Life-history evolution and the origin of multicellularity

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 fitness-survival 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.     

Survival benefits select for group living in a social spider despite reproductive costs

The evolution of cooperation requires benefits of group living to exceed costs. Hence, some components of fitness are expected to increase with increasing group size, whereas others may decrease because of competition among group members. The social spiders provide an excellent system to investigate the costs and benefits of group living: they occur in groups of various sizes and individuals are relatively short-lived, therefore life history traits and Lifetime Reproductive Success (LRS) can be estimated as a function of group size. Sociality in spiders has originated repeatedly in phylogenetically distant families and appears to be accompanied by a transition to a system of continuous intra-colony mating and extreme inbreeding. The benefits of group living in such systems should therefore be substantial. We investigated the effect of group size on fitness components of reproduction and survival in the social spider Stegodyphus dumicola in two populations in Namibia. In both populations, the major benefit of group living was improved survival of colonies and late-instar juveniles with increasing colony size. By contrast, female fecundity, female body size and early juvenile survival decreased with increasing group size. Mean individual fitness, estimated as LRS and calculated from five components of reproduction and survival, was maximized for intermediate- to large-sized colonies. Group living in these spiders thus entails a net reproductive cost, presumably because of an increase in intra-colony competition with group size. This cost is traded off against survival benefits at the colony level, which appear to be the major factor favouring group living. In the field, many colonies occur at smaller size than expected from the fitness curve, suggesting ecological or life history constraints on colony persistence which results in a transient population of relatively small colonies.     

A twelve-step program for evolving multicellularity and a division of labor

The volvocine algae provide an unrivalled opportunity to explore details of an evolutionary pathway leading from a unicellular ancestor to multicellular organisms with a division of labor between different cell types. Members of this monophyletic group of green flagellates range in complexity from unicellular Chlamydomonas through a series of extant organisms of intermediate size and complexity to Volvox, a genus of spherical organisms that have thousands of cells and a germ-soma division of labor. It is estimated that these organisms all shared a common ancestor about 50 +/- 20 MYA. Here we outline twelve important ways in which the developmental repertoire of an ancestral unicell similar to modern C. reinhardtii was modified to produce first a small colonial organism like Gonium that was capable of swimming directionally, then a sequence of larger organisms (such as Pandorina, Eudorina and Pleodorina) in which there was an increasing tendency to differentiate two cell types, and eventually Volvox carteri with its complete germ-soma division of labor.     

Extensive social choice and the measurement of group fitness in biological hierarchies

Extensive social choice theory is used to study the problem of measuring group fitness in a two-level biological hierarchy. Both fixed and variable group size are considered. Axioms are identified that imply that the group measure satisfies a form of consequentialism in which group fitness only depends on the viabilities and fecundities of the individuals at the lower level in the hierarchy. This kind of consequentialism can take account of the group fitness advantages of germ-soma specialization, which is not possible with an alternative social choice framework proposed by Okasha, but which is an essential feature of the index of group fitness for a multicellular organism introduced by Michod, Viossat, Solari, Hurand, and Nedelcu to analyze the unicellular-multicellular evolutionary transition. The new framework is also used to analyze the fitness decoupling between levels that takes place during an evolutionary transition.     

VOLVOX BARBERI,THE FASTEST SWIMMER OF THE VOLVOCALES (CHLOROPHYCEAE)1

Volvox barberi W. Shaw is a volvocalean green alga composed of biflagellated cells. Vovocales with 16 cells or more form spherical colonies, and their largest members have germ‐soma separation (all species in the genus Volvox). V. barberi is the largest Volvox species recorded in terms of cell number (10,000–50,000 cells) and has the highest somatic to reproductive cell ratio (S/R). Since they are negatively buoyant, Volvocales need flagellar beating to avoid sinking and to reach light and nutrients. We measured V. barberi swimming speed and total swimming force. V. barberi swimming speeds are the highest recorded so far for volvocine algae (～600 μm · s^?1). With this speed, V. barberi colonies have the potential to perform daily vertical migrations in the water column at speeds of 2–3 m · h^?1, consistent with what has been reported about Volvox populations in the wild. Moreover, V. barberi data fit well in the scaling relationships derived with the other smaller Volvox species, namely, that the upward swimming speed V_up∝N^0.28 and the total swimming force F_S∝N^0.77 (N = colony cell number). These allometric relationships have been important supporting evidence for reaching the conclusion that as size increases, colonies have to invest in cell specialization and increase their S/R to increase their motility capabilities to stay afloat and motile.     

Recruiting juvenile damselfish: the process of recruiting into adult colonies in the damselfish Stegastes nigricans

Juveniles of Stegastes nigricans occur in adult colonies, solitarily, and occasionally in juvenile colonies. We concentrated on solitary juveniles and those in adult colonies. We examined the costs and benefits of different settlement strategies, quantified the territory requirements of adults, and investigated the process of how juveniles make the transition to adult territorial fish. An adequate adult territory lies next to those of other adults, is proportional in area to the size of the adult, and contains a refuge tunnel whose entrance is sufficiently large. Compared with solitary juveniles, those <4 cm total length inhabiting adult colonies experienced reduced heterospecific competition for algal food and consequently benefited from a greater density of algae. A cost of recruiting into an adult colony, however, was increased attacks by adults. Juveniles that settled in adult colonies avoided attacks by retreating into small holes inaccessible to adults. As juveniles in adult colonies grew, they were chased less often by adults, whereas they themselves chased adults and heterospecific fish more often. Because territory size correlated with fish size in adult colonies, its area had to expand as the young fish grew, and that expansion was done at the expense of neighbors. Obtaining the space needed by an adult may be possible only when the juvenile settles directly into an adult colony. Juveniles that first settle down solitarily, or in juvenile colonies, may later attempt to enter adult colonies. However, because they do so as larger juveniles, they would have difficulty insinuating themselves into small refuges, which is essential for retreat from the adults. Received in revised form: 4 January 2001 Electronic Publication     

Colony size and individual fitness in the social spider Anelosimus eximius

ABSTRACT The effects of colony size on individual fitness and its components were investigated in artificially established and natural colonies of the social spider Anelosimus eximius (Araneae: Theridiidae). In the tropical rain forest understory at a site in eastern Ecuador, females in colonies containing between 23-107 females had india significantly higher lifetime reproductive success than females in smaller colonies. Among larger colonies, this trend apparently reversed. This overall fitness function was a result of the conflicting effects of colony size on different components of fitness. In particular, the probability of offspring survival to maturity increased with colony size while the probability of a female reproducing within the colonies decreased with colony size. Average clutch size increased with colony size when few or no wasp parasitoids were present in the egg sacs. With a high incidence of egg sac parasitoids, this effect disappeared because larger colonies were more likely to be infected. The product of the three fitness components measured-probability of female reproduction, average clutch size, and offspring survival-produced a function that is consistent with direct estimates of the average female lifetime reproductive success obtained by dividing the total number of offspring maturing in a colony by the number of females in the parental generation. Selection, therefore, should favor group living and itermediate colony sizes in this social spider.     

Costs and benefits of joint colony founding in Australian Acacia thrips

Facultative joint colony founding by social insects (pleometrosis) provides an outstanding opportunity to analyze the costs and benefits of sociality. Pleometrosis has been documented for a range of social insects, but most studies on the adaptive benefits of this behavior are restricted to the Hymenoptera. In this study, we provide the first analysis of costs and benefits associated with pleometrosis for Australian Dunatothrips, which form domiciles by glueing together phyllodes (leaves) of their Acacia host plant. In Dunatothrips aneurae, the distribution of foundress numbers per nest indicated that females formed associations non-randomly. Furthermore, average group size was independent of both the number of foundresses on the host plant and the number of mature colonies, suggesting that this behavior was not simply a response to limited availability of nesting sites. Although per capita reproduction declined with increasing group size, we also identified two benefits of pleometrosis: (1) individual foundresses in groups had higher survival than solitary foundresses during the brood development period, and (2) larger colony sizes resulting from pleometrosis provided a benefit later in colony development, because a higher proportion of D. aneurae adults survived invasions by the kleptoparasite Xaniothrips mulga when colony size was larger. These results demonstrate that the reproductive costs of pleometrosis are at least partially counterbalanced by survival benefits. Received 4 April 2006; revised 9 September 2006; accepted 20 September 2006.     

Per-capita productivity in a social wasp: no evidence for a negative effect of colony size

Optimal colony size in eusocial insects likely reflects a balance between ecological factors and factors intrinsic to the social group. In a seminal paper Michener (1964) showed for some species of social Hymenoptera that colony production of immature stages (productivity), when transformed to a per-female basis, was inversely related to colony size. He concluded that social patterns exist in the social insects that cause smaller groups to be more efficient than larger groups. This result has come to be known as “Michener’s paradox” because it suggests that selection on efficiency would oppose the evolution of the large and complex societies that are common in the social insects. Michener suggested that large colony size has other advantages, such as improved defense and homeostasis, that are favored by selection. For his analysis of swarm-founding wasps, Michener combined data from colonies of different species and different developmental stages in order to obtain adequate sample sizes; therefore, his study did not make a strong case that efficiency decreases with increasing colony size (across colonies) in these wasps. We tested Michener’s hypothesis on the Neotropical swarm-founding wasp Parachartergus fraternus, while controlling for stage of colony development. We found that small colonies were more variable in percapita productivity relative to larger colonies, but found no evidence for a negative relationship between efficiency and size across colonies. Received 1 February 2006; revised 5 May 2006; accepted 11 May 2006.     

What is an individual organism? A multilevel selection perspective

Most biologists implicitly define an individual organism as "one genome in one body." This definition is based on physiological and genetic criteria, but it is problematic for colonial organisms. We propose a definition based instead on the evolutionary criteria of alignment of fitness, export of fitness by germ-soma specialization, and adaptive functional organization. We consider how these concepts apply to various putative individual organisms. We conclude that complex multicellular organisms and colonies of eusocial insects satisfy these three criteria, but that, in most cases (with at least one notable exception), colonies of modular organisms and genetic chimeras do not. While species do not meet these criteria, they may meet the criteria for a broader concept--that of an evolutionary individual--and sexual reproduction may be a species-level exaptation for enhancing evolvability. We also review the costs and benefits of internal genetic heterogeneity within putative individuals, demonstrating that high relatedness is neither a necessary nor a sufficient condition for individuality, and that, in some cases, genetic variability may have adaptive benefits at the level of the whole.     

Colony size affects collective decision-making in the ant Temnothorax albipennis

Social insects are well-known for their ability to achieve robust collective behaviours even when individuals have limited information. It is often assumed that such behaviours rely on very large group sizes, but many insect colonies start out with only a few workers. Here we investigate the influence of colony size on collective decision-making in the house-hunting of the ant Temnothorax albipennis. In experiments where colony size was manipulated by splitting colonies, we show that worker number has an influence on the speed with which colonies discover new nest sites, but not on the time needed to make a decision (achieve a quorum threshold) or total emigration time. This occurred because split colonies adopted a lower quorum threshold, in fact they adopted the same threshold in proportion to their size as full-size colonies. This indicates that ants may be measuring relative quorum, i.e. population in the new nest relative to that of the old nest, rather than the absolute number. Experimentally reduced colonies also seemed to gain more from experience through repeated emigrations, as they could then reduce nest discovery times to those of larger colonies. In colonies of different sizes collected from the field, total emigration time was also not correlated with colony size. However, quorum threshold was not correlated with colony size, meaning that individuals in larger colonies adopted relatively lower quorum thresholds. Since this is a different result to that from size-manipulated colonies, it strongly suggests that the differences between natural small and large colonies were not caused by worker number alone. Individual ants may have adjusted their behaviour to their colony’s size, or other factors may correlate with colony size in the field. Our study thus shows the importance of experimentally manipulating colony size if the effect of worker number on the emergence of collective behaviour is to be studied. Received 13 December 2005; revised 9 May 2006; accepted 15 May 2006.     

TEMPERATURE-DEPENDENT CHANGES IN COLONY SIZE OF THE FRESHWATER PENNATE DIATOM ASTERIONELLA FORMOSA (BACILLARIOPHYCEAE) AND THEIR POSSIBLE ECOLOGICAL IMPLICATIONS1

Changes in colony size (cell number per colony) of Asterionella Formosa Hass. were experimentally evaluated in relation to water temperature using two types of clones having colony sizes of four or eight cells. The clones were isolated from two different temperate freshwater lakes. Both clones showed the same general trend with changing temperature. Most of the colonies were normal in size at low temperatures, but colony size was twice as large at high temperatures. Variable colony sizes were present at low percentages. Colony separation occurred at the oldest connection within the colony after cell division. Culture experiments showed that the rates of specific growth and colony separation were balanced except for a rather short period of time when the temperature was changed. Optical and scanning electron micrography did not show any distinctive morphological structure at the point of connection except for porelli and mucilage pads. Seasonal changes in colony size of A. formosa observed in a freshwater lake are discussed based on these temperature results.     

Trade-offs limiting the evolution of coloniality: ecological displacement rates used to measure small costs

Multicellular organisms that benefit from division of labour are presumably descended from colonial species that initially derived benefits from larger colony size, before the evolution of specialization. Life in a colony can have costs as well as benefits, but these can be hard to measure. We measured physiological costs to life in a colony using a novel method based on population dynamics, comparing growth rates of unicells and kairomone-induced colonies of a green alga Desmodesmus subspicatus against a reference co-occurring species. Coloniality negatively affected growth during the initial log growth phase, while no adverse effect was detected under nutrient-limited competitive conditions. The results point to costs associated with traits involved in rapid growth rather than those associated with efficient growth under resource scarcity. Some benefits of coloniality (e.g. defence from herbivory) may be different from when this trait evolved, but our approach shows how costs would have depended on conditions.     

Rapid Transition towards the Division of Labor via Evolution of Developmental Plasticity

A crucial step in several major evolutionary transitions is the division of labor between components of the emerging higher-level evolutionary unit. Examples include the separation of germ and soma in simple multicellular organisms, appearance of multiple cell types and organs in more complex organisms, and emergence of casts in eusocial insects. How the division of labor was achieved in the face of selfishness of lower-level units is controversial. I present a simple mathematical model describing the evolutionary emergence of the division of labor via developmental plasticity starting with a colony of undifferentiated cells and ending with completely differentiated multicellular organisms. I explore how the plausibility and the dynamics of the division of labor depend on its fitness advantage, mutation rate, costs of developmental plasticity, and the colony size. The model shows that the transition to differentiated multicellularity, which has happened many times in the history of life, can be achieved relatively easily. My approach is expandable in a number of directions including the emergence of multiple cell types, complex organs, or casts of eusocial insects.     

Latitudinal gradients in colony size for social insects: termites and ants show different patterns

On the basis of a comparison of Nearctic and Neotropical ants, social insects have been proposed to show a latitudinal gradient in colony size. Further, the "fasting endurance hypothesis," which predicts larger colonies in areas with extended periods of low food availability, was proposed as the mechanism driving the gradient. To test the generality of the pattern and its mechanism, we examined the relationships between termite colony size and both latitude and annual evapotranspiration, a measure of plant productivity. We found no evidence that colony size increases with increasing latitude or decreasing plant productivity. We conclude that the pattern identified for ants cannot be generalized to include social insects as a whole. As is the case for ecogeographic gradients in insect body sizes, a pattern that is reported for one taxon may not be consistent for other taxa at the global level.     

Variation in age composition among colony sizes in Cliff Swallows

Variation in group size is characteristic of most social species. The extent to which individuals sort among group sizes based on age may yield insight into why groups vary in size and the age‐specific costs and benefits of different social environments. We investigated the age composition of Cliff Swallow (Petrochelidon pyrrhonota) colonies of different sizes over 18 yr at a long‐term study site in western Nebraska, USA. Using years elapsed since banding as a relative measure of age for over 194,000 birds, we found that the proportion of age‐class‐1 swallows (birds banded as nestlings or juveniles or adults in the year of banding) of both sexes increased in larger colonies and at colony sites becoming active later in the summer. Age composition was unrelated to how often a particular colony site was used. The effect of colony size most likely reflected the fact that older birds return to the same colony site in successive years even when the colony size there decreases, and that yearlings and immigrants benefit more from larger colonies than do older, more experienced individuals. The date effect probably resulted in part from later spring arrival by younger and/or immigrant swallows. At fumigated sites where ectoparasitic swallow bugs (Oeciacus vicarius) had been removed, age composition did not vary with either colony size or colony initiation date. The patterns reported here appear to be driven partially by the presence of ectoparasites and suggest that the hematophagous bugs influence variation in Cliff Swallow group composition. Our results are consistent with the hypothesis that variation in colony size reflects, in part, age‐based sorting of individuals among groups.     

The relationship between the distribution of worker sizes and new worker production in the ant Formica neorufibarbis

While it is commonly assumed that variation in worker sizes within a single ant colony increases colony efficiency, there is little causal evidence of a link between worker size variation and colony performance. I tested whether the range of worker sizes within colonies of the ant species Formica neorufibarbis affected new worker production. Removing large workers from colonies lowered the rate of new worker production. A study of unmanipulated colonies indicated that colonies did not maintain a full range of worker sizes; mean worker head widths varied from 0.89-1.24 mm. Colonies naturally missing large workers did not have lower rates of worker production, suggesting that the relative size, not the absolute size, of workers within colonies was important. These are the first results to directly link the range of worker sizes to a component of colony fitness in a natural setting.     

Does foraging efficiency vary with colony size in the fairy martin Petrochelidon ariel?

Colonial breeding occurs in a wide range of taxa, however the advantages promoting its evolution and maintenance remain poorly understood. In many avian species, breeding colonies vary by several orders of magnitude and one approach to investigating the evolution of coloniality has been to examine how potential costs and benefits vary with colony size. Several hypotheses predict that foraging efficiency may improve with colony size, through benefits associated with social foraging and information exchange. However, it is argued that competition for limited food resources will also increase with colony size, potentially reducing foraging success. Here we use a number of measures (brood feeding rates, chick condition and survival, and adult condition) to estimate foraging efficiency in the fairy martin Petrochelidon ariel, across a range of colony sizes in a single season (17 colonies, size range 28–139 pairs). Brood provisioning rates were collected from multiple colonies simultaneously using an electronic monitoring system, controlling for temporal variation in environmental conditions. Provisioning rate was correlated with nestling condition, though we found no clear relationship between provisioning rate and colony size for either male or female parents. However, chicks were generally in worse condition and broods more likely to fail or experience partial loss in larger colonies. Moreover, the average condition of adults declined with colony size. Overall, these findings suggest that foraging efficiency declines with colony size in fairy martins, supporting the increased competition hypothesis. However, other factors, such as an increased ectoparasitise load in large colonies or change in the composition of phenotypes with colony size may have also contributed to these patterns.     

Influence of individual cell motility on the 2D front roughness dynamics of tumour cell colonies

The dynamics of in situ 2D HeLa cell quasi-linear and quasi-radial colony fronts in a standard culture medium is investigated. For quasi-radial colonies, as the cell population increased, a kinetic transition from an exponential to a constant front average velocity regime was observed. Special attention was paid to individual cell motility evolution under constant average colony front velocity looking for its impact on the dynamics of the 2D colony front roughness. From the directionalities and velocity components of cell trajectories in colonies with different cell populations, the influence of both local cell density and cell crowding effects on individual cell motility was determined. The average dynamic behaviour of individual cells in the colony and its dependence on both local spatio-temporal heterogeneities and growth geometry suggested that cell motion undergoes under a concerted cell migration mechanism, in which both a limiting random walk-like and a limiting ballistic-like contribution were involved. These results were interesting to infer how biased cell trajectories influenced both the 2D colony spreading dynamics and the front roughness characteristics by local biased contributions to individual cell motion. These data are consistent with previous experimental and theoretical cell colony spreading data and provide additional evidence of the validity of the Kardar-Parisi-Zhang equation, within a certain range of time and colony front size, for describing the dynamics of 2D colony front roughness.     

Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus

Colony size is a fundamental attribute of insect societies that appears to play an important role in their organization of work. In the harvester ant Pogonomyrmex californicus, division of labor increases with colony size during colony ontogeny and among unmanipulated colonies of the same age. However, the mechanism(s) integrating individual task specialization and colony size is unknown. To test whether the scaling of division of labor is an emergent epiphenomenon, as predicted by self-organizational models of task performance, we manipulated colony size in P. californicus and quantified short-term behavioral responses of individuals and colonies. Variation in colony size failed to elicit a change in division of labor, suggesting that colony-size effects on task specialization are mediated by slower developmental processes and/or correlates of colony size that were missing from our experiment. In contrast, the proportional allocation of workers to tasks shifted with colony size, suggesting that task needs or priorities depend, in part, on colony size alone. Finally, although task allocation was flexible, colony members differed consistently in task performance and spatial tendency across colony size treatments. Sources of interindividual behavioral variability include worker age and genotype (matriline).