Tempo and mode of multicellular adaptation in experimentally evolved saccharomyces cerevisiae

Evolution

Volumn 67, Issue 6, 2013, Pages 1573-1581

  Ratcliff, William C ^a,b   Pentz, Jennifer T ^a   Travisano, Michael ^a  

^a Biotechnology Institute   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Complexity; Development; Evo devo; Evolutionary dynamics; Major transition; Multilevel selection

Indexed keywords

ADAPTATION; COMPLEXITY; HYDRODYNAMICS; YEAST;

ADAPTATION; ARTICLE; CYTOLOGY; GENETIC SELECTION; GENETICS; MOLECULAR EVOLUTION; SACCHAROMYCES CEREVISIAE; TIME;

ADAPTATION, BIOLOGICAL; EVOLUTION, MOLECULAR; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC; TIME FACTORS;

SACCHAROMYCES CEREVISIAE;

EID: 84878661349     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12101     Document Type: Article

References (55)

1. Alfaro, M., D. Bolnick, and P. Wainwright . 2005. Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. Am. Nat. 165:E140-E154.
2. Barrick, J. E., D. S. Yu, S. H. Yoon, H. Jeong, T. K. Oh, D. Schneider, R. E. Lenski, and J. F. Kim . 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461:1243-1247.
3. Becks, L., S. P. Ellner, L. E. Jones, and N. G. Hairston Jr. 2010. Reduction of adaptive genetic diversity radically alters eco-evolutionary community dynamics. Ecol. Lett. 13:989-997.
4. Bell, G., and A. O. Mooers . 1997. Size and complexity among multicellular organisms. Biol. J. Linn. Soc. 60:345-363.
5. Blount, Z. D., C. Z. Borland, and R. E. Lenski . 2008. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc. Natl. Acad. Sci. USA 105:7899-7906.
6. Blount, Z. D., C. Z. Borland, and R. E. Lenski . 1998. The origins of multicellularity. Integr. Biol.: Issues, News, Rev. 1:27-36.
7. Bonner, J. T. 2004. Perspective: the size-complexity rule. Evolution 58:1883-1890.
8. Boraas, M. E., D. B. Seale, and J. E. Boxhorn . 1998. Phagotrophy by a flagellate selects for colonial prey: a possible origin of multicellularity. Evol. Ecol. 12:153-164.
9. Bull, L. 1999. On the evolution of multicellularity and eusociality. Artif. Life 5:1-15.
10. Buss, L. W. 1987. The evolution of individuality. Princeton Univ. Press, Princeton, NJ.
11. Cavalier-Smith, T. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Intl. J. Syst. Evol. Microbiol. 52:297-354.
12. Damuth, J., and I. L. Heisler . 1988. Alternative formulations of multilevel selection. Biol. Philos. 3:407-430.
13. Diggle, S. P., A. S. Griffin, G. S. Campbell, and S. A. West . 2007. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450:411-414.
14. Fairclough, S. R., M. J. Dayel, and N. King . 2010. Multicellular development in a choanoflagellate. Curr. Biol. 20:R875-R876.
15. Frank, S. A. 1998. Foundations of social evolution. Princeton Univ. Press, Princeton, NJ.
16. Friis, E. M., K. R. Pedersen, and P. R. Crane . 2006. Cretaceous angiosperm flowers: innovation and evolution in plant reproduction. Palaeogeogr., Palaeoclimatol., Palaeoecol. 232:251-293.
17. Gilbert, O., K. Foster, N. Mehdiabadi, J. Strassmann, and D. Queller . 2007. High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc. Natl. Acad. Sci. USA 104:8913-8917.
18. Griesemer, J. 2001. The units of evolutionary transition. Selection 1:67-80.
19. Grosberg, R. K., and R. R. Strathmann . 1998. One cell, two cell, red cell, blue cell: the persistence of a unicellular stage in multicellular life histories. Trends Ecol. Evol. 13:112-116.
20. Grosberg, R. K., and R. R. Strathmann . 2007. The evolution of multicellularity: a minor major transition? Annu. Rev. Ecol. Evol. Syst. 38:621-654.
21. Herron, M. D., and R. E. Michod . 2008. Evolution of complexity in the volvocine algae: transitions in individuality through Darwin's eye. Evolution 62:436-451.
22. Hulsey, C. D., F. J. G. de León, and R. Rodiles-Hernández . 2006. Micro- and macroevolutionary decoupling of cichlid jaws: a test of Liem's key innovation hypothesis. Evolution 60:2096-2109.
23. Ispolatov, I., M. Ackermann, and M. Doebeli . 2012. Division of labour and the evolution of multicellularity. Proc. R. Soc. B: Biol. Sci. 279:1768-1776.
24. King, N., C. T. Hittinger, and S. B. Carroll . 2003. Evolution of key cell signaling and adhesion protein families predates animal origins. Science 301:361-363.
25. Kirk, D. L. 2005. A twelve-step program for evolving multicellularity and a division of labor. BioEssays 27:299-310.
26. Koufopanou, V. 1994. The evolution of soma in the volvocales. Am. Nat. 145:907-931.
27. Koschwanez, J. H., Foster K. R., and Murray A. W. 2011. Sucrose utilization in budding yeast as a model for the origin of undifferentiated multicellularity. PLoS Biol. 9:e1001122
28. Lenski, R. E., and M. Travisano . 1994. Dynamics of adaptation and diversification: a 10, 000-generation experiment with bacterial populations. Proc. Natl. Acad. Sci. USA 91:6808-6814.
29. Lewontin, R. C. 1970. The units of selection. Annu. Rev. Ecol. Syst. 1:1-18.
30. Lürling M., and E. Van Dank . 2000. Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? Oikos 88:111-118.
31. Marks, C., and M. Lechowicz . 2006. Alternative designs and the evolution of functional diversity. Am. Nat. 167:55-66.
32. Maynard Smith J., and E. Szathmáry . 1995. The major transitions in evolution. Oxford Univ. Press, NY.
33. Meyer, J. R., D. T. Dobias, J. S. Weitz, J. E. Barrick, R. T. Quick, and R. E. Lenski . 2012. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335:428-432.
34. Michod, R. E. 1997. Cooperation and conflict in the evolution of individuality. I. Multilevel selection of the organism. Am. Nat. 607-645.
35. Michod, R. E., and M. D. Herron . 2006. Cooperation and conflict during evolutionary transitions in individuality. J. Evol. Biol. 19:1406-1409.
36. Michod, R. E., and A. M. Nedelcu . 2003. On the reorganization of fitness during evolutionary transitions in individuality. Integr. Comp. Biol. 43:64-73.
37. Niklas, K. J., and H. C. Spatz . 2012. Plant physics. University of Chicago Press, Chicago.
38. Okasha, S. 2006. Evolution and the levels of selection. Oxford Univ. Press, Oxford, U.K.
39. Pfeiffer, T., and S. Bonhoeffer . 2003. An evolutionary scenario for the transition to undifferentiated multicellularity. Proc. Natl. Acad. Sci. USA 100:1095-1098.
40. Prochnik, S. E., J. Umen, A. M. Nedelcu, A. Hallmann, S. M. Miller, I. Nishii, P. Ferris, A. Kuo, T. Mitros, L. K. Fritz-Laylin, et al. 2010. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329:223-226.
41. Ratcliff, W. C., R. F. Denison, M. Borrello, and M. Travisano . 2012. Experimental evolution of multicellularity. Proc. Natl. Acad. Sci. USA 109:1595-1600.
42. Schaefer, S. A., and G. V. Lauder . 1996. Testing historical hypotheses of morphological change: biomechanical decoupling in loricarioid catfishes. Evolution 50:1661-1675.
43. Schluter, D. 2000. The ecology of adaptive radiation. Oxford Univ. Press, Oxford, U.K.
44. Shubin, N., C. Tabin, and S. Carroll . 1997. Fossils, genes and the evolution of animal limbs. Nature 388:639-648.
45. Simpson, G. G. 1953. The major features in evolution. Columbia Univ. Press, New York.
46. Smith, J. M., R. Burian, S. Kauffman, P. Alberch, J. Campbell, B. Goodwin, R. Lande, D. Raup, and L. Wolpert . 1985. Developmental constraints and evolution: a perspective from the mountain lake conference on development and evolution. Q. Rev. Biol. 60:265-287.
47. Smukalla, S., M. Caldara, N. Pochet, A. Beauvais, S. Guadagnini, C. Yan, M. D. Vinces, A. Jansen, M. C. Prevost, J. Latgé, et al. 2008. FLO1 Is a cariable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135:726-737.
48. Travisano, M., and R. E. Lenski . 1996. Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. Genetics 143:15-26.
49. Travisano, M., J. A. Mongold, A. F. Bennett, and R. E. Lenski . 1995. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267:87-90.
50. Velicer, G. J., L. Kroos, and R. E. Lenski . 2000. Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404:598-600.
51. Wentland, E. J., P. S. Stewart, C. Huang, and G. A. McFeters . 1996. Spatial variations in growth rate within Klebsiellapneumoniae colonies and biofilm. Biotechnol. Prog. 12:316-321.
52. West, G. B., J. H. Brown, and B. J. Enquist . 1999. The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284:1677-1679.
53. Willensdorfer, M. 2009. On the evolution of differentiated multicellularity. Evolution 63:306-323.
54. Woods, R., D. Schneider, C. L. Winkworth, M. A. Riley, and R. E. Lenski . 2006. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc. Natl. Acad. Sci. 103:9107-9112.
55. Yokota, K., and R. W. Sterner . 2011. Trade-offs limiting the evolution of coloniality: ecological displacement rates used to measure small costs. Proc. R. Soc. B: Biol. Sci. 278:458-463.