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Autonomous self-fertilization in Linum sulcatum, a native annual with a previously unknown mating system

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Abstract

The mating systems of wild plant populations have profound effects on their genetic structure and evolution, yet remain unknown or incompletely described for many species. One such species, the herbaceous native annual Linum sulcatum Riddell (Linaceae), is thought to be self-compatible, but there has been no experimental evidence to date to support this claim. To assess the breeding system of this species, seeds were collected from wild populations and reared in a controlled environment. Floral manipulations and controlled pollinations were conducted to determine the degree of self-compatibility of this species and to distinguish between autonomous and facilitated modes of selfing. Additional controlled within- and between-population crosses were conducted to determine the relative degree to which this species can outcross. This study showed that self-fertilization was highly successful and can occur autonomously. In contrast, outcrossing success, both within and between populations, was very limited, suggesting this species may exhibit an extreme degree of cross-incompatibility. A pollen tube growth experiment showed that self-pollination resulted in the formation of more pollen tubes relative to cross-pollination and that complete pollen tube growth can occur less than 2 h following self-pollination. This information is relevant to the future persistence of this species, as much of its remaining habitat is distributed among small, highly fragmented patches subjected to current and future environmental stressors.

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References

  • Armbruster WS, Pérez-Barrales R, Arroyo J, Edwards ME, Vargas P (2006) Three-dimensional reciprocity of floral morphs in wild flax (Linum suffruticosum): a new twist on heterostyly. New Phytol 171:581–590

    PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Barrett SC, Harder LD (2017) The ecology of mating and its evolutionary consequences in seed plants. Annu Rev Ecol Evol Syst 48:135–157

    Article  Google Scholar 

  • Barrett SC, Harder LD, Worley AC (1996) The comparative biology of pollination and mating in flowering plants. Philos Trans Biol Sci 351:1271–1280

    Article  Google Scholar 

  • Biale JB (1964) Growth, maturation, and senescence in fruits: recent knowledge on growth regulation and on biological oxidations has been applied to studies with fruits. Science 146:880–888

    Article  CAS  PubMed  Google Scholar 

  • Bonnin I, Ronfort J, Wozniak F, Olivieri I (2001) Spatial effects and rare outcrossing events in Medicago truncatula (Fabaceae). Molec Ecol 10:1371–1383

    Article  CAS  Google Scholar 

  • Charlesworth D (2003) Effects of inbreeding on the genetic diversity of populations. Philos Trans R Soc Lond B Biol Sci 358:1051–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charlesworth D (2006) Evolution of plant breeding systems. Curr Biol 16:R726–R735

    Article  CAS  PubMed  Google Scholar 

  • Cheptou PO, Hargreaves AL, Bonte D, Jacquemyn H (2017) Adaptation to fragmentation: evolutionary dynamics driven by human influences. Philos Trans R Soc 372:20160037

    Article  Google Scholar 

  • Crnokrak P, Barrett SC (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358

    Article  PubMed  Google Scholar 

  • Cronk Q (2016) Plant extinctions take time. Science 353:446–447

    Article  CAS  PubMed  Google Scholar 

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

    Book  Google Scholar 

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

    Book  Google Scholar 

  • Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292:673–679

    Article  CAS  Google Scholar 

  • Dole JA (1990) Role of corolla abscission in delayed self-pollination of Mimulus guttatus (Scrophulariaceae). Am J Bot 77:1505–1507

    Article  Google Scholar 

  • Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO, Goodwille C et al (2010) Plant mating systems in a changing world. Trends Ecol Evol 25:35–43

    Article  Google Scholar 

  • Edmands S (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53:1757–1768

    Article  PubMed  Google Scholar 

  • Etterson JR, Mazer SJ (2016) How climate change affects plants’ sex lives. Science 353:32–33

    Article  CAS  PubMed  Google Scholar 

  • Etterson JR, Keller SR, Galloway LF (2007) Epistatic and cytonuclear interactions govern outbreeding depression in the autotetraploid Campanulastrum americanum. Evolution 61:2671–2683

    Article  PubMed  Google Scholar 

  • Fenster CB, Galloway LF (2000) Inbreeding and outbreeding depression in natural populations of Chamaecrista fasciculata (Fabaceae). Conserv Biol 14:1406–1412

    Article  Google Scholar 

  • Fisher RA (1941) Average excess and average effect of a gene substitution. Ann Eugen 11:53–63

    Article  Google Scholar 

  • Franklin-Tong VE (2008) Self-incompatibility in flowering plants: evolution, diversity, and mechanisms. Springer, New York

    Book  Google Scholar 

  • Fuentes M, Schupp EW (1998) Empty seeds reduce seed predation by birds in Juniperus osteosperma. Evol Ecol 12:823–827

    Article  Google Scholar 

  • Galen C (2000) High and dry: drought stress, sex-allocation trade-offs, and selection on flower size in the alpine wildflower Polemonium viscosum (Polemoniaceae). Am Nat 156:72–83

    Article  Google Scholar 

  • Glémin S, Bazin E, Charlesworth D (2006) Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc R Soc Lond B Biol Sci 273:3011–3019

    Article  CAS  Google Scholar 

  • Goldberg EE, Kohn JR, Lande R, Robertson KA, Smith SA, Igić B (2010) Species selection maintains self-incompatibility. Science 330:493–495

    Article  CAS  PubMed  Google Scholar 

  • Goodwillie C, Weber J (2018) The best of both worlds? A review of delayed selfing in flowering plants. Am J Bot 105:641–655

    Article  PubMed  Google Scholar 

  • Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Ann Rev Ecol Evol Syst 36:47–79

    Article  Google Scholar 

  • Grossenbacher D, Briscoe Runquist R, Goldberg EE, Brandvain Y (2015) Geographic range size is predicted by plant mating system. Ecol Lett 18:706–713

    Article  PubMed  Google Scholar 

  • Hamrick JL, Godt MW (1996) Effects of life history traits on genetic diversity in plant species. Phil Trans R Soc Lond B Biol Sci 351:1291–1298

    Article  Google Scholar 

  • Harris BD (1968) Chromosome numbers and evolution in North American species of Linum. Am J Bot 55:1197–1204

    Article  Google Scholar 

  • Igic B, Busch JW (2013) Is self-fertilization an evolutionary dead end? New Phytol 198:386–397

    Article  PubMed  Google Scholar 

  • Kalisz S, Vogler DW (2003) Benefits of autonomous selfing under unpredictable pollinator environments. Ecology 84:2928–2942

    Article  Google Scholar 

  • JMP®, Pro, Version 10, SAS Institute Inc., Cary, 1989–2012

  • Kalisz S, Vogler D, Fails B, Finer M, Shepard E, Herman T, Gonzales R (1999) The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae). Am J Bot 86:1239–1247

    Article  CAS  PubMed  Google Scholar 

  • Kalisz SD, Vogler DW, Hanley KM (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884

    Article  CAS  PubMed  Google Scholar 

  • Kearns CA, Inouye DW (1994) Fly pollination of Linum lewisii (Linaceae). Am J Bot 81:1091–1095

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Klips RA, Snow AA (1997) Delayed autonomous self-pollination in Hibiscus laevis (Malvaceae). Am J Bot 84:48–53

    Article  Google Scholar 

  • Kramer AT, Havens K (2009) Plant conservation genetics in a changing world. Trends Plant Sci 14:599–607

    Article  CAS  PubMed  Google Scholar 

  • Kuhn M (1867) Einige Bemerkungen über Vandellia und den Blüten dimorphismus. Bot Zeitung 25:65–67

    Google Scholar 

  • Leimu R, Vergeer P, Angeloni F, Ouborg N (2010) Habitat fragmentation, climate change, and inbreeding in plants. Ann N Y Acad Sci 1195:84–98

    Article  PubMed  Google Scholar 

  • Lloyd DG (1992) Self- and cross-fertilization in plants. II. The selection of self-fertilization. Int J Plant Sci 153:370–380

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lord EM (1981) Cleistogamy: a tool for the study of floral morphogenesis, function and evolution. Bot Rev 47:421–449

    Article  Google Scholar 

  • Mazer SJ, Hove AA, Miller BS, Barbet-Massin M (2010) The joint evolution of mating system and pollen performance: predictions regarding male gametophytic evolution in selfers vs. outcrossers. Perspect Plant Ecol Evol Syst 12:31–41

    Article  Google Scholar 

  • McDill J, Repplinger M, Simpson BB, Kadereit JW (2009) The phylogeny of Linum and Linaceae subfamily Linoideae, with implications for their systematics, biogeography, and evolution of heterostyly. Syst Bot 34:386–405

    Article  Google Scholar 

  • Müller H (1883) The fertilisation of flowers. Macmillan, London

    Book  Google Scholar 

  • Nasrallah JB (2017) Plant mating systems: self-incompatibility and evolutionary transitions to self-fertility in the mustard family. Curr Opin Genet Dev 47:54–60

    Article  CAS  PubMed  Google Scholar 

  • Noël E, Chemtob Y, Janicke T, Sarda V, Pélissié B, Jarne P, David P (2016) Reduced mate availability leads to evolution of self-fertilization and purging of inbreeding depression in a hermaphrodite. Evolution 70:625–640

    Article  PubMed  Google Scholar 

  • Ornduff R (1969) Reproductive biology in relation to systematics. Taxon 1:121–133

    Article  Google Scholar 

  • Petry WK, Soule JD, Iler AM, Chicas-Mosier A, Inouye DW, Miller TE, Mooney KA (2016) Sex-specific responses to climate change in plants alter population sex ratio and performance. Science 353:69–71

    Article  CAS  PubMed  Google Scholar 

  • Qu R, Li X, Luo Y, Dong M, Xu H, Chen X, Dafni A (2007) Wind-dragged corolla enhances self-pollination: a new mechanism of delayed self-pollination. Ann Bot 100:1155–1164

    Article  PubMed  PubMed Central  Google Scholar 

  • Rathcke B, Jules E (1993) Habitat fragmentation and plant-pollinator interactions. Curr Sci 65:273–277

    Google Scholar 

  • Richards AJ (1997) Plant breeding systems. Garland Science, New York

    Book  Google Scholar 

  • Roels SAB, Kelly JK (2011) Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65:2541–2552

    Article  PubMed  Google Scholar 

  • Rogers CM (1963) Yellow flowered species of Linum in eastern North America. Brittonia 15:97–122

    Article  Google Scholar 

  • Rogers CM (1969) Relationships of the North American species of Linum (flax). Bull Torrey Bot Club 96:176–190

    Article  Google Scholar 

  • Rogers CM, Xavier KS (1972) Parallel evolution in pollen structure in Linum. Grana 12:41–46

    Article  Google Scholar 

  • Samson F, Knopf F (1994) Prairie conservation in North America. Bioscience 44:418–421

    Article  Google Scholar 

  • Schoen DJ, Brown A (1991) Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proc Natl Acad Sci 88:4494–4497

    Article  CAS  PubMed  Google Scholar 

  • Schoen DJ, Lloyd DG (1992) Self-and cross-fertilization in plants. III. Methods for studying modes and functional aspects of self-fertilization. Int J Plant Sci 153:381–393

    Article  Google Scholar 

  • Shaw RG, Etterson JR (2012) Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics. New Phytol 195:752–765

    Article  PubMed  Google Scholar 

  • Spira TP, Snow AA, Whigham DF, Leak J (1992) Flower visitation, pollen deposition, and pollen-tube competition in Hibiscus moscheutos (Malvaceae). Am J Bot 79:428–433

    Article  Google Scholar 

  • Stebbins GL (1950) Variation and evolution in plants. Geoffrey Cumberlege, London

    Book  Google Scholar 

  • Stebbins GL (1970) Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annu Rev Ecol Syst 1:307–326

    Article  Google Scholar 

  • Sun SG, Guo YH, Gituru RW, Huang SQ (2005) Corolla wilting facilitates delayed autonomous self-pollination in Pedicularis dunniana (Orobanchaceae). Plant Syst Evol 251:229–237

    Article  Google Scholar 

  • Traveset A (1993) Deceptive fruits reduce seed predation by insects in Pistacia terebinthus L. (Anacardiaceae). Evol Ecol 7:357–361

    Article  Google Scholar 

  • Vogler DW, Kalisz S (2001) Sex among the flowers: the distribution of plant mating systems. Evolution 55:202–204

    Article  CAS  PubMed  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 

  • Williams JH (2012) Pollen tube growth rates and the diversification of flowering plant reproductive cycles. Int J Plant Sci 173:649–661

    Article  Google Scholar 

  • Winn AA, Elle E, Kalisz S, Cheptou PO, Eckert CG, Goodwillie C, Johnston MO et al (2011) Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution 65:3339–3359

    Article  PubMed  Google Scholar 

  • Wright SI, Kalisz S, Slotte T (2013) Evolutionary consequences of self-fertilization in plants. Proc R Soc B 280:20130133

    Article  PubMed  Google Scholar 

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  CAS  PubMed  Google Scholar 

  • Zaremba RE (2003) Linum sulcatum Riddell grooved flax. New England plant conservation program

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Acknowledgements

The authors thank Andrew Olufson for assistance with pollen tube staining, Bryan Bandli for assistance with confocal microscopy, and Sonja Smerud for assistance with the map. This work was supported by the National Science Foundation grant DEB-1142784 to JRE.

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Correspondence to Matthew R. Jahnke.

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Jahnke, M.R., Etterson, J.R. Autonomous self-fertilization in Linum sulcatum, a native annual with a previously unknown mating system. J Plant Res 132, 57–67 (2019). https://doi.org/10.1007/s10265-018-1076-z

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