Volvocine Algae: From Simple to Complex Multicellularity

Herron, Matthew D.; Nedelcu, Aurora M.

doi:10.1007/978-94-017-9642-2_7

Cited by 29 publications

(12 citation statements)

References 102 publications

(119 reference statements)

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“…Differentiation of somatic cells is regulated by RegA, a protein that suppresses photosynthesis and thereby prevents division (88). Interestingly, phylogenetic studies revealed that a close homolog of RegA is involved in photoacclimation, a plastic response that can be triggered by light deprivation (39,89). In the unicellular ancestor, photoacclimation was likely required for cells to adjust to the diurnal light cycle: inhibiting photosynthesis during light limitation prevents oxidative stress.…”

Section: Conflictmentioning

confidence: 99%

On the origin of biological construction, with a focus on multicellularity

Gestel

Tarnita

2017

Proc. Natl. Acad. Sci. U.S.A.

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Biology is marked by a hierarchical organization: all life consists of cells; in some cases, these cells assemble into groups, such as endosymbionts or multicellular organisms; in turn, multicellular organisms sometimes assemble into yet other groups, such as primate societies or ant colonies. The construction of new organizational layers results from hierarchical evolutionary transitions, in which biological units (e.g., cells) form groups that evolve into new units of biological organization (e.g., multicellular organisms). Despite considerable advances, there is no bottom-up, dynamical account of how, starting from the solitary ancestor, the first groups originate and subsequently evolve the organizing principles that qualify them as new units. Guided by six central questions, we propose an integrative bottom-up approach for studying the dynamics underlying hierarchical evolutionary transitions, which builds on and synthesizes existing knowledge. This approach highlights the crucial role of the ecology and development of the solitary ancestor in the emergence and subsequent evolution of groups, and it stresses the paramount importance of the life cycle: only by evaluating groups in the context of their life cycle can we unravel the evolutionary trajectory of hierarchical transitions. These insights also provide a starting point for understanding the types of subsequent organizational complexity. The central research questions outlined here naturally link existing research programs on biological construction (e.g., on cooperation, multilevel selection, self-organization, and development) and thereby help integrate knowledge stemming from diverse fields of biology.

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Section: Conflictmentioning

confidence: 99%

On the origin of biological construction, with a focus on multicellularity

Gestel

Tarnita

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Multicellularity comes in many forms and complexity levels, ranging from simple cell aggregations, colonies, films or filaments to the most complex organisms known (Szathmary & Smith, ; Rokas, ; Fairclough, Dayel, & King, ; Knoll, ; Niklas & Newman, ; Richter & King, ; Sebé‐Pedrós et al ., ; Niklas, ; Rainey & de Monte, ; Umen, ; Aguilar, Eichwald, & Eberl, ; Herron & Nedelcu, ). While simple cell aggregations and colonies evolved at least 25 times in both pro‐ and eukaryotes (Grosberg & Strathmann, ; Rokas, ), complex multicellularity has evolved in up to five major groups: animals, embryophytes, red and brown algae (Knoll, ; Claessen et al ., ; Niklas, ; Umen, ; Cock et al ., , ; Nagy, ; Niklas & Newman, ; Sebé‐Pedrós, Degnan & Ruiz‐Trillo, ), and fungi.…”

Section: Introduction: Simple and Complex Multicellularitymentioning

confidence: 99%

“…Simple and complex multicellularity are distinguished based on the proportion of cells in direct contact with the environment (i.e. all versus some), the extent of cellular differentiation, cell adhesion, communication, a developmental program and programmed cell death (PCD) (Cock et al ., ; Knoll, ; Knoll & Hewitt, ; Herron & Nedelcu, ). Complex multicellularity is usually used with reference to three‐dimensional differentiated structures, although how (and whether) it is defined varies widely across studies.…”

Section: Introduction: Simple and Complex Multicellularitymentioning

confidence: 99%

“…Primitive mechanisms for cell adhesion, communication and differentiation exist also in simple colonial and even unicellular protists (King, Hittinger, & Carroll, ; Richter & King, ; Brunet & King, ; Sebé‐Pedrós et al, ), although they reach their highest complexity in complex multicellular organisms. Similarly, PCD also occurs in uni‐ and simple multicellular lineages (Herron & Nedelcu, ), so the more relevant question in the context of complex multicellularity is whether unprogrammed cell death is lethal to the multicellular individual or stalls its further development and reproduction (Knoll, ). It should be noted that, as is often the case in biology, discretely categorizing a continuum of evolved forms can be challenging, nevertheless, the distinction of simple and complex multicellularity is useful for comparing phyletic and genetic patterns across distantly related multicellular groups.…”

Section: Introduction: Simple and Complex Multicellularitymentioning

confidence: 99%

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Complex multicellularity in fungi: evolutionary convergence, single origin, or both?

2018

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Complex multicellularity represents the most advanced level of biological organization and it has evolved only a few times: in metazoans, green plants, brown and red algae and fungi. Compared to other lineages, the evolution of multicellularity in fungi follows different principles; both simple and complex multicellularity evolved via unique mechanisms not found in other lineages. Herein we review ecological, palaeontological, developmental and genomic aspects of complex multicellularity in fungi and discuss general principles of the evolution of complex multicellularity in light of its fungal manifestations. Fungi represent the only lineage in which complex multicellularity shows signatures of convergent evolution: it appears 8-11 times in distinct fungal lineages, which show a patchy phylogenetic distribution yet share some of the genetic mechanisms underlying complex multicellular development. To explain the patchy distribution of complex multicellularity across the fungal phylogeny we identify four key observations: the large number of apparently independent complex multicellular clades; the lack of documented phenotypic homology between these clades; the conservation of gene circuits regulating the onset of complex multicellular development; and the existence of clades in which the evolution of complex multicellularity is coupled with limited gene family diversification. We discuss how these patterns and known genetic aspects of fungal development can be reconciled with the genetic theory of convergent evolution to explain the pervasive occurrence of complex multicellularity across the fungal tree of life.

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“…Simple multicellular organisms exhibit phenotypes based on multiple, attached cells, arising either through the aggregation of numerous unicellular individuals, or through the lack of total separation following the division of a single‐celled progenitor (Grice & Degnan, ; Herron & Nedelcu, ). The simplest multicellular phenotypes (i.e., organisms exhibiting simple multicellularity) include sheets, clusters, and chains of physically attached cells that largely remain in direct contact with the external environment and exhibit limited intercellular differentiation, communication, and resource exchange (Knoll & Hewitt, ).…”

Section: Introduction —Animals Are Trophically Uniquementioning

confidence: 99%

A trophic framework for animal origins

Mills

Canfield

2016

Geobiology

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Metazoans emerged in a microbial world and play a unique role in the biosphere as the only complex multicellular eukaryotes capable of phagocytosis. While the bodyplan and feeding mode of the last common metazoan ancestor remain unresolved, the earliest multicellular stem-metazoans likely subsisted on picoplankton (planktonic microbes 0.2-2 μm in diameter) and dissolved organic matter (DOM), similarly to modern sponges. Once multicellular stem-metazoans emerged, they conceivably modulated both the local availability of picoplankton, which they preferentially removed from the water column for feeding, and detrital particles 2-100 μm in diameter, which they expelled and deposited into the benthos as waste products. By influencing the availability of these heterotrophic food sources, the earliest multicellular stem-metazoans would have acted as ecosystem engineers, helping create the ecological conditions under which other metazoans, namely detritivores and non-sponge suspension feeders incapable of subsisting on picoplankton and DOM, could emerge and diversify. This early style of metazoan feeding, specifically the phagocytosis of small eukaryotic prey, could have also encouraged the evolution of larger, even multicellular, eukaryotic forms less prone to metazoan consumption. Therefore, the first multicellular stem-metazoans, through their feeding, arguably helped bridge the strictly microbial food webs of the Proterozoic Eon (2.5-0.541 billion years ago) to the more macroscopic, metazoan-sustaining food webs of the Phanerozoic Eon (0.541-0 billion years ago).

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Volvocine Algae: From Simple to Complex Multicellularity

Cited by 29 publications

References 102 publications

On the origin of biological construction, with a focus on multicellularity

On the origin of biological construction, with a focus on multicellularity

Complex multicellularity in fungi: evolutionary convergence, single origin, or both?

A trophic framework for animal origins

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