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.

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

eLife ◽  
2020 ◽  
Vol 9 ◽  
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 ◽  
Classical Models ◽  
Reproductive Division Of Labor ◽  
Multicellular Organisms ◽  
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, we demonstrate that reproductive specialization is strongly favored in sparse networks of cellular interactions that reflect the morphology of early, simple multicellular organisms, highlighting the importance of restricted social interactions in the evolution of reproductive specialization.

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 Toward open-ended fraternal transitions in individuality

2018 ◽  
Author(s):  
Matthew A Moreno ◽  
Charles Ofria
Keyword(s):  
Resource Sharing ◽  
Evolutionary History ◽  
Simple Cell ◽  
Reproductive Ability ◽  
Close Cooperation ◽  
Multiple Levels ◽  
Complex Forms ◽  
High Level ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

The emergence of new replicating entities from the union of simpler entities represent some of the most profound events in natural evolutionary history. Such transitions in individuality are essential to the evolution of the most complex forms of life. As such, understanding these transitions is critical to building artificial systems capable of open-ended evolution. Alas, these transitions are challenging to induce or detect, even with computational organisms. Here, we introduce the DISHTINY (DIStributed Hierarchical Transitions in IndividualitY) platform, which provides simple cell-like organisms with the ability and incentive to unite into new individuals in a manner that can continue to scale to subsequent transitions. The system is designed to encourage these transitions so that they can be studied: organisms that coordinate spatiotemporally can maximize the rate of resource harvest, which is closely linked to their reproductive ability. We demonstrate the hierarchical emergence of multiple levels of individuality among simple cell-like organisms that evolve parameters for manually-designed strategies. During evolution, we observe reproductive division of labor and close cooperation among cells, including resource-sharing, aggregation of resource endowments for propagules, and emergence of an apoptosis response to somatic mutation. Many replicate populations evolved to direct their resources toward low-level groups (behaving like multi-cellular individuals) and many others evolved to direct their resources toward high-level groups (acting as larger-scale multi-cellular individuals).

scholarly journals Toward open-ended fraternal transitions in individuality

2018 ◽  
Author(s):  
Matthew A Moreno ◽  
Charles Ofria
Keyword(s):  
Resource Sharing ◽  
Evolutionary History ◽  
Simple Cell ◽  
Reproductive Ability ◽  
Close Cooperation ◽  
Multiple Levels ◽  
Complex Forms ◽  
High Level ◽  
Reproductive Division Of Labor ◽  
Reproductive Division

The emergence of new replicating entities from the union of simpler entities represent some of the most profound events in natural evolutionary history. Such transitions in individuality are essential to the evolution of the most complex forms of life. As such, understanding these transitions is critical to building artificial systems capable of open-ended evolution. Alas, these transitions are challenging to induce or detect, even with computational organisms. Here, we introduce the DISHTINY (DIStributed Hierarchical Transitions in IndividualitY) platform, which provides simple cell-like organisms with the ability and incentive to unite into new individuals in a manner that can continue to scale to subsequent transitions. The system is designed to encourage these transitions so that they can be studied: organisms that coordinate spatiotemporally can maximize the rate of resource harvest, which is closely linked to their reproductive ability. We demonstrate the hierarchical emergence of multiple levels of individuality among simple cell-like organisms that evolve parameters for manually-designed strategies. During evolution, we observe reproductive division of labor and close cooperation among cells, including resource-sharing, aggregation of resource endowments for propagules, and emergence of an apoptosis response to somatic mutation. Many replicate populations evolved to direct their resources toward low-level groups (behaving like multi-cellular individuals) and many others evolved to direct their resources toward high-level groups (acting as larger-scale multi-cellular individuals).

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