Recent speciation associated with the evolution of selfing in Capsella

The evolution from outcrossing to predominant self-fertilization represents one of the most common transitions in flowering plant evolution. This shift in mating system is almost universally associated with the “selfing syndrome,” characterized by marked reduction in flower size and a breakdown of the morphological and genetic mechanisms that prevent self-fertilization. In general, the timescale in which these transitions occur, and the evolutionary dynamics associated with the evolution of the selfing syndrome are poorly known. We investigated the origin and evolution of selfing in the annual plant Capsella rubella from its self-incompatible, outcrossing progenitor Capsella grandiflora by characterizing multilocus patterns of DNA sequence variation at nuclear genes. We estimate that the transition to selfing and subsequent geographic expansion have taken place during the past 20,000 years. This transition was probably associated with a shift from stable equilibrium toward a near-complete population bottleneck causing a major reduction in effective population size. The timing and severe founder event support the hypothesis that selfing was favored during colonization as new habitats emerged after the last glaciation and the expansion of agriculture. These results suggest that natural selection for reproductive assurance can lead to major morphological evolution and speciation on relatively short evolutionary timescales.

[1]  D. Weigel,et al.  Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck , 2009, Proceedings of the National Academy of Sciences.

[2]  D. Charlesworth,et al.  Patterns of Polymorphism and Demographic History in Natural Populations of Arabidopsis lyrata , 2008, PloS one.

[3]  S. Wright,et al.  Genomic Consequences of Outcrossing and Selfing in Plants , 2008, International Journal of Plant Sciences.

[4]  Brian J. Smith,et al.  boa: An R Package for MCMC Output Convergence Assessment and Posterior Inference , 2007 .

[5]  M. Przeworski,et al.  A new approach to estimate parameters of speciation models with application to apes. , 2007, Genome research.

[6]  Richard M. Clark,et al.  The Evolution of Selfing in Arabidopsis thaliana , 2007, Science.

[7]  D. Charlesworth,et al.  Testing for Effects of Recombination Rate on Nucleotide Diversity in Natural Populations of Arabidopsis lyrata , 2006, Genetics.

[8]  B. Neuffer,et al.  Evolution of the self-incompatibility system in the Brassicaceae: identification of S-locus receptor kinase (SRK) in self-incompatible Capsella grandiflora , 2006, Heredity.

[9]  D. Charlesworth Evolution of Plant Breeding Systems , 2006, Current Biology.

[10]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[11]  Ron Pinhasi,et al.  Tracing the Origin and Spread of Agriculture in Europe , 2005, PLoS biology.

[12]  M. Kiefer,et al.  Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species--Capsella rubella, Arabidopsis lyrata subsp. petraea, and A. thaliana. , 2005, American journal of botany.

[13]  B. Gaut,et al.  Molecular population genetics and the search for adaptive evolution in plants. , 2005, Molecular biology and evolution.

[14]  Xavier Messeguer,et al.  DnaSP, DNA polymorphism analyses by the coalescent and other methods , 2003, Bioinform..

[15]  Peter Donnelly,et al.  A comparison of bayesian methods for haplotype reconstruction from population genotype data. , 2003, American journal of human genetics.

[16]  S. Barrett Evolution of sex: The evolution of plant sexual diversity , 2002, Nature Reviews Genetics.

[17]  P. Fearnhead,et al.  A coalescent-based method for detecting and estimating recombination from gene sequences. , 2002, Genetics.

[18]  Richard R. Hudson,et al.  Generating samples under a Wright-Fisher neutral model of genetic variation , 2002, Bioinform..

[19]  R. Hudson Two-locus sampling distributions and their application. , 2001, Genetics.

[20]  D. Charlesworth,et al.  Breeding systems and genome evolution. , 2001, Current opinion in genetics & development.

[21]  P. Donnelly,et al.  A new statistical method for haplotype reconstruction from population data. , 2001, American journal of human genetics.

[22]  T. Mitchell-Olds,et al.  Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. , 2001, American journal of botany.

[23]  M. A. Koch,et al.  Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). , 2000, Molecular biology and evolution.

[24]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[25]  S. Barrett,et al.  BAKER'S LAW REVISITED: REPRODUCTIVE ASSURANCE IN A METAPOPULATION , 1998, Evolution; international journal of organic evolution.

[26]  T. Bataillon,et al.  How Does Self-Pollination Evolve? Inferences from Floral Ecology and Molecular Genetic Variation , 1996 .

[27]  L. C. Rutledge,et al.  Genetic Data Analysis , 1991 .

[28]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[29]  H. Hurka,et al.  Aspartate aminotransferase isozymes in the genusCapsella (Brassicaceae): Subcellular location, gene duplication, and polymorphism , 1989, Biochemical Genetics.

[30]  Graeme Barker,et al.  Prehistoric Farming In Europe , 1986 .

[31]  G. A. Watterson On the number of segregating sites in genetical models without recombination. , 1975, Theoretical population biology.

[32]  Charles Darwin,et al.  The Effects of Cross and Self Fertilisation in the Vegetable Kingdom , 1972 .

[33]  H. G. Baker,et al.  SELF‐COMPATIBILITY AND ESTABLISHMENT AFTER ‘“LONG‐DISTANCE” DISPERSAL , 1955 .

[34]  G. Ledyard Stebbins,et al.  Variation and Evolution in Plants , 1951 .

[35]  G. Ramstein,et al.  The Last Glacial Maximum climate over Europe and western Siberia: a PMIP comparison between models and data , 2001 .

[36]  K. Nicholas,et al.  GeneDoc: Analysis and visualization of genetic variation , 1997 .

[37]  Deborah Charlesworth,et al.  INBREEDING DEPRESSION AND ITS EVOLUTIONARY CONSEQUENCES , 1987 .

[38]  Rory A. Fisher,et al.  AVERAGE EXCESS AND AVERAGE EFFECT OF A GENE SUBSTITUTION , 1941 .

[39]  Newton E. Morton,et al.  The Neolithic Transition and the Genetics of Populations in Europe. , 2022 .