RESUMO
In contrast with nuclear genes that are passed on through both parents, mitochondrial genes are maternally inherited in most species, most of the time. The genetic conflict stemming from this transmission asymmetry is well-documented, and there is an abundance of population-genetic theory associated with it. While occasional or aberrant paternal inheritance occurs, there are only a few cases where exclusive paternal inheritance of mitochondrial genomes is the evolved state. Why this is remains poorly understood. By examining commonalities between species with exclusive paternal inheritance, we discuss what they may tell us about the evolutionary forces influencing mitochondrial inheritance patterns. We end by discussing recent technological advances that make exploring the causes and consequences of paternal inheritance feasible.
Assuntos
Genoma Mitocondrial , Herança Paterna , Mitocôndrias/genética , Padrões de Herança/genética , Genes Mitocondriais/genética , Genoma Mitocondrial/genética , DNA Mitocondrial/genéticaRESUMO
The paradox of the organism refers to the observation that organisms appear to function as coherent purposeful entities, despite the potential for within-organismal components like selfish genetic elements and cancer cells to erode them from within. While it is commonly accepted that organisms may pursue fitness maximisation and can be thought to hold particular agendas, there is a growing recognition that genes and cells do so as well. This can lead to evolutionary conflicts between an organism and the parts that reside within it. Here, we revisit the paradox of the organism. We first outline its conception and relationship to debates about adaptation in evolutionary biology. Second, we review the ways selfish elements may exploit organisms, and the extent to which this threatens organismal integrity. To this end, we introduce a novel classification scheme that distinguishes between selfish elements that seek to distort transmission versus those that seek to distort phenotypic traits. Our classification scheme also highlights how some selfish elements elude a multi-level selection decomposition using the Price equation. Third, we discuss how the organism can retain its status as the primary fitness-maximising agent in the face of selfish elements. The success of selfish elements is often constrained by their strategy and further limited by a combination of fitness alignment and enforcement mechanisms controlled by the organism. Finally, we argue for the need for quantitative measures of both internal conflicts and organismality.
Assuntos
Adaptação Fisiológica , Evolução Biológica , Aclimatação , Modelos GenéticosRESUMO
Theoretical and applied cancer studies that use individual-based models (IBMs) have been limited by the lack of a mathematical formulation that enables rigorous analysis of these models. However, spatial cumulant models (SCMs), which have arisen from theoretical ecology, describe population dynamics generated by a specific family of IBMs, namely spatio-temporal point processes (STPPs). SCMs are spatially resolved population models formulated by a system of differential equations that approximate the dynamics of two STPP-generated summary statistics: first-order spatial cumulants (densities), and second-order spatial cumulants (spatial covariances). We exemplify how SCMs can be used in mathematical oncology by modelling theoretical cancer cell populations comprising interacting growth factor-producing and non-producing cells. To formulate model equations, we use computational tools that enable the generation of STPPs, SCMs and mean-field population models (MFPMs) from user-defined model descriptions (Cornell et al. Nat Commun 10:4716, 2019). To calculate and compare STPP, SCM and MFPM-generated summary statistics, we develop an application-agnostic computational pipeline. Our results demonstrate that SCMs can capture STPP-generated population density dynamics, even when MFPMs fail to do so. From both MFPM and SCM equations, we derive treatment-induced death rates required to achieve non-growing cell populations. When testing these treatment strategies in STPP-generated cell populations, our results demonstrate that SCM-informed strategies outperform MFPM-informed strategies in terms of inhibiting population growths. We thus demonstrate that SCMs provide a new framework in which to study cell-cell interactions, and can be used to describe and perturb STPP-generated cell population dynamics. We, therefore, argue that SCMs can be used to increase IBMs' applicability in cancer research.
Assuntos
Ecologia , Neoplasias , Humanos , Dinâmica Populacional , Crescimento Demográfico , Modelos BiológicosRESUMO
The use of intentional language in biology is controversial. It has been commonly applied by researchers in behavioral ecology, who have not shied away from employing agential thinking or even anthropomorphisms, but has been rarer among researchers from more mechanistic corners of the discipline, such as population genetics. One research area where these traditions come into contact-and occasionally clash-is the study of genetic conflicts, and its history offers a good window to the debate over the use of intentional language in biology. We review this debate, paying particular attention to how this interaction has played out in work on genomic imprinting and sex chromosomes. In light of this, we advocate for a synthesis of the two approaches, a form of licensed anthropomorphizing. Here, agential thinking's creative potential and its ability to identify the fulcrum of evolutionary pressure are combined with the rigidity of formal mathematical modeling.
RESUMO
Gerrymandering, the structuring of voting districts to favour certain politicians and political groups, undermines fair elections and presents a serious challenge to democracy. We introduce a solution to gerrymandering inspired by the biological process of cell division in sexually reproducing organisms, meiosis, in which the boundaries of electorates are frequently redrawn by randomizing algorithms. By demonstrating the deep parallels between meiosis and John Rawls's concept of a 'veil of ignorance', we also show how one of the biggest threats to the integrity of meiosis-selfish genetic elements, genes that promote their own transmission at the expense of organismal fitness-can inspire another potential advantage to frequent random redistricting.
Assuntos
Meiose , Política , Meiose/genéticaRESUMO
The gene's-eye view of evolution has played a central but contentious role in evolutionary biology for the past half-century. By envisioning evolutionary history as a struggle between competing selfish genes, it accelerated the shift from organism-centric to gene-centric explanations that began with the emergence population genetics a century ago. At the forefront of this shift were George C. Williams and Richard Dawkins, who advocated an approach to thinking about evolution first introduced by R. A. Fisher. In this Perspective, I discuss the criticism of the gene's-eye view developed by another architect of population genetics, Sewall Wright, whose "On genic and organismic selection" was published in Evolution in 1980. I start by outlining the history of the gene's-eye view and then show how some long-standing differences in opinion over its value can be traced back to disagreements between Fisher and Wright, especially over Fisher's concept of genetic variance and the importance of epistasis. I end with some reflections on the role of genes and organisms in evolutionary explanations.
Assuntos
Evolução Biológica , Seleção Genética , Genética PopulacionalRESUMO
The coordination between mitochondrial and nuclear genes is crucial to eukaryotic organisms. Predicting the nature of these epistatic interactions can be difficult because of the transmission asymmetry of the genes involved. While autosomes and X-linked genes are transmitted through both sexes, genes on the Y chromosome and in the mitochondrial genome are uniparentally transmitted through males and females, respectively. Here, we generate 36 otherwise isogenic Drosophila melanogaster strains differing only in the geographical origin of their mitochondrial genome and Y chromosome, to experimentally examine the effects of the uniparentally inherited parts of the genome, as well as their interaction, in males. We assay longevity and gene expression through RNA-sequencing. We detect an important role for both mitochondrial and Y-linked genes, as well as extensive mitochondrial-Y chromosome epistasis. In particular, genes involved in male reproduction appear to be especially sensitive to such interactions, and variation on the Y chromosome is associated with differences in longevity. Despite these interactions, we find no evidence that the mitochondrial genome and Y chromosome are co-adapted within a geographical region. Overall, our study demonstrates a key role for the uniparentally inherited parts of the genome for male biology, but also that mito-nuclear interactions are complex and not easily predicted from simple transmission asymmetries.
Assuntos
Drosophila melanogaster , Epistasia Genética/fisiologia , Cromossomo Y/genética , Animais , Núcleo Celular , DNA Mitocondrial , Feminino , Genes Ligados ao Cromossomo Y , Genoma Mitocondrial , Longevidade , Masculino , MitocôndriasRESUMO
Cooperation occurs at all levels of life, from genomes, complex cells and multicellular organisms to societies and mutualisms between species. A major question for evolutionary biology is what these diverse systems have in common. Here, we review the full breadth of cooperative systems and find that they frequently rely on enforcement mechanisms that suppress selfish behaviour. We discuss many examples, including the suppression of transposable elements, uniparental inheritance of mitochondria and plastids, anti-cancer mechanisms, reciprocation and punishment in humans and other vertebrates, policing in eusocial insects and partner choice in mutualisms between species. To address a lack of accompanying theory, we develop a series of evolutionary models that show that the enforcement of cooperation is widely predicted. We argue that enforcement is an underappreciated, and often critical, ingredient for cooperation across all scales of biological organization.
Assuntos
Evolução Biológica , Comportamento Cooperativo , Animais , Humanos , SimbioseRESUMO
In contrast with autosomes, lineages of sex chromosomes reside for different amounts of time in males and females, and this transmission asymmetry makes them hotspots for sexual conflict. Similarly, the maternal inheritance of the mitochondrial genome (mtDNA) means that mutations that are beneficial in females can spread in a population even if they are deleterious in males, a form of sexual conflict known as Mother's Curse. While both Mother's Curse and sex chromosome induced sexual conflict have been well studied on their own, the interaction between mitochondrial genes and genes on sex chromosomes is poorly understood. Here, we use analytical models and computer simulations to perform a comprehensive examination of how transmission asymmetries of nuclear, mitochondrial, and sex chromosome-linked genes may both cause and resolve sexual conflicts. For example, the accumulation of male-biased Mother's Curse mtDNA mutations will lead to selection in males for compensatory nuclear modifier loci that alleviate the effect. We show how the Y chromosome, being strictly paternally transmitted provides a particularly safe harbor for such modifiers. This analytical framework also allows us to discover a novel kind of sexual conflict, by which Y chromosome-autosome epistasis may result in the spread of male beneficial but female deleterious mutations in a population. We christen this phenomenon Father's Curse. Extending this analytical framework to ZW sex chromosome systems, where males are the heterogametic sex, we also show how W-autosome epistasis can lead to a novel kind of nuclear Mother's Curse. Overall, this study provides a comprehensive framework to understand how genetic transmission asymmetries may both cause and resolve sexual conflicts.
Assuntos
Pai , Mães , Seleção Genética , Aberrações dos Cromossomos Sexuais , Cromossomos Sexuais , Cromossomos Humanos Y , DNA Mitocondrial , Feminino , Humanos , Masculino , Modelos TeóricosRESUMO
Although social behavior can have a strong genetic component, it can also result in selection on genome structure and function, thereby influencing the evolution of the genome itself. Here we explore the bidirectional links between social behavior and genome architecture by considering variation in social and/or mating behavior among populations (social polymorphisms) and across closely related species. We propose that social behavior can influence genome architecture via associated demographic changes due to social living. We establish guidelines to exploit emerging whole-genome sequences using analytical approaches that examine genome structure and function at different levels (regulatory vs structural variation) from the perspective of both molecular biology and population genetics in an ecological context.
Assuntos
Genoma , Comportamento Social , Ecologia , Genética PopulacionalRESUMO
Selfish genetic elements (historically also referred to as selfish genes, ultra-selfish genes, selfish DNA, parasitic DNA, genomic outlaws) are genetic segments that can enhance their own transmission at the expense of other genes in the genome, even if this has no or a negative effect on organismal fitness. [1-6] Genomes have traditionally been viewed as cohesive units, with genes acting together to improve the fitness of the organism. However, when genes have some control over their own transmission, the rules can change, and so just like all social groups, genomes are vulnerable to selfish behaviour by their parts. Early observations of selfish genetic elements were made almost a century ago, but the topic did not get widespread attention until several decades later. Inspired by the gene-centred views of evolution popularized by George Williams[7] and Richard Dawkins,[8] two papers were published back-to-back in Nature in 1980-by Leslie Orgel and Francis Crick[9] and Ford Doolittle and Carmen Sapienza[10] respectively-introducing the concept of selfish genetic elements (at the time called "selfish DNA") to the wider scientific community. Both papers emphasized that genes can spread in a population regardless of their effect on organismal fitness as long as they have a transmission advantage. Selfish genetic elements have now been described in most groups of organisms, and they demonstrate a remarkable diversity in the ways by which they promote their own transmission.[11] Though long dismissed as genetic curiosities, with little relevance for evolution, they are now recognized to affect a wide swath of biological processes, ranging from genome size and architecture to speciation.[12].
Assuntos
Locos de Características Quantitativas , Característica Quantitativa Herdável , Sequências Repetitivas de Ácido Nucleico , Agricultura , Biotecnologia , Estudos de Associação Genética , Modelos GenéticosRESUMO
PREMISE OF THE STUDY: Shifts in ploidy affect the evolutionary dynamics of genomes in a myriad of ways. Population genetic theory predicts that transposable element (TE) proliferation may follow because the genomewide efficacy of selection should be reduced and the increase in gene copies may mask the deleterious effects of TE insertions. Moreover, in allopolyploids, TEs may further accumulate because of hybrid breakdown of TE silencing. However, to date the evidence of TE proliferation following an increase in ploidy is mixed, and the relative importance of relaxed selection vs. silencing breakdown remains unclear. METHODS: We used high-coverage whole-genome sequence data to evaluate the abundance, genomic distribution, and population frequencies of TEs in the self-fertilizing recent allotetraploid Capsella bursa-pastoris (Brassicaceae). We then compared the C. bursa-pastoris TE profile with that of its two parental diploid species, outcrossing C. grandiflora and self-fertilizing C. orientalis. KEY RESULTS: We found no evidence that C. bursa-pastoris has experienced a large genomewide proliferation of TEs relative to its parental species. However, when centromeric regions are excluded, we found evidence of significantly higher abundance of retrotransposons in C. bursa-pastoris along the gene-rich chromosome arms compared with C. grandiflora and C. orientalis. CONCLUSIONS: The lack of a genomewide effect of allopolyploidy on TE abundance, combined with the increases TE abundance in gene-rich regions, suggests that relaxed selection rather than hybrid breakdown of host silencing explains the TE accumulation in C. bursa-pastoris.
Assuntos
Capsella/genética , Genética Populacional , Poliploidia , Evolução Biológica , Diploide , Frequência do Gene , Tamanho do Genoma , Polinização , AutofertilizaçãoRESUMO
During the last few decades, we have seen an explosion in the influx of details about the biology of selfish genetic elements. Ever since the early days of the field, the gene's-eye view of Richard Dawkins, George Williams, and others, has been instrumental to make sense of new empirical observations and to the generation of new hypotheses. However, the close association between selfish genetic elements and the gene's-eye view has not been without critics and several other conceptual frameworks have been suggested. In particular, proponents of multilevel selection models have used selfish genetic elements to criticize the gene's-eye view. In this paper, I first trace the intertwined histories of the study of selfish genetic elements and the gene's-eye view and then discuss how their association holds up when compared with other proposed frameworks. Next, using examples from transposable elements and the major transitions, I argue that different models highlight separate aspects of the evolution of selfish genetic elements and that the productive way forward is to maintain a plurality of perspectives. Finally, I discuss how the empirical study of selfish genetic elements has implications for other conceptual issues associated with the gene's-eye view, such as agential thinking, adaptationism, and the role of fitness maximizing models in evolution.
RESUMO
Plants have contributed extensively to our understanding of selfish genetic elements. Most recently, the sequencing of the Arabis alpina genome shows how the co-evolutionary arms race between transposable elements and the silencing machinery employed to control them may drive the evolution of genome size.
Assuntos
Arabis/genética , Elementos de DNA Transponíveis , Evolução Molecular , Tamanho do Genoma , Genoma de PlantaRESUMO
Genome size varies dramatically across species, but despite an abundance of attention there is little agreement on the relative contributions of selective and neutral processes in governing this variation. The rate of sex can potentially play an important role in genome size evolution because of its effect on the efficacy of selection and transmission of transposable elements (TEs). Here, we used a phylogenetic comparative approach and whole genome sequencing to investigate the contribution of sex and TE content to genome size variation in the evening primrose (Oenothera) genus. We determined genome size using flow cytometry for 30 species that vary in genetic system and find that variation in sexual/asexual reproduction cannot explain the almost twofold variation in genome size. Moreover, using whole genome sequences of three species of varying genome sizes and reproductive system, we found that genome size was not associated with TE abundance; instead the larger genomes had a higher abundance of simple sequence repeats. Although it has long been clear that sexual reproduction may affect various aspects of genome evolution in general and TE evolution in particular, it does not appear to have played a major role in genome size evolution in the evening primroses.
Assuntos
Elementos de DNA Transponíveis , Tamanho do Genoma , Genoma de Planta , Oenothera/genética , Evolução Biológica , Hibridização Genômica Comparativa , DNA de Plantas/genética , Oenothera/classificação , FilogeniaRESUMO
Whole-genome duplication (WGD) events have occurred repeatedly during flowering plant evolution, and there is growing evidence for predictable patterns of gene retention and loss following polyploidization. Despite these important insights, the rate and processes governing the earliest stages of diploidization remain poorly understood, and the relative importance of genetic drift, positive selection, and relaxed purifying selection in the process of gene degeneration and loss is unclear. Here, we conduct whole-genome resequencing in Capsella bursa-pastoris, a recently formed tetraploid with one of the most widespread species distributions of any angiosperm. Whole-genome data provide strong support for recent hybrid origins of the tetraploid species within the past 100,000-300,000 y from two diploid progenitors in the Capsella genus. Major-effect inactivating mutations are frequent, but many were inherited from the parental species and show no evidence of being fixed by positive selection. Despite a lack of large-scale gene loss, we observe a decrease in the efficacy of natural selection genome-wide due to the combined effects of demography, selfing, and genome redundancy from WGD. Our results suggest that the earliest stages of diploidization are associated with quantitative genome-wide decreases in the strength and efficacy of selection rather than rapid gene loss, and that nonfunctionalization can receive a "head start" through a legacy of deleterious variants and differential expression originating in parental diploid populations.
Assuntos
Capsella/genética , Quimera/genética , Evolução Molecular , Genoma de Planta/fisiologia , Poliploidia , Seleção Genética , Estudo de Associação Genômica Ampla , MutaçãoRESUMO
The coordination between nuclear and organellar genes is essential to many aspects of eukaryotic life, including basic metabolism, energy production, and ultimately, organismal fitness. Although nuclear genes are biparentally inherited, mitochondrial and chloroplast genes are almost exclusively maternally inherited, and this asymmetry may lead to a bias in the chromosomal distribution of nuclear genes whose products act in the mitochondria or chloroplasts. In particular, because X-linked genes have a higher probability of cotransmission with organellar genes (2/3) compared with autosomal genes (1/2), selection for coadaptation has been predicted to lead to an overrepresentation of nuclear-mitochondrial and nuclear-chloroplast genes on the X chromosome relative to autosomes. In contrast, the occurrence of sexually antagonistic organellar mutations might lead to selection for movement of cytonuclear genes from the X chromosome to autosomes to reduce male mutation load. Recent broad-scale comparative studies of N-mt distributions in animals have found evidence for these hypotheses in some species, but not others. Here, we use transcriptome sequences to conduct the first study of the chromosomal distribution of cytonuclear interacting genes in a plant species with sex chromosomes (Rumex hastatulus; Polygonaceae). We found no evidence of under- or overrepresentation of either N-mt or N-cp genes on the X chromosome, and thus no support for either the coadaptation or the sexual-conflict hypothesis. We discuss how our results from a species with recently evolved sex chromosomes fit into an emerging picture of the evolutionary forces governing the chromosomal distribution of nuclear-mitochondrial and nuclear-chloroplast genes.
Assuntos
Cromossomos de Plantas/genética , Células Germinativas Vegetais/metabolismo , Rumex/genética , Núcleo Celular/genética , Núcleo Celular/metabolismo , Cloroplastos/genética , Cloroplastos/metabolismo , Cromossomos de Plantas/metabolismo , Evolução Molecular , Células Germinativas Vegetais/citologia , Mitocôndrias/genética , Mitocôndrias/metabolismo , Rumex/citologiaRESUMO
The history of life has been characterised by evolutionary transitions in individuality, the grouping together of independently replicating units into new larger wholes: genes to chromosomes, chromosomes in genomes, up to three genomes in cells, and cells in multicellular organisms that form groups and societies. Central to understanding these transitions is to determine what prevents selfish behaviour at lower levels from disrupting the functionality of higher levels. Here, I review work on transposable elements, a common source of disruption at the genome level, in light of the evolutionary transitions framework, and argue that the rapid influx of data on transposons from whole-genome sequencing has created a rich data source to incorporate into the study of evolutionary transitions in individuality.