Life cycles, fitness decoupling and the evolution of multicellularity

Hammerschmidt, Katrin; Rose, Caroline J.; Kerr, Benjamin; Rainey, Paul B.

doi:10.1038/nature13884

Cited by 188 publications

(290 citation statements)

References 42 publications

(63 reference statements)

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“…Complex multicellular organisms, including humans, possess sophisticated regulatory pathways that may be viewed as genetic mechanisms suppressing the fitness of individual cells to ensure the fitness of the whole organism 2,3 . However, events such as somatic mutations or viral infections may eradicate such constraints and reactivate a cell's otherwise dormant capacity of seeking its own fitness, resulting in cancer [4][5][6] .…”

mentioning

confidence: 99%

The reverse evolution from multicellularity to unicellularity during carcinogenesis

et al. 2015

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Theoretical reasoning suggests that cancer may result from a knockdown of the genetic constraints that evolved for the maintenance of metazoan multicellularity. By characterizing the whole-life history of a xenograft tumour, here we show that metastasis is driven by positive selection for general loss-of-function mutations on multicellularity-related genes. Expression analyses reveal mainly downregulation of multicellularity-related genes and an evolving expression profile towards that of embryonic stem cells, the cell type resembling unicellular life in its capacity of unlimited clonal proliferation. Also, the emergence of metazoan multicellularity B600 Myr ago is accompanied by an elevated birth rate of cancer genes, and there are more loss-of-function tumour suppressors than activated oncogenes in a typical tumour. These data collectively suggest that cancer represents a loss-of-functiondriven reverse evolution back to the unicellular 'ground state'. This cancer evolution model may account for inter-/intratumoural genetic heterogeneity, could explain distant-organ metastases and hold implications for cancer therapy.

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confidence: 99%

The reverse evolution from multicellularity to unicellularity during carcinogenesis

et al. 2015

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“…The virgin queen is simply the propagule that continues the life cycle, even after the death of the mother colony, and spreads the eusocial behavior. Although the parallels are clear, for eusocial colonies this idea is not as surprising as the results of Hammerschmidt et al (2014) for microbes, arguably because for eusociality we have a better understanding of ecology and development, which places cooperation more firmly in the appropriate context. In the absence of such a context for the study of microbes, it seems paramount to carefully consider the terms we employ to describe behavior and interactions; the use of terms such as cooperation, cheating and selfishness poses the danger of anthropomorphizing behaviors and of biasing our study of ecoevolutionary processes.…”

Section: Cheaters As Essential Propagules: Pseudomonas Fluorescensmentioning

confidence: 99%

“…This focus on persistence, however, while so far very informative, comes at the expense of: (i) alternative hypotheses that might reveal different roles and different types of interactions between the purported cooperators and cheaters; and (ii) the possibility that cooperation is not always an end in itself but that both cooperation and cheating could form a transient phase serving as a stepping stone for new interactions and behaviors. These points are elegantly emphasized by studies in two bacteria: P. fluorescens (Hammerschmidt et al, 2014;Rainey and Kerr, 2010;Rainey and Rainey, 2003;Rainey and Travisano, 1998) and M. xanthus (Fiegna et al, 2006;Velicer and Vos, 2009). …”

Section: General Framework and Findingsmentioning

confidence: 99%

“…However, SM cells have the potential to reintroduce the WS type via spontaneous mutation. This inspired Hammerschmidt et al (2014) to consider an ecological scenario in which cheating SM cells are integral to the persistence of the mat phenotype. They set up a largescale experiment consisting of hundreds of microcosms: WS cells initiate each microcosm; cheater SM cells soon follow; the mat collapses; and, in a few of the microcosms, SM cells mutate back into WS type.…”

Section: Cheaters As Essential Propagules: Pseudomonas Fluorescensmentioning

confidence: 99%

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The ecology and evolution of social behavior in microbes

Tarnita

2017

Journal of Experimental Biology

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Cooperation has been studied extensively across the tree of life, from eusociality in insects to social behavior in humans, but it is only recently that a social dimension has been recognized and extensively explored for microbes. Research into microbial cooperation has accelerated dramatically and microbes have become a favorite system because of their fast evolution, their convenience as lab study systems and the opportunity for molecular investigations. However, the study of microbes also poses significant challenges, such as a lack of knowledge and an inaccessibility of the ecological context (used here to include both the abiotic and the biotic environment) under which the trait deemed cooperative has evolved and is maintained. I review the experimental and theoretical evidence in support of the limitations of the study of social behavior in microbes in the absence of an ecological context. I discuss both the need and the opportunities for experimental investigations that can inform a theoretical framework able to reframe the general questions of social behavior in a clear ecological context and to account for eco-evolutionary feedback.

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“…However, repeated experimental evolution in this system has found the evolution of phenotypes that switch more rapidly via epigenetic mechanisms (Beaumont et al 2009;Gallie et al 2015;Hammerschmidt et al 2014). Mathematical models show that because of the coupling between environmental oscillations and organismal populations, there is a single optimal stochastic switching frequency that is mostly independent of population size, the number of competing genotypes, the switching strategies of competitors, and the relative differences in growth rates of different types (Libby and Rainey 2013).…”

Section: Introductionmentioning

confidence: 99%

Evolution of regulated phenotypic expression during a transition to multicellularity

Wolinsky

Libby

2015

Evol Ecol

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Multicellular organisms coordinate growth and differentiation from single cell starting points with developmental programs. While the evolutionary origins of these programs are unknown, it is likely that they are closely tied to the evolution of regulatednot stochastic-phenotypic expression. To determine how such regulation might arise, we consider experimental populations of Pseudomonas fluorescens which evolved stochastic switching in the lab. This switching is directly coupled with environmental oscillations generated by the bacteria themselves. This unique example of niche construction provides reliable information that organisms may incorporate into regulation of phenotypes. We use mathematical models to investigate the success of two forms of regulation that rely on sensing either external or internal information. We find that both strategies can outcompete stochastic strategies for certain combinations of parameters. In particular, external sensing mechanisms are very effective over a large range of parameter space-including parameters that correspond to poor sensing of the extracellular signal and gradual responses. We show with evolutionary simulations that this robustness makes them more likely to evolve from initially stochastically switching populations rather than internal sensing mechanisms which require more tuning of parameters. These results demonstrate that, within this oscillating system, if regulatory mechanisms can evolve to incorporate environmental information then their selective advantage is sufficient for them to fix in the population.

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Life cycles, fitness decoupling and the evolution of multicellularity

Cited by 188 publications

References 42 publications

The reverse evolution from multicellularity to unicellularity during carcinogenesis

The reverse evolution from multicellularity to unicellularity during carcinogenesis

The ecology and evolution of social behavior in microbes

Evolution of regulated phenotypic expression during a transition to multicellularity

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