Architectural constraints, male fertility variation and biased floral morph ratios in tristylous populations


Tristyly is a genetic polymorphism in which populations are comprised of three floral morphs (mating types) differing reciprocally in sex-organ height. Intermorph (disassortative) mating governed by a trimorphic incompatibility system should result in 1:1:1 morph ratios at equilibrium, but both deterministic and stochastic processes can cause skewed morph ratios in tristylous populations. Here, we investigate mechanisms causing morph-ratio bias in Pontederia parviflora, an emergent aquatic native to tropical America. We compared reproductive traits among morphs and surveyed 71 populations to determine patterns of morph-ratio bias. We then used simulation models of morph-frequency dynamics to test the hypothesis that morph-specific differences in pollen production and their influence on male fertility can explain patterns of morph-ratio bias. Ninety-seven percent of populations that we sampled were tristylous, but with a significant excess of the short-styled morph and a deficiency of the long-styled morph. Atypically for a tristylous species, mid-level anthers of the short-styled morph produced over twice as much pollen compared with the corresponding anthers of the long-styled morph. Our computer models incorporating this difference in male fertility resulted in morph ratios not significantly different from the average frequencies from our survey suggesting that the short-styled morph is more successful than the long-styled morph in siring ovules of the mid-styled morph. We propose that the difference in male fertility between morphs may be a non-adaptive consequence of a developmental constraint caused by the architecture of tristyly in Pontederiaceae.

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  1. Ågren J, Ericson L (1996) Population structure and morph-specific fitness differences in tristylous Lythrum salicaria. Evolution 50:126–139

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

  3. Balogh CM, Barrett SCH (2016) Stochastic processes during invasion: the influence of population size on style-morph frequency variation in Lythrum salicaria (purple loosestrife). Int J Plant Sci 177:409–418

  4. Balogh CM, Barrett SCH (2018) Genetic and environmental influences on partial self-incompatibility in Lythum salicaria (Lythaceae). Int J Plant Sci 179:423–425

  5. Barrett SCH (1977a) Tristyly in Eichhornia crassipes (Mart.) Solms (Water Hyacinth). Biotropica 9:230–238

  6. Barrett (1977b) The breeding system of Pontederia rotundifolia L., a tristylous species. New Phytol 78:209–220

  7. Barrett SCH, Anderson JM (1985) Variation in expression of trimorphic incompatibility in Pontederia cordata L. (Pontederiaceae). Theor Appl Genet 70:355–362

  8. Barrett SCH (1989) The evolutionary breakdown of heterostyly. In: Bock JH, Linhart YB eds. The Evolutionary Ecology of Plants. Westview press, Boulder, USA, p 151–169

  9. Barrett SCH, Harder LD, Cole WW (2004) Correlated evolution of floral morphology and mating-type frequencies in a sexually polymorphic plant. Evolution 58:964–975

  10. 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, UK, p 239–255

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

  12. Barrett SCH, Price SD, Shore JS (1983) Male fertility and anisoplethic population structure in tristylous Pontederia cordata (Pontederiaceae). Evolution 37:745–759

  13. Barrett SCH (1993) The evolutionary biology of tristyly. In: Futuyma D, Antonovics J (eds) Oxford Surveys in Evolutionary Biology 9. Oxford University Press, Oxford, UK, p 283–326

  14. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48

  15. Charlesworth D (1979) The evolution and breakdown of tristyly. Evolution 33:486–498

  16. Clarke BC, Partridge L, Robertson A (1988) Frequency-Dependent Selection. Cambridge University Press, New York, NY

  17. Costa J, Castro S, Loureiro J, Barrett SCH (2017) Experimental insights on Darwin’s cross-promotion hypothesis in tristylous purple loosestrife (Lythrum salicaria). Am J Bot 104:616–626

  18. Cunha NL, Fischer E, Lorenz-Lemke AP, Barrett SCH (2014) Floral variation and environmental heterogeneity in a tristylous clonal aquatic of the Pantanal wetlands of Brazil. Ann Bot 114:1637–1649

  19. Darwin C (1877) The Different Form of Flowers on Plants of the Same Species. John Murray, London, UK

  20. Dulberger R (1992) Floral polymorphisms and their functional significance in the heterostylous syndrome. In: Barrett SCH ed. Evolution and Function of Heterostyly. Springer-Verlag, Berlin, p 41–84

  21. Eckert CG, Barrett SCH (1992) Stochastic loss of style morphs from populations of tristylous Lythrum salicaria and Decodon verticillatus. Evolution 46:1014–1029

  22. Eckert CG, Barrett SCH (1993) The inheritance of tristyly in Decodon verticillatus (Lythraceae). Heredity 71:473–480

  23. Eckert CG, Barrett SCH (1995) Style morph ratios in tristylous Decodon verticillatus (Lythraceae): selection vs. historical contingency. Ecology 76:1051–1066

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

  25. Ferrero V, Barrett SCH, Castro S, Caldeirinha P, Navarro L, Loureiro J, Rodríguez-Echeverría (2015) Invasion genetics of the Bermuda buttercup (Oxalis pes-caprae): complex intercontinental patterns of genetic diversity, polyploidy and heterostyly characterize both native and introduced ranges. Mol Ecol 24:2143–2155

  26. Fisher RA (1941) The theoretical consequences of polyploid inheritance for the mid style form of Lythrum salicaria. Ann Eugen 11:31–38

  27. Fisher RA, Mather K (1943) The inheritance of style length in Lythrum salicaria. Ann Eugen 12:1–23

  28. Gettys LA, Wofford DS (2008) Genetic control of floral morph in tristylous Pickerelweed (Pontederia cordata L.). J Hered 99:558–563

  29. Glover DE, Barrett SCH (1983) Trimorphic incompatibility in Mexican populations of Pontederia sagittata Presl. (Pontederiaceae). New Phytol 95:439–455

  30. Heuch I, Lie RT (1985) Genotype frequencies associated with incompatibility systems in tristylous plants. Theor Popul Biol 27:318–336

  31. Heuch I (1979a) Equilibrium populations of heterostylous plants. Theor Popul Biol 15:43–57

  32. Heuch I (1979b) The effect of partial self-fertilization on type frequencies in heterostylous plants. Ann Bot 44:611–616

  33. Heuch I (1980) Loss of incompatibility types in finite populations of the heterostylous plant Lythrum salicaria. Hereditas 92:53–57

  34. 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

  35. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

  36. Husband BC, Barrett SCH (1992) Genetic drift and the maintenance of the style length polymorphism in tristylous populations of Eichhornia paniculata (Pontederiaceae). Heredity 69:440–449

  37. Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70

  38. Lewis D, Jones DA (1992) The genetics of heterostyly. In: Barrett SCH ed. Evolution and Function of heterostyly. Springer-Verlag, Berlin, p 129–150

  39. Lloyd DG, Webb CJ (1992) The evolution of heterostyly. In: Barrett SCH ed. Evolution and Function of heterostyly. Springer-Verlag, Berlin, p 151–178

  40. Lowden RM (1973) Revision of the genus Pontederia. Rhodora 75:426–487

  41. McCauley DE, Brock MT (1998) Frequency‐dependent fitness in Silene vulgaris, a gynodioecious plant. Evolution 52:30–36

  42. Meyer D, Zeileis A, Hornik K (2016) vcd: Visualizing Categorical Data. R package version 1.4-3.

  43. Morgan M (2016) Tristyly: Stochastic Simulation of Tristylous Genetic Polymorphisms. R package version 0.0.1.

  44. Morgan MT, Barrett SCH (1988) Historical factors and anisoplethic population structure in tristylous Pontederia cordata: a re-assessment. Evolution 42:496–504

  45. Ornduff R (1966) The breeding system of Pontederia cordata L. Bull Torre Bot Club 93:407–416

  46. Pott VJ, Pott A (2000) Plantas Aquáticas do Pantanal. Embrapa, Brasília

  47. Puentes A, Cole WW, Barrett SCH (2013) Trimorphic incompatibility in Pontederia subovata (Pontederiaceae): An aquatic macrophyte from lowland South America. Int J Plant Sci 174:47–56

  48. Price SD, Barrett SCH (1982) Tristyly in Pontederia cordata L. (Pontederiaceae). Can J Bot 60:897–905

  49. Richards JH, Barrett SCH (1984) The developmental basis of tristyly in Eichhornia paniculata (Pontederiaceae). Am J Bot 71:1347–1363

  50. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

  51. Richards JH, Barrett SCH (1987) Development of tristyly in Pontederia cordata (Pontederiaceae). I Mature floral structure and patterns of relative growth of reproductive organs. Am J Bot 74:1831–1841

  52. Richards JH, Barrett SCH (1992) The development of heterostyly. In: Barrett SCH ed. Evolution and Function of Heterostyly. Springer-Verlag, Berlin, p 85–127

  53. Sarkar D (2008) Lattice: Multivariate Data Visualization with R. Springer, New York, NY

  54. Sokal RR, Rohlf FJ (2011) Biometry, 4th edn. W. H. Freeman, New York, NY

  55. Vallejo-Marín M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annu Rev Ecol Evol Syst 41:193–213

  56. Weber JF, Weller SG, Sakai AK, Nguyen L-Q, Khuu D (2013a) Breeding system evolution in Oxalis alpina: asymmetrical expression of tristylous incompatibility. Int J Plant Sci 174:179–188

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

  58. Weller SG (1976a) The genetic control of tristyly in Oxalis section Ionoxalis. Heredity 37:387–393

  59. Weller SG (1976b) Breeding system polymorphism in a heterostylous species. Evolution 30:442–454

  60. Wickham H (2007) Reshaping data with the reshape package. J Stat Softw 21:1–20

  61. Wickham H (2009) ggplot2: Elegant Graphics for Data Analysis. 3rd printing, 2010 edn. Springer, New York, NY

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This research was supported by Special Visiting Researcher grant (88881.062191/2014-01) from Science Without Borders Program (CAPES and CNPq) and a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to S.C.H.B. A Special Visiting Researcher grant enabled S.C.H.B. to conduct fieldwork in the Pantanal and support a post-doctoral grant to N.L.C. (88887.067088/2014-00). We thank Milena Delatorre for assistance with field sampling, Martin Morgan for providing software used in our computer simulations, Erich Fischer for encouragement.

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NLC and SCHB planned the research and conducted the fieldwork, NLC analyzed the data and NLC and SCHB wrote the manuscript.

Correspondence to Nicolay Leme da Cunha.

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da Cunha, N.L., Barrett, S.C.H. Architectural constraints, male fertility variation and biased floral morph ratios in tristylous populations. Heredity 123, 694–706 (2019).

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