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Gender specialization in Palicourea demissa (Rubiaceae), a distylous, hummingbird-pollinated treelet

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Abstract

Distyly has been interpreted as a mechanism that promotes cross-pollination among conspecific plants and as one of the routes leading to the evolution of dioecy. In one of the possible evolutionary pathways, pollinators may disrupt intermorph pollen flow, and, as a consequence, floral morphs may gradually specialize as either male or female (functional dioecy). Natural patterns of pollen deposition and fruit and seed production were estimated in Palicourea demissa (Rubiaceae) and used as parameters to assess functional gender differences between floral morphs. Pollen flow was asymmetrical in P. demissa. Long-styled flowers were more effective than short-styled flowers in pollen deposition towards compatible stigmas, whereas short-styled flowers were more effective in legitimate pollen receipt. Accordingly, short-styled plants produced more fruits and viable seeds than long-styled plants. The contributions of male and female function to the potential functional gender were equivalent in both morphs. However, the realized functional gender deviated significantly from the potential functional gender in both morphs, in which short-styled plants were more successful through their female function, but long-styled plants through their male function. If pollinators disrupt the complementarities of pollen transfer between the two morphs (asymmetric pollen flow), the expression of a more profitable gender is expected in each morph. Thus, our results support the hypothesis that dioecy may evolve in distylous populations through the gradual specialization of each morph as either male or female.

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References

  • Ataroff M, Rada F (2000) Deforestation impact on water dynamic in a Venezuelan Andean cloud forest. Ambio 29:440–444

    Google Scholar 

  • Barrett SCH (1990) The evolution and adaptive significance of heterostyly. Trends Ecol Evol 5:144–148

    Article  PubMed  CAS  Google Scholar 

  • Barrett SCH (1992) Heterostylous genetic polymorphisms: model systems for evolutionary analysis. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 1–29

    Google Scholar 

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

    CAS  Google Scholar 

  • Barrett SCH, Glover D (1985) On the Darwinian hypothesis of the adaptive significance of tristyly. Evolution 39:766–774

    Article  Google Scholar 

  • Barrett SCH, Richards JH (1990) Heterostyly in tropical plants. Mem NY Bot Gard 55:35–65

    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, Berlin, pp 3–32

    Chapter  Google Scholar 

  • Barrett SCH, Jesson LK, Baker AM (2000) The evolution and function of stylar polymorphisms in flowering plants. An Bot 85:253–265

    Article  Google Scholar 

  • Bawa KS (1980) Evolution of dioecy in flowering plants. Ann Rev Ecol Syst 11:15–39

    Article  Google Scholar 

  • Bawa KS, Beach JH (1983) Self-incompatibility systems in the Rubiaceae of a tropical lowland wet forest. Am J Bot 70:1281–1288

    Article  Google Scholar 

  • Beach JH, Bawa KS (1980) Role of pollinators in the evolution of dioecy from distyly. Evolution 34:1138–1142

    Article  Google Scholar 

  • Boege K, Domínguez CA (2008) Pre-dispersal seed predation reduces the reproductive compensatory advantage of thrum individuals in Erythroxylum havanense (Erythroxylaceae). Evol Ecol 22:675–687

    Article  Google Scholar 

  • Brys R, Jacquemyn H (2010) Floral display size and spatial distribution of potential mates affect pollen deposition and female reproductive success in distylous Pulmonaria officinalis (Boraginaceae). Pl Biol 12:597–603

    CAS  Google Scholar 

  • Cariveau D, Irwin RE, Brody AK, Garcia-Mayeya LS, Von der Ohe A (2004) Direct and indirect effects of pollinators and seed predators to selection on plant and floral traits. Oikos 104:15–26

    Article  Google Scholar 

  • Casper BB (1992) The application of sex allocation theory to heterostylous plants. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 207–223

    Google Scholar 

  • Charlesworth D (1999) Theories of the evolution of dioecy. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer, Berlin, pp 33–60

    Google Scholar 

  • Contreras PS, Ornelas JF (1999) Reproductive conflicts of Palicourea padifolia (Rubiaceae), a distylous shrub of a tropical cloud forest in Mexico. Pl Syst Evol 219:225–241

    Article  Google Scholar 

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

    Book  Google Scholar 

  • De Jong TJ, Klinkhamer PGL (2005) Evolutionary ecology of plant reproductive strategies. Cambridge University Press, Cambridge

    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 

  • Engel EC, Irwin RE (2003) Linking pollinator visitation rate and pollen receipt. Am J Bot 90:1612–1618

    Article  Google Scholar 

  • Feinsinger P, Busby WH (1987) Pollen carryover: experimental comparisons between morphs of Palicourea lasiorrachis (Rubiaceae), a distylous, bird-pollinated, tropical treelet. Oecologia 73:231–235

    Article  Google Scholar 

  • Freeman DC, Doust L, El-Keblawy A, Miglia KJ, McArthur ED (1997) Sexual specialization and inbreeding avoidance in the evolution of dioecy. Bot Rev 63:65–92

    Article  Google Scholar 

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

    Article  Google Scholar 

  • García-Robledo C (2008) Asymmetry in pollen flow promotes gender specialization in morphs of the distylous neotropical herb Arcytophyllum lavarum (Rubiaceae). Evol Ecol 22:743–755

    Google Scholar 

  • González C, Ornelas JF, Jiménez L (2005) Between-year changes in functional gender expression of Palicourea padifolia (Rubiaceae), a distylous, hummingbird-pollinated shrub. An Bot 95:371–378

    Article  Google Scholar 

  • Hernández A, Ornelas JF (2007) Disassortative pollen transfer in distylous Palicourea padifolia (Rubiaceae), a hummingbird-pollinated shrub. Écoscience 14:8–16

    Article  Google Scholar 

  • Hodgins KA, Barrett SCH (2008) Asymmetrical mating patterns and the evolution of biased-morph ratios in a tristylous daffodil. Genetic Res 90:3–15

    Article  Google Scholar 

  • Justino DG, Maruyama PK, Oliveira PE (2012) Floral resource availability and hummingbird territorial behaviour on a Neotropical savanna shrub. J Ornithol 153:189–197

    Article  Google Scholar 

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

    Google Scholar 

  • Lau P, Bosque C (2003) Pollen flow in the distylous Palicourea fendleri (Rubiaceae): an experimental test of the disassortative pollen flow hypothesis. Oecologia 135:593–600

    PubMed  Google Scholar 

  • Li A, Wu X, Zhang D, Barrett SCH (2010) Cryptic dioecy in Mussaenda pubescens (Rubiaceae): a species with stigma-height dimorphism. An Bot 106:521–531

    Article  Google Scholar 

  • Litrico I, Pailler T, Thompson JD (2005) Gender variation and primary succession in a tropical woody plant, Antirhea borbonica (Rubiaceae). Funct Ecol 93:705–715

    Google Scholar 

  • Lloyd DG (1979) Evolution towards dioecy in heterostylous populations. Pl Syst Evol 131:71–80

    Article  Google Scholar 

  • Lloyd DG, Webb CJ (1992) The selection of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer, Berlin, pp 179–207

    Google Scholar 

  • Machado AO, Silva AP, Consolaro H, Granja e Barros MA, Oliveira PE (2010) Breeding biology and distyly in Palicourea rigida H.B. & K. (Rubiaceae) in the Cerrados of Central Brazil. Acta Bot Bras 24:686–696

    Article  Google Scholar 

  • Maruyama PK, Wanderley Amorim F, Oliveira PE (2010) Night and day service: distyly and mixed pollination system in Faramea cyanea (Rubiaceae). Flora 205:818–824

    Article  Google Scholar 

  • Naiki A, Kato M (1999) Pollination system and evolution of dioecy from distyly in Mussaenda parviflora (Rubiaceae). Pl Sp Biol 14:217–227

    Article  Google Scholar 

  • Olesen JM (1979) Floral morphology and pollen flow in the heterostylous species Pulmonaria obscura Dumort. (Boraginaceae). New Phytol 82:757–767

    Article  Google Scholar 

  • Opler PA, Baker HG, Frankie GW (1975) Reproductive biology of some Costa Rica Cordia species (Boraginaceae). Biotropica 7:234–247

    Article  Google Scholar 

  • Ornelas JF, Jiménez L, González C, Hernández A (2004a) Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. I. Hummingbirds’ effectiveness as pollen vectors. Am J Bot 91:1052–1060

    Article  PubMed  Google Scholar 

  • Ornelas JF, González C, Jiménez L, Lara C, Martínez AJ (2004b) Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. II. Attracting and rewarding mutualistic and antagonistic visitors. Am J Bot 91:1061–1069

    Article  PubMed  Google Scholar 

  • Pannell JR, Verdú M (2006) The evolution of gender specialization from dimorphic hermaphroditism: paths from heterodichogamy to gynodioecy and androdioecy. Evolution 60:660–673

    Article  PubMed  Google Scholar 

  • Pielou EC (1961) Segregation and symmetry in two-species populations as studied by nearest- neighbour relationships. J Ecol 49:255–269

    Article  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: http://www.R-project.org

  • Razafimandimbison SG, Lantz H, Mouly A, Bremer B (2009) Evolutionary trends, major lineages, and new generic limits in the dioecious group of the tribe Vanguerieae (Rubiaceae): insights into the evolution of functional dioecy. Ann Mo Bot Gard 96:161–181

    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, Barrett SCH (1992) The development of heterostyly. In: Barrett SCH (ed) Evolution and function of heterostyly. Springer-Verlag, Berlin Heidelberg, New York, pp 85–227

  • Robbrecht E (1988) Tropical woody Rubiaceae: characteristic features and progressions contributions to a new subfamilial classification. Opera Bot Belgica 1:1–271

    Google Scholar 

  • Sobrevila C, Ramirez N, de Enrech NX (1983) Reproductive biology of Palicourea flendleri and Palicourea petiolaris (Rubiaceae), heterostylous shrubs of a tropical cloud forest in Venezuela. Biotropica 15:161–169

    Article  Google Scholar 

  • Stone JL (1995) Pollen donation patterns in a tropical distylous shrub (Psychotria suerrensis, Rubiaceae). Am J Bot 82:1390–1398

    Article  Google Scholar 

  • Stone JL, Thompson JD (1994) The evolution of distyly: pollen transfer in artificial flowers. Evolution 48:1595–1606

    Article  Google Scholar 

  • Valois-Cuesta H, Novoa-Sheppard S (2006) Ecología reproductiva de Palicourea demissa (Rubiaceae): néctar y colibríes en una selva nublada de Los Andes venezolanos. Rev Inst Univ Tec Chocó 25:40–46

    Google Scholar 

  • Valois-Cuesta H, Soriano PJ, Ornelas JF (2011a) Dimorphisms and self-incompatibility in the distylous species Palicourea demissa (Rubiaceae): possible implications for its reproductive success. J Pl Res 124:137–146

    Article  Google Scholar 

  • Valois-Cuesta H, Soriano PJ, Ornelas JF (2011b) Asymmetrical legitimate pollination in distylous Palicourea demissa (Rubiaceae): the role of nectar production and pollinator visitation. J Trop Ecol 27:393–404

    Article  Google Scholar 

  • Webb CJ, Lloyd DG (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms II. Herkogamy. NZ J Bot 24:163–178

    Article  Google Scholar 

  • Wu X, Li A, Zhang D (2010) Cryptic self-incompatibility and distyly in Hedyotis acutangula Champ. (Rubiaceae). Pl Biol 12:484–494

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to S. Ecce-Homo, Z. Betancourt, C. Rengifo, R. Pacheco, J.H. Castaño, and J. Murillo for assistance during fieldwork. We thank M.E. Naranjo, J. Estrada, C. García, A. Jaramillo, N. Ramírez, Marlies Sazima and two anonymous reviewers for their constructive comments on an earlier draft of the manuscript. This work was funded by the Red Latinoamericana de Botánica (code: RLB06-M03 and RLB08-SP-1 to H.V-C.) and the Consejo de Desarrollo Científico, Humanístico y Tecnológico of the Universidad de Los Andes, Mérida-Venezuela (code: C-1557-08-01EM to H.V-C. and P.S.). Staff from La Mucuy Bird’s Observatory, Sierra Nevada National Park and the Laboratorio de Ecología Animal “A” of the Universidad de Los Andes, Mérida, Venezuela provided logistical support.

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Correspondence to Hamleth Valois-Cuesta.

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Valois-Cuesta, H., Soriano, P.J. & Ornelas, J.F. Gender specialization in Palicourea demissa (Rubiaceae), a distylous, hummingbird-pollinated treelet. Plant Syst Evol 298, 975–984 (2012). https://doi.org/10.1007/s00606-012-0607-7

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