scholarly journals Evolution of genome fragility enables microbial division of labor

2021 ◽  
Author(s):  
Enrico Sandro Colizzi ◽  
Renske MA Vroomans ◽  
Daniel E Rozen ◽  
Roeland M.H. Merks ◽  
Bram van Dijk
Keyword(s):  
Division Of Labor ◽  
Large Scale ◽  
Antibiotic Production ◽  
Streptomyces Coelicolor ◽  
Fragile Sites ◽  
Local Competition ◽  
A Genome ◽  
Growth Promoting ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

Division of labor can evolve when social groups benefit from the functional specialisation of its members. Recently, a novel means of coordinating division of labor was found in the antibiotic-producing bacterium Streptomyces coelicolor, where functionally specialized cells are generated through large-scale genomic re-organisation. Here, we investigate how the evolution of a genome architecture enables such mutation-driven division of labor, using a multi-scale mathematical model of bacterial evolution. We let bacteria compete on the basis of their antibiotic production and growth rate in a spatially structured environment. Bacterial behavior is determined by the structure and composition of their genome, which encodes antibiotics, growth-promoting genes and fragile genomic loci that can induce chromosomal deletions. We find that a genomic organization evolves that partitions growth-promoting genes and antibiotic-coding genes to distinct parts of the genome, separated by fragile genomic loci. Mutations caused by these fragile sites mostly delete growth-promoting genes, generating antibiotic-producing mutants from non-producing (and weakly-producing) progenitors, in agreement with experimental observations. Mutants protect their colony from competitors but are themselves unable to replicate. We further show that this division of labor enhances the local competition between colonies by promoting antibiotic diversity. These results show that genomic organisation can co-evolve with genomic instabilities to enable reproductive division of labor.

scholarly journals Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity

2020 ◽  
Author(s):  
Rachel A. Johnston ◽  
Philippe Vullioud ◽  
Jack Thorley ◽  
Henry Kirveslahti ◽  
Leyao Shen ◽  
...  
Keyword(s):  
Division Of Labor ◽  
Morphological Plasticity ◽  
Skeletal Morphology ◽  
Eusocial Insects ◽  
Mole Rat ◽  
Gene Regulatory ◽  
Reproductive Division Of Labor ◽  
Reproductive Division ◽  
Skeletal Integrity ◽  
Vertebral Growth

AbstractIn some mammals and many social insects, highly cooperative societies are characterized by reproductive division of labor, in which breeders and nonbreeders become behaviorally and morphologically distinct. While differences in behavior and growth between breeders and nonbreeders have been extensively described, little is known of their molecular underpinnings. Here, we investigate the consequences of breeding for skeletal morphology and gene regulation in highly cooperative Damaraland mole-rats. By experimentally assigning breeding ‘queen’ status versus nonbreeder status to age-matched littermates, we confirm that queens experience vertebral growth that likely confers advantages to fecundity. However, they also up-regulate bone resorption pathways and show reductions in femoral mass, which predicts increased vulnerability to fracture. Together, our results show that, as in eusocial insects, reproductive division of labor in mole-rats leads to gene regulatory rewiring and extensive morphological plasticity. However, in mole-rats, concentrated reproduction is also accompanied by costs to bone strength.

scholarly journals Morphological and genomic shifts in mole-rat 'queens' increase fecundity but reduce skeletal integrity

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Rachel A Johnston ◽  
Philippe Vullioud ◽  
Jack Thorley ◽  
Henry Kirveslahti ◽  
Leyao Shen ◽  
...  
Keyword(s):  
Division Of Labor ◽  
Morphological Plasticity ◽  
Skeletal Morphology ◽  
Eusocial Insects ◽  
Mole Rat ◽  
Gene Regulatory ◽  
Reproductive Division Of Labor ◽  
Reproductive Division ◽  
Skeletal Integrity ◽  
Vertebral Growth

In some mammals and many social insects, highly cooperative societies are characterized by reproductive division of labor, in which breeders and nonbreeders become behaviorally and morphologically distinct. While differences in behavior and growth between breeders and nonbreeders have been extensively described, little is known of their molecular underpinnings. Here, we investigate the consequences of breeding for skeletal morphology and gene regulation in highly cooperative Damaraland mole-rats. By experimentally assigning breeding 'queen' status versus nonbreeder status to age-matched littermates, we confirm that queens experience vertebral growth that likely confers advantages to fecundity. However, they also up-regulate bone resorption pathways and show reductions in femoral mass, which predicts increased vulnerability to fracture. Together, our results show that, as in eusocial insects, reproductive division of labor in mole-rats leads to gene regulatory rewiring and extensive morphological plasticity. However, in mole-rats, concentrated reproduction is also accompanied by costs to bone strength.

scholarly journals Topological constraints in early multicellularity favor reproductive division of labor

2019 ◽  
Author(s):  
David Yanni ◽  
Shane Jacobeen ◽  
Pedro Márquez-Zacarías ◽  
Joshua S Weitz ◽  
William C. Ratcliff ◽  
...  
Keyword(s):  
Division Of Labor ◽  
Resource Sharing ◽  
Evolutionary Biology ◽  
Large Body ◽  
Concave Function ◽  
Cellular Interactions ◽  
Wide Range ◽  
Classical Models ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

Reproductive division of labor (e.g., germ-soma specialization) is a hallmark of the evolution of multicellularity, signifying the emergence of a new type of individual and facilitating the evolution of increased organismal complexity. A large body of work from evolutionary biology, economics, and ecology has shown that specialization is beneficial when further division of labor produces an accelerating increase in absolute productivity (i.e., productivity is a convex function of specialization). Here we show that reproductive specialization is qualitatively different from classical models of resource sharing, and can evolve even when the benefits of specialization are saturating (i.e., productivity is a concave function of specialization). Through analytical theory and evolutionary individual based simulations, our work demonstrates that reproductive specialization is strongly favored in sparse networks of cellular interactions, such as trees and filaments, that reflect the morphology of early, simple multicellular organisms, highlighting the importance of restricted social interactions in the evolution of reproductive specialization. More broadly, we find that specialization is strongly favored, despite saturating returns on investment, in a wide range of scenarios in which sharing is asymmetric.

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