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We appreciate the helpful comments of the editor, Akos Kovacs, and two reviewers on a previous version of the manuscript. Divisions of labor are ubiquitous in nature and can be found at nearly every level of biological organization, from the individuals of a shared society to the cells of a single multicellular organism. Tansley review no. Alternatively, in some non-heterocystous species, e.g., Plectonema boryanum, a temporal division of labor is employed to allow cells to pursue both photosynthesis and nitrogen fixation by switching between both functions on the basis of an externally driven circadian rhythm. Gavrilets, S. Rapid transition towards the division of labor via evolution of developmental plasticity. Hanschen, E. R., Ferris, P. J. Nat. doi: 10.1111/j.1749-6632.1959.tb49369.x, Buttery, N. J., Jack, C. N., Adu-Oppong, B., Snyder, K. T., Thompson, C. R. L., Queller, D. C., et al. doi: 10.1146/annurev.ecolsys.38.091206.095740, West, S. A., Griffin, A. S., Gardner, A., and Diggle, S. P. (2006). Abstract Divisions of labor are ubiquitous in nature and can be found at nearly every level of biological organization, from the individuals of a shared society to the cells of a single multicellular organism. What is division of labor in biology? Microbiol. doi: 10.1371/journal.pbio.1002141, Veening, J.-W., Smits, W. K., and Kuipers, O. P. (2008). PubMed Mol. Biol. Compartmentalized function through cell differentiation in filamentous cyanobacteria. 7, 3649. The authors thank K. Boomsma, A. P. Escudero, K. Foster, A. Gardner, M. Ghoul, J. Gore, A. Griffin, R. May, J. Strassmann, D. Unterweger and J. van Gestel for very useful discussions. This is called the Division of Labour. -, Bhat S., Ahrendt T., Dauth C., Bode H. B., Shimkets L. J. As with myxobacterial cells that undergo PCD, heterocysts in Anabaena are unable to divide and are thus reproductively sterile (Rossetti et al., 2010). West. 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Heterogenic expression of genes encoding secreted proteins at the periphery of Aspergillus niger colonies. Social evolution theory for microorganisms. We highlight gaps in our understanding of microbial caste ratios and argue for a shift in emphasis from understanding the maintenance of divisions of labor, generally, to instead focusing on its specific ecological benefits for microbial genotypes and colonies. 70, 11011108 (2015). The multicellular nature of filamentous heterocyst-forming cyanobacteria. (2014a). Social conflict in centimeter-and global-scale populations of the bacterium Myxococcus xanthus. Curr. Biol. Sci. This work was funded by grants from the Dutch National Science Foundation (NWO) to DR (824.02.003), the Dutch Applied Research Council to DC (12957) and a studentship to ZZ from the China Scholarship Council. (2016). Tansley review no. Charnov, E. L. The Theory of Sex Allocation (Princeton Univ. In examples we discuss below, e.g., the division of labor between vegetative growth and sporulation, differentiated tasks are mutually incompatible and cannot be carried out by a single cell at once. Unauthorized use of these marks is strictly prohibited. A., and Sanchez, J. Annu. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Behav. Nature 379, 630631. Next we examine the widespread natural variation within species in their expression of divisions of labor and compare this to the idea of optimal caste ratios in social insects. Division of labor in biofilms: the ecology of cell differentiation. PubMedGoogle Scholar. doi: 10.1038/nrg2429, Smith, J., Strassmann, J. E., and Queller, D. C. (2016). Although long studied in multicellular organisms and colonies of social insects, several recent studies have established that division of labour is common in microorganisms. 102, 4166 (1968). & Buckling, A. (2005). Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). Notably, these processes are also mutually incompatible due to their distinct physical positions in the colony itself. Shimkets, L. J. 25, 10861090 (2015). Microbiol. Nat. Griffin, A. S., West, S. A. In addition, the architecture of streptomycete colonies appears to largely insulate strains from mutations that give rise to less PCD or from exploitation from strains via colony fusion (Braendle and Szybalski, 1957, 2006). Natl. 279, 34573466. Sci. This does not, however, imply that it is caused by natural differences (biological differences between women and men, for example). Rev. Am. Dawkins, R. The Selfish Gene (Oxford Univ. Interestingly, cyanobacterial divisions of labor are labile and can be regulated depending on environmental conditions. Microorganisms. Rev. Bonner, J. T. Cellular Slime Molds (Princeton Univ. Microbial divisions of labor have been best studied in the more general context of microbial sociality and multicellularity. PLoS Comput. Several mechanisms have been proposed to explain the evolutionary origins of DOL; the basic feature common to all of them is that functional differences . Acad. Although microbes often live solitary lives, many phylogenetically divergent groups have independently evolved different levels of coordinated or patterned multicellularity (Claessen et al., 2014). Rev. eCollection 2022. Solution. B., and Thompson, C. R. L. (2009). Kuzdzal-Fick, J. J., Queller, D. C., Fox, S. A. Divisions of labor are ubiquitous in nature and can be found at nearly every level of biological organization, from the individuals of a shared society to the cells of a single multicellular organism. Natl Acad. J. Theor. In recent years, several examples of division of labour in microorganisms have arisen, which suggests that this strategy may also be important in microbial species. Ghoul, M., West, S. A., Diggle, S. P. & Griffin, A. S. An experimental test of whether cheating is context dependent. Bastiaans, E., Debets, A. J. M. & Aanen, D. K. Experimental evolution reveals that high relatedness protects multicellular cooperation from cheaters. Philos. Sci. A multicellular organism has a division of labor and specialization. Interestingly, these interactions also provide suggestive evidence that the division of labor in myxobacteria is socially contingent; whereas strains in isolation produce a fixed number of spores, this value can vary during competitive interactions. Rev. MBio 5, e00939-13. NICHD provides detailed information about these topics on its Labor and Delivery page. Proc. Front Microbiol. This is known as division of labour. Nat. (2016). Thus, it is likely that the different divisions of labor that distinguish strains are maintained for reasons that may have little to do with social challenges, but rather because of ecological benefits to specific strategies that are contingent on the environment where strains are growing. In particular, we expect these to be found for secreted products, like antibiotics or enzymes, whose effects can be shared by producers and non-producers alike and whose production is metabolically costly. During fertilization, a pair of centrioles is usually provided by the sperm, indicating that the defect might be due to a paternal effect. U.S.A. 104, 89138917. doi: 10.1038/embor.2008.83, Rossetti, V., and Bagheri, H. C. (2012). Proto-eukaryotes subsequently acquired mitochondrial progenitors by the phagocytic capture of bacteria. 33 Articles, This article is part of the Research Topic, Divisions of Labor in Multicellular Microbes, Maintaining Divisions of Labor with Aggregative Multicellularity, Divisions of Labor in Patterned Multicellularity, https://www.frontiersin.org/article/10.3389/fmicb.2016.02070/full#supplementary-material, Creative Commons Attribution License (CC BY), Institute of Biology, Leiden University, Leiden, Netherlands. Additionally, it remains unclear which environmental factors serve as cues for differentiation, and whether different strains vary in these responses to these cues. B. In addition to offering insights into the evolution of microbial multicellularity and a division of labor, the examples we consider also provide the best evidence of the central factors that ensure that these divisions are stably maintained. Fatty acids from membrane lipids become incorporated into lipid bodies during Myxococcus xanthus differentiation. Cooperation and competition in pathogenic bacteria. USA 103, 13531358 (2006). doi: 10.1038/35018074, Strassmann, J. E. (2016). However, two areas of research would benefit from a fuller understanding of these mechanisms: (1) the division of labor in non-clonal groups, an area that has already been studied extensively, and (2) explaining the relative frequencies of cell types within and across genotypes, a topic that has been largely neglected. Strains with high proportions of spore:stalk, those that win during social competition, tend to make many smaller spores that individually have reduced viability (Wolf et al., 2015). 8600 Rockville Pike Evolution 65, 320. Commun. doi: 10.1146/annurev.micro.112408.134109, Strassmann, J. E., and Queller, D. C. (2011). Some of these questions have been considered in an analogous microbial system: the social eukaryote Dictyostelium discoideum. Wolf, J. Fatty acids from membrane lipids become incorporated into lipid bodies during Myxococcus xanthus differentiation. doi: 10.1073/pnas.0702723104, Gilbert, O. M., Queller, D. C., and Strassmann, J. E. (2009). Intentional Language and Adaptation (DOC 40 kb), Can You Get Division of Labour Between Species? doi: 10.1128/JB.184.10.2719-2727.2002, Velicer, G. J., and Vos, M. (2009). Sci. It is often stated that there is strength in numbers. Bigger armies tend to conquer smaller ones, while giant flocks of starlings migrate more efficiently than a single bird on its own. 12, 115124 (2014). For example, beta cells in the pancreas are responsible for releasing insulin into the bloodstream. Social insects clearly exemplify divisions of labor at the level of a society of individuals (Smith et al., 2008). However, trade-offs limit their ability to allocate energy and resources to all of these different processes. Lett. Open Access Altruism and social cheating in the social amoeba Dictyostelium discoideum. Narrowing our view to the level of a single individual, multicellular organisms also are characterized by a division of labor among distinct cell and tissue types that each play specialized roles in maintaining the fitness of the whole organism. The energetic burden associated with the formation of these reproductive structures is thought to be supported by the partial degradation of the vegetative mycelium via PCD (Manteca et al., 2006; Yage et al., 2012). Google Scholar. It is most often applied to systems of mass production and is one of the basic organizing principles of the assembly line.
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