Are hermaphrodites better adapted to the colonization process in trioecious populations of Salix myrsinifolia?

Paweł Mirski, Emilia Brzosko

Abstract


In trioecious plant populations, the role of hermaphroditism is often uncertain. We investigated the advantages of hermaphroditism in the dioecious shrub Salix myrsinifolia. The sex ratio of 30 S. myrsinifolia populations in northeastern Poland (secondary range) and Lithuania (primary range) was investigated in 2010–2011. Measures of reproductive (number of catkins, number of flowers in catkins) and vegetative traits (height, diameter, number of shoots, vitality) were taken and compared among sexual morphs. In two populations, measurements collected 14 years prior on marked individuals were used to determine the rate of changes in height, crown diameter and survivorship rates. We found trioecy mostly in the secondary part of the range with an average share of hermaphrodites reaching 21% in the trioecious populations. The sex ratio varied between populations, but tended mostly towards female domination. Several traits differed significantly among sexes. The characteristics of hermaphrodites were often intermediate between males and females and provided no evidence for the higher competitive abilities of hermaphrodites. We concluded that the possible gain of hermaphroditism in the colonization process is restricted to reproduction. We consider hermaphroditism in S. myrsinifolia as an equilibrium between the allocation of resources for growth and reproduction in unstable conditions on the margins of the range.

Keywords


subdioecy; polygamy; plant gender; size structure; sexual trimorphism; sex ratio

Full Text:

PDF

References


Dawson TE, Geber MA. Sexual dimorphism in physiology and morphology. In: Geber MA, Dawson TE, Delph LF, editors. Gender and sexual dimorphism in flowering plants. Berlin: Springer-Verlag; 1999. p. 176–215. http://dx.doi.org/10.1007/978-3-662-03908-3_7

Barrett SCH, Hough J. Sexual dimorphism in flowering plants. J Exp Bot. 2013;64:67–82. http://dx.doi.org/10.1093/jxb/ers308

Ågren J, Danell K, Elmqvist T, Ericson L, Hjältén J. Sexual dimorphism and biotic interactions. In: Geber MA, Dawson TE, Delph LF, editors. Gender and sexual dimorphism in flowering plants. Berlin: Springer-Verlag; 1999. p. 217–246. http://dx.doi.org/10.1007/978-3-662-03908-3_8

Cornelissen T, Stirling P. Sex-biased herbivory: a metaanalysis of the effects of gender on plant–herbivore interactions. Oikos. 2005;111:488–500. http://dx.doi.org/10.1111/j.1600-0706.2005.14075.x

Ashman TL. The role of herbivores in the evolution of separate sexes from hermaphroditism. Ecology. 2002;83:1175–1184. http://dx.doi.org/10.2307/3071932

Bierzychudek P, Eckhart V. Spatial segregation of the sexes in dioecious plants. Am Nat. 1988;132:34–43. http://dx.doi.org/10.1086/284836

Mercer CA, Eppley SM. Inter-sexual competition in a dioecious grass. Oecologia. 2010;164:657–664. http://dx.doi.org/10.1007/s00442-010-1675-4

Obeso JR. The costs of reproduction in plants. New Phytol. 2002;155:321–348. http://dx.doi.org/10.1046/j.1469-8137.2002.00477.x

Freeman DC, Harper KT, Charnov EL. Sex change in plants: old and new observations and new hypotheses. Oecologia. 1980;47:222–232. http://dx.doi.org/10.1007/BF00346825

Bierzychudek P. Determinants of gender in Jack-in-the-pulpit: the influence of plant size and reproductive history. Oecologia. 1984;65:14–18. http://dx.doi.org/10.1007/BF00384456

Iszkuło G, Jasińska AK, Romo A, Tomaszewski D, Szmyt J. The greater growth rate of male over female of the dioecious tree Juniperus thurifera only in worse habitat conditions. Dendrobiology. 2011;66:15–24.

Klinkhamer PGL, de Jong TJ, Metz H. Sex and size in cosexual plants. Trends Ecol Evol. 1997;12:260–265. http://dx.doi.org/10.1016/S0169-5347(97)01078-1

Lloyd DG, Bawa KS. Modification of gender of seed plants in varying conditions. Evol Biol. 1984;17:255–338. http://dx.doi.org/10.1007/978-1-4615-6974-9_6

Weiner J, Thomas SC. Size variability and competition in plant monocultures. Oikos. 1986;47:211–222. http://dx.doi.org/10.2307/3566048

Leverich WJ, Levin DA. Age-specific survivorship and reproduction in Phlox drummondii. Am Nat. 1979;113:881–903. http://dx.doi.org/10.1086/283443

Watkinson AR, Lonsdale WM, Firbank LG. A neighbourhood approach to self-thinning. Oecologia. 1983;56:381–384. http://dx.doi.org/10.1007/BF00379716

Horvitz CC, Schemske DW. Leaf herbivory and neighbourhood competition in a neotropical herb: effects on demographic fates. J Ecol. 2002;90:279–290. http://dx.doi.org/10.1046/j.1365-2745.2001.00660.x

Ashman TL. The evolution of separate sexes: a focus on the ecological context. In: Harder LD, Barrett SCH, editors. Ecology and evolution of flowers. Oxford: Oxford University Press; 2006. p. 204–222.

Bawa KS. Evolution of dioecy in flowering plants. Annu Rev Ecol Syst. 1980;11:15–39. http://dx.doi.org/10.1146/annurev.es.11.110180.000311

Mirski P. Exceptions from dioecy and sex lability in genus Salix. Dendrobiology. 2014;71:167–171. http://dx.doi.org/10.12657/denbio.071.017

Primack RB, McCall C. Gender variation in a red maple population (Acer rubrum; Aceraceae): a seven-year study of a polygamodioecious species. Am J Bot. 1986;73:1239–1248. http://dx.doi.org/10.2307/2444057

Ushimaru A, Matsui K. Sex change in tree species: long-term monitoring of sex expression in Acer rufinerve. Nord J Bot. 2001;21:397–399. http://dx.doi.org/10.1111/j.1756-1051.2001.tb00785.x

Mędrzycki P, Kołaszewska B, Browiński P. Subdioecy in invasive populations of Acer negundo (Aceraceae) in eastern Poland. Pol Bot Stud. 2006;22:355–364.

Iszkuło G, Jasińska AK.Variation in sex expression in Polish and Ukrainian populations of Taxus baccata L. Dendrobiology. 2004;52:29–32.

Rottenberg A. Fertility of exceptional bisexual individuals in four dioecious plant species. Sex Plant Reprod. 2000;12:219–221. http://dx.doi.org/10.1007/s004970050003

Dorken ME, Pannell JR. Hermaphrodite sex allocation evolves when mating opportunities change. Curr Biol. 2009;19:514–517. http://dx.doi.org/10.1016/j.cub.2009.01.067

Yu L, Lu J. Does landscape fragmentation influence sex ratio of dioecious plants? A case study of Pistacia chinensis in the Thousand-Island Lake region of China. PLoS ONE. 2011;6(8):e22903. http://dx.doi.org/10.1371/journal.pone.0022903

Ehlers BK, Bataillon T. “Inconstant males” and the maintenance of labile sex expression in subdioecious plants. New Phytol. 2007;174:194–211. http://dx.doi.org/10.1111/j.1469-8137.2007.01975.x

Faliński JB. Androgyny of individuals and polygamy in populations of Salix myrsinifolia Salisb. in the south-western part of its geographical range (NE-Poland). Perspect Plant Ecol Evol Syst. 1998;1:238–266. http://dx.doi.org/10.1078/1433-8319-00061

Charnov EL, Maynard Smith J, Bull JJ. Why be an hermaphrodite? Nature. 1976;263:125–126. http://dx.doi.org/10.1038/263125a0

Nanami S, Kawaguchi H, Yamakura T. Sex change towards female in dying Acer rufinerve trees. Ann Bot. 2004;93:733–740. http://dx.doi.org/10.1093/aob/mch093

Barrett SCH, Case AL, Peters GB. Gender modification and resource allocation in subdioecious Wurmbea dioica (Colchicaceae). J Ecol. 1999;87:123–137. http://dx.doi.org/10.1046/j.1365-2745.1999.00336.x

Sarkissian TS, Barrett SCH, Harder LD. Gender variation in Sagittaria latifolia (Alismataceae): is size all that matters? Ecology. 2001;82:360–373. http://dx.doi.org/10.2307/2679865

Pannell JR. The maintenance of gynodioecy and androdioecy in a metapopulation. Evolution. 1997;51:10–20. http://dx.doi.org/10.2307/2410955

Vaughton G, Ramsey M. Gender plasticity and sexual system stability in Wurmbea. Ann Bot. 2012;109:521–530. http://dx.doi.org/10.1093/aob/mcr163

Sakai AK, Weller SG. Gender and sexual dimorphism in flowering plants: a review of terminology, biogeographic patterns, ecological correlates, and phylogenetic approaches. In: Geber MA, Dawson TE, Delph LH, editors. Sexual and gender dimorphism in flowering plants. Heidelberg: Springer-Verlag; 1999. p. 1–31. http://dx.doi.org/10.1007/978-3-662-03908-3_1

Chmelař J, Meusel W. Die Weiden Europas. Wittenberg Lutherstadt: Die Neue Brehm – Bucherei, A Ziemsen Verlag; 1979.

Skvortsov AK. Willows of the USSR. Moscow: Nauka; 1968.

Zieliński J. Salix nigricans Sm. In: Browicz K, editor. Atlas rozmieszczenia drzew i krzewów w Polsce. Warszawa: PWN; 1976. p. 13–15. (vol 20).

Faliński JB. Inwazje w świecie roślin: mechanizmy, zagrożenia, projekt badań. Phytocenosis. 2004;16:14.

Danell K, Elmqvist T, Ericson L, Salomonson A. Sexuality in willows and preference by bark-eating voles: defense or not? Oikos. 1985;44:82–90. http://dx.doi.org/10.2307/3544047

Boecklen WJ, Price PW, Mopper S. Sex and drugs and herbivores: sex-biased herbivory in arroyo willow (Salix lasiolepis). Ecology. 1990;71:581–588. http://dx.doi.org/10.2307/1940311

Leigh A, Cosgrove MJ, Nicotra AB. Reproductive allocation in a gender dimorphic shrub: anomalous female investment in Gynatrix pulchella? J Ecol. 2006;94:1261–1271. http://dx.doi.org/10.1111/j.1365-2745.2006.01164.x

Wallace CS, Rundel PW. Sexual dimorphism and resource allocation in male and female shrubs of Simmondsia chinensis. Oecologia. 1979;44:34–39. http://dx.doi.org/10.1007/BF00346394

Ramsey M, Vaughton G. Sex expression and sexual dimorphism in subdioecious Wurmbea dioica (Colchicaceae). Int J Plant Sci. 2001;162:589–597. http://dx.doi.org/10.1086/320142

Maki M. Differences in plant size and flower production between hermaphrodites and females of two gynodioecious Chionographis (Liliaceae). Can J Bot. 1996;74:150–153. http://dx.doi.org/10.1139/b96-020

Fleming T, Maurice S, Hamrick J. Geographic variation in breeding system and the evolutionary stability in trioecious cactus, Pachycereus pringlei (Cactaceae). Evol Ecol. 1998;12:279–289. http://dx.doi.org/10.1023/A:1006548132606

Kay QON. Nectar from willow catkins as a food source for Blue Tits. Bird Study. 1985;32:40–44. http://dx.doi.org/10.1080/00063658509476853

Argus GW. An experimental study of hybridization and pollination in Salix (willows). Can J Bot. 1974;52:1613–1619. http://dx.doi.org/10.1139/b74-212

Peeters L, Totland Ø. Wind to insect pollination ratios and floral traits in five alpine Salix species. Can J Bot. 1999;77:556–563. http://dx.doi.org/10.1139/cjb-77-4-556

Fisher MJ. The morphology and anatomy of the flowers of the Salicaceae 1–2. Am J Bot. 1928;15:307–394. http://dx.doi.org/10.2307/2435733

Ishida K, Hiura T. Mating system and population genetic structure of an androdioecious tree, Fraxinus lanuginosa Koidz. (Oleaceae) in northern Japan. Heredity. 2002;88:296–301. http://dx.doi.org/10.1038/sj.hdy.6800043

Kikuchi S, Shibata M, Tanaka M, Toshimaru H, Niyama K. Analysis of the disassortative mating pattern in a heterodichogamous plant, Acer mono Maxim. using microsatellite markers. Plant Ecol. 2009;204:43–54. http://dx.doi.org/10.1007/s11258-008-9564-1

Kimura MG, Goto S, Suyama Y, Matsui M, Woeste K, Seiwa K. Morph-specific mating patterns in a low-density population of a heterodichogamous tree, Juglans ailantifolia. Plant Ecol. 2012;213:1477–1487. http://dx.doi.org/10.1007/s11258-012-0105-6

Nybakken L, Julkunen-Tiitto R. Gender differences in Salix myrsinifolia at the pre-reproductive stage are little affected by simulated climatic change. Physiol Plant. 2013;147:465–476. http://dx.doi.org/10.1111/j.1399-3054.2012.01675.x

Taylor DR, Trimble S, McCauley DE. Ecological genetics of gynodioecy in Silene vulgaris: relative fitness of females and hermaphrodites during the colonization process. Evolution. 1999;53:745–751. http://dx.doi.org/10.2307/2640714

Pannell JR, Dorken ME. Colonisation as a common denominator in plant metapopulations and range expansions: effects on genetic diversity and sexual systems. Landsc Ecol. 2006;21:837–848. http://dx.doi.org/10.1007/s10980-005-5389-7




DOI: https://doi.org/10.5586/asbp.2015.013

Journal ISSN:
  • 2083-9480 (online)
  • 0001-6977 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society