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This Article Appeared in a Journal Published by Elsevier. the Attached This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/authorsrights Author's personal copy C. R. Biologies 336 (2013) 479–485 Contents lists available at ScienceDirect Comptes Rendus Biologies ww w.sciencedirect.com Development and reproduction biology/Biologie du de´veloppement et de la reproduction Sex expression and reproductive biology in a tree species, Fraxinus excelsior L Expression du sexe et biologie de la reproduction chez un arbre, Fraxinus excelsior L a, ,1 b,1 a,b Be´atrice Albert * , Marie-E´ lise Morand-Prieur , Ste´phanie Brachet , c b,2 d,2 Pierre-Henri Gouyon , Nathalie Frascaria-Lacoste , Christian Raquin a Laboratoire E´cologie, Syste´matique et E´volution, Universite´ Paris-Sud, 91405 Orsay cedex, France b AgroParisTech, Laboratoire E´cologie, Syste´matique et E´volution, UMR 8079, 91405 Orsay cedex, France c MNHN, De´partement de syste´matique et e´volution botanique, 12, rue Buffon, 75005 Paris, France d Laboratoire E´cologie, Syste´matique et E´volution, CNRS–UPRESA 8079, 91405 Orsay cedex, France A R T I C L E I N F O A B S T R A C T Article history: We investigated Fraxinus excelsior breeding system using field data collected in a natural Received 5 May 2009 population and in a seed orchard. First, we attested functional trioecy (co-occurrence of Accepted after revision 30 August 2013 males, hermaphrodites and females), with males producing pollen, hermaphrodites Available online 24 October 2013 producing both pollen and seeds simultaneously, and females producing seeds. Second, we found that the reproductive system of F. excelsior was not labile, as sex expression seemed Keywords: to be stable through time. Third, gender is genetically determined since different trees Fraxinus excelsior belonging to the same clone in the orchard exhibit similar sexual phenotypes. Oleaceae ß 2013 Acade´mie des sciences. Published by Elsevier Masson SAS. All rights reserved. Trioecy Plant breeding system R E´ S U M E´ Mots cle´s : Nous avons e´tudie´ le syste`me de reproduction de Fraxinus excelsior a` partir des donne´es Fraxinus excelsior collecte´es dans une population naturelle et un verger a` graines. Nous montrons une trioe´cie Oleaceae fonctionnelle (pre´sence d’individus maˆles, hermaphrodites et femelles), avec des maˆles Trioe´cie produisant du pollen, des hermaphrodites produisant du pollen et des graines Syste`me de reproduction simultane´ment, et des femelles produisant des graines. Nous avons e´galement mis en e´vidence la stabilite´ du syste`me de reproduction. Enfin, nous montrons que le type sexuel est de´termine´ ge´ne´tiquement, car diffe´rents arbres appartenant a` un meˆme clone dans le verger ont le meˆme phe´notype sexuel. ß 2013 Acade´mie des sciences. Publie´ par Elsevier Masson SAS. Tous droits re´serve´s. 1. Introduction variation in sex expression, trioecy, the co-occurrence of male, hermaphrodite and female individuals within the Seed plants exhibit a wide variety of breeding systems same population represents a small percentage of flower- that has fascinated biologists since Darwin [1]. Within ing plants (3.6% of the species; [2,3]). Understanding the evolution and maintenance of such mating system is a major challenge as it involves the stable coexistence of three sexual morphs, which compete for reproduction. * Corresponding author. Stable coexistence of two sexual morphs (gyno- and E-mail address: [email protected] (B. Albert). 1 androdioecy, the coexistence of females, respectively, These two authors have contributed equally to this paper. 2 These two authors have supervised the project equally. males, and hermaphrodites) has been extensively studied 1631-0691/$ – see front matter ß 2013 Acade´mie des sciences. Published by Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.crvi.2013.08.004 Author's personal copy 480 B. Albert et al. / C. R. Biologies 336 (2013) 479–485 [4–13]. In contrast, trioecy has received little attention, hermaphroditism, Maurice et al. [13] found that trioe- mainly for three reasons. First, this mating system is rare in cious reproductive systems can be stable under nucleo- nature; second, trioecy has not been readily identified and cytoplasmic sex determination. Some of the conditions defined. Finally, trioecy is a complex system to study. for maintenance of trioecy outlined in these approaches Trioecy is usually defined as the co-occurrence of males, are highly model-specific and cannot be fruitfully used to hermaphrodites and females in the same population, but infer the stability of a trioecious mating system in natural under this definition, other mating systems may be populations. However, in the two latter models, two confused with trioecy. To date, only a few species have conditions are necessary (although not sufficient) for been recognized as trioecious: Carica papaya (Caricaceae; stability of trioecy: the male fitness (pollen production) [14]), Silene acaulis (Caryophyllaceae; [15]), Spinacea of the male individuals must be twice larger than that of oleracea (Chenopodiaceae; [16]), Thymelaea hirsuta (Thy- hermaphrodites and, the female fitness (ovule produc- melaeaceae; [17,18]), Atriplex canescens (Chenopodiaceae; tion) of the female individuals must be larger than that of [19]), Pachycereus pringlei (Cactaceae; [20]), Juniperus the hermaphrodites. All these models suppose that the seravschanica (Cupressaceae; [21]), Mercurialis annua sexual types are genetically determined. (Euphorbiaceae; [22]), and Coccoloba cereifera (Polygona- The common ash, Fraxinus excelsior L. (Oleaceae), has a ceae; [23]). However, three out of these nine species, complex, continuous distribution of three sex types [29– Atriplex canescens, Spinacea oleracea and Thymelaea hirsute 32], leading to a polymorphic breeding system that has were described by the authors as tetramorphic species, previously been described as trioecious [31]. In this paper, with dioecious individuals (males and females) and detailed information on the determination and expression sequential monoecious hermaphrodites that are either of sexual types are provided. The reproductive success of protogynous or protandrous. This specific sexual poly- males and females relative to hermaphrodites was morphism is considered more as a combination of true followed by studying the number of flowers, the pollen dioecy (males and females) and heterodichogamy or grains per flower, the fruits, and the flowering phenology. temporal dioecy (protogynous and protandrous indivi- This study was realized in a natural population of trees and, duals) by Domme´ et al. [18] than as a case of true trioecy. in a seed orchard where several genotypes were repre- Other authors found a significant degree of lability in sex sented by a varying number of trees obtained by cloning. expression of these three species under different environ- mental conditions [19,24]. In contrast, the Mexican columnar cactus Pachycereus pringlei is thought to be a 2. Materials and methods true trioecious species consisting of male, female and hermaphrodite individuals, with a stable sex expression 2.1. Study species and sites and only one type of flowers on a given individual [20]. However, both gynodioecious and trioecious populations Common ash (F. excelsior L., Oleaceae) is a deciduous of this species are found in the Sonoran Desert of Mexico forest tree distributed throughout Europe and Asia Minor [25], suggesting that trioecy is not stable. Field observa- [29]. This species is wind-pollinated and its fruits tions and a theoretical analysis suggest that pollinator (samaras) are wind-dispersed. In France, flowering occurs abundance and pollen limitation play an important role in in early spring (March–April), before foliage emergence the maintenance of trioecy in this plant [25,26]. A true (May), and flowering occurs during three to four weeks trioecious species should be defined as a species where [33]. three morphological and functional sex types co-exist: Two populations were studied; the first population is a males producing effective pollen only, hermaphrodites natural population located in the national forest of 0 00 0 00 producing simultaneously both effective pollen and viable Dourdan (latitude 488 31 47 , longitude 028 00 42 ). This seeds, and females producing seeds only. This definition of stand is of native origin and is managed by the French trioecy may include environmental variations in sex National Forest Service (ONF). F. excelsior is the dominant determination. species in this area of about 12 ha. All trees with a diameter So far, no theoretical approach has specifically at breast height larger than 10 cm were located and targeted the issue of the maintenance of trioecy. Never- marked. As the trees were very tall on average (about theless, three different general models of mating systems 30 m), we sampled branches to determine the sexual evolution have yielded conditions for the coexistence
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