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Seed germination of gynodioecious species: theoretical considerations and a comparison of females and hermaphrodites

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Abstract

Main conclusion

Better seed germination of females than of hermaphrodites is not a major contributor to the greater geometric lifetime fitness that females require to be maintained in a gynodioecious population.

Abstract

Gynodioecy is a sexually dimorphic breeding system in which females (F, male sterile) and hermaphrodites (H) coexist in the same population. For plants with nuclear (biparental) inheritance of male sterility, theory predicts that except when the product of selfing rate (s) and inbreeding depression (δ) in H is high (sδ > 0.50), F must compensate (female advantage) for the loss of gene transmission via pollen production by producing more or higher-quality offspring than H to be maintained in the population. For species with cytoplasmic (maternal) inheritance of male sterility, the female requires only a small compensation in seed production or some other offspring fitness trait to persist. Reallocation to seeds of resources saved by loss of pollen production is expected to increase the quantity (number) and/or quality (mass, germinability) of seeds produced by F, thus compensating for the lack of pollen production. The primary aim of our study was to compare seed germination of F and H via a literature review. Based on theoretical considerations, we hypothesized that seeds of F should germinate better or equally as well as those of H. We found that of 235 case studies for 47 species Fgerm > Hgerm in 48.1%, Fgerm = Hgerm in 38.3% and Fgerm < Hgerm in 13.6%. Our results are very similar to those of a previously published meta-analysis that included germination of F and H for 12 species. For 162 cases on seed size, F > H in 29.0%, F = H in 63.6% and F < H in 7.4%. Since [(Fgerm > Hgerm) < (Fgerm ≤ Hgerm)] and [(Fseedsize > Hseedsize) < (Fseedsize ≤ Hseedsize)], these results suggest that seed quality is not a major fitness component of female advantage.

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References

  • Adhikari B, Caruso CM, Cage A (2019) Beyond balancing selection: frequent mitochondrial recombination contributes to high female frequency in gynodioecious Lobelia siphilitica (Campanulaceae). New Phytol 224:1381–1393

    CAS  Google Scholar 

  • Ågren J, Willson MF (1991) Gender variation and sexual differences in reproductive characters and seed production in gynodioecious Geranium maculatum. Am J Bot 78:470–480

    Google Scholar 

  • Alonso C, Herrera CM (2001) Neither vegetative nor reproductive advantages account for high frequency of male-steriles in southern Spanish gynodioecious Daphne laureola (Thymelaeaceae). Am J Bot 88:1016–1024

    CAS  Google Scholar 

  • Arroyo MTK, Raven PH (1975) The evolution of subdioecy in morphologically gynodioecious species of Fuchsia sect. Encliandra (Onagraceae). Evolution 29:500–511

    Google Scholar 

  • Ashman T-L (1992) The relative importance of inbreeding and maternal sex in determining progeny fitness in Sidalcea oregana ssp. spicata, a gynodioecious plant. Evolution 46:1862–1874

    Google Scholar 

  • Ashman T-L (1999) Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism. J Evol Biol 12:648–661

    Google Scholar 

  • Ashman T-L (2000) Pollinator selectivity and its implications for the evolution of dioecy and sexual dimorphism. Ecology 81:2577–2591

    Google Scholar 

  • Ashman T-L (2002) The role of herbivores in the evolution of separate sexes from hermaphroditism. Ecology 83:1175–1184

    Google Scholar 

  • Ashman T-L (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, Stanton M (1991) Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregano ssp. spicata (Malvaceae). Ecology 72:993–1003

    Google Scholar 

  • Asikainen E, Mutikainen P (2003) Female frequency and relative fitness of females and hermaphrodites in gynodioecious Geranium sylvaticum (Geraniaceae). Am J Bot 90:226–234

    Google Scholar 

  • Assouad MW, Dommée Lumaret R, Valdeyron G (1978) Reproductive capacities in the sexual forms of the gynodioecious species Thymus vulgaris L. Bot J Linn Soc 77:29–39

    Google Scholar 

  • Bailey M, Delph LF (2007) Sex-ratio evolution in nuclear-cytoplasmic gynodioecy when restoration is a threshold trait. Genetics 176:2465–2476

    Google Scholar 

  • Baker HG (1966) The evolution of floral heteromorphism and gynodioecism in Silene maritima. Heredity 21:689–692

    Google Scholar 

  • Barr CM (2004) Soil moisture and sex ratio in a plant with nuclear-cytoplasmic sex inheritance. Proc R Soc Lond B 271:1935–1939

    Google Scholar 

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

    CAS  Google Scholar 

  • Barrett SCH, Case A, Peters GB (1999) Gender modification and resource allocation in subdioecious Wurmbea dioica (Colchicaceae). J Ecol 87:123–137

    Google Scholar 

  • Baskin CC, Baskin JM (2014) Seeds: ecology, biogeography, and evolution of dormancy and germination, 2nd edn. Elsevier/Academic Press, San Diego

    Google Scholar 

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

    Google Scholar 

  • Belhassen E, Trabaud L, Couvet D (1989) An example of nonequilibrium processes: gynodioecy of Thymus vulgaris L. in burned habitats. Evolution 43:662–667

    CAS  Google Scholar 

  • Bernasconi G, Antonovics J, Biere A, Charlesworth D, Delph LF, Filatov D, Giraud T, Hood ME, Marais GA, McCauley D, Pannell JR, Shykoff JA, Vyskto B, Wolfe LM, Widmer A (2009) Silene as a model system in ecology and evolution. Heredity 103:5–14

    CAS  Google Scholar 

  • Bonnemaison F, Dommée B, Jacquard P, de Preneuf J (1979) Etude experimentale de la concurrence entre forms sexuelles chez la Thym, Thymus vulgaris L. Oecol Plant 14:85–101

    Google Scholar 

  • Bu H, Du G, Chen X, Xu X, Liu K, Wen S (2008) Community-wide germination strategies in an alpine meadow on the eastern Qinghai-Tibet plateau: phylogenetic and life-history correlates. Plant Ecol 195:87–98

    Google Scholar 

  • Caruso CM, Eisen K, Case AL (2016) An angiosperm-wide analysis of the correlates of gynodioecy. Int J Plant Sci 177:115–121

    Google Scholar 

  • Case AL, Ashman TL (2009) Resources and pollinators contribute to population sex-ratio and pollen limitation in Fragaria virginiana (Rosaceae). Oikos 118:1250–1260

    Google Scholar 

  • Case A, Barrett SCH (2001) Ecological differentiation of combined and separate sexes of Wurmbea dioica (Colchicaceae) in sympatry. Ecology 82:2601–2616

    Google Scholar 

  • Case AL, Barrett SCH (2004) Environmental stress and the evolution of dioecy: Wurmbea dioica (Colchicaceae) in Western Australia. Evol Ecol 18:145–164

    Google Scholar 

  • Case AL, Caruso CM (2010) A novel approach to estimating the cost of male fertility restoration in gynodioecious plants. New Phytol 186:549–557

    Google Scholar 

  • Casimiro-Soriguer I, Buide ML, Narbona E (2015) Diversity of sexual systems within different lineages of the genus Silene. AoB Plants 7:plv037

    Google Scholar 

  • Chang S-M (2006) Female compensation through the quantity and quality of progeny in a gynodioecious plant, Geranium maculatum (Geranicaceae). Am J Bot 93:263–270

    Google Scholar 

  • Chang S-M (2007) Gender-specific inbreeding depression in a gynodioecious plant, Geranium maculatum (Geraniaceae). Am J Bot 94:1193–1204

    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-Verlag, Berlin, pp 33–60

    Google Scholar 

  • Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997

    Google Scholar 

  • Charlesworth D, Charlesworth B (1981) Allocation of resources to male and female functions in hermaphrodites. Biol J Linn Soc 15:57–74

    Google Scholar 

  • Cole DH, Ashman T-L (2005) Sexes show differential tolerance to spittlebug damage and consequences of damage for multi-species interactions. Am J Bot 92:1708–1713

    Google Scholar 

  • Collin CL, Shykoff JA (2003) Outcrossing rates in the gynomonoecious-gymnodioecious species Dianthus sylvestris (Caryophyllaceae). Am J Bot 90:579–585

    Google Scholar 

  • Collin CL, Penning PS, Rueffler C, Widmer A (2002) Natural enemies and sex: how seed predators and pathogens contribute to sex-differential reproductive success in a gynodioecious plant. Oecologia 131:94–102

    CAS  Google Scholar 

  • Collin CL, Penet L, Shykoff JA (2009) Early inbreeding depression in the sexually polymorphic plant Dianthus sylvestris (Caryophyllaceae): effects of selfing and biparental inbreeding among sex morphs. Am J Bot 96:2279–2287

    Google Scholar 

  • Connor HE (1963) Breeding systems in New Zealand grasses. IV. Gynodioecism in Cortaderia. N Zeal J Bot 1:258–264

    Google Scholar 

  • Connor HE (1965) Breeding systems in New Zealand grasses. VI. Control of gynodioecism in Cortaderia richardii (Endl.) Zotov. N Zeal J Bot 3:233–242

    Google Scholar 

  • Connor HE (1973) Breeding systems in Cortaderia (Gramineae). Evolution 27:663–678

    CAS  Google Scholar 

  • Couvet D, Bonnemaison F, Gouyon P-H (1986) The maintenance of females among hermaphrodites: the importance of nuclear-cytoplasmic interactions. Heredity 57:325–330

    Google Scholar 

  • Dalton RM, Koski MH, Ashman T-L (2013) Maternal sex effects and inbreeding depression under varied environmental conditions in gynodioecious Fragaria vesca subsp. bracteata. Ann Bot 112:613–621

    CAS  Google Scholar 

  • Darwin C (1897) The different forms of flowers on plants of the same species. D. Appleton and Company, New York

    Google Scholar 

  • De Cauwer I, Arnaud J-F, Schmitt E, Dufay M (2010) Pollen limitation of female reproductive success at fine spatial scale in a gynodioecious and wind-pollinated species, Beta vulgaris ssp. maritima. J Evol Biol 23:2636–2647

    Google Scholar 

  • De Cauwer I, Arnaud J-F, Courseaux A, Dufay M (2011) Sex-specific fitness variation in gynodioecious Beta vulgaris ssp. maritima: do empirical observations fit theoretical predictions? J Evol Biol 24:2456–2472

    Google Scholar 

  • De Cauwer I, Arnaud J-F, Klein EK, Dufay M (2012) Disentangling the causes of heterogeneity in male fecundity in gynodioecious Beta vulgaris ssp. maritima. New Phytol 195:676–687

    Google Scholar 

  • del Castillo RF (1993) Consequences of male sterility in Phacelia dubia. Evol Trends Plants 7:15–22

    Google Scholar 

  • Delph LF (1990) The evolution of gender dimorphism in New Zealand Hebe (Scrophulariaceae) species. Evol Trends Plants 4:85–97

    Google Scholar 

  • Delph LF (2004) Testing for sex differences in biparental inbreeding and its consequences in a gynodioecious species. Am J Bot 91:45–51

    Google Scholar 

  • Delph LF, Carroll SB (2001) Factors affecting relative seed fitness and female frequency in a gynodioecious species, Silene acaulis. Evol Ecol Res 3:487–505

    Google Scholar 

  • Delph LF, Mutikainen P (2003) Testing why the sex of the maternal parent affects seedling survival in a gynodioecious species. Evolution 57:231–239

    Google Scholar 

  • Delph LF, Bailey MF, Marr DL (1999) Seed provisioning in gynodioecious Silene acaulis (Caryophyllaceae). Am J Bot 86:140–144

    CAS  Google Scholar 

  • Delph LF, Touzet P, Bailey MF (2007) Merging theory and mechanism in studies of gynodioecy. Trends Ecol Evol 22:17–24

    Google Scholar 

  • Desfeux C, Henry MS, Lejeune J-P, B, Gouyon P-H, (1996) Evolution of reproductive systems in the genus Silene. Proc R Soc Lond B 263:409–414

    CAS  Google Scholar 

  • Dinnétz P, Jerling L (1997) Gynodioecy in Plantago maritima L.; no compensation for loss of male function. Acta Bot Neerl 46:193–206

    Google Scholar 

  • Dinnétz P, Jerling L (1998) Spatial distribution of male sterility in Plantago maritima. Oikos 81:255–265

    Google Scholar 

  • Dommée B, Jacquard P (1985) Gynodioecy in thyme, Thymus vulgaris L.: evidence from successional populations. In: Jacquard P, Heim G, Antonovics J (eds) Genetic differentiation and dispersal in plants. Springer-Verlag, Berlin, pp 141–164

    Google Scholar 

  • Dornier A, Dufay M (2013) How selfing, inbreeding depression, and pollen limitation impact nuclear-cytoplasmic gynodioecy: a model. Evolution 67:2674–2687

    Google Scholar 

  • Doubleday LAD, Adler LS (2017) Sex-biased oviposition by a nursery pollinator on a gynodioecious host plant: implications for breeding system evolution and evolution of mutualism. Ecol Evol 7:4694–4703

    Google Scholar 

  • Dufay M, Billard E (2012) How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species. Ann Bot 109:505–519

    Google Scholar 

  • Dufay M, Duguen J, Arnaud J-F, Touzet P (2009) Sex ratio variation among gynodioecious populations of sea beet: can it be explained by negative frequency-dependent selection? Evolution 63:1483–1497

    Google Scholar 

  • Dufay M, Lahiani E, Brachi B (2010) Gender variation and inbreeding depression in gynodioecious-gynomonoecious Silene nutans (Caryophyllaceae). Int J Plant Sci 171:53–62

    Google Scholar 

  • Dufay M, Champelovier P, Käfer J, Henry JP, Mousset S, Marais GAB (2014) An angiosperm-wide analysis of the gynodioecy-dioecy pathway. Ann Bot 114:539–548

    CAS  Google Scholar 

  • Dulberger R, Horovitz A (1984) Gender polymorphism in flowers of Silene vulgaris (Moench) Garcke (Caryophyllaceae). Bot J Linn Soc 89:101–117

    Google Scholar 

  • Eckhart VM (1992a) The genetics of gender and the effects of gender on floral characters in gynodioecious Phacelia linearis (Hydrophyllaceae). Am J Bot 79:792–800

    Google Scholar 

  • Eckhart VM (1992b) Resource compensation and the evolution of gynodioecy in Phacelia linearis (Hydrophyllaceae). Evolution 46:1313–1328

    Google Scholar 

  • Ehlers B, Bataillon T (2007) ‘Inconstant males’ and the maintenance of labile sex expression in subdioecious plants. New Phytol 174:194–211

    Google Scholar 

  • Emery SN, McCauley DE (2002) Consequences of inbreeding for offspring fitness and gender in Silene vulgaris, a gynodioecious plants. J Evol Biol 15:1057–1066

    Google Scholar 

  • Fleming TH, Maurice S, Buchmann SL, Tuttle MD (1994) Reproductive biology and relative male and female fitness in a trioecious cactus, Pachycereus pringlei (Cactaceae). Am J Bot 81:858–867

    Google Scholar 

  • Gigord L, Lavigne C, Shykoff JA, Atlan A (1998) No evidence for local adaptation between cytoplasmic male sterility and nuclear restorer genes in the gynodioecious species Thymus vulgaris. Heredity 81:156–163

    Google Scholar 

  • Gigord L, Lavigne C, Shykoff JA, Atlan A (1999) Evidence for effects of restorer genes on male and female reproductive functions of hermaphrodites in the gynodioecious species Thymus vulgaris L. J Evol Biol 12:596–604

    Google Scholar 

  • Godin VN, Demyanova EI (2013) On the distribution of gynodioecy in flowering plants. Bot Zhur 98:1465–1487 (in Russian with English summary)

    Google Scholar 

  • Graff A (1999) Population sex structure and reproductive fitness in gynodioecious Sidalcea malviflora malviflora (Malvaceae). Evolution 53:1714–1722

    Google Scholar 

  • Guitián P, Medrano M (2000) Sex expression and fruit set in Silene littorea (Caryophyllaceae): variation among populations. Nord J Bot 20:467–473

    Google Scholar 

  • Jolls CL, Chenier TC (1989) Gynodioecy in Silene vulgaris (Caryophyllaceae): progeny success, experimental design, and maternal effects. Am J Bot 76:1360–1367

    Google Scholar 

  • Jordano P (1993) Pollination biology of Prunus mahaleb L.: deferred consequences of gender variation for fecundity and seed size. Biol J Linn Soc 50:65–84

    Google Scholar 

  • Kaul MLH (1988) Male sterility in higher plants. Springer-Verlag, Berlin

    Google Scholar 

  • Kay QON (1985) Hermaphrodites and subhermaphrodites in a reputedly dioecious plant, Cirsium arvense (L.) Scop. New Phytol 100:457–472

    Google Scholar 

  • Keller SR, Schwaegerle KE (2006) Maternal sex and mate relatedness affect offspring quality in the gynodioecious Silene acaulis. J Evol Biol 19:1128–1138

    CAS  Google Scholar 

  • Kikuzawa K (1989) Floral biology and evolution of gynodioecism in Daphne kamtchatica var. jezoensis. Oikos 56:196–202

    Google Scholar 

  • Klinkhamer PGL, de Jong TJ, Wesselingh R (1991) Implications of differences between hermaphrodite and female flowers for attractiveness to pollinators and seed production. Neth J Zool 41:130–143

    Google Scholar 

  • Klinkhamer PGL, de Jong TJ, Nell HW (1994) Limiting factors for seed production and phenotypic gender in the gynodioecious species Echium vulgare (Boraginaceae). Oikos 71:469–478

    Google Scholar 

  • Koelewijn HP (1996) Sexual differences in reproductive characters in gynodioecious Plantago coronopus. Oikos 75:443–452

    Google Scholar 

  • Koelewijn HP, Van Damme JMM (1996) Gender variation, partial male sterility and labile sex expression in gynodioecious Plantago coronopus. New Phytol 132:67–76

    Google Scholar 

  • Koelewijn HP, Van Damme JMM (2005) Effects of seed size, inbreeding and maternal sex on offspring fitness in gynodioecious Plantago coronopus. J Ecol 93:373–383

    Google Scholar 

  • Kohn JR (1989) Sex ratio, seed production, biomass allocation, and the cost of male function in Cucurbita foetidissima HBK (Cucurbitaceae). Evolution 43:1424–1434

    Google Scholar 

  • Koide RT (2010) Mycorrhizal symbiosis and plant reproduction. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function, 2nd edn. Springer, Dordrecht, pp 297–320

    Google Scholar 

  • Krohne DT, Baker I, Baker HG (1980) The maintenance of the gynodioecious breeding system in Plantago lanceolata. Am Midl Nat 103:269–279

    Google Scholar 

  • Lafuma L, Maurice S (2006) Reproductive characters in a gynodioecious species, Silene italica (Caryophyllaceae), with attention to the gynomonoecious phenotype. Biol J Linn Soc 87:583–591

    Google Scholar 

  • Leishman MR, Westoby M (1994) Hypotheses on seed size: tests using the semiarid flora of western New South Wales, Australia. Am Nat 143:890–906

    Google Scholar 

  • Lewis D (1941) Male sterility in natural populations of hermaphrodite plants. The equilibrium between females and hermaphrodites to be expected with different types of inheritance. New Phytol 40:56–63

    Google Scholar 

  • Lloyd DG (1974) Theoretical sex ratios of dioecious and gynodioecious angiosperms. Heredity 31:11–34

    Google Scholar 

  • Lloyd DG (1976) The transmission of genes via pollen and ovules in gynodioecious angiosperms. Theor Popul Biol 9:299–316

    CAS  Google Scholar 

  • Lloyd DG (1979) Parental strategies of angiosperms. N Zeal J Bot 17:595–606

    Google Scholar 

  • Lloyd DG (1980) Sexual strategies in plants. III. A quantitative method for describing the gender of plants. N Zeal J Bot 18:103–108

    Google Scholar 

  • Lloyd DG, Bawa KS (1984) Modification of the gender of seed plants in varying conditions. Evol Biol 17:255–338

    Google Scholar 

  • Lloyd DG, Myall AJ (1976) Sexual dimorphism in Cirsium arvense (L.) Scop. Ann Bot 40:115–123

    Google Scholar 

  • López-Villavicencio M, Genton BJ, Porcher E, Shykoff JA (2005) The role of pollination level on the reproduction of females and hermaphrodites in the gynodioecious plant Gypsophila repens (Caryophyllaceae). Am J Bot 92:1995–2002

    Google Scholar 

  • Manicacci D, Couvet D, Belhassen E, Gouyon P-H, Atlan A (1996) Founder effects and sex ratio in the gynodioecious Thymus vulgaris L. Mol Ecol 5:63–72

    Google Scholar 

  • Manicacci D, Atlan A, Rossello JAE, Couvet D (1998) Gynodioecy and reproductive trait variation in three Thymus species (Lamiaceae). Int J Plant Sci 159:948–957

    Google Scholar 

  • Marr DL (2006) Seed Fitness of hermaphrodites in areas with females and anther smut disease: Silene acaulis and Microbotryum violaceum. New Phytol 169:741–752

    Google Scholar 

  • Marshall M, Ganders FR (2001) Sex-biased seed predation and the maintenance of females in a gynodioecious plant. Am J Bot 88:1437–1443

    CAS  Google Scholar 

  • Maurice S (1999) Gynomonoecy in Silene italica (Caryophyllaceae): sexual phenotypes in natural populations. Plant Biol 1:346–350

    Google Scholar 

  • Maurice S, Desfeux C, Migno A, Henry J-P (1998) Is Silene acaulis (Caryophyllaceae) a trioecious species? Reproductive biology of two subspecies. Can J Bot 76:478–485

    Google Scholar 

  • McCall AC, Barr CM (2012) Why do florivores prefer hermaphrodites over females in Nemophila menziesii (Boraginaceae)? Oecologia 170:147–157

    Google Scholar 

  • McCauley DE, Bailey MF (2009) Recent advances in the study of gynodioecy: the interface of theory and empiricism. Ann Bot 104:611–620

    Google Scholar 

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

    Google Scholar 

  • McCauley DE, Olson MS, Emery SN, Taylor DR (2000) Population structure influences sex ratio evolution in a gynodioecious plant. Am Nat 155:814–819

    Google Scholar 

  • McCusker A (1962) Gynodioecism in Leucopogon melaleucoides A. Cunn. Proc Linn Soc N S Wales 87:286–289

    Google Scholar 

  • Miyake K, Olson MS (2009) Experimental evidence for frequency dependent self-fertilization in the gynodioecious plant, Silene vulgaris. Evolution 63:1644–1652

    Google Scholar 

  • Miyake K, Miyake T, Terachi T, Yahara T (2009) Relative fitness of females and hermaphrodites in a natural gynodioecious population of wild radish, Raphanus sativus L. (Brassicaceae): comparison based on molecular genotyping. J Evol Biol 22:2012–2019

    CAS  Google Scholar 

  • Miyake T, Satake I, Miyake K (2018) Sex-biased seed predation in gynodioecious Dianthus superbus var. longicalycinus (Caryophyllaceae) and differential influence of two seed predator species on the floral traits. Plant Species Biol 33:42–50

    Google Scholar 

  • Molina-Freaner F, Jain SK (1992) Female frequencies and fitness components between sex phenotypes among gynodioecious populations of the colonizing species Trifolium hirtum All. in California. Oecologia 92:279–286

    CAS  Google Scholar 

  • Molina-Freaner F, Cervantes-Salas M, Morales-Romero D, Buchmann S, Fleming TH (2003) Does the pollinator abundance hypothesis explain geographic variation in the breeding system of Pachycereus pringlei? Int J Plant Sci 164:383–393

    Google Scholar 

  • Mutikainen P, Delph LF (1998) Inbreeding depression in gynodioecious Lobelia siphiliticia: among-family differences override between-morph differences. Evolution 52:1572–1582

    Google Scholar 

  • Nilsson E, Ågren J (2006) Population size, female fecundity, and sex ratio variation in gynodioecious Plantago maritima. J Evol Biol 19:825–833

    Google Scholar 

  • Norden N, Daws MI, Antoine C, Gonzalea M, Garwood NC, Chave J (2009) The relationship between seed mass and mean time to germination for 1037 tree species across five tropical forests. Funct Ecol 23:203–210

    Google Scholar 

  • Olson MS, McCauley DE, Taylor D (2005) Genetics and adaptation in structured populations: sex ratio evolution in Silene vulgaris. Genetica 123:49–62

    Google Scholar 

  • Olson MS, Gra AV, Niles KR (2006) Fine scale spatial structuring of sex and mitochondria in Silene vulgaris. J Evol Biol 19:1190–1201

    CAS  Google Scholar 

  • Pettersson MW (1992) Advantages of being a specialist female in gynodioecious Silene vulgaris s.l. (Caryophyllaceae). Am J Bot 79:1389–1395

    Google Scholar 

  • Philipp M (1980) Reproductive biology of Stellaria longipes Goldie as revealed by a cultivation experiment. New Phytol 85:557–569

    Google Scholar 

  • Pickering CM, Ash JE (1993) Gender variation in hermaphrodite plants: evidence from five species of alpine Ranunculus. Oikos 68:539–548

    Google Scholar 

  • Primack RB, Lloyd DG (1980) Sexual strategies in plants. IV. The distributions of gender in two monomorphic shrub populations. N Zeal J Bot 18:109–114

    Google Scholar 

  • Puterbaugh M, Wied A, Galen C (1997) The functional ecology of gynodioecy in Eritrichium aretioides (Boraginaceae), the alpine forget-me-not. Am J Bot 84:393–400

    CAS  Google Scholar 

  • Ramsey M, Vaughton G (2002) Maintenance of gynodioecy in Wurmbea biglandulosa (Colchicaceae): gender differences in seed production and progeny success. Plant Syst Evol 232:189–200

    Google Scholar 

  • Ramula S, Mutikainen P (2003) Sex allocation of females and hermaphrodites in the gynodioecious Geranium sylvaticum. Ann Bot 92:207–213

    Google Scholar 

  • Ramula S, Toivonen E, Mutikainen P (2007) Demographic consequences of pollen limitation and inbreeding depression in a gynodioecious herb. Int J Plant Sci 168:443–453

    Google Scholar 

  • Rees M (1993) Trade-offs among dispersal strategies in British plants. Nature 366:150–152

    Google Scholar 

  • Rees M (1994) Delayed germination of seeds: a look at the effects of adult longevity, the timing of reproduction, and population age/stage structure. Am Nat 144:43–64

    Google Scholar 

  • Rees M (1996) Evolutionary ecology of seed dormancy and seed size. Philos Trans R Soc Lond B 351:1299–1308

    Google Scholar 

  • Renner SS (2014) The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am J Bot 101:1588–1596

    Google Scholar 

  • Robertson AW, Kelly D, Ladley JJ (2011) Futile selfing in the trees Fuchsia excorticata (Onagraceae) and Sophora microphylla (Fabaceae): inbreeding depression over 11 years. Int J Plant Sci 172:191–219

    Google Scholar 

  • Ruffatto DM, Zaya DN, Molano-Flores B (2015) Reproductive success of the gynodioecious Lobelia spicata Lam. (Campanulaceae): female frequency, population demographics, and latitudinal patterns. Int J Plant Sci 176:120–130

    Google Scholar 

  • Sakai AK, Weller S (1999) Gender and sexual dimorphism in flowering plants: a review of terminology, biogeographic patterns, ecological correlates, and phylogenetic approaches. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer-Verlag, Berlin, pp 1–31

    Google Scholar 

  • Sakai A, Wagner WL, Ferguson DM, Herbst DR (1995) Origins of dioecy in the Hawaiian flora. Ecology 76:2517–2529

    Google Scholar 

  • Sakai AK, Weller SG, Chen M-L, Chou SY, Tasanont C (1997) Evolution of gynodioecy and maintenance of females: the role of inbreeding depression, outcrossing rates, and resource allocation in Schiedea adamantis (Caryophyllaceae). Evolution 51:724–736

    Google Scholar 

  • Schat H (1981) Seed polymorphism and germination ecology of Plantago coronopus L. Acta Oecol 2:367–380

    Google Scholar 

  • Schrader PJ (1986) Gynodioecy in Minuartia obtusiloba (Rydb.) House on Pennsylvania Mountain, Colorado. Ph.D. Thesis. University of California, Berkeley

  • Schultz ST (2003) Sexual dimorphism in gynodioecious Sidalcea hirtipes (Malvaceae). I. Seed, fruit, and ecophysiology. Int J Plant Sci 164:165–173

    Google Scholar 

  • Schultz ST, Ganders FR (1996) Evolution of unisexuality in the Hawaiian flora. A test of microevolutionary theory. Evolution 50:842–855

    Google Scholar 

  • Shykoff JA (1988) Maintenance of gynodioecy in Silene acaulis (Caryophyllaceae): stage-specific fecundity and viability selection. Am J Bot 7:844–850

    Google Scholar 

  • Shykoff JA, Kolokotronis SO, Collin CL, López-Villavicencio M (2003) Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135:1–9

    Google Scholar 

  • Sosa VJ, Fleming TH (1999) Seedling performance in a trioecious cactus, Pachycereus pringlei: effects of maternity and paternity. Plant Syst Evol 218:145–151

    Google Scholar 

  • Spigler RB, Ashman T-L (2012) Gynodioecy to dioecy: are we there yet? Annu Bot 109:531–543

    Google Scholar 

  • Stevens DP (1988) On the gynodioecious polymorphism in Saxifraga granulata L. (Saxifragaceae). Biol J Linn Soc 35:15–28

    Google Scholar 

  • Stevens DP, Richards AJ (1985) Gynodioecy in Saxifraga granulata L. (Saxifragaceae). Plant Syst Evol 151:43–54

    Google Scholar 

  • Sun M, Ganders FR (1986) Female frequencies in gynodioecious populations correlated with selfing rates in hermaphrodites. Am J Bot 73:1645–1648

    Google Scholar 

  • Sun M, Ganders FR (1988) Mixed mating systems in Hawaiian Bidens (Asteraceae). Evolution 42:516–527

    CAS  Google Scholar 

  • Svoen ME, Müller E, Brysting AK, Kålås IH, Eidesen PB, (2019) Female advantage? Investigating female frequency and establishment performance in high-Arctic Silene acaulis. Botany 97:245–261

    Google Scholar 

  • Taylor DR, Trimble S, McCauley DE (1999) Ecological genetics of gynodioecy in Silene vulgaris: relative fitness of females and hermaphrodites during the colonization process. Evolution 53:745–751

    Google Scholar 

  • Thompson JD, Tarayre M (2000) Exploring the genetic basis and proximate causes of female fertility advantage in gynodioecious Thymus vulgaris. Evolution 54:1510–1520

    CAS  Google Scholar 

  • Uno GE (1982) Ccomparative reproductive biology of hermaphroditic and male-sterile Iris douglasiana Herb. (Iridaceae). Am J Bot 69:818–823

    Google Scholar 

  • Vaarama A, Jääskeläinen O (1967) Studies on gynodioecium in the Finnish populations of Geranium silvaticum L. Ann Acad Sci Fenn Biol 108:2–39

    Google Scholar 

  • Van Damme JMM, Van Delden W (1984) Gynodioecy in Plantago lanceolata L. IV. Fitness components of sex types in different life cycle stages. Evolution 38:1326–1336

    Google Scholar 

  • Van Etten ML, Prevost LB, Deen AC, Ortiz BV, Donovan LA, Chang S-M (2008) Gender differences in reproductive and physiological traits in an gynodioecious species, Geranium maculatum (Genaniaceae). Int J Plant Sci 169:271–279

    Google Scholar 

  • Varga S (2014) Pre-dispersal seed predation in gynodioecious Geranium sylvaticum is not affected by plant gender or flowering phenology. Arthropod Plant Interact 8:253–260

    Google Scholar 

  • Varga S, Kytöviita M-M (2010a) Mycorrhizal benefit differs among the sexes in a gynodioecious species. Ecology 91:2583–2593

    Google Scholar 

  • Varga S, Kytöviita M-M (2010b) Gender dimorphism and mycorrhizal symbiosis affect floral visitors and reproductive output in Geranium sylvaticum. Funct Ecol 24:750–758

    Google Scholar 

  • Varga S, Vega-Frutis R, Kytöviita M-M (2013) Transgenerational effects of plant sex and arbuscular mycorrhizal symbiosis. New Phytol 199:812–821

    Google Scholar 

  • Varga S, Laaksoneen E, Siikamäki P, Kytöviita M-M (2015) Absence of sex differential plasticity to light availability during seed maturation in Geranium sylvaticum. PLoS ONE 10:e0118981

    Google Scholar 

  • Vaughton G, Ramsey M (2004) Dry environments promote the establishment of females in monomorphic populations of Wurmbea biglandulosa (Colchicaceae). Evol Ecol 18:323–341

    Google Scholar 

  • Venable DL, Brown JS (1988) The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments. Am Nat 131:360–384

    Google Scholar 

  • Wagner W, Weller SG, Sakai AK (2005) Monograph of Schiedea (Caryophyllaceae-Alsinoideae). Syst Bot Monogr 72:1–169

    Google Scholar 

  • Webb CJ (1979) Breeding system and seed set in Euonymus europaeus (Celastraceae). Plant Syst Evol 132:299–303

    Google Scholar 

  • Webb CJ (1981a) Gynodioecy in Gingidia flabellata (Umbelliferae). N Zeal J Bot 19:111–113

    Google Scholar 

  • Webb CJ (1981b) Test of a model predicting equilibrium frequencies of females in populations of gynodioecious angiosperms. Heredity 46:397–405

    Google Scholar 

  • Webb CJ (1999) Empirical studies: evolution and maintenance of dimorphic breeding systems. In: Geber MA, Dawson TE, Delph LF (eds) Gender and sexual dimorphism in flowering plants. Springer-Verlag, Berlin, pp 61–95

    Google Scholar 

  • Weller SG, Sakai AK (2005) Selfing and resource allocation in Schiedea salicaria (Caryophyllaceae), a gynodioecious species. J Evol Biol 18:301–308

    CAS  Google Scholar 

  • Widén M (1992) Sexual reproduction in a clonal, gynodioecious herb Glechoma hederacea. Oikos 63:430–438

    Google Scholar 

  • Williams CR, Kuchenreuther MA, Drew A (2000) Floral dimorphism, pollination, and self-fertilization in gynodioecious Geranium richardsonii (Geraniaceae). Am J Bot 87:661–669

    CAS  Google Scholar 

  • Wolfe LM, Burns JL (2001) A rare continual flowering strategy and its influence on offspring quality in a gynodioecious plant. Am J Bot 88:1419–1423

    CAS  Google Scholar 

  • Wolfe LM, Shmida A (1997) The ecology of sex expression in a gynodioecious Israeli desert shrub (Ochradenus baccatus). Ecology 78:101–110

    Google Scholar 

  • Wolff K, Friso B, Van Damme JMM (1988) Outcrossing rates and male sterility in natural populations of Plantago coronopus. Theor Appl Genet 76:190–196

    CAS  Google Scholar 

  • Yampolsky C, Yampolsky H (1922) Distribution of sex forms in the phanerogamic flora. Bibliotheca Genet 3:1–62

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of Kentucky, Lexington, KY, 40506-0225, USA

    Jerry M. Baskin & Carol C. Baskin

  2. Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, 40546-0312, USA

    Carol C. Baskin

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  1. Jerry M. Baskin
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Correspondence to Carol C. Baskin.

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Appendices

Appendix 1

Comparison of the F/H relationships for seed germination of 24 species in present study with those included in reviews by Shykoff et al. (2003) and Dufay and Billard (2012). F female, H hermaphrodite, cms cytoplasmic male sterility. For present study, numbers in parentheses indicate number of case studies.

Family/species

Shykoff et al. (2003)

Dufay and Billard (2012)

This study

Amaranthaceae

 Beta vulgaris subsp. maritima

–

F = H

Fcms = Hrestored cms (1) Fcms = Hnon-cms (1)

Boraginaceae

 Echium vulgare

–

F = H

F = H (1)

 Eritichium aretioides

–

F > H

F > H (1)

 Phacelia dubia var. dubia

F < H

–

F < H (1)

 Phacelia linearis

–

F = H

F > H (8), F = H (2), F < H (6)

Brassicaceae

 Raphanus sativus

–

F < H

Fcms = Hcms (1), Fcms < Hnon-cms (1)

Caryophyllaceae

 Dianthus sylvestris

F = H

F = H

F = H (1)

 Schiedea adamantis

F > H, F = H

F = H

F > H (2)

 Schiedea salicaria

–

F > H, F = H

F > H (8)

 Silene acaulis

F = H

–

F = H (12)

 Silene vulgaris

–

F = H

F > H (12), F = H (17), F < H (3)

Colchicaceae

 Wurmbea biglandulosa subsp. biglandulosa

–

F > H

F > H (3)

Fabaceae

 Trifolium hirtum

F = H

–

F = H (4)

Geraniaceae

 Geranium maculatum

–

F > H, F = H

F > H (2), F = H (1), F < H (1)

 Geranium sylvaticum

–

F = H

F > H (2), F = H (1), F < H (1)

Lamiaceae

 Thymus vulgaris

F > H

F > H

F > H (34), F = H (3), F < H (5)

Plantaginaceae

 Plantago lanceolata

–

F = H

F = H (1)

 Plantago maritima

F < H

–

F < H (1), F < H (1)

Poaceae

 Cortaderia richardii

F > H

F > H

F > H (2), F = H (1)

 Cortaderia selloana

F > H

–

F > H (1)

Rosaceae

 Prunus mahaleb

F = H

F = H

F = H (1)

Saxifragaceae

 Saxifraga granulata

–

F > H

F > H (2)

Resedaceae

 Ochradenus baccatus

F > H

–

F > H (3)

Thymelaeaceae

 Daphnus laureola

F = H

–

F > H (2)

Appendix 2

A selected sample of comparisons of our results using relative performance (RP, as described in “Materials and methods”) and results (ns nonsignificant, s significant) of statistical tests (p) by authors of 11 papers (21 case studies) for germination of females and males; agree (yes or no), do RP and p agree?

Paper

RP

p

Agree

Alonzo and Herrera (2001)

0.36

ns

No

Ashman (1992)

 Greenhouse

0.26

s

Yes

 Field

− 0.08

ns

Yes

Dalton et al. (2013)

0.04

s

No

Dinnétz and Jerling (1997)

− 0.12

s

Yes

Jordano (1993)

− 0.04

ns

Yes

Lopez-Villavicencio et al. (2005)

− 0.10

s

Yes

McCauley et al. (2000)

0.14

ns

No

Ramsey and Vaughton (2002)

0.11

ns

No

Stevens (1988)

 Experiment 1

0.24

ns

No

 Experiment 2

0.26

ns

No

Webb (1981b)

 Species 1

0.08

ns

Yes

 Species 2

− 0.13

ns

No

Weller and Sakai (2005)

 Population 1a

0.57

s

Yes

 Population 2

0.20

ns

No

 Population 3

0.34

ns

No

 Population 4

0.23

ns

No

 Population 5

0.23

s

Yes

 Population 6

0.20

ns

No

 Population 7

0.48

s

Yes

 Population 8

0.32

s

Yes

  1. aPopulations of Schiedea salicaria

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Baskin, J.M., Baskin, C.C. Seed germination of gynodioecious species: theoretical considerations and a comparison of females and hermaphrodites. Planta 252, 73 (2020). https://doi.org/10.1007/s00425-020-03472-5

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