Abstract:

The evolution of complex multicellularity opened paths to increased morphological diversity and organizational novelty. This transition involved three processes: cells remained attached to one another to form groups, cells within these groups differentiated to perform different tasks, and the groups evolved new reproductive strategies ADDIN ZOTERO_ITEM CSL_CITATION {"citationID":"0OvDkK4g","properties":{"formattedCitation":"\\super 1\\uc0\\u8211{}5\\nosupersub{}","plainCitation":"1–5","noteIndex":0},"citationItems":[{"id":824,"uris":["http://zotero.org/users/1864512/items/LTQRGVLX"],"itemData":{"id":824,"type":"article-journal","abstract":"Benefits of increased size and functional specialization of cells have repeatedly promoted the evolution of multicellular organisms from unicellular ancestors. Many requirements for multicellular organization (cell adhesion, cell-cell communication and coordination, programmed cell death) likely evolved in ancestral unicellular organisms. However, the evolution of multicellular organisms from unicellular ancestors may be opposed by genetic conflicts that arise when mutant cell lineages promote their own increase at the expense of the integrity of the multicellular organism. Numerous defenses limit such genetic conflicts, perhaps the most important being development from a unicell, which minimizes conflicts from selection among cell lineages, and redistributes genetic variation arising within multicellular individuals between individuals. With a unicellular bottleneck, defecting cell lineages rarely succeed beyond the life span of the multicellular individual. When multicellularity arises through aggregation of scattered cells or when multicellular organisms fuse to form genetic chimeras, there are more opportunities for propagation of defector cell lineages. Intraorganismal competition may partly explain why multicellular organisms that develop by aggregation generally exhibit less differentiation than organisms that develop clonally.","container-title":"Annual Review of Ecology, Evolution, and Systematics","DOI":"10.1146/annurev.ecolsys.36.102403.114735","issue":"1","page":"621-654","source":"Annual Reviews","title":"The Evolution of Multicellularity: A Minor Major Transition?","title-short":"The Evolution of Multicellularity","volume":"38","author":[{"family":"Grosberg","given":"Richard K."},{"family":"Strathmann","given":"Richard R."}],"issued":{"date-parts":}}},{"id":840,"uris":["http://zotero.org/users/1864512/items/IANLNNEE"],"itemData":{"id":840,"type":"article-journal","abstract":"Over 600 million years ago, animals evolved from a unicellular or colonial organism whose cell(s) captured bacteria with a collar complex, a flagellum surrounded by a microvillar collar. Using principles from evolutionary cell biology, we reason that the transition to multicellularity required modification of pre-existing mechanisms for extracellular matrix synthesis and cytokinesis. We discuss two hypotheses for the origin of animal cell types: division of labor from ancient plurifunctional cells and conversion of temporally alternating phenotypes into spatially juxtaposed cell types. Mechanistic studies in diverse animals and their relatives promise to deepen our understanding of animal origins and cell biology.","container-title":"Developmental Cell","DOI":"10.1016/j.devcel.2017.09.016","ISSN":"1534-5807","issue":"2","journalAbbreviation":"Developmental Cell","page":"124-140","source":"ScienceDirect","title":"The Origin of Animal Multicellularity and Cell Differentiation","volume":"43","author":[{"family":"Brunet","given":"Thibaut"},{"family":"King","given":"Nicole"}],"issued":{"date-parts":}}},{"id":1001,"uris":["http://zotero.org/users/1864512/items/BVBESP47"],"itemData":{"id":1001,"type":"article-journal","abstract":"Simple multicellularity has evolved numerous times within the Eukarya, but complex multicellular organisms belong to only six clades: animals, embryophytic land plants, florideophyte red algae, laminarialean brown algae, and two groups of fungi. Phylogeny and genomics suggest a generalized trajectory for the evolution of complex multicellularity, beginning with the co-optation of existing genes for adhesion. Molecular channels to facilitate cell-cell transfer of nutrients and signaling molecules appear to be critical, as this trait occurs in all complex multicellular organisms but few others. Proliferation of gene families for transcription factors and cell signals accompany the key functional innovation of complex multicellular clades: differentiated cells and tissues for the bulk transport of oxygen, nutrients, and molecular signals that enable organisms to circumvent the physical limitations of diffusion. The fossil records of animals and plants document key stages of this trajectory.","container-title":"Annual Review of Earth and Planetary Sciences","DOI":"10.1146/annurev.earth.031208.100209","issue":"1","page":"217-239","source":"Annual Reviews","title":"The Multiple Origins of Complex Multicellularity","volume":"39","author":[{"family":"Knoll","given":"Andrew H."}],"issued":{"date-parts":}}},{"id":2527,"uris":["http://zotero.org/users/1864512/items/7HAL827T"],"itemData":{"id":2527,"type":"book","abstract":"Within a single captivating narrative, John Bonner combines an intensely personal memoir of scientific progress and an overview of what we now know about living things. Bonner, a major participant in the development of biology as an experimental science, draws on his life-long study of slime molds for an understanding of the life cycle-the foundation of all biology. In an age of increasing specialization and fragmentation among subfields of biology, this is a unique work of reflection and integration.  Originally published in 1995.  ThePrinceton Legacy Libraryuses the latest print-on-demand technology to again make available previously out-of-print books from the distinguished backlist of Princeton University Press. These paperback editions preserve the original texts of these important books while presenting them in durable paperback editions. The goal of the Princeton Legacy Library is to vastly increase access to the rich scholarly heritage found in the thousands of books published by Princeton University Press since its founding in 1905.","publisher":"Princeton University Press","source":"JSTOR","title":"Life Cycles: Reflections of an Evolutionary Biologist","title-short":"Life Cycles","URL":"https://www.jstor.org/stable/j.ctt13x19s8","author":[{"family":"BONNER","given":"JOHN TYLER"}],"accessed":{"date-parts":},"issued":{"date-parts":}}},{"id":1018,"uris":["http://zotero.org/users/1864512/items/UZJUBSXG"],"itemData":{"id":1018,"type":"article-journal","abstract":"The volvocine algae provide an unrivalled opportunity to explore details of an evolutionary pathway leading from a unicellular ancestor to multicellular organisms with a division of labor between different cell types. Members of this monophyletic group of green flagellates range in complexity from unicellular Chlamydomonas through a series of extant organisms of intermediate size and complexity to Volvox, a genus of spherical organisms that have thousands of cells and a germ-soma division of labor. It is estimated that these organisms all shared a common ancestor about 50 +/- 20 MYA. Here we outline twelve important ways in which the developmental repertoire of an ancestral unicell similar to modern C. reinhardtii was modified to produce first a small colonial organism like Gonium that was capable of swimming directionally, then a sequence of larger organisms (such as Pandorina, Eudorina and Pleodorina) in which there was an increasing tendency to differentiate two cell types, and eventually Volvox carteri with its complete germ-soma division of labor.","container-title":"BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology","DOI":"10.1002/bies.20197","ISSN":"0265-9247","issue":"3","journalAbbreviation":"Bioessays","language":"eng","note":"PMID: 15714559","page":"299-310","source":"PubMed","title":"A twelve-step program for evolving multicellularity and a division of labor","volume":"27","author":[{"family":"Kirk","given":"David L."}],"issued":{"date-parts":}}}],"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citatio...} ^1–5. Recent experiments identified selective pressures and mutations that can drive the emergence of simple multicellularity and cell differentiation ADDIN ZOTERO_ITEM CSL_CITATION {"citationID":"n1T1fxsM","properties":{"formattedCitation":"\\super 6\\uc0\\u8211{}11\\nosupersub{}","plainCitation":"6–11","noteIndex":0},"citationItems":[{"id":810,"uris":["http://zotero.org/users/1864512/items/WCHHY64X"],"itemData":{"id":810,"type":"article-journal","abstract":"Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes.","container-title":"Proceedings of the National Academy of Sciences","DOI":"10.1073/pnas.1115323109","ISSN":"0027-8424, 1091-6490","issue":"5","journalAbbreviation":"PNAS","language":"en","license":"©  . Freely available online through the PNAS open access option.","note":"PMID: 22307617","page":"1595-1600","source":"www-pnas-org.ezp-prod1.hul.harvard.edu","title":"Experimental evolution of multicellularity","volume":"109","author":[{"family":"Ratcliff","given":"William C."},{"family":"Denison","given":"R. Ford"},{"family":"Borrello","given":"Mark"},{"family":"Travisano","given":"Michael"}],"issued":{"date-parts":}}},{"id":896,"uris":["http://zotero.org/users/1864512/items/RUF389WK"],"itemData":{"id":896,"type":"article-journal","abstract":"We do not know how or why multicellularity evolved. We used the budding yeast, Saccharomyces cerevisiae, to ask whether nutrients that must be digested extracellularly select for the evolution of undifferentiated multicellularity. Because yeast use invertase to hydrolyze sucrose extracellularly and import the resulting monosaccharides, single cells cannot grow at low cell and sucrose concentrations. Three engineered strategies overcame this problem: forming multicellular clumps, importing sucrose before hydrolysis, and increasing invertase expression. We evolved populations in low sucrose to ask which strategy they would adopt. Of 12 successful clones, 11 formed multicellular clumps through incomplete cell separation, 10 increased invertase expression, none imported sucrose, and 11 increased hexose transporter expression, a strategy we had not engineered. Identifying causal mutations revealed genes and pathways, which frequently contributed to the evolved phenotype. Our study shows that combining rational design with experimental evolution can help evaluate hypotheses about evolutionary strategies.","container-title":"eLife","DOI":"10.7554/eLife.00367","ISSN":"2050-084X","page":"e00367","source":"eLife","title":"Improved use of a public good selects for the evolution of undifferentiated multicellularity","volume":"2","author":[{"family":"Koschwanez","given":"John H"},{"family":"Foster","given":"Kevin R"},{"family":"Murray","given":"Andrew W"}],"editor":[{"family":"Tautz","given":"Diethard"}],"issued":{"date-parts":}}},{"id":833,"uris":["http://zotero.org/users/1864512/items/KPHGAVEJ"],"itemData":{"id":833,"type":"article-journal","abstract":"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.","container-title":"Proceedings of the National Academy of Sciences","DOI":"10.1073/pnas.1608278113","ISSN":"0027-8424, 1091-6490","issue":"30","journalAbbreviation":"PNAS","language":"en","license":"©  . Freely available online through the PNAS open access option.","note":"PMID: 27402737","page":"8362-8367","source":"www-pnas-org.ezp-prod1.hul.harvard.edu","title":"Multicellularity makes somatic differentiation evolutionarily stable","volume":"113","author":[{"family":"Wahl","given":"Mary E."},{"family":"Murray","given":"Andrew W."}],"issued":{"date-parts":}}},{"id":2504,"uris":["http://zotero.org/users/1864512/items/I2XDBQ6N"],"itemData":{"id":2504,"type":"article-journal","abstract":"Volvox has two cell types: mortal somatic cells and immortal germ cells. Here we describe the transposon-tagging, cloning and characterization of regA, which plays a central role as a master regulatory gene in Volvox germ-soma differentiation by suppressing reproductive activities in somatic cells. The 12.5 kb regA transcription unit generates a 6,725 nucleotide mRNA that appears at the beginning of somatic cell differentiation, and that encodes a 111 kDa RegA protein that localizes to the nucleus, and has an unusual abundance of alanine, glutamine and proline. This is a compositional feature shared by functional domains of many ‘active’ repressors. These findings are consistent with the hypothesis that RegA acts in somatic cells to repress transcription of genes required for growth and reproduction, including 13 genes whose products are required for chloroplast biogenesis.","container-title":"Development","DOI":"10.1242/dev.126.4.639","ISSN":"0950-1991","issue":"4","journalAbbreviation":"Development","page":"639-647","source":"Silverchair","title":"regA, a Volvox gene that plays a central role in germ-soma differentiation, encodes a novel regulatory protein","volume":"126","author":[{"family":"Kirk","given":"M.M."},{"family":"Stark","given":"K."},{"family":"Miller","given":"S.M."},{"family":"Muller","given":"W."},{"family":"Taillon","given":"B.E."},{"family":"Gruber","given":"H."},{"family":"Schmitt","given":"R."},{"family":"Kirk","given":"D.L."}],"issued":{"date-parts":}}},{"id":2529,"uris":["http://zotero.org/users/1864512/items/8MX5NKWN"],"itemData":{"id":2529,"type":"article-journal","container-title":"PLoS biology","issue":"3","note":"publisher: Public Library of Science San Francisco, CA USA","page":"e3001551","source":"Google Scholar","title":"Regulation of sedimentation rate shapes the evolution of multicellularity in a close unicellular relative of animals","volume":"20","author":[{"family":"Dudin","given":"Omaya"},{"family":"Wielgoss","given":"Sébastien"},{"family":"New","given":"Aaron M."},{"family":"Ruiz-Trillo","given":"Iñaki"}],"issued":{"date-parts":}}},{"id":1309,"uris":["http://zotero.org/users/1864512/items/XG34XCEC"],"itemData":{"id":1309,"type":"article-journal","abstract":"Laboratory evolution of the yeast Saccharomyces cerevisiae in bioreactor batch cultures yielded variants that grow as multicellular, fast-sedimenting clusters. Knowledge of the molecular basis of this phenomenon may contribute to the understanding of natural evolution of multicellularity and to manipulating cell sedimentation in laboratory and industrial applications of S. cerevisiae. Multicellular, fast-sedimenting lineages obtained from a haploid S. cerevisiae strain in two independent evolution experiments were analyzed by whole genome resequencing. The two evolved cell lines showed different frameshift mutations in a stretch of eight adenosines in ACE2, which encodes a transcriptional regulator involved in cell cycle control and mother-daughter cell separation. Introduction of the two ace2 mutant alleles into the haploid parental strain led to slow-sedimenting cell clusters that consisted of just a few cells, thus representing only a partial reconstruction of the evolved phenotype. In addition to single-nucleotide mutations, a whole-genome duplication event had occurred in both evolved multicellular strains. Construction of a diploid reference strain with two mutant ace2 alleles led to complete reconstruction of the multicellular-fast sedimenting phenotype. This study shows that whole-genome duplication and a frameshift mutation in ACE2 are sufficient to generate a fast-sedimenting, multicellular phenotype in S. cerevisiae. The nature of the ace2 mutations and their occurrence in two independent evolution experiments encompassing fewer than 500 generations of selective growth suggest that switching between unicellular and multicellular phenotypes may be relevant for competitiveness of S. cerevisiae in natural environments.","container-title":"Proceedings of the National Academy of Sciences","DOI":"10.1073/pnas.1305949110","ISSN":"0027-8424, 1091-6490","issue":"45","journalAbbreviation":"PNAS","language":"en","license":"©  . Freely available online through the PNAS open access option.","note":"PMID: 24145419","page":"E4223-E4231","source":"www-pnas-org.ezp-prod1.hul.harvard.edu","title":"Genome duplication and mutations in ACE2 cause multicellular, fast-sedimenting phenotypes in evolved Saccharomyces cerevisiae","volume":"110","author":[{"family":"Oud","given":"Bart"},{"family":"Guadalupe-Medina","given":"Victor"},{"family":"Nijkamp","given":"Jurgen F."},{"family":"Ridder","given":"Dick","dropping-particle":"de"},{"family":"Pronk","given":"Jack T."},{"family":"Maris","given":"Antonius J. A.","dropping-particle":"van"},{"family":"Daran","given":"Jean-Marc"}],"issued":{"date-parts":}}}],"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citatio...} ^6–11 but the evolution of life cycles, in particular, how simple multicellular forms reproduce has been understudied. The selective pressure and mechanisms that produced a regular alternation between single cells and multicellular collectives are still unclear ADDIN ZOTERO_TEMP ¹². To probe the factors regulating simple multicellular life cycles, we examined a collection of wild isolates of the budding yeast, S. cerevisiae ADDIN ZOTERO_ITEM CSL_CITATION {"citationID":"SqjupY1q","properties":{"formattedCitation":"\\super 12\\nosupersub{}","plainCitation":"12","noteIndex":0},"citationItems":[{"id":2040,"uris":["http://zotero.org/users/1864512/items/P6JB8ZCH"],"itemData":{"id":2040,"type":"article-journal","abstract":"Saccharomyces cerevisiae has proved to be an invaluable model in classical and molecular genetics studies. Despite several hundreds of isolates already available, the scientific community relies on the use of only a handful of unrelated strains. The lack of sequence information, haploid derivatives and genetic markers has prevented novel strains from being used. Here, we release a set of 55 S. cerevisiae and Saccharomyces paradoxus genetically tractable strains, previously sequenced in the Saccharomyces Genome Resequencing Project. These strains are stable haploid derivatives and ura3 auxotrophs tagged with a 6-bp barcode, recognized by a restriction enzyme to allow easy identification. We show that the specific barcode can be used to accurately measure the prevalence of different strains during competition experiments. These strains are now amenable to a wide variety of genetic experiments and can be easily crossed with each other to create hybrids and segregants, providing a valuable resource for breeding programmes and quantitative genetic studies. Three versions of each strain (haploid Mat a and Mat alpha and diploid Mat a/alpha all as ura3::KanMX-Barcode) are available through the National Culture Yeast Collection.","container-title":"FEMS yeast research","DOI":"10.1111/j.1567-1364.2009.00583.x","ISSN":"1567-1364","issue":"8","journalAbbreviation":"FEMS Yeast Res","language":"eng","note":"PMID: 19840116","page":"1217-1225","source":"PubMed","title":"Generation of a large set of genetically tractable haploid and diploid Saccharomyces strains","volume":"9","author":[{"family":"Cubillos","given":"Francisco A."},{"family":"Louis","given":"Edward J."},{"family":"Liti","given":"Gianni"}],"issued":{"date-parts":}}}],"schema":"https://github.com/citation-style-language/schema/raw/master/csl-citatio...} ¹². We found that all these strains can exist as multicellular clusters, a phenotype that is controlled by the mating type locus and strongly influenced by the nutritional environment. Inspired by this variation, we engineered inducible dispersal in a multicellular laboratory strain and demonstrated that a regulated life cycle has an advantage over constitutively single-celled or constitutively multicellular life cycles when the environment alternates between favoring intercellular cooperation (a low sucrose concentration) and dispersal (a patchy environment generated by emulsion). Our results suggest that simple multicellularity in wild isolates could be under selection and is regulated by their genetic composition and the environments they encounter and that alternating patterns of resource availability may have played a role in the evolution of life cycles.