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How a heterostylous plant species responds to life on remote islands: a comparative study of the morphology and reproductive biology of Waltheria ovata on the coasts of Ecuador and the Galápagos Islands

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Abstract

Heterostylous reproductive systems are usually absent on oceanic island. Self-compatibility would, generally, be advantageous for long-distance dispersing species, as it provides reproductive assurance when density of mates is low. The heterostylous reproductive system, often associated with an incompatibility system, may be a constraint on the colonization of remote habitats. It is, therefore, surprising that the distylous shrub Waltheria ovata has colonized all of the Galápagos Islands, situated more than a thousand kilometres off the shore of Ecuador. The present study confirmed the reciprocal herkogamy of W. ovata. A comparison of mainland and the Galápagos Island populations showed a reduction in flower size, including distance between anthers and stigmas and size of anthers on the islands. Some reductions are quite large but not significantly different, mainly due to a high degree of variation among populations on the islands. The pin morph of W. ovata has undergone the most radical adaptive changes in morphology. Pollination experiments of W. ovata disclosed a leak in the incompatibility system on the Galápagos Islands, allowing higher selfing rates as well as intra-morph seed set compared to the mainland populations. This was most pronounced in the thrum morph. The deficient distylous reproductive system may be an adaptation to a pollinator and mate sparse environment on the Galápagos Islands. We conclude that the heterostylous mating system has changed in response to colonization of the Galápagos Islands, giving room for reproductive assurance by seed set after selfings and intra-morph pollinations.

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References

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

    Article  Google Scholar 

  • Barrett SCH (1992a) Gender variation in Wurmbea (Liliaceae) and the evolution of dioecy. J Evolution Biol 5:423–444

    Article  Google Scholar 

  • Barrett SCH (1992b) Heterostylous genetic polymorphisms: Model systems for evolutionary analysis. In: Barrett SCH (ed) Evolution and Function of Heterostyly. Springer-Verlag, Berlin Heidelberg New york, pp 1–29

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Barrett SCH (2010) Darwin’s legacy: the forms, function and sexual diversity of flowers. Philos T R Soc B 365:351–368

    Article  Google Scholar 

  • Barrett SCH, Husband BC (1990) Variation in outcrossing rates in Eichhornia paniculata: the role of demographic and reproductive factors. Plant Species Biol 5:41–55

    Article  Google Scholar 

  • Barrett SCH, Richards HJ (1990) Heterostyly in tropical plants. Mem NY Bot Gard 55:35–61

    Google Scholar 

  • Barrett SCH, Shore JS (1987) Variation and evolution of breeding systems in the Turnera ulmifolia L. complex (Turneraceae). Evolution 41:340–354

    Article  Google Scholar 

  • Barrett SCH, Shore JS (2008) New insights on heterostyly: Comparative biology, ecology and genetics. In: Franklin-Tong VE (ed) Self-incompatibility in Flowering Plants - Evolution, Diversity, and Mechanisms. Springer-Verlag, Berlin, pp 3–32

    Chapter  Google Scholar 

  • Barrett SCH, Morgan MT, Husband BC (1989) The dissolution of a complex genetic polymorphism: the evolution of self-fertilization in the tristylous Eichhornia paniculata (Pontederiaceae). Evolution 43:1398–1416

    Article  Google Scholar 

  • Belaoussoff S, Shore JS (1995) Floral correlates and fitness consequences of mating-system variation in Turnera ulmifolia. Evolution 49:545–556

    Article  Google Scholar 

  • Benjamin RB, Hainsworth FR (1986) Sex change with inbreeding: experiments on separate versus combined sexes. Evolution 40:843–855

    Article  Google Scholar 

  • Björkman T (1995) The effectiveness of heterostyly in preventing illegitimate pollination in dish-shaped flowers. Sex Plant Reprod 8:143–146

    Article  Google Scholar 

  • Carlquist S (1974) Island Biology. Colombia University Press, New York

    Google Scholar 

  • Caruso CM (2000) Competition for pollination influences selection on floral traits of Ipomopsis aggregata. Evolution 54:1546–1557

    PubMed  CAS  Google Scholar 

  • Castro CC, Oliveira PE (2002) Pollination biology of distylous Rubiaceae in the Atlantic rain forest, SE Brazil. Plant Biol 4:640–646

    Article  Google Scholar 

  • Castro CC, Oliveira P, Alves MC (2004) Breeding system and floral morphometry of distylous Psychotria L. species in the Atlantic rain forest, SE Brazil. Plant Biol 6:760–775

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Cruden RW, Lyon DL (1985) Patterns of biomass allocation to male and female functions in plants with different mating systems. Oecologia 66:299–306

    Google Scholar 

  • Darwin CR (1877) The different forms of flowers on plants of the same species. John Murray, London

    Book  Google Scholar 

  • Dulberger R (1992) Floral polymorphisms and their functional significance in the heterostylous syndrome. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 41–84

    Google Scholar 

  • Fenster CB, Diggle PK, Barrett SCH, Ritland KR (1995) The genetics of floral development differentiating two species of Mimulus (Scrophulariaceae). Heredity 74:258–266

    Article  Google Scholar 

  • Ganders FR (1975) Heterostyly, homostyly and fecundity in Amsinckia spectabilis (Boraginaceae). Madrono 23:56–62

    Google Scholar 

  • Ganders FR (1979) The biology of heterostyly. New Neal J Bot 17:607–635

    Article  Google Scholar 

  • Godley EJ (1979) Flower biology of New Zealand. New Zeal J Bot 17:441–466

    Article  Google Scholar 

  • Kohn JR, Barrett SCH (1992) Experimental studies on the functional significance of heterostyly. Evolution 46:43–55

    Article  Google Scholar 

  • Lewis D, Jones DA (1992) The genetics of heterostyly. In: Barrett SCH (ed) Evolution and Function of Heterostyly. Springer-Verlag, Berlin Heidelberg New York, pp 129–150

    Google Scholar 

  • Lloyd DG, Webb CJ (1992) The evolution of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 151–175

    Google Scholar 

  • McKone MJ (1987) Sex allocation and outcrossing rate: a test of theoretical predictions using bromegrasses (Bromus). Evolution 41:591–598

    Article  Google Scholar 

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

    Article  Google Scholar 

  • McMullen CK (1993) Flower visiting insects of the Galapagos Islands. Pan-Pac Entomol 69:95–106

    Google Scholar 

  • McMullen CK (2009) Pollination biology of a night-flowering Galápagos endemic, Ipomoea habeliana (Convolvulaceae). Bot J Linn Soc 160:11–20

    Article  Google Scholar 

  • McMullen CK (2011) Nocturnal and diurnal pollination of Clerodendrum molle (Verbenaceae) in the Galápagos Islands. Plant Syst Evol 292:15–23

    Article  Google Scholar 

  • McMullen CK (2012) Pollination of the heterostylous Galápagos native, Cordia lutea (Boraginaceae). Plant Syst Evol 298:569–579

    Article  Google Scholar 

  • Moeller DA (2006) Geographic structure of pollinator communities, reproductive assurance, and the evolution of self.pollination. Ecology 87:1510–1522

    Article  PubMed  Google Scholar 

  • Motten AE, Antonovics J (1992) Determinants of outcrossing rate in a predominantly self-fertilizing weed, Datura stramonium (Solanaceae). Am J Bot 79:419–427

    Article  Google Scholar 

  • Nielsen LR, Philipp M, Siegismund HR (2001) Selective advantage of ray florets in Scalesia affinis and S. pedunculata (Asteraceae), two endemic species from the Galápagos. Evol Ecol 16:502–512

    Google Scholar 

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

    Article  Google Scholar 

  • Ornduff R (1988) Distyly and monomorphism in Villarsia (Menyanthaceae): some evolutionary considerations. Ann Mo Bot Gard 75:761–767

    Article  Google Scholar 

  • Pailler T, Thompson JD (1997) Distyly and variation in heteromorphic incompatibility in Gaertnera vaginata (Rubiaceae) endemic to the Reunion Island. Am J Bot 84:315–327

    Article  PubMed  CAS  Google Scholar 

  • Philipp M, Hansen LB, Adsersen H, Siegismund HR (2004) Reproductive ecology of the endemic Lecocarpus pinnatifidus (Asteraceae) in an isolated population in the Galápagos Islands. Bot J Lin Soc 146:171–180

    Article  Google Scholar 

  • Ree RH (1997) Pollen flow, fecundity, and the adaptive significance of heterostyly in Palicourea padifolia (Rubiaceae). Biotropica 29:298–308

    Article  Google Scholar 

  • Richards JH, Koptur S (1993) Floral variation and distyly in Guettarda scabra L. (Rubiaceae). Am J Bot 80:31–40

    Article  Google Scholar 

  • Sánchez JM, Ferrero V, Navarro L (2008) A new approach to the quantification of degree of reciprocity in distylous (sensu lato) plant populations. Ann Bot London 102:463–472

    Article  Google Scholar 

  • Saunders JG (1993) Four new distylous species of Waltheria (Sterculiaceae) and a key to the Mexican and Central American species and species groups. Syst Bot 18:356–376

    Article  Google Scholar 

  • Schoen DJ (1982) Male reproductive effort and breeding system in an hermaphroditic plant. Oecologia 53:255–257

    Article  Google Scholar 

  • Schofield E (1989) Morphological variation in Waltheria ovata Cav. from the Galápagos Islands and South America. Noticias de Galapagos 48:3–7

  • Schultz ST, Ganders FR (1986) Evolution of unisexuality in the Hawaiian flora: a test of microevolutionary theory. Evolution 50:842–855

    Article  Google Scholar 

  • Shore JS, Barrett SCH (1985) The genetic of distyly in Turnera ulmifolia L. (Turneraceae). Heredity 55:167–174

    Article  Google Scholar 

  • Shore JS, Arbo MM, Fernandéz A (2006) Breeding system variation, genetics and evolution in the Turneraceae. New Phytol 171:539–551

    PubMed  CAS  Google Scholar 

  • Takebayashi N, Delph LF (2000) An association between a floral trait and inbreeding depression. Evolution 54:840–846

    PubMed  CAS  Google Scholar 

  • Vuilleumier BS (1967) The origin and evolutionary development of heterostyly in the angiosperms. Evolution 21:210–226

    Article  Google Scholar 

  • Weller SG (2009) The different forms of flowers: what have we learned since Darwin. Bot J Lin Soc 160:249–261

    Article  Google Scholar 

  • Werner R, Hoernle K, van den Bogaard P, Ranero C, von Huene R (1999) Drowned 14-m.y.-old Galapagos archipelago off the coast of Costa Rica: implications for tectonic and evolutionary models. Geology 27:499–502

    Article  CAS  Google Scholar 

  • White WM, Mcbirney AR, Duncan RA (1993) Petrology and geochemistry of the Galapagos-Islands: portrait of a pathological mantle plume. J Geophys Res-Sol Ea 98:19533–19563

    Article  CAS  Google Scholar 

  • Wiggins IL, Porter DM (1971) Flora of the Galápagos Islands. Stanford University Press, Stanford

    Google Scholar 

Download references

Acknowledgments

We want to thank The National Park Service of Galápagos for permission to carry out our study and The Charles Darwin Research Station for arranging our travels. We are in debt to The Villum Kann Rasmussen Foundation, Brødrene Hartmanns Fond and Torben og Alice Frimodts Fond for financial support. We are obliged to Erik Dahl Kjær for valuable statistical help and Lene Rostgaard Nielsen gave helpful comments on earlier versions of the manuscript and Sylvia Mathiasen corrected the language. Furthermore, reviewers provided us with important and constructive comments.

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Correspondence to Marianne Philipp.

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Bramow, C., Hartvig, I., Larsen, S.B. et al. How a heterostylous plant species responds to life on remote islands: a comparative study of the morphology and reproductive biology of Waltheria ovata on the coasts of Ecuador and the Galápagos Islands. Evol Ecol 27, 83–100 (2013). https://doi.org/10.1007/s10682-012-9588-9

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