Topological constraints in early multicellularity favor reproductive division of labor

Yanni, David; Jacobeen, Shane; Márquez-Zacarías, Pedro; Weitz, Joshua S.; Ratcliff, William C.; Yunker, Peter

doi:10.7554/elife.54348

Cited by 42 publications

(50 citation statements)

References 75 publications

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“…Many of the major conceptual topics surrounding the evolution of multicellularity fall under this category. These include: (i) how multicellular groups form and become Darwinian units capable of adaptation [ 18 , 29 , 30 , 31 , 32 , 33 ], (ii) how the transition to multicellularity affects subsequent evolutionary processes [ 6 , 34 ], (iii) how cooperative behaviors associated with complex multicellular organisms (e.g., cellular differentiation) evolve and remain stable in the face of social defection [ 35 , 36 , 37 , 38 , 39 , 40 ], (iv) how multicellular life cycles arise and shape the subsequent evolution of multicellularity [ 13 , 14 , 41 ], and (v) how multicellular lineages co-opt and modify traits of their unicellular ancestor for novel multicellular purposes [ 21 , 27 , 42 , 43 , 44 ].…”

Section: Introductionmentioning

confidence: 99%

“…They can ‘come together’ via aggregation or ‘stay together’ by failing to separate after reproduction [ 51 ]. In this paper, we focus on multicellular organisms that form by ‘staying together’ because it is a common mode of multicellular development [ 45 ]; it favors the evolution of cooperation [ 52 ] and cellular differentiation [ 37 ]; and all ‘complex’ multicellular organisms (i.e., animals, plants, red algae, brown algae, and fungi) grow through cell adhesion following cell reproduction [ 53 ]. If multicellularity evolves via cells staying together, then the physical connection between cells must be maintained, at least until the multicellular organism fragments.…”

Section: Introductionmentioning

confidence: 99%

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The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity

Isaksson

Conlin

Kerr

et al. 2021

Genes

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Early multicellular organisms must gain adaptations to outcompete their unicellular ancestors, as well as other multicellular lineages. The tempo and mode of multicellular adaptation is influenced by many factors including the traits of individual cells. We consider how a fundamental aspect of cells, whether they reproduce via binary fission or budding, can affect the rate of adaptation in primitive multicellularity. We use mathematical models to study the spread of beneficial, growth rate mutations in unicellular populations and populations of multicellular filaments reproducing via binary fission or budding. Comparing populations once they reach carrying capacity, we find that the spread of mutations in multicellular budding populations is qualitatively distinct from the other populations and in general slower. Since budding and binary fission distribute age-accumulated damage differently, we consider the effects of cellular senescence. When growth rate decreases with cell age, we find that beneficial mutations can spread significantly faster in a multicellular budding population than its corresponding unicellular population or a population reproducing via binary fission. Our results demonstrate that basic aspects of the cell cycle can give rise to different rates of adaptation in multicellular organisms.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity

Isaksson

Conlin

Kerr

et al. 2021

Genes

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“…Consider a one-dimensional chain of cells, as examined by Yanni et al Chains are found in species like cyanobacteria that form filaments of cells, and such structures might have been important at the onset of the evolution of multicellularity (Figure 4B) (Yanni et al, 2020). We assume arbitrarily that "odd" cells along the filament are putative helpers and "even" cells are putative reproductives.…”

Section: (B) Can Topological Constraints Lead To Division Of Labour By Reciprocal Specialisation?mentioning

confidence: 99%

Does the evolution of division of labour require accelerating returns from individual specialisation?

Cooper

Frost

Liu

et al. 2021

Preprint

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Recent theory has overturned the assumption that accelerating returns from individual specialisation are required to favour the evolution of division of labour. Yanni et al. (2020) showed that topologically constrained groups, where cells cooperate with only direct neighbours such as for filaments or branching growths, can evolve a reproductive division of labour even with diminishing returns from individual specialisation. We developed a conceptual framework and specific models to investigate the factors that can favour the initial evolution of reproductive division of labour. We found that selection for division of labour in topologically constrained groups: (1) is not a single mechanism to favour division of labour – depending upon details of the group structure, division of labour can be favoured for different reasons; (2) always involves an efficiency benefit at the level of group fitness; and (3) requires a mechanism of coordination to determine which individuals perform which tasks. Given that such coordination is unlikely to evolve before division of labour, this limits the extent to which topological constraints could have favoured the initial evolution of division of labour. We conclude by suggesting experimental designs that could determine why division of labour is favoured in the natural world.

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“…The establishment and maintenance of germ cells are critical for ensuring the survival of a species [ 1 ]. Many factors affect germ cell maintenance, with temperature being a major factor [ 2 , 3 ]. Male germ cells (sperm) are produced through the complex process of spermatogenesis in the scrotum, where the temperature is lower than the core body temperature of most male mammals [ 4 ].…”

Section: Introductionmentioning

confidence: 99%

“…a,b Means in same column with different superscripts differ (p < 0.05 to p < 0.001) 1. Significant different expression of PCNA vs. apoptosis of germ cells in preweaning, cryptorchid, and contrascrotal testes (p < 0.05) 2. Significantly different expression of PCNA vs. apoptosis of germ cells in preweaning, cryptorchid, and contrascrotal testes (p < 0.01) 3.…”

mentioning

confidence: 99%

Effect of Cryptorchidism on the Histomorphometry, Proliferation, Apoptosis, and Autophagy in Boar Testes

Fan

Liu

Yue

et al. 2021

Animals

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Spontaneous unilateral cryptorchid boars have one testis in the abdomen or inguinal canal, causing its temperature to be at or near the body temperature, which impairs spermatogenesis, although the histomorphometry and molecular mechanisms underlying this process remain unclear. The aim of the present study was to determine the histomorphometry, proliferation, apoptosis, and autophagy alterations in spermatogonia and Sertoli cells in unilateral cryptorchid, scrotal (contrascrotal), and preweaning piglet (preweaning) testes. Histomorphometrical analysis of cryptorchid testes showed that the seminiferous tubules contained only Sertoli cells and a few spermatogonia, but did not contain post-meiotic germ cells. The number of spermatogonia markedly decreased, and the number of Sertoli cells did not change remarkably in cryptorchid testes. TUNEL assay results showed that apoptosis signals were predominantly observed in spermatogonia. In cryptorchid and contrascrotal testes, proliferating cell nuclear antigen (PCNA) and LC3 were located in spermatogonia. The number of PCNA-positive, TUNEL-positive, and LC3-positive germ cells was low, and the protein and mRNA levels of PCNA and LC3 were significantly decreased in cryptorchid testes. Taken together, the number of Sertoli cells did not change remarkably, whereas the number of germ cells decreased in the cryptorchid testes, compared with that in the contrascrotal testes. Insufficient proliferation, excessive apoptosis, and autophagy were involved in the regulation of the decrease in spermatogonia in cryptorchid boar testes.

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Topological constraints in early multicellularity favor reproductive division of labor

Cited by 42 publications

References 75 publications

The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity

The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity

Does the evolution of division of labour require accelerating returns from individual specialisation?

Effect of Cryptorchidism on the Histomorphometry, Proliferation, Apoptosis, and Autophagy in Boar Testes

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