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Relative Embryo Length As an Adaptation to Habitat and Life Cycle in Apiaceae

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Relative Embryo Length As an Adaptation to Habitat and Life Cycle in Apiaceae Research Relative embryo length as an adaptation to habitat and life cycle in Apiaceae Filip Vandelook1, Steven B. Janssens2 and Robin J. Probert3 1Plant Ecology, Philipps-Universita¨t Marburg, Karl-von-Frisch-Strasse 8, D-35043 Marburg, Germany; 2Laboratory of Plant Systematics, Institute of Botany and Microbiology, KU Leuven, PO Box 2437, BE-3001 Leuven, Belgium; 3Seed Conservation Department, Royal Botanic Gardens Kew, Wakehurst Place, Ardingly, West Sussex RH17 6TN, UK Summary Author for correspondence: • The factors driving the evolution of the relative embryo length in Apiaceae were examined. Filip Vandelook We tested the hypothesis that seeds with large relative embryo length, because of more rapid Tel: +49 6421 2822053 germination, are beneficial in dry and open habitats and for short-lived species. We also ana- Email: fi[email protected] lyzed to what extent delayed germination as a result of embryo growth can be considered a Received: 13 March 2012 dormancy mechanism. Accepted: 5 April 2012 • Hypotheses were tested by correlating the relative embryo length with other plant traits, habitat and climatic variables. The adaptive nature of the relative embryo length was deter- New Phytologist (2012) mined by comparing the performance of a pure drift, Brownian motion (BM) model of trait doi: 10.1111/j.1469-8137.2012.04172.x evolution with that of a selection–inertia, Ornstein–Uhlenbeck (OU) model. • A positive correlation of the relative embryo length with germination speed and negative correlations with the amount of habitat shade, longevity and precipitation were found. An Key words: Apiaceae, comparative method, dormancy, embryo, evolution, seed size. OU model, in which the evolution of longer embryos corresponded to a transition to habitats of high light, or to a short life cycle, outperformed significantly a BM model. • The results indicated that the relative embryo length may have evolved as an adaptation to habitat and life cycle, whereas dormancy was mainly related to temperature at the sampling sites. The storage of food reserves in an external tissue, rather than Introduction in the embryo, has been suggested to be related to germination Angiosperm seeds usually contain not only an embryo, but also timing and seedling vigor (Stebbins, 1974). The predicted nutrient reserves consisting of either endosperm or perisperm. To positive relation between germination speed and relative embryo understand evolutionary changes in the size of the embryo size was confirmed for Mediterranean plant species (Vivrette, relative to the amount of nutritive tissue, both phylogenetic and 1995), but later disputed when phylogeny was taken into account ecological factors should be considered (Nikolaeva, 2004). Over (Verdu´, 2006). It has been argued that a large relative embryo size 100 yr ago, the ecological significance of relative embryo size was is especially beneficial in dry habitats, where rapid germination already recognized (Goebel, 1898; Crocker, 1916; Findeis, during short wet periods is advantageous (Hodgson & Mackey, 1917). The importance of phylogeny in the distribution of rela- 1986; Vivrette, 1995). Embryo size may also be related to adult tive embryo size among angiosperms became clear from the work longevity, as short-lived species often have long-lived seeds that of Martin (1946). Species with small embryos embedded in copi- are incorporated in the soil seed bank (Rees, 1993; Thompson ous endosperm are generally considered to be the plesiomorphic et al., 1998). Seeds in a seed bank usually germinate during short condition in angiosperms, whereas more derived species often spells of suitable environmental conditions, for example after dis- have a more developed embryo (Martin, 1946; Stebbins, 1974; turbance of soil or vegetation (Fenner & Thompson, 2005). The Forbis et al., 2002). Small relative embryos sizes are typical of production of seeds with a small underdeveloped embryo that primitive taxa, such as the Ranunculales in the Eudicots and requires an extensive period of embryo growth before germina- some representatives of the ANITA grade, the most basal tion would be disadvantageous under such conditions. Species angiosperms (Chien et al., 2011; but see Baskin & Baskin, with small embryos are, however, common in moist habitats such 2007). Verdu´ (2006) suggested that this evolutionary trend as woodlands or damp grasslands (Baskin & Baskin, 1988, towards increased relative embryo size was not driven by either 1998). It is in these environments that seeds are imbibed for an anagenesis or cladogenesis, but that the evolution of embryo size uninterrupted sufficiently long period for extensive embryo rather occurred as a passive process away from a minimum size. growth to be completed (Fenner & Thompson, 2005). Ó 2012 The Authors New Phytologist (2012) 1 New Phytologist Ó 2012 New Phytologist Trust www.newphytologist.com New 2 Research Phytologist Some angiosperm taxa typically have other mechanisms not Materials and Methods related to embryo size that control germination rate and dormancy. These mechanisms may obscure analyses of selective Data sampling forces that drive changes in relative embryo size across all angio- sperms. Therefore, we confined our study to the Apiaceae, A dataset of 275 Apiaceae species was compiled, containing data which all require post-dispersal embryo growth. This family on seed traits, plant traits, niche characteristics and the climate includes almost 3500 species divided into four subfamilies of conditions in which the species grow. Seed material of the study which the Saniculoideae and Apioideae are by far the largest species was obtained from seed banks, botanical gardens and by (Plunkett & Lowry, 2001; Magee et al., 2010). A southern field sampling. A complete species list with detailed information African origin of these two subfamilies, followed by migrations on the source of the data and references is available in Supporting northwards into Eurasia, has been suggested (Calvino et al., Information Table S1. 2006, 2008). Fruits typically consist of two mericarps, each con- The mean relative embryo length (embryo length · seed ) taining a seed with copious nuclear endosperm and a small length 1) of each species was determined by incubating 20 seeds embryo (Corner, 1976). Despite these general characteristics, in water for 24 h, cutting them in half and measuring embryo considerable interspecific variation in relative embryo size exists and seed length under a dissecting microscope equipped with an within the Apiaceae, ranging from species with tiny rudimentary ocular micrometer. Seeds were incubated in water for 24 h before embryos to species with embryos more than one-half the length measurement. Data on seed dry mass were either obtained from of the seed (Martin, 1946). A period of post-dispersal embryo the seed information database (Royal Botanic Gardens Kew Seed growth, varying from 1–2 wk to several months, usually Information Database, 2008) or, if not available, by weighing precedes root protrusion and germination (reviewed in 100 air-dried seeds and calculating the mean mass per seed. Ger- Vandelook, 2009). These seed characteristics, together with the mination data were based on germination trials performed at the large variation in habitats in which Apiaceae grow, and the Millennium Seed Bank (Kew), using 20 seeds incubated on moist enormous amount of effort that has been put into resolving the filter paper in Petri dishes and placed in temperature-controlled phylogenetic relationships between Apiaceae during the last 15 incubators at 5 or 15°C for at least 30 d. Germinated seeds were yr (see Downie et al., 2010), make the Apiaceae a good choice counted and usually discarded weekly, until no further germina- for studying questions related to factors driving embryo size tion occurred for at least 2 wk. The germinationP rate was evolution. expressed as the mean time to germinate = ( (gd · d )) ⁄ D, Although the functional ecology of embryo size has been where gd is the number of seeds that germinated on day d from studied extensively, the environmental conditions driving the sowing and D is the total number of seeds that germinated in the evolution of relative embryo size, and correlations with other test. Species with < 10% germination were excluded from the plant traits, have never been analyzed explicitly. In this study, analyses of germination rate. Before testing germination, seeds we first aim to analyze the factors driving the evolution of the were stored for variable periods of time at ) 18°C after drying to relative embryo length in the Apiaceae by applying phylogenetic equilibrium at 15% relative humidity (RH). No correlation regressions. We tested the hypotheses that seeds with a large rel- existed between the storage time (d) and mean time to germinate ative embryo length germinate faster and to a higher percentage. at 5°C(r2 = 0.04, P = 0.08) or 15°C(r2 < 0.01, P = 0.56), or As a result of the advantages related to faster germination, we with the final germination percentage at 5°C(r2 = 0.01, expect species with a large relative embryo length to be frequent P = 0.36) or 15°C(r2 < 0.01, P = 0.95). Data on the germina- in open, dry habitats and among short-lived species. Although tion rate of seeds incubated at 5 and 15°C were obtained for a previous work has suggested that only weak relationships subset of 60 and 59 species, respectively. The final germination between plant traits and climatic factors are to be expected, percentages at 5°C and 15°C were determined for 69 and 122 because of often considerable differences in plant traits between species, respectively. coexisting species (Wright et al., 2004; Moles et al., 2005), we Maximum plant height and adult longevity were retrieved expect more species with a large relative embryo length in dry from floras and online databases. The species were divided into regions. three adult longevity classes: annuals, biennials and perennials. Finally, we tested to what extent the relative embryo length is When plants were listed as both annual and biennial, or as mono- an adaptation to habitat and plant longevity by means of carpic perennial, we assigned them to the biennial class.
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