On the Evolutionary Modification of Self-Incompatibility: Implications of Partial Clonality for Allelic Diversity and Genealogical Structure

  • M. Vallejo-Marín
  • M. K. Uyenoyama


Experimental investigations of homomorphic self-incompatibility (SI) have revealed an unanticipated level of complexity in its expression, permitting fine regulation over the course of a lifetime or a range of environmental conditions. Many flowering plants express some level of clonal reproduction, and phylogenetic analyses suggest that clonality evolves in a correlated fashion with SI in Solanum (Solanaceae). Here, we use a diffusion approximation to explore the effects on the evolutionary dynamics of SI of vegetative propagation with SI restricted to reproduction through seed. While clonality reduces the strength of frequency-dependent selection maintaining S-allele diversity, much of the great depth typical of S-allele genealogies is preserved. Our results suggest that clonality can play an important role in the evolution of SI systems, and may afford insight into unexplained features of allele genealogies in the Solanaceae.


Effective Population Size Diffusion Approximation Clonal Reproduction Much Recent Common Ancestor Correlate Evolution 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anderson MA, Cornish EC, Mau SL, Williams EG, Hoggart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penschow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE (1986) Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Nature 321:38-44CrossRefGoogle Scholar
  2. Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:347-349CrossRefGoogle Scholar
  3. Baker HG (1967) Support for Baker’s Law - as a rule. Evolution 21:853-856CrossRefGoogle Scholar
  4. Baker HG, Cox PA (1984) Further thoughts on dioecism and islands. Ann Mo Bot Gard 71:244-253CrossRefGoogle Scholar
  5. Barrett S (1988). The evolution, maintenance, and loss of self-incompatibility systems. In: Lovett Doust J, Lovett Doust L (eds) Plant reproductive ecology: Patterns and strategies. Oxford University Press, Oxford, pp 98-124Google Scholar
  6. Charlesworth D, Charlesworth B (1979) The evolution and breakdown of S-allele systems. Heredity 43:41-55CrossRefGoogle Scholar
  7. Charpentier A (2002) Consequences of clonal growth for plant mating. Evol Ecol 15:521-530CrossRefGoogle Scholar
  8. Dwyer KG, Balent MA, Nasrallah JB, Nasrallah ME (1991) DNA sequences of self-incompatibility genes from Brassica campestris and B. oleracea: Polymorphism predating speciation. Plant Mol Biol 16:481-486CrossRefPubMedGoogle Scholar
  9. Ferrer MM, Good-Ávila SV (2007) Macrophylogenetic analyses of the gain and loss of self-incompatibility in the Asteraceae. New Phytol 173:401-414CrossRefPubMedGoogle Scholar
  10. Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Oxford University Press, Dover, New YorkGoogle Scholar
  11. Good-Ávila SV, Stephenson AG (2002) The inheritance of modifiers conferring self-fertility in the partially self-incompatible perennial, Campanula rapunculoides L. (Campanulaceae). Evolution 56:263-272PubMedGoogle Scholar
  12. Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: Occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Evol Syst 36:47-79CrossRefGoogle Scholar
  13. Groenendale JMv, Klimes L, Klimesova J, Hendriks RJJ (1996) Comparative ecology of clonal plants. Philos Trans R Soc Lond B 351:1331-1339CrossRefGoogle Scholar
  14. Honnay O, Jacquemyn H (2008) Mating system evolution under strong clonality: towards self-compatibility or self-incompatibility? Evol Ecol DOI 10.1007/s10682-007-9207-3Google Scholar
  15. Igic B, Bohs L, Kohn JR (2006) Ancient polymorphism reveals unidirectional breeding system shifts. Proc Natl Acad Sci USA 103:1359-1363CrossRefPubMedGoogle Scholar
  16. Ioerger TR, Clark AG, Kao Th (1990) Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Natl Acad Sci USA 87:9732-9735CrossRefPubMedGoogle Scholar
  17. Karlin S, Taylor HM (1981) A second course in stochastic processes. Academic, New YorkGoogle Scholar
  18. Koch MA, Kiefer M (2005) Genome evolution among cruciferous plants: A lecture from the com-parison of the genetic maps of three diploid species - Capsella rubella, Arabidopsis lyrata subsp. petraea, and A. thaliana. Am J Bot 92:761-767CrossRefGoogle Scholar
  19. Koch MA, Haubold B, Mitchell-Olds T (2001) Molecular systematics of the Brassicaceae: Evidence from coding plastidic matK and nuclear Chs sequences. Am J Bot 88:534-544CrossRefPubMedGoogle Scholar
  20. Kusaba M, Dwyer K, Hendershot J, Vrebalov J, Nasrallah JB, Nasrallah ME (2001) Self-incompatibility in the genus Arabidopsis: Characterization of the S-locus in the outcrossing A. lyrata and its autogamous relative A. thaliana. Plant Cell 13:627-643CrossRefPubMedGoogle Scholar
  21. Lawrence MJ (2000) Population genetics of the homomorphic self-incompatibility polymorphisms in flowering plants. Ann Bot (Lond) 85( Suppl. A):221-226CrossRefGoogle Scholar
  22. Levin DA (1996) The evolutionary significance of pseudo-self-fertility. Am Nat 148:321-332CrossRefGoogle Scholar
  23. Liu P, Sherman-Broyles S, Nasrallah ME, Nasrallah JB (2007) A cryptic modifier causing transient self-incompatibility in Arabidopsis thaliana. Curr Biol 17:734-740CrossRefPubMedGoogle Scholar
  24. Mena-Alí JI, Stephenson AG (2007) Segregation analyses of partial self-incompatibility in self and cross progeny of Solanum carolinense reveal a leaky s-allele. Genetics 177:501-510CrossRefPubMedGoogle Scholar
  25. Nasrallah JB, Kao Th, Goldberg ML, Nasrallah ME (1985) A cDNA clone encoding an S-locus-specific glycoprotein from Brassica oleracea. Nature 318:263-267CrossRefGoogle Scholar
  26. Nasrallah ME, Liu P, Sherman-Broyles S, Nasrallah JB (2004) Natural variation in expression of self-incompatibility in Arabidopsis thaliana: Implications for the evolution of selfing. Proc Natl Acad Sci USA 101:16070-16074CrossRefPubMedGoogle Scholar
  27. Neuhauser C (1999) The ancestral graph and gene genealogy under frequency-dependent selection. Theor Popul Biol 56:203-214CrossRefPubMedGoogle Scholar
  28. Newbigin E, Uyenoyama MK (2005) The evolutionary dynamics of self-incompatibility systems. Trends Genet 21:500-505CrossRefPubMedGoogle Scholar
  29. Pagel M, Meade A (2006) Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am Nat 167:808-825CrossRefGoogle Scholar
  30. Pagel MD (1994) Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Philos Trans R Soc Lond B 255:37-45Google Scholar
  31. Pannell JR, Barrett SCH (1998) Baker’s law revisited: Reproductive assurance in a metapopulation. Evolution 52:657-668CrossRefGoogle Scholar
  32. Richards AJ (1986) Plant breeding systems. George Allen & Unwin, LondonGoogle Scholar
  33. Richman AD, Kohn JR (1999) Self-incompatibility alleles from Physalis: Implications for histori-cal inference from balanced genetic polymorphisms. Proc Natl Acad Sci USA 96:168-172CrossRefPubMedGoogle Scholar
  34. Sherman-Broyles S, Boggs N, Farkas A, Liu P, Vrebalov J, Nasrallah ME , Nasrallah JB (2007) S-locus genes and the evolution of self-fertility in Arabidopsis thaliana. Plant Cell 19:94-106CrossRefPubMedGoogle Scholar
  35. Shimizu KK, Cork JM, Caicedo AL, Mays CA, Moore RC, Olsen KM, Ruzsa S, Coop G, Busta-mante CD, Awadalla P, Purugganan MD (2004) Darwinian selection on a selfing locus. Science 306:2081-2084CrossRefPubMedGoogle Scholar
  36. Shimizu KK, Shimizu-Inatsugi R, Tsuchimatsu T, Purugganan MD (2008) Independent origins of self-compatibility in Arabidopsis thaliana. Mol Ecol 17:704-714PubMedGoogle Scholar
  37. Stebbins GL (1974) Flowering plants: Evolution above the species level. Harvard University Press, Cambridge, MAGoogle Scholar
  38. Stone JL (2004) Sheltered load associated with S-alleles in Solanum carolinense. Am J Bot 92:335-342Google Scholar
  39. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437-460PubMedGoogle Scholar
  40. Takahata N (1990) A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proc Natl Acad Sci USA 87:2419-2423CrossRefPubMedGoogle Scholar
  41. Tang C, Toomajian C, Sherman-Broyles S, Plagnol V, Guo YL, Ho TT, Clark RM, Nasrallah JB, Weigel D, Nordborg M (2007) The evolution of selfing in Arabidopsis thaliana. Science 317:1070-1072CrossRefPubMedGoogle Scholar
  42. Travers SE, Mena-Alí JI, Stephenson AG (2004) Plasticity in the self-incompatibility of Solanum carolinense. Plant Species Biol 19:127-135CrossRefGoogle Scholar
  43. Uyenoyama MK (1995) A generalized least-squares estimate for the origin of sporophytic self-incompatibility. Genetics 139:975-992PubMedGoogle Scholar
  44. Uyenoyama MK (1997) Genealogical structure among alleles regulating self-incompatibility in natural populations of flowering plants. Genetics 147:1389-1400PubMedGoogle Scholar
  45. Uyenoyama MK (2003) Genealogy-dependent variation in viability among self-incompatibility genotypes. Theor Popul Biol 63:281-293CrossRefPubMedGoogle Scholar
  46. Uyenoyama MK, Takebayashi N (2004) Genus-specific diversification of mating types. In: Singh R, Uyenoyama MK (eds) The evolution of population biology. Cambridge University Press, New York, pp 254-271Google Scholar
  47. Uyenoyama MK, Zhang Y, Newbigin E (2001) On the origin of self-incompatibility haplotypes: Transition through self-compatible intermediates. Genetics 157:1805-1817PubMedGoogle Scholar
  48. Vallejo-Marín M (2007) The paradox of clonality and the evolution of self-incompatibility. Plant Signal Behav 2:265-266PubMedGoogle Scholar
  49. Vallejo-Marín M, O’Brien HE (2007) Correlated evolution of self-incompatibility and clonal reproduction in Solanum (Solanaceae). New Phytol 173:415-421CrossRefPubMedGoogle Scholar
  50. Vallejo-Marín M, Uyenoyama MK (2004) On the evolutionary costs of self-incompatibility: Incomplete reproductive compensation due to pollen limitation. Evolution 58:1924-1935PubMedGoogle Scholar
  51. Vekemans X, Slatkin M (1994) Gene and allelic genealogies at a gametophytic self-incompatibility locus. Genetics 137:1157-1165PubMedGoogle Scholar
  52. Wilcock C, Neiland R (2002) Pollination failure in plants: Why it happens and when it matters. Trends Plant Sci 7:270-277CrossRefPubMedGoogle Scholar
  53. Wright S (1939) The distribution of self-sterility alleles in populations. Genetics 24:538-552PubMedGoogle Scholar
  54. Wright S (1960) On the number of self-incompatibility alleles maintained in equilibrium by a given mutation rate in a population of a given size: A reexamination. Biometrics 16:61-85CrossRefGoogle Scholar
  55. Yokoyama S, Hetherington LE (1982) The expected number of self-incompatibility alleles in finite plant populations. Heredity 48:299-303CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • M. Vallejo-Marín
    • 1
  • M. K. Uyenoyama
    • 2
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada
  2. 2.Department of BiologyDuke UniversityDurhamUSA

Personalised recommendations