Philosophical Transactions of the Royal Society B: Biological Sciences最新文献

While ecological specialization, social differentiation and division of labour are found in many species, extensive and irreversible interdependence among culturally specialized producers is a characteristic feature of humans. By extending the concept of cultural ratcheting (or the evolution of cultural products of such complexity that they become very unlikely to be recreated from scratch by naive individuals), we present simulation models showing how cumulative cultural evolution may have engendered a parallel process of 'social ratcheting' or the origin of culturally differentiated and irreversible interdependent individuals and groups. We provide evidence that the evolution of cultural division of labour in humans may have been associated with social network structures splitting the cognitive costs of cultural production across differentiated specialists, significantly reducing the burden of cultural learning on individual cognition and memory. While previous models often assumed agents with unlimited memories, we show that limiting individual memories to a fraction of available cultural repertoires has a noticeable accelerating effect on both cultural evolution and social differentiation among producers. We conclude that cultural and social ratcheting may have been two linked outcomes of cultural evolution in the hominin lineage.This article is part of the theme issue 'Division of labour as key driver of social evolution'.

The evolution of primitive eusociality from non-social ancestors in organisms such as bees and wasps is often regarded as a major evolutionary transition. The division of labour between reproductives that specialize on egg production and workers that specialize on tasks such as foraging is the key feature defining eusociality and is why social insects are so successful ecologically. In taxa with morphological castes, individuals are often irreversibly specialized for particular roles when they reach adulthood. At the origin of sociality, however, such adaptations were absent, and we must consider why selection would favour individuals specializing when they are undifferentiated from the ancestral, non-social phenotype. Here, I focus on constraints based on life-history tradeoffs and plasticity that would be faced by ancestral females when specializing. These include limited efficiency of within-individual tradeoffs between reproductive and worker functions, imperfect matching of the productivities of social partners and lack of coordination. I also discuss the possibility that payoffs through specialization could be condition dependent. Eusocial taxa lacking morphological castes have traditionally been the testing grounds to understand the origin of eusociality, but significant adaptation has occurred since helping first evolved. Investigating role specialization at the origin of eusociality therefore requires utilizing non-social taxa.This article is part of the theme issue 'Division of labour as key driver of social evolution'.

The social division of labour (DoL) has been renowned as a key driver of the economic success of human societies dating back to ancient philosophers such as Plato (in The Republic, ca 380 BCE), Xenophon (in Cyropaedia, ca 370 BCE) and Aristotle (in Politics, ca 350 BCE, and Nicomachean Ethics, ca 340 BCE). Over time, this concept evolved into a cornerstone of political economic thought, most prominently expressed in Smith (in The Wealth of Nations, 1776). In his magnum opus, Adam Smith posited that DoL has caused a greater increase in production than any other factor in human history. There is little doubt that DoL immensely increases productive output, both in humans and in other organisms, but it is less clear how it comes about, how it is organized and what the biological roots are of this human 'turbo enhancer'. We address these questions here using results from studies of a wide range of organisms and various modelling approaches.This article is part of the theme issue 'Division of labour as key driver of social evolution'.

Variation in the composition of different ribosomes, termed ribosome heterogeneity, is a now well established phenomenon. However, the functional implications of this heterogeneity on the regulation of protein synthesis are only now beginning to be revealed. While there are numerous examples of heterogeneous ribosomes, there are comparatively few bona fide specialized ribosomes described. Specialization requires that compositionally distinct ribosomes, through their subtly altered structure, have a functional consequence to the translational output. Even for those examples of ribosome specialization that have been characterized, the precise mechanistic details of how changes in protein and rRNA composition enable the ribosome to regulate translation are still missing. Here, we suggest looking at the evolution of specialization across the tree of life may help reveal central principles of translation regulation. We consider functional and structural studies that have provided insight into the potential mechanisms through which ribosome heterogeneity could affect translation, including through mRNA and open reading frame selectivity, elongation dynamics and post-translational folding. Further, we highlight some of the challenges that must be addressed to show specialization and review the contribution of various models. Several studies are discussed, including recent studies that show how structural insight is starting to shed light on the molecular details of specialization. Finally, we discuss the future of ribosome specialization studies, where advances in technology will likely enable the next wave of research questions. Recent work has helped provide a more comprehensive understanding of how ribosome heterogeneity affects translational control.This article is part of the discussion meeting issue 'Ribosome diversity and its impact on protein synthesis, development and disease'.

Recent advances in the fields of RNA translation and ribosome biology have demonstrated the heterogeneous nature of ribosomes. This manifests not only across different cellular contexts but also within the same cell. Such variations in ribosomal composition, be it in ribosomal RNAs or proteins, can significantly influence cellular processes and responses by altering the mRNAs being translated or the dynamics of ribosomes during the translation process. Therefore, identifying this heterogeneity is crucial for unravelling the complexity of gene expression across different fields of biology. Here we provide an overview of recent advances in high-throughput techniques for identifying ribosomal heterogeneity. We cover methodologies for probing both rRNA and protein components of the ribosome and encompass the most recent next-generation sequencing and computational analyses, as well as a diverse array of mass spectrometry techniques.This article is part of the discussion meeting issue 'Ribosome diversity and its impact on protein synthesis, development and disease'.

Since the framing of the Central Dogma, it has been speculated that physically distinct ribosomes within cells may influence gene expression and cellular physiology. While heterogeneity in ribosome composition has been reported in bacteria, protozoans, fungi, zebrafish, mice and humans, its functional implications remain actively debated. Here, we review recent evidence demonstrating that expression of conserved variant ribosomal DNA (rDNA) alleles in bacteria, mice and humans renders their actively translating ribosome pool intrinsically heterogeneous at the level of ribosomal RNA (rRNA). In this context, we discuss reports that nutrient limitation-induced stress in Escherichia coli leads to changes in variant rRNA allele expression, programmatically altering transcription and cellular phenotype. We highlight that cells expressing ribosomes from distinct operons exhibit distinct drug sensitivities, which can be recapitulated in vitro and potentially rationalized by subtle perturbations in ribosome structure or in their dynamic properties. Finally, we discuss evidence that differential expression of variant rDNA alleles results in different populations of ribosome subtypes within mammalian tissues. These findings motivate further research into the impacts of rRNA heterogeneities on ribosomal function and predict that strategies targeting distinct ribosome subtypes may hold therapeutic potential.This article is part of the discussion meeting issue 'Ribosome diversity and its impact on protein synthesis, development and disease'.

The definition of the ribosome as the monolithic machinery in cells that synthesizes all proteins in the cell has persisted for the better part of a century. Yet, research has increasingly revealed that ribosomes are dynamic, multimodal complexes capable of fine-tuning gene expression. This translation regulation may be achieved by ribosome-associated proteins (RAPs), which play key roles as modular trans-acting factors that are dynamic across different cellular contexts and can mediate the recruitment of specific transcripts or the modification of RNA or ribosomal proteins. As a result, RAPs have the potential to rapidly regulate translation within specific subcellular regions, across different cell or tissue types, in response to signalling, or in disease states. In this article, we probe the definition of the eukaryotic ribosome and review the major layers of additional proteins that expand the definition of ribosomes in the twenty-first century. We pose RAPs as key modulators that impart ribosome function in cellular processes, development and disease.This article is part of the discussion meeting issue 'Ribosome diversity and its impact on protein synthesis, development and disease'.

The ribosome consists of protein and RNA components. Deletion of genes encoding specific ribosomal proteins has revealed that heterogeneity in the ribosome must exist in vertebrates; however, this has not been tested for ribosomal RNA (rRNA). In zebrafish (Danio rerio), the '45S-M' ribosomal RNA-encoding locus undergoes massive extrachromosomal amplification during oocyte growth and ovary differentiation and is distinct from the regular ribosomal DNA (rDNA) locus encoding somatic rRNA (45S-S). Although the 45S-M rDNA locus falls within the only described sex-linked region in multiple wild zebrafish strains, its role in sexual differentiation is unclear. We used CRISPR-Cas9 gene editing to alter 45S-M rDNA sequences in zygotes and found that although there was no effect on growth or male development, there was dramatic suppression of female differentiation. Males with edited 45S-M rDNA produced phenotypically normal sperm and were able to fertilize eggs from wild-type females, with resulting embryos once more displaying normal development. Our work supports the hypothesis that specialized 45S-M rDNA is the elusive apical sex-determining locus in zebrafish and that this region represents the most tractable genetic system to date for studying ribosomal RNA heterogeneity and function in a vertebrate.This article is part of the discussion meeting issue 'Ribosome diversity and its impact on protein synthesis, development and disease'.

Ribosomes, the molecular machines that translate the genetic code from mRNA into proteins in all living cells, are highly structurally conserved across all domains of life and hence are believed to have evolved from a structurally unified pocket. Initially perceived as uniform cellular factories for protein synthesis, currently, ribosomes have emerged as more complex entities. Structural, medical and biochemical studies, including ours, have revealed significant variability in their compositions across tissues, species, functions and developmental stages, highlighting their multifunctional potential. Moreover, the diversity of ribosomes, their components and their associated biological factors challenge the traditional perception of uniform interactions under various conditions, including stress, and expose their mobility and heterogeneity. Evidence for their functional diversity can be seen even in modifications of ribosomal genes, where minor changes may play critical roles under stress or may lead to diseases called ribosomopathies, including Diamond-Blackfan anaemia, some types of cancer and Alzheimer's disease. Thus, through in-depth structural explorations, we improve the understanding of the mechanisms regulating protein biosynthesis in response to various environmental stressors. These findings should potentially reshape the perceptions of the various ribosomal roles.This article is part of the discussion meeting issue 'Ribosome diversity and its impact on protein synthesis, development and disease'.

Ribosomes are macromolecular complexes responsible for protein synthesis, comprising ribosomal proteins (RPs) and ribosomal RNA. While most RPs are present as single copies in higher eukaryotes, a handful of them have paralogues that emerged through duplication events. However, it is still unclear why a small subset of RP paralogues were preserved through evolution, and whether they can endow ribosomes with specialized functions. In this review, we focus on RP paralogue pairs present in humans, providing an overview of the most recent findings on RP paralogue functions and their roles in ribosome specialization.This article is part of the discussion meeting issue 'Ribosome diversity and its impact on protein synthesis, development and disease'.