scholarly journals Multicellularity makes somatic differentiation evolutionarily stable

2014 ◽  
Author(s):  
Mary Elizabeth Wahl ◽  
Andrew Wood Murray

Many multicellular organisms produce two cell lineages: germ cells, whose descendants form the next generation, and somatic cells which support, protect, and disperse the germ cells. This distinction has evolved independently in dozens of multicellular taxa but is absent in unicellular species. We propose that unicellular, soma-producing populations are intrinsically susceptible to invasion by non-differentiating mutants which ultimately eradicate the differentiating lineage. We argue that multicellularity can prevent the victory of such mutants. To test this hypothesis, we engineer strains of the budding yeastSaccharomyces cerevisiaethat differ only in the presence or absence of multicellularity and somatic differentiation, permitting direct comparisons between organisms with different lifestyles. We find that non-differentiating mutants overtake unicellular populations but are outcompeted by multicellular differentiating strains, suggesting that multicellularity confers evolutionary stability to somatic differentiation.

2016 ◽  
Vol 113 (30) ◽  
pp. 8362-8367 ◽  
Author(s):  
Mary E. Wahl ◽  
Andrew W. Murray

Many multicellular organisms produce two cell lineages: germ cells, whose descendants produce the next generation, and somatic cells, which support, protect, and disperse the germ cells. This germ-soma demarcation has evolved independently in dozens of multicellular taxa but is absent in unicellular species. A common explanation holds that in these organisms, inefficient intercellular nutrient exchange compels the fitness cost of producing nonreproductive somatic cells to outweigh any potential benefits. We propose instead that the absence of unicellular, soma-producing populations reflects their susceptibility to invasion by nondifferentiating mutants that ultimately eradicate the soma-producing lineage. We argue that multicellularity can prevent the victory of such mutants by giving germ cells preferential access to the benefits conferred by somatic cells. The absence of natural unicellular, soma-producing species previously prevented these hypotheses from being directly tested in vivo: to overcome this obstacle, we engineered strains of the budding yeast Saccharomyces cerevisiae that differ only in the presence or absence of multicellularity and somatic differentiation, permitting direct comparisons between organisms with different lifestyles. Our strains implement the essential features of irreversible conversion from germ line to soma, reproductive division of labor, and clonal multicellularity while maintaining sufficient generality to permit broad extension of our conclusions. Our somatic cells can provide fitness benefits that exceed the reproductive costs of their production, even in unicellular strains. We find that nondifferentiating mutants overtake unicellular populations but are outcompeted by multicellular, soma-producing strains, suggesting that multicellularity confers evolutionary stability to somatic differentiation.


I wonder whether Anthony van Leeuwenhoek would have considered me as an appropriate choice for this lecture. For the past six years my interests have been in the rather unmanageable field of the genetics of cultured human somatic cells. These cells are animalcules only because we make them so. I can therefore look at the genetics of micro-organisms as an outsider, admittedly not wholly dispassionate. This is a pleasant task, because if there is a field of biology which has made great, unexpected and illuminating advances since 1940, this is it. Genetic analysis up to that time consisted in deducing the genetic constitution (‘genotype’) of an individual, which underlies its relevant somatic characters (‘phenotype’), from the distribution of these characters among its ascendants and its descendants. It therefore required the analysis of the results of breeding— experimental or not—and was limited to organisms with sexual reproduction. It was particularly illuminating in those multicellular organisms in which there is a clear distinction between germ cells (‘gametes’) and soma. Here, short of a preformistic process, it is clear that we can distinguish between determinants of hereditary characters and the characters themselves.


2021 ◽  
Author(s):  
Adrian Stencel ◽  
Javier Suárez

AbstractAn understanding of the factors behind the evolution of multicellularity is one of today’s frontiers in evolutionary biology. This is because multicellular organisms are made of one subset of cells with the capacity to transmit genes to the next generation (germline cells) and another subset responsible for maintaining the functionality of the organism, but incapable of transmitting genes to the next generation (somatic cells). The question arises: why do somatic cells sacrifice their lives for the sake of germline cells? How is germ/soma separation maintained? One conventional answer refers to inclusive fitness theory, according to which somatic cells sacrifice themselves altruistically, because in so doing they enhance the transmission of their genes by virtue of their genetic relatedness to germline cells. In the present article we will argue that this explanation ignores the key role of policing mechanisms in maintaining the germ/soma divide. Based on the pervasiveness of the latter, we argue that the role of altruistic mechanisms in the evolution of multicellularity is limited and that our understanding of this evolution must be enriched through the consideration of coercion mechanisms.


Microbiology ◽  
1997 ◽  
Vol 143 (6) ◽  
pp. 1867-1876 ◽  
Author(s):  
P. A. Radcliffe ◽  
K. M. Binley ◽  
J. Trevethick ◽  
M. Hall ◽  
P. E. Sudbery

Endocrinology ◽  
2007 ◽  
Vol 149 (4) ◽  
pp. 1813-1819 ◽  
Author(s):  
Eri Shiraishi ◽  
Norifumi Yoshinaga ◽  
Takeshi Miura ◽  
Hayato Yokoi ◽  
Yuko Wakamatsu ◽  
...  

Müllerian inhibiting substance (MIS) is a glycoprotein belonging to the TGF-β superfamily. In mammals, MIS is responsible for the regression of Müllerian ducts in the male fetus. However, the role of MIS in gonadal sex differentiation of teleost fish, which have no Müllerian ducts, has yet to be clarified. In the present study, we examined the expression pattern of mis and mis type 2 receptor (misr2) mRNAs and the function of MIS signaling in early gonadal differentiation in medaka (teleost, Oryzias latipes). In situ hybridization showed that both mis and misr2 mRNAs were expressed in the somatic cells surrounding the germ cells of both sexes during early sex differentiation. Loss-of-function of either MIS or MIS type II receptor (MISRII) in medaka resulted in suppression of germ cell proliferation during sex differentiation. These results were supported by cell proliferation assay using 5-bromo-2′-deoxyuridine labeling analysis. Treatment of tissue fragments containing germ cells with recombinant eel MIS significantly induced germ cell proliferation in both sexes compared with the untreated control. On the other hand, culture of tissue fragments from the MIS- or MISRII-defective embryos inhibited proliferation of germ cells in both sexes. Moreover, treatment with recombinant eel MIS in the MIS-defective embryos dose-dependently increased germ cell number in both sexes, whereas in the MISRII-defective embryos, it did not permit proliferation of germ cells. These results suggest that in medaka, MIS indirectly stimulates germ cell proliferation through MISRII, expressed in the somatic cells immediately after they reach the gonadal primordium.


2006 ◽  
Vol 22 (4) ◽  
pp. 746-753 ◽  
Author(s):  
Kyu-Bom Koh ◽  
Yoshiro Toyama ◽  
Masatoshi Komiyama ◽  
Tetsuya Adachi ◽  
Hideki Fukata ◽  
...  

Sign in / Sign up

Export Citation Format

Share Document