Evolution in Action pp 119-135 | Cite as
Population Genetics of Speciation and Demographic Inference Under Population Subdivision: Insights from Studies on Wild Tomatoes (Solanum sect. Lycopersicon)
Abstract
Multilocus sequencing studies assessing patterns of nucleotide polymorphism within and among closely related species provide valuable insights into the evolutionary processes involved in species divergence. We have employed the analytical framework of divergence population genetics in testing models of speciation in two species of wild tomatoes (clade Lycopersicon). However, all current implementations of divergence models assume panmixia within ancestral and extant species which introduces biases of potentially large magnitude, depending on the sampling scheme employed in empirical studies. Moreover, our coalescent simulations of samples from subdivided expanding populations confirm that, except at very high migration rates, sampling local populations is not equivalent to sampling from panmictic populations, with implications for studies spanning the range from Drosophila to humans. Within the constraints imposed by the complexities of the coalescent process in subdivided populations that are not accounted for in current divergence models, we found evidence for recent speciation (≤0.55 million years) of the two wild tomato species, which based on patterns of linkage disequilibrium has occurred under residual gene flow.
Keywords
Population Subdivision Divergence Population Genetic Panmictic Population Wild Tomato Coalescent SimulationNotes
Acknowledgments
We thank our past and present graduate students and technicians for their invaluable contributions to these studies: U. Arunyawat, G. Feldmaier-Fuchs, H. Lainer, T. Marczewski, C. Merino, and K. Roselius. The coalescent analyses benefitted from contributions by B. Haubold, S. Mousset, P. Pfaffelhuber, and A. Tellier. Our field work in Peru was greatly facilitated by administrative and logistical support from A. Cano and G. Clostre; permits to sample and export leaf material to Germany were granted by the Peruvian Instituto Nacional de Recursos Naturales (INRENA). Finally, we are grateful to the generous research funding from the Deutsche Forschungsgemeinschaft throughout the duration of the SPP-1127 “Radiations – Origins of Biological Diversity” (grants Ste 325/5-1 to 325-3).
References
- Arnold ML (2006) Evolution through genetic exchange. Oxford University Press, New YorkGoogle Scholar
- Arunyawat U, Stephan W, Städler T (2007) Using multilocus sequence data to assess population structure, natural selection and linkage disequilibrium in wild tomatoes. Mol Biol Evol 24:2310–2322PubMedCrossRefGoogle Scholar
- Baudry E, Kerdelhué C, Innan H, Stephan W (2001) Species and recombination effects on DNA variability in the tomato genus. Genetics 158:1725–1735PubMedGoogle Scholar
- Becquet C, Przeworski M (2007) A new approach to estimate parameters of speciation models with application to apes. Genome Res 17:1505–1519PubMedCrossRefGoogle Scholar
- Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, MAGoogle Scholar
- De A, Durrett R (2007) Stepping-stone spatial structure causes slow decay of linkage disequilibrium and shifts the site frequency spectrum. Genetics 176:969–981PubMedCrossRefGoogle Scholar
- Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton, NJGoogle Scholar
- Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864PubMedCrossRefGoogle Scholar
- Foxe JP, Slotte T, Stahl EA, Neuffer B, Hurka H, Wright SI (2009) Recent speciation associated with the evolution of selfing in Capsella. Proc Natl Acad Sci USA 106:5241–5245PubMedCrossRefGoogle Scholar
- Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedGoogle Scholar
- Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760PubMedCrossRefGoogle Scholar
- Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790PubMedCrossRefGoogle Scholar
- Hudson RR (2002) Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18:337–338PubMedCrossRefGoogle Scholar
- Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945–953PubMedCrossRefGoogle Scholar
- Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026PubMedCrossRefGoogle Scholar
- Kliman RM, Andolfatto P, Coyne JA, Depaulis F, Kreitman M et al (2000) The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156:1913–1931PubMedGoogle Scholar
- Machado CA, Kliman RM, Markert JA, Hey J (2002) Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives. Mol Biol Evol 19:472–488PubMedCrossRefGoogle Scholar
- Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237PubMedCrossRefGoogle Scholar
- Moeller DA, Tenaillon MI, Tiffin P (2007) Population structure and its effects on patterns of nucleotide polymorphism in teosinte (Zea mays ssp. parviglumis). Genetics 176:1799–1809PubMedCrossRefGoogle Scholar
- Moyle LC (2008) Ecological and evolutionary genomics in the wild tomatoes (Solanum sect. Lycopersicon). Evolution 62:2995–3013PubMedCrossRefGoogle Scholar
- Nakazato T, Bogonovich M, Moyle LC (2008) Environmental factors predict adaptive phenotypic differentiation within and between two wild Andean tomatoes. Evolution 62:774–792PubMedCrossRefGoogle Scholar
- Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896PubMedGoogle Scholar
- Pannell JR (2003) Coalescence in a metapopulation with recurrent local extinction and recolonization. Evolution 57:949–961PubMedGoogle Scholar
- Peralta IE, Spooner DM, Knapp S (2008) Taxonomy of wild tomatoes and their relatives (Solanum sect. Lycopersicoides, sect. Juglandifolia, sect. Lycopersicon; Solanaceae). Syst Bot Monogr 84:1–186Google Scholar
- Pool JE, Aquadro CF (2006) History and structure of sub-Saharan populations of Drosophila melanogaster. Genetics 174:915–929PubMedCrossRefGoogle Scholar
- Ptak SE, Przeworski M (2002) Evidence for population growth in humans is confounded by fine-scale population structure. Trends Genet 18:559–563PubMedCrossRefGoogle Scholar
- Ramos-Onsins SE, Stranger BE, Mitchell-Olds T, Aguadé M (2004) Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166:373–388PubMedCrossRefGoogle Scholar
- Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86PubMedCrossRefGoogle Scholar
- Rice WR, Hostert EE (1993) Laboratory experiments on speciation: what have we learned in forty years? Evolution 47:1637–1653CrossRefGoogle Scholar
- Rick CM (1979) Biosystematic studies in Lycopersicon and closely related species of Solanum. In: Hawkes JG, Lester RN, Skelding AD (eds) The biology and taxonomy of the Solanaceae. Academic, New York, pp 667–678Google Scholar
- Rick CM (1986) Reproductive isolation in the Lycopersicon peruvianum complex. In: D’Arcy WG (ed) Solanaceae – biology and systematics. Columbia University Press, New York, pp 477–495Google Scholar
- Rick CM, Lamm R (1955) Biosystematic studies on the status of Lycopersicon chilense. Am J Bot 42:663–675CrossRefGoogle Scholar
- Roselius K, Stephan W, Städler T (2005) The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics 171:753–763PubMedCrossRefGoogle Scholar
- Ross-Ibarra J, Wright SI, Foxe JP, Kawabe A, DeRose-Wilson L, Gos G, Charlesworth D, Gaut BS (2008) Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata. PLoS ONE 3:e2411PubMedCrossRefGoogle Scholar
- Ross-Ibarra J, Tenaillon M, Gaut BS (2009) Historical divergence and gene flow in the genus Zea. Genetics 181:1399–1413PubMedCrossRefGoogle Scholar
- Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207PubMedCrossRefGoogle Scholar
- Slotte T, Huang H, Lascoux M, Ceplitis A (2008) Polyploid speciation did not confer instant reproductive isolation in Capsella (Brassicaceae). Mol Biol Evol 25:1472–1481PubMedCrossRefGoogle Scholar
- Spooner DM, Peralta IE, Knapp S (2005) Comparison of AFLPs with other markers for phylogenetic inference in wild tomatoes [Solanum L. section Lycopersicon (Mill.) Wettst.]. Taxon 54:43–61CrossRefGoogle Scholar
- Städler T, Roselius K, Stephan W (2005) Genealogical footprints of speciation processes in wild tomatoes: demography and evidence for historical gene flow. Evolution 59:1268–1279PubMedGoogle Scholar
- Städler T, Arunyawat U, Stephan W (2008) Population genetics of speciation in two closely related wild tomatoes (Solanum section Lycopersicon). Genetics 178:339–350PubMedCrossRefGoogle Scholar
- Städler T, Haubold B, Merino C, Stephan W, Pfaffelhuber P (2009) The impact of sampling schemes on the site frequency spectrum in nonequilibrium subdivided populations. Genetics 182:205–216PubMedCrossRefGoogle Scholar
- Stephan W, Langley CH (1998) DNA polymorphism in Lycopersicon and crossing-over per physical length. Genetics 150:1585–1593PubMedGoogle Scholar
- Strasburg JL, Rieseberg LH (2008) Molecular demographic history of the annual sunflowers Helianthus annuus and H. petiolaris – large effective population sizes and rates of long-term gene flow. Evolution 62:1936–1950PubMedCrossRefGoogle Scholar
- Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
- Turelli M, Barton NH, Coyne JA (2001) Theory and speciation. Trends Ecol Evol 16:330–343PubMedCrossRefGoogle Scholar
- Wakeley J (1999) Nonequilibrium migration in human history. Genetics 153:1863–1871PubMedGoogle Scholar
- Wakeley J (2000) The effects of subdivision on the genetic divergence of populations and species. Evolution 54:1092–1101PubMedGoogle Scholar
- Wakeley J (2001) The coalescent in an island model of population subdivision with variation among demes. Theor Popul Biol 59:133–144PubMedCrossRefGoogle Scholar
- Wakeley J, Aliacar N (2001) Gene genealogies in a metapopulation. Genetics 159:893–905PubMedGoogle Scholar
- Wakeley J, Hey J (1997) Estimating ancestral population parameters. Genetics 145:847–855PubMedGoogle Scholar
- Wang RL, Wakeley J, Hey J (1997) Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics 147:1091–1106PubMedGoogle Scholar
- Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276PubMedCrossRefGoogle Scholar
- Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22:506–519PubMedCrossRefGoogle Scholar
- Zhang L-B, Ge S (2007) Multilocus analysis of nucleotide variation and speciation in Oryza officinalis and its close relatives. Mol Biol Evol 24:769–783PubMedCrossRefGoogle Scholar