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The Major Evolutionary Transitions
Abstract
There is no theoretical reason to expect evolutionary lineages to increase in complexity with time, and no empirical evidence that they do so. Nevertheless, eukaryotic cells are more complex than prokaryotic ones, animals and plants are more complex than protists, and so on. This increase in complexity may have been achieved as a result of a series of major evolutionary transitions. These involved changes in the way information is stored and transmitted.
... Accumulation of culture may be unique to humans [24,26,27], although some have suggested that it is present in a small number of non-human animals such as birds and chimpanzees [2,25]. Nevertheless, humans exhibit by far the greatest degree of cumulative culture, and human societies have been considered a major evolutionary transition (MET) [28][29][30]. This cumulative culture is supported by physiological, cognitive and behavioural adaptations, such as the capacity for spoken and written language, prolonged (and often biparental) childcare, strong social structures and more, which allow the preservation and accurate long-term transmission of larger quantities of information compared to what is possible in non-human animals. ...
... Our goal has been to elucidate conditions that favour the evolution of social learning as well as cumulative culture-critical features of human evolution that are likely to have facilitated the formation of complex societies, institutions, technology, and language, rendering humans an MET [28][29][30]. METs encompass fusions of formerly independent entities into novel types of 'individuals,' as well as novel types of information storage and transmission [29]. There is debate about whether human societies may eventually qualify as the former [56][57][58][59][60], but little dispute that human language exemplifies the latter [30,61,62]. ...
... Our goal has been to elucidate conditions that favour the evolution of social learning as well as cumulative culture-critical features of human evolution that are likely to have facilitated the formation of complex societies, institutions, technology, and language, rendering humans an MET [28][29][30]. METs encompass fusions of formerly independent entities into novel types of 'individuals,' as well as novel types of information storage and transmission [29]. There is debate about whether human societies may eventually qualify as the former [56][57][58][59][60], but little dispute that human language exemplifies the latter [30,61,62]. ...
The emergence of human societies with complex language and cumulative culture is considered a major evolutionary transition. Why such a high degree of cumulative culture is unique to humans is perplexing given the potential fitness advantages of cultural accumulation. Here, Boyd & Richerson’s (1996 Why culture is common, but cultural evolution is rare. Proc. Br. Acad. 88 , 77–93) discrete-cultural-trait model is extended to incorporate arbitrarily strong selection; conformist, anti-conformist and unbiased frequency-dependent transmission; random and periodic environmental variation; finite population size; and multiple ‘skill levels.’ From their infinite-population-size model with success bias and a single skill level, Boyd and Richerson concluded that social learning is favoured over individual learning under a wider range of conditions when social learning is initially common than initially rare. We find that this holds only if the number n of individuals observed by a social learner is sufficiently small, but with a finite population and/or a combination of success-biased and conformist or unbiased transmission, this result holds with larger n . Assuming social learning has reached fixation, the increase in a population’s mean skill level is lower if cumulative culture is initially absent than initially present, if population size is finite, or if cultural transmission has a frequency-dependent component. Hence, multiple barriers to cultural accumulation may explain its rarity.
This article is part of the theme issue ‘Human socio-cultural evolution in light of evolutionary transitions’.
... The trends are empirically controversial (Gregory, 2008), but their theoretical possibility remains a persistent question. The second class represents the major evolutionary transitions (Szathmary and Smith, 2000), such as the increase in a structural hierarchy from RNA molecules to prokaryotes and eukaryotes, from single-cell eukaryotes to multi-cellularity, and from solitary individuals to eusociality. The unusual endurance of major transitions in evolution relates them to a third class of phenomena, sometimes described as "generative entrenchment" (Schank and Wimsatt, 1986;Wimsatt, 1986), where developmental events are profoundly conserved over time. ...
... The evolution of structural hierarchies captures major transitions in evolution (Szathmary and Smith, 2000) including the transition from the RNA world (Orgel, 2003) to the first cells, from prokaryotes to eukaryotes (Lang et al., 1999), from unicellular to multicellular eukaryotes (Bonner, 1998), and from multicellular organisms to eusociality, such as ants or naked mole-rats, and perhaps humans (Wilson and Hölldobler, 2005). ...
... This intuition has been criticized from the view that macro-evolution is "nothing but" successive rounds of micro-evolution. Balanced against the latter view, some see evolutionary biology to be an essentially historical science (Gould, 1989;Beatty, 1995Beatty, , 2008, contingent upon historically significant events such as major evolutionary transitions (Szathmary and Smith, 2000;Szathmáry et al., 2011). These problems still resist standard explanations of modern theory. ...
Many well-documented macro-evolutionary phenomena still challenge current evolutionary theory. Examples include long-term evolutionary trends, major transitions in evolution, conservation of certain biological features such as hox genes, and the episodic creation of new taxa. Here, we present a framework that may explain these phenomena. We do so by introducing a probabilistic relationship between trait value and reproductive fitness. This integration allows mutation bias to become a robust driver of long-term evolutionary trends against environmental bias, in a way that is consistent with all current evolutionary theories. In cases where mutation bias is strong, such as when detrimental mutations are more common than beneficial mutations, a regime called “supply-driven” evolution can arise. This regime can explain the irreversible persistence of higher structural hierarchies, which happens in the major transitions in evolution. We further generalize this result in the long-term dynamics of phenotype spaces. We show how mutations that open new phenotype spaces can become frozen in time. At the same time, new possibilities may be observed as a burst in the creation of new taxa.
... ETIs hold an important role in evolutionary literature [7]. Szathmáry [8] models these major events in the history of life via two dimensions: the evolution of new levels of individuality (e.g. ...
... Such increased cooperative interactions also increase within-and between-group trait differences, in turn facilitating within-and betweengroup selection. In such a connected collection of cooperating individuals, 'group fitness' is no longer a mere aggregate of 'individual fitnesses' ( [7]; for detail on group versus individual fitness, see [12,14]). The group's expected success in reproducing its group characteristics (i.e. group fitness) now causally depends not only on the number and average reproductive success of its individual members (i.e. ...
The ‘Neolithic Revolution,’ sometimes referred to as the emergence of agriculture at its earliest in the southern Levant, is the most significant shift in human history, shaping the world we live in today. Yet, after 100 years of study, its major cause, tempo (gradual or revolutionary), and impact of human intentionality remain disputed. Here, we examine the research potential of an evolutionary transition in individuality (ETI) to clarify this dramatic shift. Applying an ETI research perspective reveals how different causes and conditions lead to the same result, enabling a holistic view rather than a reduction of ‘Neolithic' to ‘agriculture,' or to one major climatic condition, inheritance system or standard evolutionary model, thus allowing us to clarify and bypass some of these heated, unresolved disputes. Additionally, unlike current archaeological emphasis on ‘where,' ‘when,' ‘why' and ‘how' questions, the ETI perspective offers a productive path for resolving a fundamental preliminary anomaly: why and how could the Neolithic lifeway evolve at all, given the selfish interest of individuals in a hunter–gatherer group? We do not intend to solve the shift to Neolithic lifeways, only to offer a fresh lens for examining it, emphasizing the relevance of tracking within and between group differences.
This article is part of the theme issue ‘Human socio-cultural evolution in light of evolutionary transitions’.
... While known to be important for health, the precise effects of such internal organization can be hard to directly measure experimentally. The study of superorganisms, groups of organisms that form a single functional unit that is the primary level on which selection acts (Hölldobler & Wilson, 2009;Szathmáry & Smith, 1995;Wheeler, 1928), allows researchers to study internal organization at a scale observable to humans. Superorganisms must also carry out the same core biological tasks as any other biological reproductive unit -survival and growth leading to successful reproductionbut coordinating across possibly thousands of distinct individuals (Hölldobler & Wilson, 2009). ...
... The emergence of animal societies is a major evolutionary transition that is still insufficiently understood [1]. Bees are ideal models for testing ideas regarding the rise of animal sociality and its evolutionary implications. ...
The emergence of animal societies is a major evolutionary transition, but its implications for learning-dependent innovations are insufficiently understood. Bees, with lifestyles ranging from solitary to eusocial, are ideal models for exploring social evolution. Here, we ask how and why bees may acquire a new ‘technology’, foraging on morphologically complex flowers, and whether eusociality facilitates this technological shift. We consider ‘complex’ flowers that produce high food rewards but are difficult to access, versus ‘simple’ flowers offering easily accessible yet lower rewards. Complex flowers are less profitable than simple flowers to naive bees but become more rewarding after a learning period. We model how social bees optimally choose between simple and complex flowers over time, to maximize their colony's food balance. The model predicts no effect of colony size on the bees' flower choices. More foraging on complex flowers is predicted as colony longevity, its proportion of foragers, individual longevity and learning ability increase. Of these traits, only long-lived colonies and abundant foragers characterize eusocial bees. Thus, we predict that eusociality supports, but is not mandatory for, learning to exploit complex flowers. A re-analysis of a large published dataset of bee–flower interactions supports these conclusions. We discuss parallels between the evolution of insect sociality and other major transitions that provide scaffolds for learning innovations.
This article is part of the theme issue ‘Human socio-cultural evolution in light of evolutionary transitions’.
... Evolution is characterized by a general increase in organismic complexity in certain lineages [13]. A few pioneering studies [14][15][16][17][18] have revealed that this increase is not linear; long periods of slow changes are interrupted by transformative leaps of increase in complexity. Such major evolutionary transitions (METs) occur in different times and contexts, via different mechanisms and systems, yet are explained by a few basic characteristics that reveal a surprising family resemblance among them all. ...
Human societies are no doubt complex. They are characterized by division of labour, multiple hierarchies, intricate communication networks and transport systems. These phenomena and others have led scholars to propose that human society may be, or may become, a new hierarchical level that may dominate the individual humans within it, similar to the relations between an organism and its cells, or an ant colony and its members. Recent discussions of the possibility of this major evolutionary transition in individuality (ETI) raise interesting and controversial questions that are explored in the present issue from four different complementary perspectives. (i) The general theory of ETIs. (ii) The unique aspects of cultural evolution. (iii) The evolutionary history and pre-history of humans. (iv) Specific routes of a possible human ETI. Each perspective uses different tools provided by different disciplines: biology, anthropology, cultural evolution, systems theory, psychology, economy, linguistics and philosophy of science. Altogether, this issue provides a broad and rich application of the notion of ETI to human past, present and perhaps also future evolution. It presents important case studies, new theoretical results and novel questions for future research.
This article is part of the theme issue ‘Human socio-cultural evolution in light of evolutionary transitions’.
... The term 'social protocell' draws a direct parallel with the specific 'egalitarian' ETI [61] believed to be responsible for the emergence of cellular life [62][63][64][65][66][67][68]. The biotic protocell describes the settings believed to have produced an ETI from proto-genes to simple cells, while the SPH proposes that a 'social protocell' became the origin of human culture via the re-appearance of the same abstract entities and relations in a substrate that hardly could have been more different. ...
One contribution of 18 to a theme issue 'Human socio-cultural evolution in light of evolutionary transitions'. The origin of human cumulative culture is commonly envisioned as the appearance (some 2.0-2.5 million years ago) of a capacity to faithfully copy the know-how that underpins socially learned traditions. While certainly plausible, this story faces a steep 'startup problem'. For example, it presumes that ape-like early Homo possessed specialized cognitive capabilities for faithful know-how copying and that early toolmaking actually required such a capacity. The social protocell hypothesis provides a leaner story, where cumulative culture may have originated even earlier-as cumulative systems of non-cumulative traditions ('institutions' and 'cultural lifestyles'), via an emergent group-level channel of cultural inheritance. This channel emerges as a side-effect of a specific but in itself unremarkable suite of social group behaviours. It is independent of faithful know-how copying, and an ancestral version is argued to persist in Pan today. Hominin cultural lifestyles would thereby have gained in complexity and sophistication, eventually becoming independent units of selection (socionts) via a cultural evolutionary transition in individuality, abstractly similar to the origin of early cells. We here explore this hypothesis by simulating its basic premises. The model produces the expected behaviour and reveals several additional and non-trivial phenomena as fodder for future work. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.
Cellular life exhibits order and complexity, which typically increase over the course of evolution. Cell polarization is a well-studied example of an ordering process that breaks the internal symmetry of a cell by establishing a preferential axis. Like many cellular processes, polarization is driven by self-organization, meaning that the macroscopic pattern emerges as a consequence of microscopic molecular interactions at the biophysical level. However, the role of self-organization in the evolution of complex protein networks remains obscure. In this Review, we provide an overview of the evolution of polarization as a self-organizing process, focusing on the model species Saccharomyces cerevisiae and its fungal relatives. Moreover, we use this model system to discuss how self-organization might relate to evolutionary change, offering a shift in perspective on evolution at the microscopic scale.
The evolution of multicellular life spurred evolutionary radiations, fundamentally changing many of Earth's ecosystems. Yet little is known about how early steps in the evolution of multicellularity transform eco-evolutionary dynamics, e.g., via niche expansion processes that may facilitate coexistence. Using long-term experimental evolution in the snowflake yeast model system, we show that the evolution of multicellularity drove niche partitioning and the adaptive divergence of two distinct, specialized lineages from a single multicellular ancestor. Over 715 daily transfers, snowflake yeast were subject to selection for rapid growth in rich media, followed by selection favoring larger group size. Both small and large cluster-forming lineages evolved from a monomorphic ancestor, coexisting for over ~4,300 generations. These small and large sized snowflake yeast lineages specialized on divergent aspects of a trade-off between growth rate and survival, mirroring predictions from ecological theory. Through modeling and experimentation, we demonstrate that coexistence is maintained by a trade-off between organismal size and competitiveness for dissolved oxygen. Taken together, this work shows how the evolution of a new level of biological individuality can rapidly drive adaptive diversification and the expansion of a nascent multicellular niche, one of the most historically-impactful emergent properties of this evolutionary transition.
Xunzi 荀子 provided naturalistic answers to questions regarding human sociality and our characteristic “groupishness” (qun 羣). Central to his theories were so-called “social divisions and righteousness” (fenyi 分義), which can be interpreted as a uniquely human package of “cultural technology” produced via cultural evolution to suppress intragroup conflict stemming from what Xunzi calls “the mind of covetous comparison” (liangyi zhi xin 兩疑之心). For Xunzi, fenyi is the uniquely human attribute which kickstarts a salutary causal chain which facilitates prosociality and the upscaling of cooperation, and ultimately results in human ecological dominance. This essay will argue that an incipient form of cultural evolution is discoverable in the Xunzi, and moreover that a solution to the problem of the origin of the “ritual and righteousness” (liyi 禮義) cultural package derives neatly from the incipient cultural evolution of the Xunzi. That is to say, while this solution is not explicitly adduced in the Xunzi, it is nonetheless consistent with Xunzian ideas and is an improvement on the much-lambasted solution Xunzi actually gives, according to which “the former kings hated … chaos, and so they established rituals and righteousness.”
Before enzymes and templates: theory of surface metabolism.
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.
Autocatalysis in a nonenzymatic, templete-directed condensation has been demonstrated in a system consisting of three oligonucleotides. A simple form of self-replication occurs, albeit only to a small extent: the template T organizes the building blocks Å and B in such a way that condensation can occur, leading to a second template molecule. Such a nonenzymatic process has long been sought, because it is postulated as a sine qua non for prebiotic evolution in theories on the origin of life.
Different ways in which evolution can be modelled will be reviewed. Two
asexual models -- `Muller's ratchet' and a model due to Eigen and
Schuster -- both lead to the conclusion that the accuracy of replication
must reach a limiting value, but the details are different. In classic
population genetics models, difficulties arise if fitnesses depend on
interactions with others. Two approaches -- `trait group' methods, and
game theory -- are discussed. If the interacting individuals are
relatives, there is again a choice between the exact
`neighbour-modulated fitness' approach and the more intuitive `inclusive
fitness' method. A more drastic change in the nature of the model arises
if the units of the evolving system are not individual organisms, but
either genes or species. There are conceptual difficulties which must be
clarified before species selection can be analysed mathematically.
Ultra-selfish genes increase in frequency in a population despite the harm they inflict on their host. The spread of both ultra-selfish genes and their suppressors is evidence of conflicts between genes within an individual for transmission into the next generation. Here I synthesize a body of past work, and argue that intragenomic conflict might be an important evolutionary force. I discuss the evolutionary history of cytoplasmic genes as an illustration. I first consider the evolution of sex. Recent evidence suggests that the initial evolution of sex might have been driven by an ultra-selfish gene. The existence of sex in turn creates a series of new conflicts which may explain the existence of sexes and uniparental inheritance of cytoplasmic genes. Uniparental inheritance of cytoplasmic genes sets up a new set of conflicts over the sex ratio, which in turn may influence the evolution of sex determining systems, sex allocation systems and post-zygotic isolating mechanisms.
Binary mating types are proposed to arise in a three-stage process through selection of nuclear genes to minimize cytoplasmic gene conflict at the time of gamete fusion. In support of this view we argue that: (i) in systems with fusion of gametes, the mating type genes are typically binary and regulate cytoplasmic inheritance; (ii) binary sexes have evolved several times independently associated with fusion, although at least twice binary types have been lost, associated with a loss of fusion; further, in accordance with the theory are findings for isogamous species that (iii) close inbreeding may correlate with less than two sexes and biparental inheritance of cytoplasmic genes; and (iv) species with more than two sexes may have uniparental inheritance of cytoplasmic genes, be rare and be afflicted by deleterious cytoplasmic genes which attempt to pervert normal cytoplasmic genetics. Such facts and their rationale support a new and unified definition of sexes based on the control of the inheritance of cytoplasmic genes. For the common cases, the male sex is that which resigns attempts to contribute cytoplasmic genes to the next generation. We differentiate between sexes and the incompatibility types of ciliates, basidiomycetes, some angiosperms and a few other organisms which are independent of organelle contribution.