Adaptive Divergence in Sunflowers

Jared L Strasburg, Indiana University, Bloomington, Indiana, USA

Published online: October 2010

DOI: 10.1002/9780470015902.a0022900

Annual sunflowers have been developed into a model system for the study of adaptation, hybridisation and speciation. Various species and populations have adapted to a wide range of extreme habitats, including salt marshes, sand dunes, desert floor and agricultural environments. In many cases, the process of adaptation has been facilitated by hybridisation between distinct species. Population genetic analyses of several species have revealed evidence of natural selection at loci potentially associated with adaptation to different environments, and genomic analyses indicate that the signature of adaptive divergence is found throughout the genomes of these species. In some cases, the genetic architecture of reproductive isolation and species differences may facilitate adaptive introgression and the formation of new hybrid species through adaptive ecological divergence.

Key Concepts:

  • Hybridisation has played an important role in adaptation in sunflowers, both through adaptive introgression and through the formation of adaptively divergent hybrid species.
  • Evidence for adaptive divergence in sunflowers comes from a number of sources, including field experiments, genetic mapping of adaptive traits and DNA sequence analyses.
  • The early morphological and ecological divergence of hybrid species can be experimentally replicated under environmental conditions similar to those encountered by the hybrid species in nature, providing strong evidence that it is adaptive.
  • Data from a number of sunflower species support the hypothesis that adaptive divergence is associated with large population size.

Keywords: sunflowers; Helianthus; hybridisation; homoploid hybrid speciation; adaptation; adaptive divergence; chromosomal rearrangements; positive selection; selective sweeps

Figure 1. Map showing the ranges of most of the annual sunflower species discussed here. Figure adapted from Strasburg et al. (2009), with permission from Oxford University Press.
Figure 2. Schematic of recombinational speciation. Vertical lines represent pairs of homologous chromosomes. In this case, the parental species differ by two reciprocal translocations.
Figure 3. The three homoploid hybrid sunflower species. Photos from Jason Rick and Mark Welch, used with permission.
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 References
    book Anderson E (1949) Introgressive Hybridization. New York: Wiley.
    Anderson E and Stebbins GL Jr (1954) Hybridization as an evolutionary stimulus. Evolution 8: 378–388.
    book Arnold ML (2006) Evolution Through Genetic Exchange. Oxford: Oxford University Press.
    Barton NH and Keightley PD (2002) Understanding quantitative genetic variation. Nature Reviews. Genetics 3: 11–21.
    Burke JM, Lai Z, Salmaso M et al. (2004) Comparative mapping and rapid karyotypic evolution in the genus Helianthus. Genetics 167: 449–457.
    deVicente MC and Tanksley SD (1993) QTL analysis of transgressive segregation in an interspecific tomato cross. Genetics 134: 585–596.
    Donovan LA, Rosenthal DR, Sanchez-Velenosi M, Rieseberg LH and Ludwig F (2010) Are hybrid species more fit than ancestral parent species in the current hybrid species habitats? Journal of Evolutionary Biology 23: 805–816.
    Edelist C, Lexer C, Dillmann C, Sicard D and Rieseberg LH (2006) Microsatellite signature of ecological selection for salt tolerance in a wild sunflower hybrid species, Helianthus paradoxus. Molecular Ecology 15: 4623–4634.
    Eyre-Walker A and Keightley PD (2009) Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Molecular Biology and Evolution 26: 2097–2108.
    Gossmann T, Song B-H, Windsor A et al. (2010) Genome wide analyses reveal little evidence for adaptive evolution in plants. Molecular Biology and Evolution 27: 1822–1832.
    book Grant V (1981) Plant Speciation. New York: Columbia University Press.
    Gross BL, Kane NC, Lexer C et al. (2004) Reconstructing the origin of Helianthus deserticola: survival and selection on the desert floor. American Naturalist 164: 145–156.
    Gross BL and Rieseberg LH (2005) The ecological genetics of homoploid hybrid speciation. Journal of Heredity 96: 241–252.
    Gross BL, Schwarzbach AE and Rieseberg LH (2003) Origin(s) of the diploid hybrid species Helianthus deserticola (Asteraceae). American Journal of Botany 90: 1708–1719.
    Gross BL, Turner KG and Rieseberg LH (2007) Selective sweeps in the homoploid hybrid species Helianthus deserticola: evolution in concert across populations and across origins. Molecular Ecology 16: 5246–5258.
    Heiser CB (1947) Hybridization between the sunflower species Helianthus annuus and H. petiolaris. Evolution 1: 249–262.
    Heiser CB (1951a) Hybridization in the annual sunflowers: Helianthus annuus x H. argophyllus. American Naturalist 85: 65–72.
    Heiser CB (1951b) Hybridization in the annual sunflowers: Helianthus annuus x H. debilis var. cucumerifolius. Evolution 5: 42–51.
    Heiser CB (1954) Variation and subspeciation in the common sunflower, Helianthus annuus. American Midland Naturalist 51: 287–305.
    Heiser CB (1958) Three new annual sunflowers (Helianthus) from the southwestern United States. Rhodora 60: 272–283.
    Heiser CB, Smith DM, Clevenger S and Martin WC (1969) The North American sunflowers (Helianthus). Memoirs of the Torrey Botanical Club 22: 1–218.
    Kane NC and Rieseberg LH (2007) Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus. Genetics 175: 1823–1834.
    Kane NC and Rieseberg LH (2008) Genetics and evolution of weedy Helianthus annuus populations: adaptation of an agricultural weed. Molecular Ecology 17: 384–394.
    Karrenberg S, Lexer C and Rieseberg LH (2007) Reconstructing the history of selection during homoploid hybrid speciation. American Naturalist 169: 725–737.
    Kim SC and Rieseberg LH (1999) Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153: 965–977.
    Lai Z, Nakazato T, Salmaso M et al. (2005) Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171: 291–303.
    Lexer C, Lai Z and Rieseberg LH (2004) Candidate gene polymorphisms associated with salt tolerance in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. New Phytologist 161: 225–233.
    Lexer C, Rosenthal DM, Raymond O, Donovan LA and Rieseberg LH (2005) Genetics of species differences in the wild annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 169: 2225–2239.
    Lexer C, Welch ME, Durphy JL and Rieseberg LH (2003a) Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. Molecular Ecology 12: 1225–1235.
    Lexer C, Welch ME, Raymond O and Rieseberg LH (2003b) The origin of ecological divergence in Helianthus paradoxus (Asteraceae): selection on transgressive characters in a novel hybrid habitat. Evolution 57: 1989–2000.
    Ludwig F, Rosenthal DM, Johnston JA et al. (2004) Selection on leaf ecophysiological traits in a desert hybrid Helianthus species and early generation hybrids. Evolution 58: 2682–2692.
    book Mayr E (1963) Animal Species and Evolution. Cambridge, MA: Belknap Press of Harvard University Press.
    McDonald JH and Kreitman M (1991) Adaptive protein evolution at the ADH locus in Drosophila. Nature 351: 652–654.
    Nielsen R (2005) Molecular signatures of natural selection. Annual Review of Genetics 39: 197–218.
    Orr HA (1998) Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics 149: 2099–2104.
    Rieseberg LH (1997) Hybrid origins of plant species. Annual Review of Ecology and Systematics 28: 359–389.
    Rieseberg LH, Archer MA and Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83: 363–372.
    Rieseberg LH, Raymond O, Rosenthal DM et al. (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301: 1211–1216.
    book Rose MR and Lauder GV (1996) Adaptation. San Diego: Academic Press.
    Rosenthal DM, Schwarzbach AE, Donovan LA, Raymond O and Rieseberg LH (2002) Phenotypic differentiation between three ancient hybrid taxa and their parental species. International Journal of Plant Sciences 163: 387–398.
    Sapir Y, Moody ML, Brouillette LC, Donovan LA and Rieseberg LH (2007) Patterns of genetic diversity and candidate genes for ecological divergence in a homoploid hybrid sunflower, Helianthus anomalus. Molecular Ecology 16: 5017–5029.
    Scascitelli M, Whitney KD, Randell RA et al. (2010) Genome scan of hybridizing sunflowers from Texas (Helianthus annuus and H. debilis) reveals asymmetric patterns of introgression and small islands of genomic differentiation. Molecular Ecology 19: 521–541.
    Schlotterer C (2002) A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics 160: 753–763.
    Schwarzbach AE and Rieseberg LH (2002) Likely multiple origins of a diploid hybrid sunflower species. Molecular Ecology 11: 1703–1715.
    Soltis DE and Soltis PS (1993) Molecular data and the dynamic nature of polyploidy. Critical Reviews in Plant Sciences 12: 243–273.
    Strasburg JL, Kane NC, Raduski AR and Rieseberg LH (in press) Effective population size is positively correlated with levels of adaptive divergence among annual sunflowers. Molecular Biology and Evolution.
    Strasburg JL, Scotti-Saintagne C, Scotti I, Lai Z and Rieseberg LH (2009) Genomic patterns of adaptive divergence between chromosomally differentiated sunflower species. Molecular Biology and Evolution 26: 1341–1355.
    Templeton AR (1981) Mechanisms of speciation – a population genetic approach. Annual Review of Ecology and Systematics 12: 23–48.
    Welch ME and Rieseberg LH (2002) Patterns of genetic variation suggest a single, ancient origin for the diploid hybrid species Helianthus paradoxus. Evolution 56: 2126–2137.
    Whitney KD, Randell RA and Rieseberg LH (2006) Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. American Naturalist 167: 794–807.
 Further Reading
    Eyre-Walker A (2006) The genomic rate of adaptive evolution. Trends in Ecology & Evolution 21: 569–575.
    book Heiser CB (1976) The Sunflower. Norman: University of Oklahoma Press.
    McKay JK and Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends in Ecology & Evolution 17: 285–291.
    book Nurminsky D (2005) Selective Sweep. Landes Bioscience/Eurekah.com Georgetown, TX: Kluwer Academic/Plenum Publishers.
    Rieseberg LH, Kim SC, Randell RA et al. (2007) Hybridization and the colonization of novel habitats by annual sunflowers. Genetica 129: 149–165.
    Rieseberg LH, Widmer A, Arntz AM and Burke JM (2002) Directional selection is the primary cause of phenotypic diversification. Proceedings of the National Academy of Sciences of the USA 99: 12242–12245.
    book Rogers CE, Thompson TE and Seiler GJ (1982) Sunflower Species of the United States. Bismarck, ND: National Sunflower Association.
    Strasburg JL and 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: 1936–1950.

Related Sub-Topics:

Adaptive Evolution | Evolution of Species | Evolutionary Ecology | Plant Evolution
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Article Title: Adaptive Divergence in Sunflowers
 
How to Cite close
Strasburg, Jared L(Oct 2010) Adaptive Divergence in Sunflowers. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022900]