual, the gene is expressed in response to an environmental cue in a temporal context and has the effect of increasing survival while decreasing effort at reproduction. (B) This same gene is expressed in a spatial context within a multicellular individual in response to a developmental cue. The cells in which the gene is expressed increase their effort at survival and decrease their effort at reproduction. This figure was modified from ref. .

Fig. 3.

Fitness tradeoffs. Contribution to viability (v) on y axis and reproduction (b) on x axis. (A) A concave curve changes to a convex curve as group size increases. The piece-wise linear reproduction curve (solid line in B) with linear viability curve (dotted line in B) approximates a convex tradeoff curve (C) at the cell level. (D) Isoclines of group fitness are plotted with this convex tradeoff curve at the cell level. The reproductive effort e_N in B is the cost of reproduction, which increases with group size N, and in C v_max − v_max(1 − e_N) is the “bonus” of soma specialization. This bonus can be obtained only by groups. Alternatively, the bonus of specialization in soma may be viewed as the initial cost of somatic cells dedifferentiating into reproductive cells.

Fig. 4.

Two cells jointly specializing in reproduction and viability. Cell i specializes in reproductive effort, b_i, with less effort put into vegetative functions, v_i. Cell j does the reverse. Alone they would each have low fitness, but together in a group they may have high fitness if the tradeoff between reproduction and viability is convex.