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Strength through unity: spatial affinity between morphs improves fitness in incompatible heterostylous Melochia (Malvaceae) species

Abstract

In heterostylous plants, both stylar polymorphism and incompatibility system favor legitimate pollination among individuals. Weak or partial expression of incompatibility may ensure progeny when mates or pollinators are scarce in unstable habitats, but under these conditions plants with heteromorphic incompatibility would be in disadvantage. In this work we determine how the spatial distribution of morphs and the effect of proximity to the nearest potential mates affect plants’ reproductive output in four Melochia species. The general prediction of decreasing reproductive success with an increasing isolation of floral morphs in plants with heteromorphic incompatibility was corroborated only in one species (i.e. M. tomentosa). Meanwhile, the other species exhibit a spatial affinity between morphs (i.e. the number of individuals with the nearest neighbor of the opposite morph exceeds expectations upon a random distribution). For M. savannarum and M. villosa we could not detect any effect of proximity to potential mates on the seed-ovule ratio. This may be due to: (1) existence of pollinators with long flying distances, like butterflies, in the populations and/or, (2) the possible occurrence of resource limitation. Spatial affinity between morphs in populations of heterostylous plants with heteromorphic incompatibility system increases reproductive success and may facilitate colonization of ephemeral habitats.

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References

  • Ashman TL (2006) The evolution of separate sexes: a focus on the ecological context. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, pp 204–222

    Google Scholar 

  • Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MR, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Chapter  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Barrett SCH, Cruzan B (1994) Incompatibility in heterostylous plants. In: Williams EG, Clarke AE, Knox RB (eds) Genetic control of self-incompatibility and reproductive development in flowering plants. Kluwer, Dordrecht, pp 189–219

    Chapter  Google Scholar 

  • Barrett SCH, Harder LD (2005) The evolution of polymorphic sexual systems in daffodils (Narcissus). New Phytol 165:45–53

    PubMed  Article  Google Scholar 

  • Barrett SCH, Hodgins KA (2006) Floral design and the evolution of asymmetrical mating systems. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, pp 239–259

    Google Scholar 

  • Borhidi A (1991) Phytogeography and vegetation ecology of Cuba. Akadémiai Kiado, Budapest

    Google Scholar 

  • Brookes RH, Jesson LK, Burd M (2008) A test of simultaneous resource and pollen limitation in Stylidium armeria. New Phytol 179:557–565

    PubMed  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). Plant Biol 12:597–603

    CAS  PubMed  Google Scholar 

  • Brys R, Jacquemyn H, Hermy M (2007) Impact of mate availability, population size, and spatial aggregation of morphs on sexual reproduction in a distylous, aquatic plant. Am J Bot 94:119–127

    PubMed  Article  Google Scholar 

  • Brys R, Jacquemyn H, Hermy M, Beeckman T (2008) Pollen deposition rates and the functioning of distyly in the perennial Pulmonaria officinalis (Boraginaceae). Plant Syst Evol 273:1–12

    Article  Google Scholar 

  • Colautti RI, White NA, Barrett SCH (2010) Variation of self-incompatibility within invasive populations of purple loosestrife (Lythrum salicaria L.) from eastern North America. Int J Plant Sci 171:158–166

    Article  Google Scholar 

  • Darwin C (1876) The effects of cross and self fertilisation in the vegetable kingdom. John Murray, London

    Google Scholar 

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

    Book  Google Scholar 

  • Eckert CG, Manicacci D, Barrett SCH (1996) Frequency-dependent selection on morph ratios in tristylous Lythrum salicaria (Lythraceae). Heredity 77:581–588

    Article  Google Scholar 

  • Faife-Cabrera M (2014) Ecology of stylar polymorphism in the genus Melochia (Malvaceae) in Cuba. PhD dissertation, University of Vigo, Spain

  • Faife-Cabrera M, Ferrero V, Navarro L (2014) Unravelling the stylar polymorphism in Melochia (Malvaceae): reciprocity and ancillary characters. Bot J Linnean Soc. doi:10.1111/boj.12196

  • Faria RR, Ferrero V, Navarro L, Araújo AC (2012) Flexible mating system in distylous populations of Psychotria carthagenensis Jacq. (Rubiaceae) in Brazilian Cerrado. Plant Syst Evol 298:619–627

    Article  Google Scholar 

  • Ferger WF (1931) The nature and use of the harmonic mean. J Am Stat Assoc 26:36–40

    Article  Google Scholar 

  • Ferrero V, Arroyo J, Castro S, Navarro L (2012) Unusual heterostyly: style dimorphism and self-incompatibility are not tightly associated in Lithodora and Glandora (Boraginaceae). Ann Bot 109:655–665

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Goldberg A (1967) The genus Melochia L. (Sterculiaceae). Contrib US Natl Herbarium 34:191–363

    Google Scholar 

  • Guitián J, Navarro L (1996) Allocation of reproductive resources within inflorescences of Petrocoptis grandiflora (Caryophyllaceae). Can J Bot 74:1482–1486

    Article  Google Scholar 

  • Guitián J, Guitián P, Navarro L (1996) Fruit set, fruit reduction, and the fruiting strategy of Cornus sanguinea (Cornaceae). Am J Bot 83:744–748

    Article  Google Scholar 

  • Herrera CM (1987) Components of pollinator “quality”: comparative analysis of a diverse insect assemblage. Oikos 50:79–90

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ishihama F, Ueno S, Tsumura Y, Washitani I (2006) Effects of density and floral morph on pollen flow and seed reproduction of an endangered heterostylous herb, Primula sieboldii. J Ecol 94:846–855

    Article  Google Scholar 

  • Kato M, Kosaka Y, Kawakita A, Okuyama Y, Kobayashi C, Phimminith T, Thongphan D (2008) Plant-pollinator interactions in New Caledonia influenced by introduced honey bees. Am J Bot 91:1814–1827

    Article  Google Scholar 

  • Knight TM, Steets JA, Ashman TL (2006) A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation. Am J Bot 93:271–277

    PubMed  Article  Google Scholar 

  • Levin DA (1974) Spatial segregation of pins and thrums in populations of Hedyotis nigricans. Evolution 28:648–655

    Article  Google Scholar 

  • Machado IC, Lopes AV (2004) Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest. Ann Bot 94:365–376

    PubMed Central  PubMed  Article  Google Scholar 

  • Machado IC, Sazima M (2008) Pollination and breeding system of Melochia tomentosa L. (Malvaceae), a keystone floral resource in the Brazilian Caatinga. Flora 203:484–490

    Article  Google Scholar 

  • Machado IC, Lopes AV, Sazima M (2006) Plant sexual systems and a review of the breeding system studies in the Caatinga, a Brazilian tropical dry forest. Ann Bot 97:277–287

    PubMed Central  PubMed  Article  Google Scholar 

  • Martin FW (1967) Distyly, self-incompatibility, and evolution in Melochia. Evolution 21:493–499

    Article  Google Scholar 

  • Navarro L (1996) Fruit set and seed weight variation in the herb Anthyllis vulneraria subsp. vulgaris (Fabaceae). Plant Syst Evol 201:139–148

    Article  Google Scholar 

  • Navarro L (1998) Effect of pollen limitation, additional nutrients, flower position and flowering phenology on fruit and seed production in Salvia verbenaca (Lamiaceae). Nord J Bot 18:441–446

    Article  Google Scholar 

  • Nicholls MS (1986) Pollen flow, population composition and the adaptive significance of distyly in Linum tenuifolium L. (Linaceae). Biol J Linn Soc 25:235–242

    Article  Google Scholar 

  • Ornduff R (1980) Heterostyly, population composition, and pollen flow in Hedyotis caerulea. Am J Bot 67:95–103

    Article  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 

  • Ramírez N, Navarro L (2010) Trends in the reproductive biology of Venezuelan Melochia (Malvaceae) species. Plant Syst Evol 289:147–163

    Article  Google Scholar 

  • Rodríguez A (2000) Sterculiaceae. Flora de la república de Cuba, Fascículo 3(4) Serie A, Plantas vasculares. Koeltz Scientific Books, Konigstein

  • Santos-Gally R, González-Voyer A, Arroyo J (2013) Deconstructing heterostyly: the evolutionary role of incompatibility system, pollinators, and floral architecture. Evolution 67:2072–2082

    PubMed  Article  Google Scholar 

  • Schemske DW, Pautler LP (1984) The effects of pollen composition on fitness components in a neotropical herb. Oecologia 62:31–36

    Article  Google Scholar 

  • Schou O (1983) The distyly in Primula elatior (L.) Hill (Primulaceae), with a study of flowering phenology and pollen flow. Bot J Linn Soc 86:261–274

    Article  Google Scholar 

  • Shore JS, Barrett SCH (1984) The effect of pollination intensity and incompatible pollen on seed set in Turnera ulmifolia (Turneraceae). Can J Bot 62:1298–1303

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, website: http://www.r-project.org/

  • Thompson JD, Barrett SCH, Baker AM (2003) Frequency-dependent variation in reproductive success in Narcissus: implications for the maintenance of stigma-height dimorphism. Proc R Soc B 270:949–953

    PubMed Central  PubMed  Article  Google Scholar 

  • van Rossum F, Triest L (2007) Fine-scale spatial genetic structure of the distylous Primula veris in fragmented habitats. Plant Biol 9:374–382

    PubMed  Article  Google Scholar 

  • van Rossum F, Campos de Sousa S, Triest L (2006) Morph-specific differences in reproductive success in the distylous Primula veris in a context of habitat fragmentation. Acta Oecol 30:426–433

    Article  Google Scholar 

  • Waddington KD (1980) Flight patterns of foraging bees relative to density of artificial flowers and distribution of nectar. Oecologia 44:199–204

    Article  Google Scholar 

  • Weber JJ, Weller SG, Sakai AK, Nguyen A, Tai ND, Domínguez CA, Molina-Freaner FE (2012) Purging of inbreeding depression within a population of Oxalis alpina (Oxalidaceae). Am J Bot 99:923–932

    PubMed  Article  Google Scholar 

  • Weber JJ, Weller SG, Sakai AK, Tsyusko OV, Glenn TC, Domínguez CA, Molina-Freaner FE, Fornoni J, Tran M, Nguyen N, Nguyen K, Tran LK, Joice G, Harding E (2013) The role of inbreeding depression and mating system in the evolution of heterostyly. Evolution 67:2309–2322

    PubMed  Article  Google Scholar 

  • Weller SG (1981) Pollination biology of heteromorphic populations of Oxalis alpina (Rose) (Oxalidaceae) in south-eastern Arizona. Bot J Linn Soc 83:189–198

    Article  Google Scholar 

  • Willmer P (2011) Pollination and floral ecology. Princeton University Press, New Jersey

    Book  Google Scholar 

  • Wolfe LM (2001) Associations among multiple floral polymorphisms in Linum pubescens (Linaceae), a heterostylous plant. Int J Plant Sci 162:335–342

    Article  Google Scholar 

  • Yang CF, Sun SG, Guo YH (2005) Resource limitation and pollen source (self and outcross) affecting seed production in two louseworts, Pedicularis siphonantha and P. longiflora (Orobanchaceae). Bot J Linn Soc 147:83–89

    Article  Google Scholar 

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Acknowledgments

We thanks to A. Pérez-Obregón, D. Sánchez and A. Vale for field assistant. We thanks also to A. Vale and D. Rojas for many suggestions for manuscript improvement. This research was supported by DGICYT (CGL2009-10466), FEDER funds from the EU, CYTED (409AC0369), and the Xunta de Galicia (INCITE09-3103009PR). The work of V. Ferrero was funded by a postdoctoral contract of the Xunta de Galicia.

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Correspondence to Luis Navarro.

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Faife-Cabrera, M., Navarro, L. & Ferrero, V. Strength through unity: spatial affinity between morphs improves fitness in incompatible heterostylous Melochia (Malvaceae) species. J Plant Res 128, 139–146 (2015). https://doi.org/10.1007/s10265-014-0668-5

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  • DOI: https://doi.org/10.1007/s10265-014-0668-5

Keywords

  • Heterostyly
  • Nearest-neighbor distance
  • Seed-ovule ratio
  • Segregation pattern
  • Spatial distribution