Abstract
Successive range expansions occur within all domains of life, where one population expands first (primary expansion) and one or more secondary populations then follow (secondary expansion). In general, genetic drift reduces diversity during range expansion. However, it is not clear whether the same effect applies during successive range expansion, mainly because the secondary population must expand into space occupied by the primary population. Here we used an experimental microbial model system to show that, in contrast to primary range expansion, successive range expansion promotes local population diversity. Because of mechanical constraints imposed by the presence of the primary population, the secondary population forms fractal-like dendritic structures. This divides the advancing secondary population into many small sub-populations and promotes intermixing between the primary and secondary populations. We further developed a mathematical model to simulate the formation of dendritic structures in the secondary population during succession. By introducing mutations in the primary or dendritic secondary populations, we found that mutations are more likely to accumulate in the dendritic secondary populations. Our results thus show that successive range expansion can promote intermixing over the short term and increase genetic diversity over the long term. Our results therefore have potentially important implications for predicting the ecological processes and evolutionary trajectories of microbial communities.
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References
Anderson AR, Quaranta V . (2008). Integrative mathematical oncology. Nat Rev Cancer 8: 227–234.
Ben-Jacob E, Schochet O, Tenenbaum A, Cohen I, Czirók A, Vicsek T . (1994). Generic modelling of cooperative growth patterns in bacterial colonies. Nature 368: 46–49.
Ben-Jacob E, Cohen I, Levine H . (2000). Cooperative self-organization of microorganisms. Adv Phys 49: 37–41.
Cavalli-Sforza LL, Menozzi P, Piazza A . (1993). Demic expansions and human evolution. Science 259: 639–646.
Connell JH, Slatyer RO . (1977). Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111: 1119–1144.
Dale MRT . (1999) Spatial Pattern Analysis in Plant Ecology. Cambridge University Press: Cambridge, UK.
Elena SF, Lenski RE . (2003). Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4: 457–469.
Excoffier L, Foll M, Petit RJ . (2009). Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40: 481–501.
Excoffier L, Ray N . (2008). Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23: 347–351.
Ferreira SC, Martins ML, Vilela MJ . (2002). Reaction–diffusion model for the growth of avascular tumor. Phys Rev E 65: 21907.
Fierer N, Nemergut D, Knight R, Craine JM . (2010). Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161: 635–642.
Fujikawa H, Matsushita M . (1989). Fractal growth of Bacillus subtilis on agar plates. J Phys Soc Japan 58: 3875–3878.
Golding I, Kozlovsky Y, Cohen I, Ben-Jacob E . (1998). Studies of bacterial branching growth using reaction–diffusion models for colonial development. Phys A 260: 510–554.
Hallatschek O, Hersen P, Ramanathan S, Nelson DR . (2007). Genetic drift at expanding frontiers promotes gene segregation. Proc Natl Acad Sci USA 104: 19926–19930.
Henrichsen J . (1972). Bacterial surface translocation: a survey and a classification. Bacteriol Rev 36: 478–503.
Hewitt G . (2000). The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.
Kawasaki K, Mochizuki A, Matsushita M, Umeda T, Shigesada N . (1997). Modeling spatio-temporal patterns generated by Bacillus subtilis. J Theor Biol 188: 177–185.
Kolenbrander PE, Palmer RJ, Periasamy S, Jakubovics NS . (2010). Oral multispecies biofilm development and the key role of cell–cell distance. Nat Rev Microbiol 8: 471–480.
Lalucat J, Bennasar A, Bosch R, García-Valdés E, Palleroni NJ . (2006). Biology of Pseudomonas stutzeri. Microbiol Mol Biol Rev 70: 510–547.
Lilja EE, Johnson DR . (2016). Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates. ISME J 10: 1568–1578.
Lilja EE, Johnson DR . (2017). Metabolite toxicity determines the pace of molecular evolution within microbial populations. BMC Evol Biol 17: 52.
Mather W, Mondragón-Palomino O, Danino T, Hasty J, Tsimring LS . (2010). Streaming instability in growing cell populations. Phys Rev Lett 104: 208101.
Mathiesen J, Procaccia I, Swinney HL, Thrasher M . (2006). The universality class of diffusion-limited aggregation and viscous fingering. Europhys Lett 76: 257–263.
May SE, Maher JV . (1989). Fractal dimension of radial fingering patterns. Phys Rev A 40: 1723–1726.
Mimura M, Sakaguchi H, Matsushita M . (2000). Reaction–diffusion modelling of bacterial colony patterns. Phys A 282: 283–303.
Mitri S, Clarke E, Foster KR . (2016). Resource limitation drives spatial organization in microbial groups. ISME J 10: 1471–1482.
Momeni B, Brileya KA, Fields MW, Shou W . (2013). Strong inter-population cooperation leads to partner intermixing in microbial communities. Elife 2: e00230.
Niehus R, Mitri S, Fletcher AG, Foster KR . (2015). Migration and horizontal gene transfer divide microbial genomes into multiple niches. Nature Commun 6: 8924.
Nittmann J, Stanley HE . (1986). Tip splitting without interfacial tension and dendritic growth patterns arising from molecular anisotropy. Nature 321: 663–668.
Pielou EC . (1966). Species-diversity and pattern-diversity in the study of ecological succession. J Theor Biol 10: 370–383.
Reich D, Patterson N, Campbell D, Tandon A, Mazieres S, Ray N et al. (2012). Reconstructing Native American population history. Nature 488: 370–374.
Rickard AH, Gilbert P, High NJ, Kolenbrander PE, Handley PS . (2003). Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol 11: 94–100.
Rudge T, Federici F, Steiner PJ, Haseloff J . (2013). Cell polarity-driven instability generates self-organized, fractal patterning of cell layers. ACS Synthetic Biol 2: 705–714.
Sokal RR, Oden NL, Wilson C . (1991). Genetic evidence for the spread of agriculture in Europe by demic diffusion. Nature 351: 143–145.
Sørensen SJ, Bailey M, Hansen LH, Kroer N, Wuertz S . (2005). Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol 3: 700–710.
Tilman D, Kareiva PM . (1997) Spatial Ecology: The Role of Space in Population Dynamics and Interspecific Interactions. Princeton University Press: Princeton, NJ.
van de Koppel J, Gupta R, Vuik C . (2011). Scaling-up spatially-explicit ecological models using graphics processors. Ecol Modell 222: 3011–3019.
Volfson D, Cookson S, Hasty J, Tsimring LS . (2008). Biomechanical ordering of dense cell populations. Proc Natl Acad Sci USA 105: 15346–15351.
Zumft WG . (1997). Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61: 533–616.
Acknowledgements
We thank Fordyce A. Davidson for valuable insights and suggestions on how to design the non-linear diffusion term of the microbial populations in the model; Lara Pfister, Selina Derksen-Müller and Anja Bernet for help with the strain construction; Lea Caduff for help with the microscopy; and Martin Ackermann and Will Macnair for helpful discussions and comments on early versions of the manuscript. We also thank two anonymous reviewers for significantly improving the quality and clarity of this manuscript. This work was supported by grants from the Swiss National Science Foundation (31003A_149304) and SystemsX.ch, The Swiss Initiative in Systems Biology (MicroScapesX.ch).
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Goldschmidt, F., Regoes, R. & Johnson, D. Successive range expansion promotes diversity and accelerates evolution in spatially structured microbial populations. ISME J 11, 2112–2123 (2017). https://doi.org/10.1038/ismej.2017.76
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DOI: https://doi.org/10.1038/ismej.2017.76
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