Skip to main content
SpringerLink
Log in

Breeding systems in Tolpis (Asteraceae) in the Macaronesian islands: the Azores, Madeira and the Canaries

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Plants on oceanic islands often originate from self-compatible (SC) colonizers capable of seed set by self-fertilization. This fact is supported by empirical studies, and is rooted in the hypothesis that one (or few) individuals could find a sexual population, whereas two or more would be required if the colonizers were self-incompatible (SI). However, a SC colonizer would have lower heterozygosity than SI colonizers, which could limit radiation and diversification of lineages following establishment. Limited evidence suggests that several species-rich island lineages in the family Asteraceae originated from SI colonizers with some “leakiness” (pseudo-self-compatibility, PSC) such that some self-seed could be produced. This study of Tolpis (Asteraceae) in Macaronesia provides first reports of the breeding system in species from the Azores and Madeira, and additional insights into variation in Canary Islands. Tolpis from the Azores and Madeira are predominately SI but with PSC. This study suggests that the breeding systems of the ancestors were either PSC, possibly from a single colonizer, or from SI colonizers by multiple disseminules either from a single or multiple dispersals. Long-distance colonists capable of PSC combine the advantages of reproductive assurance (via selfing) in the establishment of sexual populations from even a single colonizer with the higher heterozygosity resulting from its origin from an outcrossed source population. Evolution of Tolpis on the Canaries and Madeira has generated diversity in breeding systems, including the origin of SC. Macaronesian Tolpis is an excellent system for studying breeding system evolution in a small, diverse lineage.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allen AM, Thorogood CJ, Hegarty MJ, Lexer C, Hiscock SJ (2011) Pollen-pistil interactions and self-incompatibility in the Asteraceae: new insights from studies of Senecio squalidus (Oxford ragwort). Ann Bot (Oxford) 108:687–698

    Article  CAS  Google Scholar 

  • Anderson GJ, Bernardello G, Stuessy TF, Crawford DJ (2001) Breeding system and pollination of selected plants endemic to Juan Fernández Islands. Amer J Bot 88:220–233

    Article  CAS  Google Scholar 

  • Andersson S (2012) Does inbreeding promote evolutionary reduction of flower size? Experimental evidence from Crepis tectorum (Asteraceae). Amer J Bot 99:1388–1398

    Article  Google Scholar 

  • Baker HG (1955) Self-compatibility and establishment after “long-distance” dispersal. Evolution 9:347–348

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Barrett SCH (1996) The reproductive biology and genetics of island plants. Phil Trans Royal Soc B 351:725–733

    Article  Google Scholar 

  • Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284

    Article  CAS  PubMed  Google Scholar 

  • Barrett SCH (2003) Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philos Trans Ser B 358:991–1004

    Article  Google Scholar 

  • Barrett SCH, Arunkumar R, Wright SI (2014) The demography and genomics of evolutionary transitions to self-fertilization in plants. Philos Trans Ser B 369:1648. doi:10.1098/rstb.2013.0344

    Article  Google Scholar 

  • Bernardello G, Anderson GJ, Stuessy TF, Crawford DJ (2001) A survey of floral traits, breeding systems, floral visitors, and pollination systems of the angiosperms of the Juan Fernández Islands (Chile). Bot Rev 67:255–308

    Article  Google Scholar 

  • Bernardello G, Anderson GJ, Stuessy TF, Crawford DJ (2006) The angiosperm flora of the Archipelago Juan Fernandez (Chile): origin and dispersal. Canad J Bot 84:1266–1281

    Article  Google Scholar 

  • Bramwell D, Bramwell Z (2001) Wild flowers of the Canary Islands, 2nd edn. Editorial Ruida, Madrid

    Google Scholar 

  • Brauner S, Gottlieb LD (1987) A self-compatible plant of Stephanomeria exigua subsp. coronaria (Asteraceae) and its relevance to the origin of its self-pollinating derivative S. malheurensis. Syst Bot 12:299–304

    Article  Google Scholar 

  • Brennan AC, Tabah TA, Harris SA, Hiscock SJ (2011) Sporophytic self-incompatibility in Senecio squalidus (Asteraceae): S allele dominance interactions and modifiers of cross-compatibility and selfing rates. Heredity 106:113–123

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Busch JW, Delph LF (2012) The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Ann Bot (Oxford) 109:553–562

    Article  Google Scholar 

  • Busch JW, Schoen DJ (2008) The evolution of self-incompatibility when mates are limiting. Trends Pl Sci 13:128–136

    Article  CAS  Google Scholar 

  • Busch JW, Joly S, Schoen DJ (2011) Demographic signatures accompanying the evolution of selfing in Leavenworthia alabamica. Molec Biol Evol 28:1717–1729

    Article  CAS  PubMed  Google Scholar 

  • Carlquist S (1974) Island biology. Columbia University Press, New York

    Book  Google Scholar 

  • Carr GD, Powell EA, Kyhos DW (1986) Self-incompatibility in the Hawaiian Madiinae (Compositae): an exception to Baker’s rule. Evolution 40:430–434

    Article  Google Scholar 

  • Carracedo JC, Day S (2002) Canary Islands: Classic Geology in Europe 4. Terra Publishing, Hertfershire

    Google Scholar 

  • Caujapé-Castells J, Tye A, Crawford DJ et al (2010) Conservation of oceanic island floras: present and future global challenges. Persp Pl Ecol Evol Syst 21:107–129

    Article  Google Scholar 

  • Chamorro S, Heleno R, Olesen JM, McMullen CK, Traveset A (2012) Pollination patterns and plant breeding systems in the Galápagos: a review. Ann Bot (Oxford) 110:1489–1501

    Article  Google Scholar 

  • Cheptou P-O, Lepart J, Escarr J (2002) Mating system variation along a successional gradient in the allogamous colonizing plant Crepis sancta (Asteraceae). J Evol Biol 15:753–762

    Article  Google Scholar 

  • Crawford DJ, Archibald JK, Stormer D, Mort ME, Kelly JK, Santos-Guerra A (2008) A test of Baker’s law: the radiation of Tolpis (Asteraceae) in the Canary Islands. Int J Pl Sci 169:782–791

    Article  Google Scholar 

  • Crawford DJ, Archibald JK, Mort ME, Santos-Guerra A (2009) Pollen fertility of synthetic intra- and interspecific F1 hybrids in Canary Islands Tolpis (Asteraceae). Pl Syst Evol 279:103–113

    Article  Google Scholar 

  • Crawford DJ, Archibald JK, Kelly JK, Mort ME, Santos-Guerra A (2010) Mixed mating in the “obligately outcrossing” Tolpis (Asteraceae) of the Canary Islands. Pl Spec Biol 25:114–119

    Article  Google Scholar 

  • Crawford DJ, Anderson GJ, Bernardello B (2011) The reproductive biology of island plants. In: Bramwell D, Caujape-Castells J (eds) The biology of island floras. Cambridge University Press, Cambridge, pp 11–36

    Chapter  Google Scholar 

  • Crawford DJ, Mort ME, Archibald JK (2013) Tolpis santosii (Asteraceae: Cichorieae), a new species from La Palma, the Canary Islands. Vieraea 41:169–175

    Google Scholar 

  • Cruden RW (1977) Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31:32–46

    Article  Google Scholar 

  • Danton P, Perrier C, Martinez de Reyes G (2006) Nouveau catalogue de la flore vasculaire de l’archipel Juan Fernández (Chili) Nuevo catálogo de la flora vascular del Archipiélago Juan Fernández (Chile). Act Bot Gal 153:399–587. doi:10.1080/12538078.2006.10515559

    Article  Google Scholar 

  • de Nettancourt D (1977) Incompatibility in angiosperms. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Diggle PK (1991) Labile sex expression in andromonoecious Solanum hirtum: floral morphogenesis and sex determination. Amer J Bot 78:377–393

    Article  Google Scholar 

  • Ehrendorfer E (1979) Reproductive biology of island plants. In: Bramwell D (ed) Plants and islands. Academic Press, New York, pp 293–306

    Google Scholar 

  • Fernández-Palacios JM (2010) The islands of Macaronesia. In: Serrano ARM, Borges PAV, Boiero M Oromí P (eds) Terrestrial arthropods of Macaronesia: biodiversity, ecology and evolution. Security Print, Sociedade de Indústria Gráfica, Lda, pp 1–30

  • Foxe JP, Stift M, Tedder A, Haundry A, Wright SI, Mable BK (2010) Reconstructing origins of loss of self-incompatibility and selfing in North American Arabidopsis lyrata: a population genetic context. Evolution 64:3495–3510

    Article  PubMed  Google Scholar 

  • Good-Avila 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 

  • Good-Avila SV, Mena-Alí JI, Stephenson AG (2008) Genetic and environmental causes and evolutionary consequences of variations in self-fertility in self incompatible species. In: Franklin-Tong VE (ed) Self-Incompatibility in flowering plants—evolution, diversity, and mechanisms. Springer-Verlag, Berlin, pp 33–51

    Chapter  Google Scholar 

  • Goodwillie C, Partis KL, West JW (2004) Transient self-incompatibility confers delayed selfing in Leptosiphon jepsonii (Polemoniaceae). Int J Pl Sci 165:387–394

    Article  Google Scholar 

  • Gottlieb LD (1973) Differentiation, sympatric speciation, and the origin of a diploid species of Stephanomeria. Amer J Bot 60:545–553

    Article  CAS  Google Scholar 

  • Gruenstaeudl M, Santos-Guerra A, Jansen RK (2013) Phylogenetic analyses of Tolpis Adans. (Asteraceae) reveal patterns of adaptive radiation, multiple colonization and interspecific hybridization. Cladistics 29:416–434

    Article  Google Scholar 

  • Hiscock SJ, Tabah DA (2003) The different mechanisms of sporophytic self-incompatibility. Philos Trans Ser B 358:1037–1045

    Article  CAS  Google Scholar 

  • Hoernle K, Carracedo JC (2009) Canary Islands, geology. In: Gillespie RG, Clague DA (eds) Encyclopedia of Islands. Univ. Calif. Press, Berkeley, pp 133–143

  • Igic B, Lande R, Kohn JR (2008) Loss of self-incompatibility and its evolutionary consequences. Int J Pl Sci 169:93–104

    Article  Google Scholar 

  • Jarvis CE (1980) Systematic studies in the genus Tolpis Adanson. PhD diss. University of Reading, UK

  • Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot

    Google Scholar 

  • Kreft H, Jetz W, Mutke J, Kier G, Barthlott W (2008) Global diversity of island floras from a macroecological perspective. Ecol Lett 11:116–127

    PubMed  Google Scholar 

  • Lafuma L, Maurice S (2007) Increase in mate availability without loss of self-incompatibility in the invasive species Senecio inaequidens (Asteraceae). Oikos 116:201–208

    Article  Google Scholar 

  • Levin DA (1996) The evolutionary significance of pseudo-self-fertility. Amer Naturalist 148:321–332

    Article  Google Scholar 

  • Lloyd DG, Schoen DJ (1992) Self-fertilization and cross-fertilization in plants. I Functional dimensions. Int J Pl Sci 153:358–369

    Article  Google Scholar 

  • López de Heredia U, López R, Collada C, Emerson BC, Gill L (2014) Signatures of volcanism and aridity in the evolution of an insular pine (Pinus canariensis Chr. Sm. Ex DC in Buch). Heredity 113:240–249

    Article  PubMed  Google Scholar 

  • López-García MC, Maillet J (2005) Biological characteristics of an invasive South African species. Biol Invasions 7:181–194

    Article  Google Scholar 

  • Mable BK, Robertson AV, Dart S, Di Berardo C, Witham L (2005) Breakdown of self-incompatibility in the perennial Arabidopsis lyrata (Brassicaceae) and its genetic consequences. Evolution 59:1437–1448

    Article  PubMed  Google Scholar 

  • Maddux DM, Jolly DB, Supkoff DM, Mayfield A (1996) Pollination biology of yellow starthistle (Centaurea solstitialis) in California. Canad J Bot 74:262–267

    Article  Google Scholar 

  • Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Stain Tech 34:125–128

    CAS  Google Scholar 

  • McMullen CK (1987) Breeding systems of selected Galápagos Islands angiosperms. Amer J Bot 74:1694–1705

    Article  Google Scholar 

  • McMullen CK (1990) Reproductive biology of Galápagos Islands angiosperms. In: Lawesson JE, Hamann O, Rogers G, Reck G, Ochoa H (eds) Botanical research and management in the Galápagos. Missouri Botanical Garden, St. Louis, pp 25–45

    Google Scholar 

  • McMullen CK (1999) Flowering plants of the Galápagos. Cornell University Press, Ithaca

    Google Scholar 

  • Neal PR, Anderson GJ (2005) Are ‘mating systems’ ‘breeding systems’ of inconsistent and confusing terminology in plant reproductive biology? or is it the other way around? Pl Syst Evol 250:173–185

    Article  Google Scholar 

  • Nielsen LR, Philipp M, Adsersen H, Siegismund HR (2000) Breeding system of Scalesia divisa Andersson, an endemic Asteraceae from the Galápagos Islands. Det Norske Videnskaps-Akademi I. Matematisk-Naturvidenskapelige Klasse, Shrifter, Ny Serie 39:127–138

  • Nielsen L, Siegismund HS, Philipp M (2003) Partial self-incompatibility in the polyploid endemic species Scalesia affinis (Asteraceae) from the Galápagos: remnants of a self-incompatibility system? Bot J Linn Soc 142:93–101

    Article  Google Scholar 

  • Ornduff R (1969) Reproductive biology in relation to systematics. Taxon 18:121–133

    Article  Google Scholar 

  • Ortiz MÁ, Talavera S, García-Castaño JL, Tremetsberger K, Stuessy T, Balao F, Casimiro-Soriguer R (2006) Self-incompatibility and floral parameters in Hypochaeris sect. Hypochaeris (Asteraceae). Amer J Bot 93:234–244

    Article  Google Scholar 

  • Pannell JR (2015) Evolution of the mating system in colonizing plants. Ecol, Molec. doi:10.1111/mec.13087

    Google Scholar 

  • Pettengill JB, Moeller DA (2011) Tempo and mode of mating system evolution between incipient Clarkia species. Evolution 66:1210–1225

    Article  PubMed  Google Scholar 

  • Roderick GK, Croucher PJP, Vandergast AG, Gillespie RG (2012) Species differentiation on a dynamic landscape: shifts in metapopulation genetic structure using chronology of the Hawaiian archipelago. Evol Biol 39:192–206

    Article  PubMed Central  PubMed  Google Scholar 

  • Sakai AK, Weller SG, Chen M-L, Chou S-Y, Tasanont C (1997) Evolution of gynodioecy and maintenance of females: the role of inbreeding depression, outcrossing rates, and resource allocation in Schiedea adamantis (Caryophyllaceae). Evolution 51:724–736

    Article  Google Scholar 

  • Sakai AK, Weller SG, Wagner WL, Nepokroeff M, Culley TM (2006) Adaptive radiation and evolution of breeding systems in Schiedea (Caryophyllaceae), an endemic Hawaiian genus. Ann Missouri Bot Gard 93:49–63

    Article  Google Scholar 

  • Sicard A, Lenhard M (2011) The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Ann Bot (Oxford) 107:1433–1443

    Article  Google Scholar 

  • Silva LB, Sardos J, Menezes de Sequeira M, Silva L, Maciel MGB, Moura M (2012) Microsatellite markers reveal the genetic structure of the Macaronesian Tolpis azorica and Tolpis succulenta. International Symposium Flora MAC 2012, 5–8 September 2012, Universidade da Madeira, Funchal, Madeira

  • Slotte T, Hazzouri KM, Stern D, Andolfatto P, Wright SI (2012) Genetic architecture and adaptive significance of the selfing syndrome in Capsella. Evolution 66:1360–1374

    Article  PubMed  Google Scholar 

  • Soto-Trejo F, Kelly JK, Archibald JK, Mort ME, Santos-Guerra A, Crawford DJ (2013) The genetics of self-compatibility and associated floral characters in Tolpis (Asteraceae) in the Canary Islands. Int J Pl Sci 174:171–178

    Article  Google Scholar 

  • Stebbins GL (1957) Self-fertilization and population variability in the higher plants. Amer Naturalist 91:337–354

    Article  Google Scholar 

  • Stone JL, Sasuclark MA, Blomberg CP (2006) Variation in the self-incompatibility response within and among populations of the tropical shrub Witheringia solanacea (Solanaceae). Amer J Bot 93:592–598

    Article  Google Scholar 

  • Sun M, Ganders FR (1988) Mixed mating systems in Hawaiian Bidens (Asteraceae). Evolution 42:516–527

    Article  Google Scholar 

  • Travers SE, Mena-Ali JI, Stephenson AG (2004) Plasticity of the self-incompatibility system of Solanum carolinense. Pl Sp Biol 19:127–135

    Article  Google Scholar 

  • Vogler DW, Das C, Stephenson AG (1998) Phenotypic plasticity in the expression of self-incompatibility in Campanula rapunculoides. Heredity 81:546–555

    Article  Google Scholar 

  • Wagner WL, Herbst DR, Sohmer SH (1990) Manual of the flowering plants of Hawai‘i, vol 2. University of Hawaii Press and Bishop Museum Press, Honolulu

    Google Scholar 

  • Weller SG, Sakai AK, Thai DA, Tom J, Rankin AE (2005) Inbreeding depression and heterosis in populations of Schiedea viscosa, a highly selfing species. J Evol Biol 18:1434–1444

    Article  CAS  PubMed  Google Scholar 

  • Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography: ecology, evolution, and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Wright SI, Kalisz S, Slotte T (2013) Evolutionary consequences of self-fertilization in plants. Proc Roy Soc London Ser B Biol Sci 280:20130133. doi:10.1098/rspb.2013.0133

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a General Research Fund grant from KU EEB to MEM. The authors wish to thank Katie Sadler, Clare Prohaska, Sidrah Sheikh, Matthew Gibson, Jacob Ressler, Ben Kerbs, and Luke Greene for assistance with plant propagation, and for assessing levels of pollen fertility and seed set. Hanno Schäfer provided seeds of Tolpis succulenta from the Azores.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, and the Biodiversity Institute, University of Kansas, Lawrence, KS, 66045-7534, USA

    Daniel J. Crawford & Mark E. Mort

  2. Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, 06269-3043, USA

    Gregory J. Anderson

  3. Departamento de Biologia, CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Pólo dos Açores, Universidade dos Açores, Rua da Mãe de Deus, Apartado 1422, 9501-801, Ponta Delgada, Açores, Portugal

    Lurdes Borges Silva & Mónica Moura

  4. Grupo de Botânica da Madeira, Universidade da Madeira, Centro de Ciências da Vida, Campus da Penteada, 9000-390, Funchal, Portugal

    Miguel Menezes de Sequeira

  5. Calle Guaidil 16, Urbanización Tamarco, Tegueste, 38280, Tenerife, Canary Islands, Spain

    Arnoldo Santos-Guerra

  6. Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, 66045-7534, USA

    John K. Kelly

Authors
  1. Daniel J. Crawford
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gregory J. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lurdes Borges Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Miguel Menezes de Sequeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mónica Moura
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Arnoldo Santos-Guerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. John K. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mark E. Mort
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark E. Mort.

Additional information

Handling editor: Marcus Koch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online resource 1 (PDF 71 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Crawford, D.J., Anderson, G.J., Silva, L.B. et al. Breeding systems in Tolpis (Asteraceae) in the Macaronesian islands: the Azores, Madeira and the Canaries. Plant Syst Evol 301, 1981–1993 (2015). https://doi.org/10.1007/s00606-015-1210-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-015-1210-5

Keywords

Search

Navigation