Life: social to its core

DEEP SOCIALITY

The history of life is characterised by an increase in biological complexity from simple replicators to multicellular organisms. These major evolutionary transitions have in common that independent entities came together and cooperated and that finally a new entity was formed with a new fitness and a single evolutionary fate. Yet, the stable evolution of cooperation poses a classical Darwinian puzzle: Organisms compete over reproduction and selfish individuals that reap the benefits of the cooperation without paying the costs (cheaters) can invade a population of cooperators and drive the disappearance of cooperation. Social insects have become model organisms to study stable cooperation and how conflict between individuals is resolved. Here, I will first summarise what we have learned from social insect research about the evolution of stable cooperation. Besides little-studied ecological factors that determine the benefits and costs of cooperation, two common mechanisms to prevent the spread of cheaters have been identified: (i) common ancestry and aligned evolutionary interests mainly achieved through relatedness and (ii) enforcement mechanisms that make cheating costly. Then, I will show that similar mechanisms have evolved at other levels of the biological hierarchy that favour cooperation. Thirdly, I will present the multilevel selection approach, which promises to be a useful tool to study evolution at multiple selection levels. I will end by showing how a multilevel selection approach in future research might help to quantify benefits and costs of cooperation, so that insect societies and all major evolutionary transitions alike are being recognised as more than the sum of their components.

Over the history of life there have been several major changes in the way genetic information is organized and transmitted from one generation to the next. These transitions include the origin of life itself, the first eukaryotic cells, reproduction by sexual means, the appearance of multicellular plants and animals, the emergence of cooperation and of animal societies, and the unique language ability of humans. This ambitious book provides the first unified discussion of the full range of these transitions. The authors highlight the similarities between different transitions--between the union of replicating molecules to form chromosomes and of cells to form multicellular organisms, for example--and show how understanding one transition sheds light on others. They trace a common theme throughout the history of evolution: after a major transition some entities lose the ability to replicate independently, becoming able to reproduce only as part of a larger whole. The authors investigate this pattern and why selection between entities at a lower level does not disrupt selection at more complex levels. Their explanation encompasses a compelling theory of the evolution of cooperation at all levels of complexity. Engagingly written and filled with numerous illustrations, this book can be read with enjoyment by anyone with an undergraduate training in biology. It is ideal for advanced discussion groups on evolution and includes accessible discussions of a wide range of topics, from molecular biology and linguistics to insect societies.

Systematic extinctions can leave major morphological gaps between living crown‐group clades. Such morphological gaps would be perceived, from a neontological point of view, as major evolutionary transitions. In order to fill these morphological gaps and to map the evolutionary steps toward major evolutionary transitions, we need to integrate extinct stem‐group taxa in phylogenetic studies. However, the recognition of stem group has not been widely adopted in the study of early animal fossils, despite that all fossils are stem groups at one level or another. Part of the difficulty is that stem groups may not have all features that collectively diagnose the respective crown group, and they can have unique (autapomorphic) features, making them tantalizingly similar to and frustratingly different from the crown group (e.g., stem‐group eukaryotes can be prokaryotic and stem‐group animals can be protistan). The need to embrace stem groups and to implement the PhyloCode, in order to achieve phylogenetic clarity and to offer key paleontological insights into the origin and early animal evolution, is illustrated in debates on several controversial Ediacaran and Cambrian fossils.

The evolution of multicellularity has given rise to a remarkable diversity of multicellular life cycles and life histories. Whereas some multicellular organisms are long-lived, grow through cell division, and repeatedly release single-celled propagules (for example, animals), others are short-lived, form by aggregation, and propagate only once, by generating large numbers of solitary cells (for example, cellular slime moulds). There are no systematic studies that explore how diverse multicellular life cycles can come about. Here, we focus on the origin of multicellularity and develop a mechanistic model to examine the primitive life cycles that emerge from a unicellular ancestor when an ancestral gene is co-opted for cell adhesion. Diverse life cycles readily emerge, depending on ecological conditions, group-forming mechanism, and ancestral constraints. Among these life cycles, we recapitulate both extremes of long-lived groups that propagate continuously and short-lived groups that propagate only once, with the latter type of life cycle being particularly favoured when groups can form by aggregation. Our results show how diverse life cycles and life histories can easily emerge at the origin of multicellularity, shaped by ancestral constraints and ecological conditions. Beyond multicellularity, this finding has similar implications for other major transitions, such as the evolution of sociality.

The bee tribe Ceratinini is important for understanding early stages in social evolution. Their extant sister tribe Allodapini contains no strictly solitary species, and while some Ceratinini are commonly regarded as solitary, little behavioural data exist to substantiate this. Studies on Asian congeners have shown recurrent sociality in temperate and subtropical ranges while behavioural data are lacking in tropical regions. Field work along the west coast of Borneo in Sarawak, Malaysia, has provided some insight into these tropical taxa. Here we describe the nesting biology and social behaviour of four taxonomically described yet behaviourally unclassified Ceratina species. These four species are from three subgenera, namely Ceratina (Ceratinidia) accusator Cockerell, C. (Ceratinidia) nigrolateralis Cockerell, C. (Neoceratina) dentipes Friese, C. (Pithitis) smaragdula Fabricius. Nests of all species were typically attended by an adult female while all species except C. accusator had a low frequency of multi-female nesting assemblages. The four tropical ceratinines described here and all other behaviourally classified species exhibit recurrent patterns of maternal care, maternal longevity, and nest protection. Prolonged parental care found across the genus and occasional transitions into sociality make Ceratina of future interest for the study of life history and social evolution. The evolution of eusociality is considered one of the major transitions in evolution (Maynard Smith and Szathamary, 1995). In solitary species, offspring disperse and reproduce independently whereas workers in eusocial societies remain at the natal nest and largely forego reproduction to aid the queen in rearing siblings. Socially polymorphic lineages, those containing both solitary and social species, retain the plasticity to allow intra-specific comparisons of solitary with social life. The key to understanding the transition to sociality requires a group of closely related taxa possessing broad social, taxonomic and geographic diversity. Bees provide numerous contrasts to offer insights into the origin of sociality with their range of solitary to social forms. The small carpenter bees Hymenoptera: Apidae (Xylocopinae: Ceratinini) are commonly regarded as solitary (Michener, 1974). All behaviourally classified species share a relatively simple life history. Females disperse from their natal nests and find appropriate nesting substrate. These twig-nesting bees excavate linear burrows in the cores of dead exposed pithy stems. Subsequent to burrow construction, females forage for pollen and nectar provisions that they form into a pollen mass on which they lay an egg. After provisioning and oviposition, brood cells are cappe dw ith a partition of wood pith, and the process is repeated in a serial manner along the linear nest chamber.

Drawing on recent advances in evolutionary biology, prominent scholars return to the question posed in a pathbreaking book: how evolution itself evolved. In 1995, John Maynard Smith and Eörs Szathmáry published their influential book The Major Transitions in Evolution. The "transitions" that Maynard Smith and Szathmáry chose to describe all constituted major changes in the kinds of organisms that existed but, most important, these events also transformed the evolutionary process itself. The evolution of new levels of biological organization, such as chromosomes, cells, multicelled organisms, and complex social groups radically changed the kinds of individuals natural selection could act upon. Many of these events also produced revolutionary changes in the process of inheritance, by expanding the range and fidelity of transmission, establishing new inheritance channels, and developing more open-ended sources of variation. Maynard Smith and Szathmáry had planned a major revision of their work, but the death of Maynard Smith in 2004 prevented this. In this volume, prominent scholars (including Szathmáry himself) reconsider and extend the earlier book's themes in light of recent developments in evolutionary biology. The contributors discuss different frameworks for understanding macroevolution, prokaryote evolution (the study of which has been aided by developments in molecular biology), and the complex evolution of multicellularity.

Group-living has been recognized as one of the major transitions in evolution. Male sociality along with solitary females is rare in mammals, but it can provide unique insights into the evolution of sociality and cooperation. Because males compete with each other over females, male cooperation in mammals has been explained by joint defense of females against other males. Here, we demonstrate that the benefits of male cooperative hunting can play a major role in shaping sociality. By quantifying differences in morphology, activity, diet, and mating success, we show that in Madagascar’s top predator, the fosa (Cryptoprocta ferox), some males associate to jointly hunt large prey, which allows them to grow bigger than both solitary males and females. These associated males’ physical superiority also represents an advantage in contest competition for females, as reflected by higher mating success. Our results demonstrate that enhanced access to food resources by cooperative hunting is a key to physical development and competitiveness in fosas. In contrast to previous findings, we show that male sociality must not be limited to joint defense of territory and females, but that cooperation in food acquisition can favor sociality in sexually dimorphic species. Key wor ds: cooperative hunting, Cryptoprocta ferox, evolution of group-living, fosa, Madagascar mongoose, male sociality, male–male competition. [Behav Ecol]

This commentary poses an evolutionary hypothesis about the nature of the human condition: that we are stalled part way through a major evolutionary transition from individuals to groups, a transition that may never be completed but that has already shaped our history, politics, psychology, and social life. The conditions causing the transition to stall include the decreasing congruence of group boundaries with kinship boundaries, growth in group size, increasing interdependence of groups, membership of individuals in several types of groups, divided loyalties of individuals among groups, and the emergence of institutions as novel entities uncoupled from the individuals who temporarily belong to them. Those conditions combine to decrease the ability of cultural group selection to effect genetic change in group-oriented traits. The theory supporting this hypothesis deals with major transitions (e.g., Maynard Smith and Szathmary 1995), hierarchical selection (e.g., Price 1970, 1972; Frank 1995, 2003; Rice 2004), conflicts and conflict resolution (e.g., Burt and Trivers 2006), and gene-culture coevolution (e.g., Boyd and Richerson 2005; Richerson and Boyd 2005). The evidence is diverse. It comes from biological anthropology (e.g., Hill and Hurtado 1995), behavioral economics (e.g., Hammerstein 2003; Bowles 2004; Henrich et al. 2004), evolutionary psychology (e.g., Barkow et al. 1992), and history. The research programs it suggests are at least in anthropology, history, and political science.

The groundbreaking first book by a major evolutionary biologist, published in 1912, that anticipated current thinking about organismal complexity. Julian Huxley's The Individual in the Animal Kingdom, published in 1912, is a concise and groundbreaking work that is almost entirely unknown today. In it, Huxley analyzes the evolutionary advances in life's organizational complexity, anticipating many of today's ideas about changes in individuality. Huxley's overarching system of concepts and his coherent logical principles were so far ahead of their time that they remain valid to this day. In part, this is because his explicitly Darwinian approach carefully distinguished between the integrated form and function of hierarchies within organisms and loosely defined, nonorganismal ecological communities. In The Individual in the Animal Kingdom, we meet a youthful Huxley who uses his commanding knowledge of natural history to develop a nonreductionist account of life's complexity that aligns with seminal early insights by Darwin, Wallace, Weismann, and Wheeler. As volume editors Richard Gawne and Jacobus Boomsma point out, this work disappeared into oblivion despite its relevance for contemporary research on organismal complexity and major evolutionary transitions. This MIT Press edition gives Huxley's book a second hearing, offering readers a unique vantage point on the discoveries of evolutionary biology past and present.

The Major Transitions in Evolution. By John Maynard Smith and Eors Szathmary. W. H. Freeman: 1995. Pp. 346. £16.99, $29.95 (pbk).

Novel Predators Reshape Holozoan Phylogeny and Reveal the Presence of a Two-Component Signaling System in the Ancestor of Animals

Language as an evolutionary system

Most recent models of the partitioning of reproduction attempt to explain patterns of skew on the assumption that dominant individuals have complete control over breeding opportunities within the group, but may nevertheless concede a share of direct reproduction to subordinates as an incentive to remain peacefully in the association. Although these models may be applicable to some animal societies, we argue that they fail to provide a comprehensive theory of skew. Instead, we suggest that subordinates may often be able to claim unsanctioned reproduction for themselves, but will be forced to exercise a degree of reproductive restraint lest they incite ejection by the dominant. Reproductive skew, in other words, may reflect the threat of ejection (inducing subordinate restraint) rather than the threat of subordinate departure (inducing reproductive concessions by dominants). We present a simple ESS model of reproductive skew under these circumstances, which demonstrates that a shift in emphasis from reproductive concessions by dominants to reproductive restraint on the part of subordinates, radically alters the predictions of skew models. High group productivity, high relatedness and (when group members are related) strong ecological constraints are all expected to lead to reduced skew (the opposite conclusions to those of previous, concession-based analyses). The reason is that these factors reduce the benefits (or increase the costs) of ejection to the dominant, who therefore does best to tolerate more subordinate reproduction.

EDITORIAL article Front. Ecol. Evol., 19 December 2022Sec. Social Evolution Volume 10 - 2022 | https://doi.org/10.3389/fevo.2022.1109484