Skip to main content

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

  • Chapter
Self-Incompatibility in Flowering Plants

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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 321:38-44

    Article  CAS  Google Scholar 

  • Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:347-349

    Article  Google Scholar 

  • Baker HG (1967) Support for Baker’s Law - as a rule. Evolution 21:853-856

    Article  Google Scholar 

  • Baker HG, Cox PA (1984) Further thoughts on dioecism and islands. Ann Mo Bot Gard 71:244-253

    Article  Google Scholar 

  • 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 98-124

    Google Scholar 

  • Charlesworth D, Charlesworth B (1979) The evolution and breakdown of S-allele systems. Heredity 43:41-55

    Article  Google Scholar 

  • Charpentier A (2002) Consequences of clonal growth for plant mating. Evol Ecol 15:521-530

    Article  Google Scholar 

  • 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 16:481-486

    Article  CAS  PubMed  Google Scholar 

  • Ferrer MM, Good-Ávila SV (2007) Macrophylogenetic analyses of the gain and loss of self-incompatibility in the Asteraceae. New Phytol 173:401-414

    Article  PubMed  Google Scholar 

  • Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Oxford University Press, Dover, New York

    Google Scholar 

  • Good-Ávila SV, Stephenson AG (2002) The inheritance of modifiers conferring self-fertility in the partially self-incompatible perennial, Campanula rapunculoides L. (Campanulaceae). Evolution 56:263-272

    PubMed  Google Scholar 

  • 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 36:47-79

    Article  Google Scholar 

  • Groenendale JMv, Klimes L, Klimesova J, Hendriks RJJ (1996) Comparative ecology of clonal plants. Philos Trans R Soc Lond B 351:1331-1339

    Article  Google Scholar 

  • Honnay O, Jacquemyn H (2008) Mating system evolution under strong clonality: towards self-compatibility or self-incompatibility? Evol Ecol DOI 10.1007/s10682-007-9207-3

    Google Scholar 

  • Igic B, Bohs L, Kohn JR (2006) Ancient polymorphism reveals unidirectional breeding system shifts. Proc Natl Acad Sci USA 103:1359-1363

    Article  CAS  PubMed  Google Scholar 

  • Ioerger TR, Clark AG, Kao Th (1990) Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Natl Acad Sci USA 87:9732-9735

    Article  CAS  PubMed  Google Scholar 

  • Karlin S, Taylor HM (1981) A second course in stochastic processes. Academic, New York

    Google Scholar 

  • 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 92:761-767

    Article  Google Scholar 

  • 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 88:534-544

    Article  CAS  PubMed  Google Scholar 

  • 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 13:627-643

    Article  CAS  PubMed  Google Scholar 

  • Lawrence MJ (2000) Population genetics of the homomorphic self-incompatibility polymorphisms in flowering plants. Ann Bot (Lond) 85( Suppl. A):221-226

    Article  Google Scholar 

  • Levin DA (1996) The evolutionary significance of pseudo-self-fertility. Am Nat 148:321-332

    Article  Google Scholar 

  • Liu P, Sherman-Broyles S, Nasrallah ME, Nasrallah JB (2007) A cryptic modifier causing transient self-incompatibility in Arabidopsis thaliana. Curr Biol 17:734-740

    Article  CAS  PubMed  Google Scholar 

  • 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 177:501-510

    Article  PubMed  Google Scholar 

  • Nasrallah JB, Kao Th, Goldberg ML, Nasrallah ME (1985) A cDNA clone encoding an S-locus-specific glycoprotein from Brassica oleracea. Nature 318:263-267

    Article  CAS  Google Scholar 

  • 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 101:16070-16074

    Article  CAS  PubMed  Google Scholar 

  • Neuhauser C (1999) The ancestral graph and gene genealogy under frequency-dependent selection. Theor Popul Biol 56:203-214

    Article  CAS  PubMed  Google Scholar 

  • Newbigin E, Uyenoyama MK (2005) The evolutionary dynamics of self-incompatibility systems. Trends Genet 21:500-505

    Article  CAS  PubMed  Google Scholar 

  • Pagel M, Meade A (2006) Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am Nat 167:808-825

    Article  Google Scholar 

  • Pagel MD (1994) Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Philos Trans R Soc Lond B 255:37-45

    Google Scholar 

  • Pannell JR, Barrett SCH (1998) Baker’s law revisited: Reproductive assurance in a metapopulation. Evolution 52:657-668

    Article  Google Scholar 

  • Richards AJ (1986) Plant breeding systems. George Allen & Unwin, London

    Google Scholar 

  • Richman AD, Kohn JR (1999) Self-incompatibility alleles from Physalis: Implications for histori-cal inference from balanced genetic polymorphisms. Proc Natl Acad Sci USA 96:168-172

    Article  CAS  PubMed  Google Scholar 

  • 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 19:94-106

    Article  CAS  PubMed  Google Scholar 

  • 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 306:2081-2084

    Article  CAS  PubMed  Google Scholar 

  • Shimizu KK, Shimizu-Inatsugi R, Tsuchimatsu T, Purugganan MD (2008) Independent origins of self-compatibility in Arabidopsis thaliana. Mol Ecol 17:704-714

    CAS  PubMed  Google Scholar 

  • Stebbins GL (1974) Flowering plants: Evolution above the species level. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Stone JL (2004) Sheltered load associated with S-alleles in Solanum carolinense. Am J Bot 92:335-342

    CAS  Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437-460

    CAS  PubMed  Google Scholar 

  • Takahata N (1990) A simple genealogical structure of strongly balanced allelic lines and trans-species evolution of polymorphism. Proc Natl Acad Sci USA 87:2419-2423

    Article  CAS  PubMed  Google Scholar 

  • 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 317:1070-1072

    Article  CAS  PubMed  Google Scholar 

  • Travers SE, Mena-Alí JI, Stephenson AG (2004) Plasticity in the self-incompatibility of Solanum carolinense. Plant Species Biol 19:127-135

    Article  Google Scholar 

  • Uyenoyama MK (1995) A generalized least-squares estimate for the origin of sporophytic self-incompatibility. Genetics 139:975-992

    CAS  PubMed  Google Scholar 

  • Uyenoyama MK (1997) Genealogical structure among alleles regulating self-incompatibility in natural populations of flowering plants. Genetics 147:1389-1400

    CAS  PubMed  Google Scholar 

  • Uyenoyama MK (2003) Genealogy-dependent variation in viability among self-incompatibility genotypes. Theor Popul Biol 63:281-293

    Article  PubMed  Google Scholar 

  • 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 254-271

    Google Scholar 

  • Uyenoyama MK, Zhang Y, Newbigin E (2001) On the origin of self-incompatibility haplotypes: Transition through self-compatible intermediates. Genetics 157:1805-1817

    CAS  PubMed  Google Scholar 

  • Vallejo-Marín M (2007) The paradox of clonality and the evolution of self-incompatibility. Plant Signal Behav 2:265-266

    PubMed  Google Scholar 

  • Vallejo-Marín M, O’Brien HE (2007) Correlated evolution of self-incompatibility and clonal reproduction in Solanum (Solanaceae). New Phytol 173:415-421

    Article  PubMed  Google Scholar 

  • Vallejo-Marín M, Uyenoyama MK (2004) On the evolutionary costs of self-incompatibility: Incomplete reproductive compensation due to pollen limitation. Evolution 58:1924-1935

    PubMed  Google Scholar 

  • Vekemans X, Slatkin M (1994) Gene and allelic genealogies at a gametophytic self-incompatibility locus. Genetics 137:1157-1165

    CAS  PubMed  Google Scholar 

  • Wilcock C, Neiland R (2002) Pollination failure in plants: Why it happens and when it matters. Trends Plant Sci 7:270-277

    Article  CAS  PubMed  Google Scholar 

  • Wright S (1939) The distribution of self-sterility alleles in populations. Genetics 24:538-552

    CAS  PubMed  Google Scholar 

  • 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 16:61-85

    Article  Google Scholar 

  • Yokoyama S, Hetherington LE (1982) The expected number of self-incompatibility alleles in finite plant populations. Heredity 48:299-303

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Vallejo-Marín, M., Uyenoyama, M.K. (2008). On the Evolutionary Modification of Self-Incompatibility: Implications of Partial Clonality for Allelic Diversity and Genealogical Structure. In: Self-Incompatibility in Flowering Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-68486-2_3

Download citation

Publish with us

Policies and ethics