Sympatric Speciation: When Is It Possible in Bacteria?

According to theory, sympatric speciation in sexual eukaryotes is favored when relatively few loci in the genome are sufficient for reproductive isolation and adaptation to different niches. Here we show a similar result for clonally reproducing bacteria, but which comes about for different reasons. In simulated microbial populations, there is an evolutionary tradeoff between early and late stages of niche adaptation, which is resolved when relatively few loci are required for adaptation. At early stages, recombination accelerates adaptation to new niches (ecological speciation) by combining multiple adaptive alleles into a single genome. Later on, without assortative mating or other barriers to gene flow, recombination generates unfit intermediate genotypes and homogenizes incipient species. The solution to this tradeoff may be simply to reduce the number of loci required for speciation, or to reduce recombination between species over time. Both solutions appear to be relevant in natural microbial populations, allowing them to diverge into ecological species under similar constraints as sexual eukaryotes, despite differences in their life histories.

[1]  Jeremy Schmutz,et al.  Widespread Parallel Evolution in Sticklebacks by Repeated Fixation of Ectodysplasin Alleles , 2005, Science.

[2]  Omar E. Cornejo,et al.  The Population and Evolutionary Dynamics of Homologous Gene Recombination in Bacteria , 2009, PLoS genetics.

[3]  P. Nosil,et al.  Space, sympatry and speciation , 2009, Journal of evolutionary biology.

[4]  D. Schluter,et al.  Evidence for Ecological Speciation and Its Alternative , 2022 .

[5]  C. Fraser,et al.  Recombination and the Nature of Bacterial Speciation , 2007, Science.

[6]  F. Cohan,et al.  A Systematics for Discovering the Fundamental Units of Bacterial Diversity , 2007, Current Biology.

[7]  A. Darling,et al.  Patterns of Gene Flow Define Species of Thermophilic Archaea , 2012, PLoS biology.

[8]  C. Fraser,et al.  The Bacterial Species Challenge: Making Sense of Genetic and Ecological Diversity , 2009, Science.

[9]  T. Cooper Recombination Speeds Adaptation by Reducing Competition between Beneficial Mutations in Populations of Escherichia coli , 2007, PLoS biology.

[10]  Daniel Falush,et al.  Mismatch induced speciation in Salmonella: model and data , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  J. Lawrence,et al.  Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes. , 1999, Current opinion in genetics & development.

[12]  J. Mallet What does Drosophila genetics tell us about speciation? , 2006, Trends in ecology & evolution.

[13]  S. Via Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  E. Siggia,et al.  Analysis of Combinatorial cis-Regulation in Synthetic and Genomic Promoters , 2008, Nature.

[15]  F. C. Kafatos,et al.  SNP Genotyping Defines Complex Gene-Flow Boundaries Among African Malaria Vector Mosquitoes , 2010, Science.

[16]  Eric J Alm,et al.  Looking for Darwin's footprints in the microbial world. , 2009, Trends in microbiology.

[17]  M. Vos,et al.  A species concept for bacteria based on adaptive divergence. , 2011, Trends in microbiology.

[18]  S. Via,et al.  Sympatric speciation in animals: the ugly duckling grows up. , 2001, Trends in ecology & evolution.

[19]  Simon H. Martin,et al.  Butterfly genome reveals promiscuous exchange of mimicry adaptations among species , 2012, Nature.

[20]  Maureen L. Coleman,et al.  Ecosystem-specific selection pressures revealed through comparative population genomics , 2010, Proceedings of the National Academy of Sciences.

[21]  Lawrence A. David,et al.  Metapopulation structure of Vibrionaceae among coastal marine invertebrates. , 2011, Environmental microbiology.

[22]  D. Schluter,et al.  Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks , 2004, Nature.

[23]  Matthew W. Hahn,et al.  Genomic Islands of Speciation in Anopheles gambiae , 2005, PLoS biology.

[24]  A. Kondrashov Multilocus model of sympatric speciation. III. Computer simulations. , 1986, Theoretical population biology.

[25]  A. Kondrashov,et al.  Multidimensional epistasis and the disadvantage of sex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[26]  X. Didelot,et al.  A comparison of homologous recombination rates in bacteria and archaea , 2009, The ISME Journal.

[27]  N. Besansky,et al.  Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae , 2010, Molecular ecology.

[28]  Vincent J. Denef,et al.  Proteogenomic basis for ecological divergence of closely related bacteria in natural acidophilic microbial communities , 2010, Proceedings of the National Academy of Sciences.

[29]  Vincent J. Denef,et al.  AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature , 2010, The ISME Journal.

[30]  G. Bush,et al.  Sympatric speciation in animals: new wine in old bottles. , 1994, Trends in ecology & evolution.

[31]  A. Kondrashov Multilocus model of sympatric speciation. I: One character , 1983 .

[32]  Janice K. Wiedenbeck,et al.  Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. , 2011, FEMS microbiology reviews.

[33]  J. Felsenstein SKEPTICISM TOWARDS SANTA ROSALIA, OR WHY ARE THERE SO FEW KINDS OF ANIMALS? , 1981, Evolution; international journal of organic evolution.

[34]  Omar E. Cornejo,et al.  Polymorphic competence peptides do not restrict recombination in Streptococcus pneumoniae. , 2010, Molecular biology and evolution.

[35]  E. Ruby,et al.  A single regulatory gene is sufficient to alter bacterial host range , 2009, Nature.

[36]  Alexey S. Kondrashov,et al.  Sympatric speciation: when is it possible? , 1986 .

[37]  W. E. Ritter AS TO THE CAUSES OF EVOLUTION. , 1923, Science.

[38]  U. Dieckmann,et al.  On the origin of species by sympatric speciation , 1999, Nature.

[39]  A. Kondrashov Selection against harmful mutations in large sexual and asexual populations. , 1982, Genetical research.

[40]  P. Gerrish,et al.  Fitness Effects of Fixed Beneficial Mutations in Microbial Populations , 2002, Current Biology.

[41]  Wayne M. Getz,et al.  Genetic Exchange Across a Species Boundary in the Archaeal Genus Ferroplasma , 2007, Genetics.

[42]  H. Levine,et al.  Optimal Strategy for Competence Differentiation in Bacteria , 2010, PLoS genetics.

[43]  John W. Taylor,et al.  Geographic Barriers Isolate Endemic Populations of Hyperthermophilic Archaea , 2003, Science.

[44]  H. Rundle,et al.  Speciation in nature : the threespine stickleback model systems , 2002 .

[45]  James Mallet,et al.  Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[46]  J. Majewski,et al.  Sexual isolation in bacteria. , 2001, FEMS microbiology letters.

[47]  Otto X. Cordero,et al.  Population Genomics of Early Events in the Ecological Differentiation of Bacteria , 2012, Science.

[48]  F. C. Kafatos,et al.  Widespread Divergence Between Incipient Anopheles gambiae Species Revealed by Whole Genome Sequences , 2010, Science.

[49]  Fyodor A. Kondrashov,et al.  Interactions among quantitative traits in the course of sympatric speciation , 1999, Nature.

[50]  Alex A. Pollen,et al.  The genomic basis of adaptive evolution in threespine sticklebacks , 2012, Nature.