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The Price equation embodies the ‘conditions approach’ to evolution in which the Darwinian conditions of heritable variation in fitness are represented in equation form. The equation can be applied recursively, leading to a partition of selection at the group and individual levels. After reviewing the well-known issues with the Price partition, as well as issues with a partition based on contextual analysis, we summarize a partition of group and individual selection based on counterfactual fitness, the fitness that grouped cells would have were they solitary. To understand ‘group selection’ in multi-level selection models, we assume that only group selection can make cells suboptimal when they are removed from the group. Our analyses suggest that there are at least three kinds of selection that can be occurring at the same time: group-specific selection along with two kinds of individual selection, within-group selection and global individual selection. Analyses based on counterfactual fitness allow us to specify how close a group is to being a pseudo-group, and this can be a basis for quantifying progression through an evolutionary transition in individuality (ETI). During an ETI, fitnesses at the two levels, group and individual, become decoupled, in the sense that fitness in a group may be quite high, even as counterfactual fitness goes to zero. This article is part of the theme issue ‘Fifty years of the Price equation’.

Adaptations can occur at different hierarchical levels (e.g., cells and multicellular organisms), but it can be difficult to identify the level(s) of adaptation in specific cases. A major problem is that selection at a lower level can filter up, creating the illusion of selection at a higher level. We use optimality modeling of the volvocine algae to explore the emergence of genuine group (i.e., colony-level) adaptations. We find that it is helpful to develop an explicit model for what group fitness would be in the absence of group-level relationships between traits and group fitness. We call this “counterfactual fitness,” because in many actual cases of interest there are group-level relationships. Once counterfactual fitness is modeled, the difference between effects that filter up and genuine group selection is explicit and so, therefore, is the distinction between apparent and genuine group adaptations. We call the latter group-specific adaptations. Recognizing group-specific adaptations is important because only group-specific adaptations would cause the lower-level units (cells in this case) to be maladapted if they were to leave the group and enter a global cell-level population. Thus, as group-specific adaptations evolve, they create selective pressure for increased cohesiveness and individuality of groups. This article suggests that group-specific adaptations could be present in the simplest, earliest branching colonial volvocine species, which do not have distinct specialized cells. The article also makes predictions about the kind of empirical evidence needed to support or refute the hypothesis that a particular trait is a group-level adaptation.

Understanding good design requires addressing the question of what units undergo natural selection, thereby becoming adapted. There is, therefore, a natural connection between the formal Darwinism project (which aims to connect population genetics with the evolution of design and fitness maximization) and levels of selection issues. We argue that the formal Darwinism project offers contradictory and confusing lines of thinking concerning level(s) of selection. The project favors multicellular organisms over both the lower (cell) and higher (social group) levels as the level of adaptation. Grafen offers four reasons for giving such special status to multicellular organisms: (1) they lack appreciable within-organism cell selection, (2) they have multiple features that appear contrived for the same purpose, (3) they possess a set of phenotypes, and (4) they leave offspring according to their phenotypes. We discuss why these rationales are not compelling and suggest that a more even-handed approach, in which multicellular organisms are not assumed to have special status, would be desirable for a project that aims to make progress on the foundations of evolutionary theory.

Biology needs a concept of individuality in order to distinguish organisms from parts of organisms and from groups of organisms, to count individuals and compare traits across taxa, and to distinguish growth from reproduction. Most of the proposed criteria for individuality were designed for ‘unitary’ or ‘paradigm’ organisms: contiguous, functionally and physiologically integrated, obligately sexually reproducing multicellular organisms with a germ line sequestered early in development. However, the vast majority of the diversity of life on Earth does not conform to all of these criteria. We consider the issue of individuality in the ‘minor’ multicellular taxa, which collectively span a large portion of the eukaryotic tree of life, reviewing their general features and focusing on a model species for each group. When the criteria designed for unitary organisms are applied to other groups, they often give conflicting answers or no answer at all to the question of whether or not a given unit is an individual. Complex life cycles, intimate bacterial symbioses, aggregative development, and strange genetic features complicate the picture. The great age of some of the groups considered shows that ‘intermediate’ forms, those with some but not all of the traits traditionally associated with individuality, cannot reasonably be considered ephemeral or assumed transitional. We discuss a handful of recent attempts to reconcile the many proposed criteria for individuality and to provide criteria that can be applied across all the domains of life. Finally, we argue that individuality should be defined without reference to any particular taxon and that understanding the emergence of new kinds of individuals requires recognizing individuality as a matter of degree.

The evolution of multicellular organisms from their unicellular ancestors is an example of an evolutionary transition in individuality (ETI), i.e. a change in the units of selection and adaptation. The theory of ETIs poses particular challenges because, by definition, key theoretical constructs such as fitness are shifting during an ETI. Past work emphasized the importance of life history tradeoffs during ETIs in which lower level units form groups and become individuals at a higher level. In particular, it has been hypothesized that the convexity of the lower-level tradeoff between viability and fecundity changes with group size and determines the optimality of lower-level specialization in the fitness components of the group. This is important because lower-level specialization is a key indicator of higher-level individuality. Here we show that increasing generation time can increase the convexity of the lower-level viability-fecundity tradeoff. This effect is a novel hypothesis for the positive association between cell-group size and cellular specialization in a major model system for ETIs, the volvocine algae. The pattern in this clade is thought to be an example of a more general size-complexity rule. Our hypothesis is that larger groups have longer generation times and longer generation times lead to more convex lower-level viability-fecundity tradeoffs, which could account for specialization being optimal only in larger cell groups (colonies). We discuss the robustness of this effect to various changes in the assumptions of our model. Our work is important for the study of ETIs in general because viability and fecundity are fundamental components of fitness in all systems and because generation time is expected to be changing during many ETIs.

We review Evolution and the Levels of Selection by Samir Okasha. This important book provides a cohesive philosophical framework for understanding levels-of-selections problems in biology. Concerning evolutionary transitions, Okasha proposes that three stages characterize the shift from a lower level of selection to a higher one. We discuss the application of Okasha’s three-stage concept to the evolutionary transition from unicellularity to multicellularity in the volvocine green algae. Okasha’s concepts are a provocative step towards a more general understanding of the major evolutionary transitions; however, the application of certain ideas to the volvocine model system is not straightforward.

In this study, monthly changes in dusky dolphin (Lagenorhynchus obscurus) feeding tactics and multi‐species associations in Admiralty Bay and Current Basin, New Zealand were described from August to November 2005 and from May through August 2006. Concurrent changes in dusky dolphin abundance, prey characteristics, and locations of feeding bouts were examined. Data were collected during systematic surveys and focal follows of dolphin groups. During 335 dolphin feeding bouts (52 observed underwater), data were recorded on number of associated fur seal (Arctocephalus forsteri), seabirds, and sharks; dolphin behaviour; prey ball parameters; and locations. Dolphin feeding tactics, multi‐species associations, and locations of feeding bouts were different from May through July than from August to November. From May through July, dolphins fed on mobile prey at depth; from August to November, they herded small schools of fish (including pilchard Sardinops neopilchardus) to the surface. Primarily shearwate...

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.

The volvocine green algae have been extensively used to address various questions related to the evolution of multicellularity and cell differentiation, in terms of the genetics, developmental constraints, and underlying selective forces specific to this group. More recently, physical characteristics of the environment and of the emerging multi-celled entities have also been considered as potential contributors to the evolution of multicellularity in this lineage. However, the role of light in the evolution of multicellularity—beyond its direct photosynthetic role—has not been explored. The objectives of this work are (1) to show that algal cells, in both unicellular and multicellular algae, concentrate incident light, and (2) to suggest that this concentrated light might have contributed to the evolution of multicellularity in volvocine algae. We show that single algal cells can act as lenses and concentrate light from a remote source (e.g., the Sun) into beams, by a combination of standard refractive imaging of transmitted light and diffractive Arago-Poisson imaging of the light surrounding the cells. In the spheroidal multicellular volvocine algae, the peripheral cells facing the Sun can concentrate incident sunlight towards the interior of the colony. We suggest that the evolution of morphological asymmetries associated with the anterior-posterior polarity exhibited by multicellular spheroidal volvocine algae may have been influenced by this phenomenon. Whether the effect of these light beams is still important to extant spheroidal volvocine algae remains to be investigated. Future experiments are also needed to assess the relative contributions of the two light concentrating mechanisms by algal cells.

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.

A selective explanation for the evolution of multicellular organisms from unicellular ones requires knowledge of both selective pressures and factors affecting the response to selection. Understanding the response to selection is particularly challenging in the case of evolutionary transitions in individuality, because these transitions involve a shift in the very units of selection. We develop a conceptual framework in which three fundamental processes (growth, division, and splitting) are the scaffold for unicellular and multicellular life cycles alike. We (i) enumerate the possible ways in which these processes can be linked to create more complex life cycles, (ii) introduce three genes based on growth, division and splitting that, acting in concert, determine the architecture of the life cycles, and finally, (iii) study the evolution of the simplest five life cycles using a heuristic model of coupled ordinary differential equations in which mutations are allowed in the three genes. We demonstrate how changes in the regulation of three fundamental aspects of colonial form (cell size, colony size, and colony cell number) could lead unicellular life cycles to evolve into primitive multicellular life cycles with group properties. One interesting prediction of the model is that selection generally favors cycles with group level properties when intermediate body size is associated with lowest mortality. That is, a universal requirement for the evolution of group cycles in the model is that the size-mortality curve be U-shaped. Furthermore, growth must decelerate with size.

ForFor each of fiveWe compare the distribution of reproductive cell numbers to a Poisson distribution. We also compare the overall dispersion of reproductive cell number among species by calculating the coefficient of variation (CV). We compare the bivariate (reproductive and somatic cell) dataset to simulated datasets produced from a simple model of cell-type specification with intrinsic variability and colony size variation. This allows us to roughly estimate the level of intrinsic variability that is most consistent with our observed bivariate data (given an unknown level of size variation).The overall variability (CV) in reproductive cell number is high in

Natural selection acts primarily on organisms, and the existence of evolved, active, internal mechanisms that cause organismal death would seem paradoxical. However, there is substantial evidence that internal death promoting mechanisms exist and are taxonomically widespread. Where these are argued to be ‘programmed organismal death’ (POD), they require evolutionary explanations. Any such explanation must draw on our understanding of fitness trade-offs and multiple levels of selection in evolution. This review includes two main categories of putative POD: senescence in multicellular-organisms, and programmed cell death in unicellular organisms. The evidence for POD as a genetically controlled phenotype is strong for semelparous and significant but more controversial for iteroparous plants and animals. In multicellular organisms the program frequently (although not always) appears to be the result of fitness trade-offs. Here the death phenotype itself is not adaptive but the fitness related program most likely is. However, in some cases of behavioral suicide, particularly in insects, there are distinct advantages to kin and group level benefits may play a role. In unicells, programmed death is ubiquitous and POD often provides benefits to others. While benefits do not equate with adaptations, they are consistent with it. Here, death may be adaptive at a level other than the individual cell. In other instances of POD in unicells the phenotype (eg autophagy) can be explained as pleiotropy. The overall picture of POD as a natural phenomenon is still emerging, and continued work on diverse lines of evidence is necessary to complete our evolutionary understanding of this apparent paradox. While some questions remain, we conclude that POD is most likely, in some circumstances at least, adaptive.

Biology needs a concept of individuality in order to distinguish organisms from parts of organisms and from groups of organisms, to count individuals and compare traits across taxa, and to distinguish growth from reproduction. Most of the proposed criteria for individuality were designed for ‘unitary’ or ‘paradigm’ organisms: contiguous, functionally and physiologically integrated, obligately sexually reproducing multicellular organisms with a germ line sequestered early in development. However, the vast majority of the diversity of life on Earth does not conform to all of these criteria. We consider the issue of individuality in the ‘minor’ multicellular taxa, which collectively span a large portion of the eukaryotic tree of life, reviewing their general features and focusing on a model species for each group. When the criteria designed for unitary organisms are applied to other groups, they often give conflicting answers or no answer at all to the question of whether or not a given unit is an individual. Complex life cycles, intimate bacterial symbioses, aggregative development, and strange genetic features complicate the picture. The great age of some of the groups considered shows that ‘intermediate’ forms, those with some but not all of the traits traditionally associated with individuality, cannot reasonably be considered ephemeral or assumed transitional. We discuss a handful of recent attempts to reconcile the many proposed criteria for individuality and to provide criteria that can be applied across all the domains of life. Finally, we argue that individuality should be defined without reference to any particular taxon and that understanding the emergence of new kinds of individuals requires recognizing individuality as a matter of degree.

Publisher Summary A useful starting point in the study of large-brained animals is to scale back from an interest in specific neural structures, and instead look at a much coarser metric, i.e., brain size. “Large-brained” is a relative concept and depends on the group used for the comparison. Great apes, dolphins, and corvids are all large-brained when compared to their close relatives. These groups have diverse neuroanatomical characteristics, yet their similarly complex behavior indicates that they have convergently evolved a remarkable adaptation: high general intelligence. However, for dusky dolphins and other large-brained and cognitively complex species, more studies are needed to generate a consensus about the evolution of “braininess,” especially with respect to the social brain hypothesis (SBH). Complementing efforts to document animal relationships in nature are controlled experiments that illuminate the mechanistic connections between feeling, thinking, and behaving. The mechanisms linking large, complex brains and particular types of social relationships should be explored further in relation to the SBH. Finally, the issue of how to disentangle cause and effect in systems with feedbacks should be addressed further. The path analysis used by Dunbar and Shultz and ancestral character state reconstruction of sociality and brain size both seem to be promising approaches. Additionally, discerning the timescale of relevant ecological and evolutionary processes is critical for establishing the importance of feedback between the two processes.

Publisher Summary This chapter adds detail to the current picture of dusky dolphin sociality by investigating the sex and relatedness of interacting individuals across different habitats and different behavioral contexts. The same features that make dusky dolphins such a challenging system for addressing social behavior questions (e.g., marine habitat, large group sizes, “semi-pelagic”) also make knowledge of dusky dolphin social life important from a comparative perspective. Future work on the composition and behavior of dusky dolphin groups will continue to make the system more relevant to evolutionary questions about social behavior. A major challenge in cetacean sociobiology is to move beyond “the gambit of the group” to uncover the content and quality of social interactions. This level of detail is difficult to achieve, yet is essential if social behavior is to be understood in an evolutionary context. In terms of within-group relatedness, data hint that relatedness could be high within small nursery groups. Data also suggest that foraging partners tend to be unrelated. High relatedness among interacting individuals is a mechanism that can promote pro-social behaviors. Whether social organization with respect to relatedness is an important determinant of behavior in dusky dolphin behaviors is yet unknown.