Hidden paths to endless forms most wonderful: ecology latently shapes evolution of multicellular development in predatory bacteria

  • Carroll, S. B. Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom (Quercus, 2005).

  • Dobzhansky, T. & Spassky, B. Genetics of natural populations. XI. Manifestation of genetic variants in Drosophila pseudoobscura in different environments. Genetics 29, 270–290 (1944).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • van Valen, L. Review of Festschrift, by Theodosius Dobzhansky, Max K. Hecht, and William C. Steere. Science 180, 488–488 (1973).


    Google Scholar
     

  • Abouheif, E. et al. Eco-evo-devo: the time has come. Adv. Exp. Med. Biol. 781, 107–125 (2014).

  • Sultan, S. E. In Evolutionary Developmental Biology (eds Nuno de la Rosa, L. & Müller, G.) (Springer, 2021).

  • Skúlason, S. et al. A way forward with eco-evo-devo: an extended theory of resource polymorphism with postglacial fishes as model systems. Biol. Rev. 94, 1786–1808 (2019).

    PubMed 

    Google Scholar
     

  • Gomez-Mestre, I. & Warkentin, K. M. To hatch and hatch not: similar selective trade-offs but different responses to egg predators in two closely related, syntopic treefrogs. Oecologia 153, 197–206 (2007).

    PubMed 

    Google Scholar
     

  • Herron, M. D. et al. De novo origins of multicellularity in response to predation. Sci. Rep. 9, 2328 (2019).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fisher, R. M., Bell, T. & West, S. A. Multicellular group formation in response to predators in the alga Chlorella vulgaris. J. Evol. Biol. 29, 551–559 (2016).

    CAS 
    PubMed 

    Google Scholar
     

  • Noh, S., Christopher, L., Strassmann, J. E. & Queller, D. C. Wild Dictyostelium discoideum social amoebae show plastic responses to the presence of nonrelatives during multicellular development. Ecol. Evol. 10, 1119–1134 (2020).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • La Fortezza, M. & Velicer, G. J. Social selection within aggregative multicellular development drives morphological evolution. Proc. R. Soc. B. 288, 20211522 (2021).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • West-Eberhard, M. J. Sexual selection, social competition, and speciation. Q. Rev. Biol. 58, 155–183 (1983).


    Google Scholar
     

  • Saxon, A. D., O’Brien, E. K. & Bridle, J. R. Temperature fluctuations during development reduce male fitness and may limit adaptive potential in tropical rainforest Drosophila. J. Evol. Biol. 31, 405–415 (2018).

    CAS 
    PubMed 

    Google Scholar
     

  • García‐Roa, R., Garcia‐Gonzalez, F., Noble, D. W. A. & Carazo, P. Temperature as a modulator of sexual selection. Biol. Rev. 95, 1607–1629 (2020).

    PubMed 

    Google Scholar
     

  • McGlashan, J. K., Spencer, R.-J. & Old, J. M. Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings. Proc. R. Soc. B. 279, 1709–1715 (2011).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bozdag, G. O., Libby, E., Pineau, R., Reinhard, C. T. & Ratcliff, W. C. Oxygen suppression of macroscopic multicellularity. Nat. Commun. 12, 2838 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reinhard, C. T., Planavsky, N. J., Olson, S. L., Lyons, T. W. & Erwin, D. H. Earth’s oxygen cycle and the evolution of animal life. Proc. Natl Acad. Sci. USA 113, 8933–8938 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Callier, V. & Nijhout, H. F. Control of body size by oxygen supply reveals size-dependent and size-independent mechanisms of molting and metamorphosis. Proc. Natl Acad. Sci. USA 108, 14664–14669 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Taubenheim, J. et al. Bacteria- and temperature-regulated peptides modulate β-catenin signaling in Hydra. Proc. Natl Acad. Sci. USA doi.org/10.1073/pnas.2010945117 (2020).

  • Sikkink, K. L., Reynolds, R. M., Ituarte, C. M., Cresko, W. A. & Phillips, P. C. Rapid evolution of phenotypic plasticity and shifting thresholds of genetic assimilation in the nematode Caenorhabditis remanei. G3 4, 1103–1112 (2014).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Scoville, A. G. & Pfrender, M. E. Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl Acad. Sci. USA 107, 4260–4263 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nijhout, H. F., Kudla, A. M. & Hazelwood, C. C. Genetic assimilation and accommodation: models and mechanisms. Curr. Top. Dev. Biol. 141, 337–369 (2020).

  • Hintze, M. et al. A cell fate switch in the Caenorhabditis elegans seam cell lineage occurs through modulation of the WNT asymmetry pathway in response to temperature increase. Genetics 214, 927–939 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Paaby, A. B. & Testa, N. D. In Evolutionary Developmental Biology (eds Nuno de la Rosa, L. & Müller, G.) (Springer, 2021).

  • Sultan, S. E. In Phenotypic Plasticity & Evolution (ed. Pfennig, P.) (CRC Press, 2021).

  • Gonzalez, P. N. & Barbeito-Andrés, J. In Evolutionary Developmental Biology (eds Nuno de la Rosa, L. & Müller, G.) (Springer, 2021).

  • Kawecki, T. J. et al. Experimental evolution. Trends Ecol. Evol. 27, 547–560 (2012).

    PubMed 

    Google Scholar
     

  • Wagner, A. The white-knight hypothesis, or does the environment limit innovations? Trends Ecol. Evol. 32, 131–140 (2017).

    PubMed 

    Google Scholar
     

  • Lafuente, E. & Beldade, P. Genomics of developmental plasticity in animals. Front. Genet. 10, 720, (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nijhout, H. F. Problems and paradigms: metaphors and the role of genes in development. Bioessays 12, 441–446 (1990).

    CAS 
    PubMed 

    Google Scholar
     

  • Berger, D., Bauerfeind, S. S., Blanckenhorn, W. U. & Schäfer, M. A. High temperatures reveal cryptic genetic variation in a polymorphic female sperm storage organ. Evolution 65, 2830–2842 (2011).

    PubMed 

    Google Scholar
     

  • Ledon‐Rettig, C. C., Pfennig, D. W. & Nascone‐Yoder, N. Ancestral variation and the potential for genetic accommodation in larval amphibians: implications for the evolution of novel feeding strategies. Evol. Dev. 10, 316–325 (2008).

    PubMed 

    Google Scholar
     

  • Rendueles, O. & Velicer, G. J. Hidden paths to endless forms most wonderful: complexity of bacterial motility shapes diversification of latent phenotypes. BMC Evol. Biol. 20, 145 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Freund, L., Vasse, M. & Velicer, G. J. Hidden paths to endless forms most wonderful: parasite-blind diversification of host quality. Proc. R. Soc. B. 288, 20210456, (2021).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kinsler, G., Geiler-Samerotte, K. & Petrov, D. A. Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation. eLife 9, e61271, doi.org/10.7554/elife.61271 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Paaby, A. B. & Rockman, M. V. The many faces of pleiotropy. Trends Genet. 29, 66–73 (2013).

    CAS 
    PubMed 

    Google Scholar
     

  • Paaby, A. B. & Rockman, M. V. Cryptic genetic variation: evolution’s hidden substrate. Nat. Rev. Genet. 15, 247–258 (2014).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Payne, J. L. & Wagner, A. Latent phenotypes pervade gene regulatory circuits. BMC Syst. Biol. 8, 64, (2014).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Payne, J. L. & Wagner, A. The causes of evolvability and their evolution. Nat. Rev. Genet. 20, 24–38 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • Zheng, J., Payne, J. L. & Wagner, A. Cryptic genetic variation accelerates evolution by opening access to diverse adaptive peaks. Science 365, 347–353 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • La Fortezza, M., Schaal, K. A. & Velicer, G. J. In The Evolution of Multicellularity (eds Herron, M. D., Conlin, P. & Ratcliff, W. C.) Ch. 6 (CRC Press, 2022).

  • Dawid, W. Biology and global distribution of myxobacteria in soils. FEMS Microbiol. Rev. 24, 403–427 (2000).

    CAS 
    PubMed 

    Google Scholar
     

  • Thiery, S. & Kaimer, C. The predation strategy of Myxococcus xanthus. Front. Microbiol. 11, 2, doi.org/10.3389/fmicb.2020.00002 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arend, K. I. et al. Myxococcus xanthus predation of Gram-positive or Gram-negative bacteria is mediated by different bacteriolytic mechanisms. Appl. Environ. Microbiol. 87, e02382–20, doi.org/10.1128/aem.02382-20 (2020).

    CAS 
    Article 

    Google Scholar
     

  • Muñoz-Dorado, J., Marcos-Torres, F. J., García-Bravo, E., Moraleda-Muñoz, A. & Pérez, J. Myxobacteria: moving, killing, feeding, and surviving together. Front. Microbiol. 7, 2475–18, doi.org/10.3389/fmicb.2016.00781 (2016).

    Article 

    Google Scholar
     

  • Wu, S. S. & Kaiser, D. Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol. Microbiol. 18, 547–558 (1995).

    CAS 
    PubMed 

    Google Scholar
     

  • Faure, L. M. et al. The mechanism of force transmission at bacterial focal adhesion complexes. Nature 539, 530–535 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shimkets, L. J., Dworkin, M. & Reichenbach, H. In The Prokaryotes, Volume 7: Proteobacteria: Delta, Epsilon Subclass (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K. & Stackebrandt, E.) Ch. 3.4.3 (Springer, 2006).

  • Mercier, R. & Mignot, T. Regulations governing the multicellular lifestyle of Myxococcus xanthus. Curr. Opin. Microbiol. 34, 104–110 (2016).

    CAS 
    PubMed 

    Google Scholar
     

  • Kawecki, T. J. & Ebert, D. Conceptual issues in local adaptation. Ecol. Lett. 7, 1225–1241 (2004).


    Google Scholar
     

  • Levins, R. Evolution in Changing Environments (Princeton Univ. Press, 1968).

  • Satterwhite, R. S. & Cooper, T. F. Constraints on adaptation of Escherichia coli to mixed‐resource environments increase over time. Evolution 69, 2067–2078 (2015).

    CAS 
    PubMed 

    Google Scholar
     

  • Williams, G. C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11, 398 (1957).


    Google Scholar
     

  • Ackermann, M., Schauerte, A., Stearns, S. C. & Jenal, U. Experimental evolution of aging in a bacterium. BMC Evol. Biol. 7, 126, (2007).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Moreno-Gámez, S. et al. Wide lag time distributions break a trade-off between reproduction and survival in bacteria. Proc. Natl Acad. Sci. USA 117, 18729–18736 (2020).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Paepe, M. D. & Taddei, F. Viruses’ life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biol. 4, e193, (2006).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zakrzewska, A. et al. Genome-wide analysis of yeast stress survival and tolerance acquisition to analyze the central trade-off between growth rate and cellular robustness. Mol. Biol. Cell. 22, 4435–4446 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stearns, S. C. The Evolution of Life Histories (Oxford Univ. Press, 1992).

  • Wagner, G. P. & Zhang, J. The pleiotropic structure of the genotype–phenotype map: the evolvability of complex organisms. Nat. Rev. Genet. 12, 204–213 (2011).

    CAS 
    PubMed 

    Google Scholar
     

  • Velicer, G. J., Kroos, L. & Lenski, R. E. Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404, 598–601 (2000).

    CAS 
    PubMed 

    Google Scholar
     

  • Hillesland, K. L., Velicer, G. J. & Lenski, R. E. Experimental evolution of a microbial predator’s ability to find prey. Proc. R. Soc. B. 276, 459–467 (2009).

    PubMed 

    Google Scholar
     

  • Pham, V. D., Shebelut, C. W., Diodati, M. E., Bull, C. T. & Singer, M. Mutations affecting predation ability of the soil bacterium Myxococcus xanthus. Microbiology 151, 1865–1874 (2005).

    CAS 
    PubMed 

    Google Scholar
     

  • Zee, P. C., Liu, J. & Velicer, G. J. Pervasive, yet idiosyncratic, epistatic pleiotropy during adaptation in a behaviourally complex microbe. J. Evol. Biol. 30, 257–269 (2016).

    PubMed 

    Google Scholar
     

  • Nair, R. R., Fiegna, F. & Velicer, G. J. Indirect evolution of social fitness inequalities and facultative social exploitation. Proc. R. Soc. B. 285, 20180054, (2018).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, P. & Zhang, J. Antagonistic pleiotropy conceals molecular adaptations in changing environments. Nat. Ecol. Evol. 4, 461–469 (2020).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bono, L. M., Smith, L. B., Pfennig, D. W. & Burch, C. L. The emergence of performance trade‐offs during local adaptation: insights from experimental evolution. Mol. Ecol. 26, 1720–1733 (2017).

    PubMed 

    Google Scholar
     

  • Ferenci, T. Trade-off mechanisms shaping the diversity of bacteria. Trends Microbiol 24, 209–223 (2016).

    CAS 
    PubMed 

    Google Scholar
     

  • Amherd, M., Velicer, G. J. & Rendueles, O. Spontaneous nongenetic variation of group size creates cheater-free groups of social microbes. Behav. Ecol. 29, 393–403 (2018).


    Google Scholar
     

  • Fiegna, F. & Velicer, G. J. Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol. 3, e370, (2005).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kraemer, S. A., Toups, M. A. & Velicer, G. J. Natural variation in developmental life-history traits of the bacterium Myxococcus xanthus. FEMS Microbiol. Ecol. 73, 226–233 (2010).

    CAS 
    PubMed 

    Google Scholar
     

  • Kadam, S. V. & Velicer, G. J. Variable patterns of density-dependent survival in social bacteria. Behav. Ecol. 17, 833–838 (2006).


    Google Scholar
     

  • Rajagopalan, R., Wielgoss, S., Lippert, G., Velicer, G. J. & Kroos, L. devI is an evolutionarily young negative regulator of Myxococcus xanthus development. J. Bacteriol. 197, 1249–1262 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Harris, B. Z., Kaiser, D. & Singer, M. The guanosine nucleotide (p)ppGpp initiates development and A-factor production in Myxococcus xanthus. Genes Dev. 12, 1022–1035 (1998).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rivera-Yoshida, N. et al. Plastic multicellular development of Myxococcus xanthus: genotype–environment interactions in a physical gradient. R. Soc. Open sci. 6, 181730–181739, doi.org/10.1098/rsos.181730 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fiegna, F., Yu, Y.-T. N., Kadam, S. V. & Velicer, G. J. Evolution of an obligate social cheater to a superior cooperator. Nature 441, 310–314 (2006).

    CAS 
    PubMed 

    Google Scholar
     

  • Moczek, A. Developmental plasticity and evolution—quo vadis? Heredity. 115, 302–305 (2015).

  • Levis, N. A. & Pfennig, D. W. Phenotypic plasticity, canalization, and the origins of novelty: Evidence and mechanisms from amphibians. Semin. Cell Dev. Biol. 88, 80–90 (2019).

    PubMed 

    Google Scholar
     

  • Velicer, G. J. & Yu, Y. N. Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 425, 75–78 (2003).

    CAS 
    PubMed 

    Google Scholar
     

  • Rendueles, O. & Velicer, G. J. Evolution by flight and fight: diverse mechanisms of adaptation by actively motile microbes. ISME J. 11, 555–568 (2016).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shi, W. & Zusman, D. R. The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc. Natl Acad. Sci. USA 90, 3378–3382 (1993).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Olson, E. C. & Miller, R. L. Morphological Integration (Uni. Chicago Press, 1958).

  • Pavlicev, M., Cheverud, J. M. & Wagner, G. P. Measuring morphological integration using eigenvalue variance. Evol. Biol. 36, 157–170 (2009).


    Google Scholar
     

  • Machado, F. A., Hubbe, A., Melo, D., Porto, A. & Marroig, G. Measuring the magnitude of morphological integration: the effect of differences in morphometric representations and the inclusion of size. Evolution 73, 2518–2528 (2019).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Muñoz-Dorado, J. et al. Transcriptome dynamics of the Myxococcus xanthus multicellular developmental program. eLife 8, e50374, (2019).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gill, R. E., Karlok, M. & Benton, D. Myxococcus xanthus encodes an ATP-dependent protease which is required for developmental gene transcription and intercellular signaling. J. Bacteriol. 175, 4538–4544 (1993).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tojo, N., Inouye, S. & Komano, T. The lonD gene is homologous to the lon gene encoding an ATP-dependent protease and is essential for the development of Myxococcus xanthus. J. Bacteriol. 175, 4545–4549 (1993).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Caberoy, N. B., Welch, R. D., Jakobsen, J. S., Slater, S. C. & Garza, A. G. Global mutational analysis of NtrC-like activators in Myxococcus xanthus: Identifying activator mutants defective for motility and fruiting body development. J. Bacteriol. 185, 6083–6094 (2003).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ueki, T. & Inouye, S. Transcriptional activation of a heat-shock gene, lonD, of Myxococcus xanthus by a two component histidine-aspartate phosphorelay system. J. Biol. Chem. 277, 6170–6177 (2002).

    CAS 
    PubMed 

    Google Scholar
     

  • Schlichting, C. D. In Phenotypic Plasticity & Evolution (ed. Pfennig, P.) Ch. 15 (CRC Press, 2021).

  • Schlichting, C. D. Hidden reaction norms, cryptic genetic variation, and evolvability. Ann. N. Y. Acad. Sci. 1133, 187–203 (2008).

    PubMed 

    Google Scholar
     

  • Travisano, M., Mongold, J., Bennett, A. & Lenski, R. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267, 87–90 (1995).

    CAS 
    PubMed 

    Google Scholar
     

  • Niklas, K. J. & Newman, S. A. The many roads to and from multicellularity. J. Exp. Bot. 71, 3247–3253 (2019).

    PubMed Central 

    Google Scholar
     

  • Morgan, A. D., MacLean, R. C., Hillesland, K. L. & Velicer, G. J. Comparative analysis of myxococcus predation on soil bacteria. Appl. Environ. Microbiol. 76, 6920–6927 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rendueles, O., Amherd, M. & Velicer, G. J. Positively frequency-dependent interference competition maintains diversity and pervades a natural population of cooperative microbes. Curr. Biol. 25, 1673–1681 (2015).

    CAS 
    PubMed 

    Google Scholar
     

  • Rosenberg, E., Keller, K. H. & Dworkin, M. Cell density-dependent growth of Myxococcus xanthus on casein. J. Bacteriol. 129, 770–777 (1977).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Velicer, G. J., Kroos, L. & Lenski, R. E. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl Acad. Sci. USA 95, 12376–12380 (1998).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cooper, T. F. & Lenski, R. E. Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evol. Biol. 10, 11, (2010).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lobkovsky, A. E. & Koonin, E. V. Replaying the tape of life: quantification of the predictability of evolution. Front. Genet. 3, 246, (2012).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kinnersley, M., Schwartz, K., Yang, D.-D., Sherlock, G. & Rosenzweig, F. Evolutionary dynamics and structural consequences of de novo beneficial mutations and mutant lineages arising in a constant environment. BMC Biol. 19, 20 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dahl, J. L., Ulrich, C. H. & Kroft, T. L. Role of phase variation in the resistance of Myxococcus xanthus fruiting bodies to Caenorhabditis elegans predation. J. Bacteriol. 193, 5081–5089 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Luciano, J. et al. Emergence and modular evolution of a novel motility machinery in bacteria. PLoS Genet 7, e1002268, (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Goldman, B., Bhat, S. & Shimkets, L. J. Genome evolution and the emergence of fruiting body development in Myxococcus xanthus. PLoS ONE 2, e1329, (2007).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schaal, K. A., Yu, Y.-T. N., Vasse, M. & Velicer, G. J. Allopatric divergence limits cheating range and alters genetic requirements for a cooperative trait. Preprint at bioRxiv doi.org/10.1101/2021.01.07.425765 (2021).

  • Rendueles, O. et al. Rapid and widespread de novo evolution of kin discrimination. Proc. Natl Acad. Sci. USA 112, 9076–9081 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yang, Z. & Higgs, P. I. Myxobacteria: Genomics, Cellular and Molecular Biology (Caister Academic, 2014).

  • Pfennig, P. In Phenotypic Plasticity & Evolution (ed. Pfennig, P.) Ch. 3 (CRC Press, 2021).

  • Gibson, G. & Dworkin, I. Uncovering cryptic genetic variation. Nat. Rev. Genet. 5, 681–690 (2004).

    CAS 
    PubMed 

    Google Scholar
     

  • Bretscher, A. P. & Kaiser, D. Nutrition of Myxococcus xanthus, a fruiting myxobacterium. J. Bacteriol. 133, 763–768 (1978).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    CAS 
    PubMed 

    Google Scholar
     

  • Team, R. C. R: a language and environment for statistical computing. www.R-project.org/ (2018).

  • Melo, D., Garcia, G., Hubbe, A., Assis, A. P. & Marroig, G. EvolQG – An R package for evolutionary quantitative genetics. F1000Res 4, 925, (2015).

    PubMed 

    Google Scholar
     

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