scholarly journals The order of trait emergence in the evolution of cyanobacterial multicellularity

2019 ◽  
Author(s):  
Katrin Hammerschmidt ◽  
Giddy Landan ◽  
Fernando Domingues Kümmel Tria ◽  
Jaime Alcorta ◽  
Tal Dagan
Keyword(s):  
Division Of Labor ◽  
Phenotypic Trait ◽  
Evolutionary Transition ◽  
Evolutionary Transitions ◽  
Differentiated Cells ◽  
Labor Theory ◽  
Significant Events ◽  
Reproductive Life ◽  
History Of ◽  
Multicellular Organisms

AbstractThe transition from unicellular to multicellular organisms is one of the most significant events in the history of life. Key to this process is the emergence of Darwinian individuality at the higher level: groups must become single entities capable of reproduction for selection to shape their evolution. Evolutionary transitions in individuality are characterized by cooperation between the lower level entities and by division of labor. Theory suggests that division of labor may drive the transition to multicellularity by eliminating the trade-off between two incompatible processes that cannot be performed simultaneously in one cell. Here we examine the evolution of the most ancient multicellular transition known today, that of cyanobacteria, where we reconstruct the sequence of ecological and phenotypic trait evolution. Our results show that the prime driver of multicellularity in cyanobacteria was the expansion in metabolic capacity offered by nitrogen fixation, which was accompanied by the emergence of the filamentous morphology and succeeded by a reproductive life cycle. This was followed by the progression of multicellularity into higher complexity in the form of differentiated cells and patterned multicellularity.Significance StatementThe emergence of multicellularity is a major evolutionary transition. The oldest transition, that of cyanobacteria, happened more than 3 to 3.5 billion years ago. We find N2 fixation to be the prime driver of multicellularity in cyanobacteria. This innovation faced the challenge of incompatible metabolic processes since the N2 fixing enzyme (nitrogenase) is sensitive to oxygen, which is abundantly found in cyanobacteria cells performing photosynthesis. At the same time, N2-fixation conferred an adaptive benefit to the filamentous morphology as cells could divide their labour into performing either N2-fixation or photosynthesis. This was followed by the culmination of complex multicellularity in the form of differentiated cells and patterned multicellularity.

scholarly journals The order of trait emergence in the evolution of cyanobacterial multicellularity

2020 ◽  
Author(s):  
Katrin Hammerschmidt ◽  
Giddy Landan ◽  
Fernando Domingues KüMmel Tria ◽  
Jaime Alcorta ◽  
Tal Dagan
Keyword(s):  
Division Of Labor ◽  
Phenotypic Trait ◽  
Metabolic Capacity ◽  
Evolutionary Transitions ◽  
Differentiated Cells ◽  
Labor Theory ◽  
Significant Events ◽  
Reproductive Life ◽  
History Of ◽  
Multicellular Organisms

Abstract The transition from unicellular to multicellular organisms is one of the most significant events in the history of life. Key to this process is the emergence of Darwinian individuality at the higher level: groups must become single entities capable of reproduction for selection to shape their evolution. Evolutionary transitions in individuality are characterized by cooperation between the lower level entities and by division of labor. Theory suggests that division of labor may drive the transition to multicellularity by eliminating the trade-off between two incompatible processes that cannot be performed simultaneously in one cell. Here we examine the evolution of the most ancient multicellular transition known today, that of cyanobacteria, where we reconstruct the sequence of ecological and phenotypic trait evolution. Our results show that the prime driver of multicellularity in cyanobacteria was the expansion in metabolic capacity offered by nitrogen fixation, which was accompanied by the emergence of the filamentous morphology and succeeded by a reproductive life cycle. This was followed by the progression of multicellularity into higher complexity in the form of differentiated cells and patterned multicellularity.

scholarly journals Conflict and cooperation in eukaryogenesis: implications for the timing of endosymbiosis and the evolution of sex

2015 ◽  
Author(s):  
Arunas L Radzvilavicius ◽  
Neil W Blackstone
Keyword(s):  
Cell Fusion ◽  
Mitochondrial Gene ◽  
Evolutionary Process ◽  
Eukaryotic Cell ◽  
Evolutionary Transition ◽  
Evolutionary Transitions ◽  
Conflict And Cooperation ◽  
Conflict Mediation ◽  
Considerable Debate ◽  
History Of

The complex eukaryotic cell is a result of an ancient endosymbiosis and one of the major evolutionary transitions. The timing of key eukaryotic innovations relative to the acquisition of mitochondria remains subject to considerable debate, yet the evolutionary process itself might constrain the order of these events. Endosymbiosis entailed levels-of-selection conflicts, and mechanisms of conflict mediation had to evolve for eukaryogenesis to proceed. The initial mechanisms of conflict mediation were based on the pathways inherited from prokaryotic symbionts and led to metabolic homeostasis in the eukaryotic cell, while later mechanisms (e.g., mitochondrial gene transfer) contributed to the expansion of the eukaryotic genome. Perhaps the greatest opportunity for conflict arose with the emergence of sex involving whole-cell fusion. While early evolution of cell fusion may have affected symbiont acquisition, sex together with the competitive symbiont behaviour would have destabilised the emerging higher-level unit. Cytoplasmic mixing, on the other hand, would have been beneficial for selfish endosymbionts, capable of using their own metabolism to manipulate the life history of the host. Given the results of our mathematical modelling, we argue that sex represents a rather late proto- eukaryotic innovation, allowing for the growth of the chimeric nucleus and contributing to the successful completion of the evolutionary transition.

scholarly journals Viruses and mobile elements as drivers of evolutionary transitions

2016 ◽  
Vol 371 (1701) ◽  
pp. 20150442 ◽  
Author(s):  
Eugene V. Koonin
Keyword(s):  
Genomic Analysis ◽  
Life Forms ◽  
Comparative Genomic ◽  
Biological Organization ◽  
Evolutionary Transitions ◽  
Selfish Genetic Elements ◽  
Cellular Life ◽  
History Of ◽  
Eusocial Animals ◽  
Multicellular Organisms

The history of life is punctuated by evolutionary transitions which engender emergence of new levels of biological organization that involves selection acting at increasingly complex ensembles of biological entities. Major evolutionary transitions include the origin of prokaryotic and then eukaryotic cells, multicellular organisms and eusocial animals. All or nearly all cellular life forms are hosts to diverse selfish genetic elements with various levels of autonomy including plasmids, transposons and viruses. I present evidence that, at least up to and including the origin of multicellularity, evolutionary transitions are driven by the coevolution of hosts with these genetic parasites along with sharing of ‘public goods’. Selfish elements drive evolutionary transitions at two distinct levels. First, mathematical modelling of evolutionary processes, such as evolution of primitive replicator populations or unicellular organisms, indicates that only increasing organizational complexity, e.g. emergence of multicellular aggregates, can prevent the collapse of the host–parasite system under the pressure of parasites. Second, comparative genomic analysis reveals numerous cases of recruitment of genes with essential functions in cellular life forms, including those that enable evolutionary transitions. This article is part of the themed issue ‘The major synthetic evolutionary transitions’.

scholarly journals Eukaryogenesis, how special really?

2015 ◽  
Vol 112 (33) ◽  
pp. 10278-10285 ◽  
Author(s):  
Austin Booth ◽  
W. Ford Doolittle
Keyword(s):  
Eukaryotic Cell ◽  
Evolutionary Transition ◽  
Evolutionary Potential ◽  
Evolutionary Transitions ◽  
History Of Research ◽  
Evolution Of Life ◽  
Widespread Acceptance ◽  
Statistical Support ◽  
History Of ◽  
Rhetorical Value

Eukaryogenesis is widely viewed as an improbable evolutionary transition uniquely affecting the evolution of life on this planet. However, scientific and popular rhetoric extolling this event as a singularity lacks rigorous evidential and statistical support. Here, we question several of the usual claims about the specialness of eukaryogenesis, focusing on both eukaryogenesis as a process and its outcome, the eukaryotic cell. We argue in favor of four ideas. First, the criteria by which we judge eukaryogenesis to have required a genuinely unlikely series of events 2 billion years in the making are being eroded by discoveries that fill in the gaps of the prokaryote:eukaryote “discontinuity.” Second, eukaryogenesis confronts evolutionary theory in ways not different from other evolutionary transitions in individuality; parallel systems can be found at several hierarchical levels. Third, identifying which of several complex cellular features confer on eukaryotes a putative richer evolutionary potential remains an area of speculation: various keys to success have been proposed and rejected over the five-decade history of research in this area. Fourth, and perhaps most importantly, it is difficult and may be impossible to eliminate eukaryocentric bias from the measures by which eukaryotes as a whole are judged to have achieved greater success than prokaryotes as a whole. Overall, we question whether premises of existing theories about the uniqueness of eukaryogenesis and the greater evolutionary potential of eukaryotes have been objectively formulated and whether, despite widespread acceptance that eukaryogenesis was “special,” any such notion has more than rhetorical value.

scholarly journals Colonial Life-history: A Major Evolutionary Transition, Involving Modularization of Multicellular Individuals and Heterochrony (Miniaturization and Adultation)

2020 ◽  
Author(s):  
Stefania Gutierrez
Keyword(s):  
Gene Expression ◽  
Life History ◽  
Division Of Labor ◽  
Blood Cells ◽  
Life Histories ◽  
Biological Information ◽  
Evolutionary Transition ◽  
Evolutionary Transitions ◽  
The Family ◽  
Individual Size

The diversification of life-histories is mediated by cooperation, innovations of biological information, modularity, and heterochrony in developmental processes. These processes are defined, contextualized, and exemplified, studying the evolution of coloniality (i.e. life-history involving modularization of the multicellular individual) in the family of benthic tunicates Styelidae. This study proposes that in these colonial tunicates there is an inter-generational division of labor, where one generation is feeding, a second is developing by morphogenetic processes, and a third is aging by programmed cell death and phagocytosis. The communication system developed in these colonies is mediated, by changes in proportion, location, and gene expression of specialized blood cells. Colonial life-history in animals is related to the reduction of individual size; development of extra-corporeal tissues to interconnect zooids; the inter-generational division of labor; and the reduction of zooid’s individuality. Processes analogous with the widely accepted major evolutionary transitions (METs), suggesting that coloniality could be studied as a MET. The understanding of colonial life-histories could provide information about key mechanisms for life diversification.

scholarly journals Did Human Culture Emerge in a Cultural Evolutionary Transition in Individuality?

2021 ◽  
Author(s):  
Dinah R. Davison ◽  
Claes Andersson ◽  
Richard E. Michod ◽  
Steven L. Kuhn
Keyword(s):  
Hierarchical Organization ◽  
Evolutionary Transitions ◽  
Major Transitions ◽  
Social Communities ◽  
Human Culture ◽  
Eusocial Insects ◽  
The Social ◽  
History Of ◽  
Cultural Evolutionary ◽  
Multicellular Organisms

AbstractEvolutionary Transitions in Individuality (ETI) have been responsible for the major transitions in levels of selection and individuality in natural history, such as the origins of prokaryotic and eukaryotic cells, multicellular organisms, and eusocial insects. The integrated hierarchical organization of life thereby emerged as groups of individuals repeatedly evolved into new and more complex kinds of individuals. The Social Protocell Hypothesis (SPH) proposes that the integrated hierarchical organization of human culture can also be understood as the outcome of an ETI—one that produced a “cultural organism” (a “sociont”) from a substrate of socially learned traditions that were contained in growing and dividing social communities. The SPH predicts that a threshold degree of evolutionary individuality would have been achieved by 2.0–2.5 Mya, followed by an increasing degree of evolutionary individuality as the ETI unfolded. We here assess the SPH by applying a battery of criteria—developed to assess evolutionary individuality in biological units—to cultural units across the evolutionary history of Homo. We find an increasing agreement with these criteria, which buttresses the claim that an ETI occurred in the cultural realm.

scholarly journals Division of labor and fitness decoupling in evolutionary transitions in individuality

2020 ◽  
Author(s):  
Guilhem Doulcier ◽  
Katrin Hammerschmidt ◽  
Pierrick Bourrat
Keyword(s):  
Division Of Labor ◽  
Life History Traits ◽  
Linear Functions ◽  
Evolutionary Constraints ◽  
Evolutionary Transitions ◽  
Evolutionary Transitions In Individuality ◽  
Reproductive Division Of Labor ◽  
Multicellular Organisms ◽  
Reproductive Division

AbstractReproductive division of labor has been proposed to play a key role for evolutionary transitions in individuality (ETIs). This chapter provides a guide to a theoretical model that addresses the role of a tradeoff between life-history traits in selecting for a reproductive division of labor during the transition from unicellular to multicellular organisms. In particular, it focuses on the five keys assumptions of the model, namely (1) fitness is viability times fecundity; (2) collective traits are linear functions of their cellular counterparts; (3) there is a tradeoff between cell viability and fecundity; (4) cell contribution to the collective is optimal; and (5) there is an initial reproductive cost in large collectives. Thereafter the chapter contrasts two interpretations of the model in the context of ETIs. Originally, the model was interpreted as showing that during the transition to multicellularity the fitness of the lower-level (the cells) is “transferred” to the higher level (the collective). Despite its apparent intuitiveness, fitness transfer may obscure actual mechanisms in metaphorical language. Thus, an alternative and more conservative interpretation of the model that focuses on cell traits and the evolutionary constraints that links them is advocated. In addition, it allows for pursuing subsequent questions, such as the evolution of development.

scholarly journals Geometry shapes evolution of early multicellularity

2014 ◽  
Author(s):  
Eric Libby ◽  
Will Ratcliff ◽  
Mike Travisano ◽  
Ben Kerr
Keyword(s):  
Cell Death ◽  
Division Of Labor ◽  
Cell Number ◽  
Evolutionary Transition ◽  
Yeast Saccharomyces Cerevisiae ◽  
Evolutionary Transitions ◽  
Major Transitions ◽  
Reproductive Differentiation ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

Organisms have increased in complexity through a series of major evolutionary transitions, in which formerly autonomous entities become parts of a novel higher-level entity. One intriguing feature of the higher-level entity after some major transitions is a division of reproductive labor among its lower-level units. Although it can have clear benefits once established, it is unknown how such reproductive division of labor originates. We consider a recent evolution experiment on the yeast Saccharomyces cerevisiae as a unique platform to address the issue of reproductive differentiation during an evolutionary transition in individuality. In the experiment, independent yeast lineages evolved a multicellular “snowflake-like” cluster form in response to gravity selection. Shortly after the evolution of clusters, the yeast evolved higher rates of cell death. While cell death enables clusters to split apart and form new groups, it also reduces their performance in the face of gravity selection. To understand the selective value of increased cell death, we create a mathematical model of the cellular arrangement within snowflake yeast clusters. The model reveals that the mechanism of cell death and the geometry of the snowflake interact in complex, evolutionarily important ways. We find that the organization of snowflake yeast imposes powerful limitations on the available space for new cell growth. By dying more frequently, cells in clusters avoid encountering space limitations, and, paradoxically, reach higher numbers. In addition, selection for particular group sizes can explain the increased rate of apoptosis both in terms of total cell number and total numbers of collectives. Thus, by considering the geometry of a primitive multicellular organism we can gain insight into the initial emergence of reproductive division of labor during an evolutionary transition in individuality.

scholarly journals What do we mean by multicellularity? The Evolutionary Transitions Framework provides answers

2021 ◽  
Author(s):  
Caroline Rose ◽  
Katrin Hammerschmidt
Keyword(s):  
Common Sense ◽  
Recent Literature ◽  
Evolutionary Transition ◽  
Research Directions ◽  
Evolutionary Transitions ◽  
Broad Field ◽  
Community Of Researchers ◽  
Multicellular Organisms

The meaning of the word ‘multicellularity’ appears to be unambiguous – a concept that can be grasped with common sense. On closer inspection, however, there is notable disparity in the recent literature regarding the usage of the term ‘multicellularity’, which can describe complex organisms, simple microbial colonies or even multi-species biofilms. In addition, while emerging research directions, such as ‘the evolutionary transition to multicellularity’, have brought together a highly interdisciplinary community of researchers, they tend to (mis)use historically relevant language that does not adequately describe the marginal or nascent cases of multicellularity that are the focus of this new field. We argue that clarity can be achieved with the realisation that the various definitions of multicellularity are in fact describing different stages that can occur during the course of evolution. With the aim of gaining semantic continuity among researchers in this broad field, we provide a framework for identifying the stages of the evolutionary transition to multicellularity: from multicellular groups, to multicellular individuals, and finally to multicellular organisms.

scholarly journals Cooperation, clumping and the evolution of multicellularity

2015 ◽  
Vol 282 (1813) ◽  
pp. 20151075 ◽  
Author(s):  
Jay M. Biernaskie ◽  
Stuart A. West
Keyword(s):  
Public Goods ◽  
Public Good ◽  
Genetic Relatedness ◽  
Evolution Of Cooperation ◽  
Evolutionary Transitions ◽  
History Of ◽  
Major Shift ◽  
Multicellular Organisms ◽  
Number Of Cells

The evolution of multicellular organisms represents one of the major evolutionary transitions in the history of life. A potential advantage of forming multicellular clumps is that it provides an efficiency benefit to pre-existing cooperation, such as the production of extracellular ‘public goods’. However, this is complicated by the fact that cooperation could jointly evolve with clumping, and clumping could have multiple consequences for the evolution of cooperation. We model the evolution of clumping and a cooperative public good, showing that (i) when considered separately, both clumping and public goods production gradually increase with increasing genetic relatedness; (ii) in contrast, when the traits evolve jointly, a small increase in relatedness can lead to a major shift in evolutionary outcome—from a non-clumping state with low public goods production to a cooperative clumping state with high values of both traits; (iii) high relatedness makes it easier to get to the cooperative clumping state and (iv) clumping can be inhibited when it increases the number of cells that the benefits of cooperation must be shared with, but promoted when it increases relatedness between those cells. Overall, our results suggest that public goods sharing can facilitate the formation of well-integrated cooperative clumps as a first step in the evolution of multicellularity.

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