Andromonoecy in an Old World Papilionoid Legume, Erophaca Baetica R
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Plant Biology ISSN 1435-8603 RESEARCH PAPER Andromonoecy in an Old World Papilionoid legume, Erophaca baetica R. Casimiro-Soriguer, J. Herrera & S. Talavera Departamento de Biologı´a Vegetal y Ecologı´a, Facultad de Biologı´a, Universidad de Sevilla, Sevilla, Spain Keywords ABSTRACT Fabaceae; legume; male functionality; resource limitation; sexual system. Andromonoecy (i.e. the occurrence on individual plants of hermaphroditic and male flowers) is a rare sexual system among the angiosperms, regarded by some Correspondence authors as a transitional stage from hermaphroditism to monoecy. Having discov- R. Casimiro-Soriguer, Departamento de ered the occurrence of andromonoecy in Erophaca baetica (a Mediterranean Biologı´a Vegetal y Ecologı´a, Facultad de shrubby legume with two subspecies), a novelty for Old World papilionoid legumes, Biologı´a, Universidad de Sevilla, Apdo. 1095, we investigated the morpho-functional correlates and the geographical distribution E-41080 Sevilla, Spain. of this phenomenon in the species. The relative frequencies of hermaphrodite and E-mail: [email protected] male flowers were determined in two field and 111 herbarium populations. Biomass allocation within flowers, pollen production and viability, pollen tube growth, nec- Editor tar production and the temporal pattern of male flower production were also stud- A. Dafni ied in two nearby southern Spanish populations. Virtually all of the studied populations were andromonoecious. Male flowers tended to appear at apical posi- Received: 25 January 2012; Accepted: 5 June tions within the inflorescence, and became more abundant by the end of the flower- 2012 ing season. Male flowers were externally similar to hermaphroditic flowers (although with less biomass and smaller parts) and released equivalent amounts of doi:10.1111/j.1438-8677.2012.00648.x pollen and nectar; however, their pollen germinated significantly better. Erophaca is the first example of an andromonecious Papilionoid in the Old World. Since the main difference among floral morphs in this species is functional (i.e. pollen germi- nation rate) rather than morphological, andromonoecy is not readily noticeable, and very careful inspection may be required to reveal it. The potential effect of andromonoecy in enhancing outcrossing rate in this species is discussed. authors to be a relatively primitive trait that has evolved INTRODUCTION independently more than once in different plant groups, and The impressive diversity of sexual systems found in the which may represent a transitional stage from hermaphrodit- angiosperms (Bawa & Beach 1981; Cruden & Lloyd 1995; ism to monoecy (Barrett 2002; de Jong et al. 2008; Schless- Barrett 2002) is unevenly distributed across species: while mann 2010; Torices et al. 2011). hermaphroditism is the most widespread sexual system (de The set of morpho-functional traits described for Jong et al. 2008), others, such as andromonecy (i.e. the coex- andromonoecious species exhibit considerable variation. In istence of both hermaphroditic and male flowers on the same some species, for example, male and hermaphroditic flowers plant) are rare. Somewhat <2% of angiosperms are andro- are equal in size and morphology, while in others the male monecious (Yampolsky & Yampolsky 1922; Bawa & Beach flowers are smaller (Solomon 1986; Emms 1993; Zhang & 1981; Torices et al. 2011), although the condition may be Tan 2009). The pollen production of male flowers may be overrepresented in Neotropical (Machado et al. 2006) and equivalent to that of perfect ones, or the pollen production Mediterranean environments (Steiner 1988) and among taxa of male flowers may be significantly larger (Solomon 1986; with relatively large seeds or fruits (Miller & Diggle 2007). Huang 2003; Zhang & Tan 2009). Female-sterile flowers may Other than that, andromonoecy has few ecological correlates appear either in terminal positions within inflorescences or and occurs in a number of unrelated angiosperm families, branches, or in basal positions (Primack & Lloyd 1980; such as Solanaceae (Solomon 1985, 1986; Diggle 1994), cae- Anderson & Symon 1989; Diggle 1994; Miller & Diggle salpinoid and mimosoid legumes (Arroyo 1981; Gibbs et al. 2003). As for the evolution of andromonoecy, it has been 1999; Ortiz et al. 2003; Calvin˜o & Galetto 2010; Beavon & hypothesised that the coexistence of perfect and female-sterile Chapman 2011), Myrtaceae (Primack & Lloyd 1980), Col- flowers on the same plant can be evolutionary stable if one chicaceae (Dafni & Shmida 2002) and Alismataceae (Huang or more of the following conditions are met: there are 2003). In Cucumis (Cucurbitaceae) a mechanism of genetic resource limitations to fertility, so that a reduction in the control of andromonecy has been proposed by Boualem et al. number of ovaries results into increased fertility in the (2008), in which transition from monoecy to andromonoecy remaining ones (Emms 1993; Dafni & Shmida 2002; Liao results from mutation in the 1-aminocyclopropane-1-carbox- et al. 2006); if extra male flowers induce increased pollen ylic acid synthase gene. Andromonoecy is considered by some receipt by perfect flowers (Vallejo Marı´n & Rausher 2007; Plant Biology 15 (2013) 353–359 ª 2012 German Botanical Society and The Royal Botanical Society of the Netherlands 353 Andromonoecy of Erophaca Casimiro-Soriguer, Herrera & Talavera Calvin˜o & Galetto 2010); or if pollen from male flowers is We observed that in E. baetica ssp. baetica some flowers more efficient at siring seeds than pollen from hermaphro- have aborted or reduced ovaries (with vestigial, shrunken pri- ditic flowers (Charlesworth & Morgan 1991; Brunet & mordia) that never set fruit. Fully developed flowers with Charlesworth 1995; Dai & Galloway 2011). Given the rarity non-functional ovaries can be distinguished (with the naked of andromonoecy, each new occurrence can yield valuable eye) from more abundant hermaphroditic flowers, but their information and provide insights into the phenomenon. pollen release is apparently normal. We studied the sexual In the huge family Leguminosae, andromonoecy is almost expression of flowers in two populations in SW Spain (Hino- non-existent in the largest (ca. 13,600 species; Lewis et al. jos 37°17¢ N, 6°25¢ W, and Don˜ana National Par, 37°0¢ N, 2005) subfamily, Papilionoideae. To date, only two andromo- 6°30¢ W) during 2006 and 2007. The two locations are 30- noecious papilionoid species are known: Abrus precatorius km apart, 25–90 m a.s.l., and present very similar climate (Percival 1974) and Erythrina leptorhiza (Hernandez & conditions. The climate is typically mediterranean, with Toledo 1979). The monotypic Mediterranean genus Erophaca yearly temperature averages around 17 °C. Accumulated pre- often presents flowers with reduced ovaries, so it is a good cipitation during the first year of study was 468 mm, and candidate as a third example of an andromonoecious papilio- during the second 729 mm. In addition to the two main noid legume. Furthermore, the only species of the genus study sites, we checked flower sex expression in 111 popula- (E. baetica) has two subspecies that can be differentiated both tions (1–10 plants per locality) distributed across the whole on morphological and genetic grounds (Casimiro-Soriguer et range of the species (Fig. 1), using specimens from seven al. 2010) and are distributed at opposite ends of the Mediter- large European herbaria (BCN, G, LISU, MA, MGC, SEV, ranean Basin. Therefore Erophaca is a good subject to provide VAL). For each locality represented in the herbaria, all new data on the morphology, function and within-species vouchers were examined and the presence or absence of male distribution of andromonoecy. flowers noted. Most of the herbarium sheets belonged to the typical (western) subspecies baetica, and five were of the east- ern subspecies orientalis. MATERIAL AND METHODS Plant and study area Flower size and within-plant variations of sexual expression We studied Erophaca baetica (L.) Boiss. (previously known as To investigate whether the presence of a functional ovary was Astragalus lusitanicus Brot.), a Tertiary relict of the Legumi- associated with size variations in other floral organs, we col- nosae subfamily Papilionoideae (nomenclature follows Lewis lected 21 female-sterile and 19 perfect flowers from 20 plants et al. 2005). The species is endemic to the Mediterranean (chosen at random in the Don˜ana National Park population), Basin, and has two disjunct subspecies: E. baetica ssp. baetica, and weighed separately the calyx, the banner, wings and keel endemic to the Iberian Peninsula and NW Africa, and E. bae- petals, as well as the androecium and gynoecium. Flowers tica ssp. orientalis, endemic to Greece, Cyprus and SW Asia. were fully developed when collected. Masses of freshly dis- Plants of E. baetica are long-lived perennials with a woody, sected organs were determined using an electronic balance tuber-like underground organ (xylopodium) from which numerous (1–20) herbaceous stems sprout at the beginning of winter (December). Plants up to 2 m in height can be found in shady places, but most are around 1-m tall (mean length ± SD: 0.96 ± 0.24 m; n = 112). From January to April the stems develop axillary inflorescences (1–7 per stem, with those lower on the stem opening first) with relatively large (29.02 ± 1.06 mm; n = 126) cream-white nectariferous flow- ers (10–30 per inflorescence) that are visited mainly by bees and bumblebees. Total flower production varies from >1000 to as few as 12 flowers per plant (mean 196 ± 229, n = 338; Casimiro-Soriguer 2010). Ovaries develop into large inflated legume pods (length 70.7 ± 4.9 mm, width 19.7 ± 1.7 mm; n = 40) containing up to nine relatively large (ca. 10-mm long and ca. 180 mg in weight) seeds. Biotic dispersal agents are unknown, but seeds are dispersed ballistically through the explosive dehiscence of pods. Vegetative reproduction (e.g.by stolons) has never been observed. By mid-spring (May) or early summer the plants shed their leaves, the stems become dry and plants survive the summer due to their buried xylo- podia, which remain dormant until next winter. Throughout its distribution, populations of E.