The Avoidance of Self-Interference in the Endemic Daffodil Narcissus Cyclamineus (Amaryllidaceae)
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Plant Ecol (2012) 213:1813–1822 DOI 10.1007/s11258-012-0137-y The avoidance of self-interference in the endemic daffodil Narcissus cyclamineus (Amaryllidaceae) Luis Navarro • Garbin˜e Ayensa • Victoria Ferrero • Jose´ Marı´aSa´nchez Received: 27 July 2012 / Accepted: 10 October 2012 / Published online: 26 October 2012 Ó Springer Science+Business Media Dordrecht 2012 Abstract Hermaphrodite flowers usually possess mechanisms. N. cyclamineus is self-incompatible floral traits to avoid the negative effects derived and dichogamy can be rejected for this species. Even from inbreeding depression and/or self-interference though the species is self-incompatible, when cross- between pollen export and reception, both acting as pollination is preceded by self-pollination the number the main selective pressures on those floral traits. The of ovules available for legitimate crosses is diminished avoidance of self-interference is widely accepted as (ovule discounting). Pollinators are scarce during the the primary force promoting the separation between flowering period, resulting in pollen limitation. It is sexes within the flowers in time (dichogamy) and/or suggested that both the scarcity of pollinators and space (herkogamy) for self-incompatible species, which ovule discounting may be acting synergically to are already protected from the negative effects of promote herkogamy or its maintenance in this species. inbreeding depression by the incompatibility system. Different degrees of incompatibility, herkogamy, and Keywords Herkogamy Á Dichogamy Á Narcissus dichogamy have been reported for the genus Narcis- cyclamineus Á Self-incompatibility Á Self-interference Á sus. However, the only mechanism for the separation Ovule discounting of sexes reported up to date for Narcissus cyclamineus is herkogamy, while the presence of dichogamy and the type of incompatibility in this species remain Introduction uncertain. In this study, we analyze the patterns of sexual reproduction in N. cyclamineus to ascertain The co-location of female and male function within whether there is any selective pressure favouring the same floral structure is a common feature in sexual segregation or its maintenance and their flowering plants. There are some advantages derived from this hermaphroditic condition, namely the econ- omy of resources invested in attracting pollinators L. Navarro Á G. Ayensa Á V. Ferrero Á J. M. Sa´nchez (&) and increasing probability of selfing when mates or Departamento de Biologı´a Vegetal, Facultad de Biologı´a, pollinators are scarce (Charlesworth and Charlesworth Campus As Lagoas-Marcosende, Universidad de Vigo, 36200 Vigo, Spain 1987; Lloyd 1987). But, hermaphroditism may be e-mail: [email protected] inconvenient because it may increase inbreeding depression and/or self-interference (interference between V. Ferrero the pollen-export and the pollen-reception functions) CFE, Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, PO Box 3046, 3001-401 (Lloyd and Webb 1986; Webb and Lloyd 1986; Coimbra, Portugal Barrett and Harder 1996). A number of floral traits 123 1814 Plant Ecol (2012) 213:1813–1822 have evolved to prevent those disadvantages, and the anthers); this state was inferred to be ancestral for the spatial separation of stigmas and anthers within genus (Graham and Barrett 2004). the flower (herkogamy) is one of the most frequent Narcissus cyclamineus is a monomorphic approach- (Webb and Lloyd 1986). However, many plant species herkogamous endemic species from the northwestern are known to be self-incompatible and therefore Iberian Peninsula. The type of compatibility in this protected from the negative effects of inbreeding by species is a subject of controversy since it has been their inability to self-reproduce (e.g. Cesaro et al. characterized not only as self-incompatible (Bateman 2004); in these cases, the avoidance of the self- 1954) but also as self-compatible (Larrinaga et al. interference is the main selective force promoting 2009). In order to understand the significance of floral traits related to self-pollination avoidance rather herkogamy for this species, first of all, we intend to than the prevention of the inbreeding depression confirm or rule out whether there are other mechanisms (Harder and Barrett 1996; Harder et al. 2000; Barrett to prevent self-pollination, namely dichogamy. To this 2002, 2003; Medrano et al. 2005). end, an accurate assessment of temporal patterns of the It is therefore important to assess whether plant sexual functions within the flowers must be accom- species are self-compatible or self-incompatible to plished to know if a temporal between-sex separation is understand the evolutionary significance of the traits also present as for other species of the genus (e.g., associated with avoiding self-pollination in flowering Cesaro et al. 2004); then, we will study the morpho- plants. Self-incompatibility has been defined as the logical floral traits of N. cyclamineus to precisely ‘‘partial or complete inability of a functionally bisex- characterize herkogamy and the variability of the floral ual seed plant to produce zygotes after self-pollina- shape as phenotypic floral integration. In order to tion’’ (Becerra and Lloyd 1992). Importantly, those assess whether the function of herkogamy in this authors acknowledge that self-incompatibility seldom species is to prevent inbreeding, self-interference, or results in the complete loss of all ovules, and should be both, we will study whether the species is self- characterized quantitatively. Seavey and Bawa (1986) compatible or self-incompatible. Since self-incompat- acknowledge the difference between ‘‘self-incompat- ibility was confirmed, we will then determine the ibility’’ (at the level of the stigma or style), and ‘‘late- existence of ovule discounting as described for other acting incompatibility,’’ when ‘‘the barriers are in the polymorphic species of the genus. Finally, we assess ovary.’’ In this context, ovule discounting (i.e., the loss the main patterns of the pollination process to deter- of ovules after self-pollination) in Narcissus has been mine the importance of the pollen flow on the sexual considered a late-acting self-incompatibility mecha- reproduction for this species. nism since it occurs before the pollen tube entry into the ovary (Sage et al. 1999), which would involve a still unknown long-distance signaling mechanism Methods between pollen tubes, ovary, and ovules (Sage et al. 1999; Barrett 2002; Cesaro et al. 2004). The mecha- Study species and site nism of ovule discounting may vary among lineages, and some cases have even been documented of a Narcissus cyclamineus DC. (Amaryllidaceae) is a tall reversible effect of the interference: for Brassica (20–30 cm), unifloral, bulbous herb with yellow nigra, Ockendon and Currah (1977) reported an flowers. Flowering starts in mid-February and lasts inhibitory effect of self-pollen on the stigma which until the end of March, and fruits mature until June– decreases over time although such results could not be July, when the capsules open to allow seed release. confirmed for other Brassicaceae (Raphanus raphani- The single flower of each plant is protected by a spathe strum, Koelling and Karoly 2007). The existence of and consists of six deflexed tepals and a corona with a ovule discounting in polymorphic species of the genus crenate–serrate margins. The corona encloses six Narcissus has been also documented (e.g., Barrett equal-sized stamens and a stigma positioned above et al. 1997; Sage et al. 1999; Arroyo et al. 2002; Cesaro the anthers (approach-herkogamy). Its area of distri- et al. 2004), but to our knowledge it remains to be bution is restricted to the north-western part of the proven in a monomorphic approach-herkogamous Iberian Peninsula, where it grows close to river banks species (with a stigma protruding further than the at low altitude (Pino Pe´rez et al. 2005). 123 Plant Ecol (2012) 213:1813–1822 1815 The studied population is located near the village of Zama´ns (Vigo—Spain, 4280902800N884103000W), in meadows at the confluence of the Amial and Zamans streams, comprising an area of about 385 m2. Annual mean temperature and precipitation are 13.6 °C and 1,909 mm, respectively, [data from the nearest recording meteorological station, at about 8.5 km from the study site, INM (Instituto Nacional de Meteorologı´a) 2004]. The number of flowering indi- viduals in this population is about 6,900. Since N. cyclamineus is an endangered species, all exper- iments carried out in this study were non-destructive; bulbs gathered for the experiments conducted in the laboratory were planted back in the field once the experiments were concluded. Fig. 1 Schematic representation of a flower of N. cyclamineus, showing the measures taken for the present study, modified from Larrinaga et al. (2009). Variable numbers correspond to: 1 corona length; 2 tepal length; 3 corona aperture; 4 corona Floral morphology diameter; 5 style length; 6 stigma diameter; 7 tube length; 8 ovary length; 9 stamen length; 10 anther length; 11 stem angle The flowers from 112 randomly selected individuals were collected and kept in ethanol (70 %) until being processed. Each flower was photographed in the before nectar extraction. We used nylon mesh bags; laboratory against calibrated graph paper, before and these bags have been regularly used in this type of after dissection. We measured the following floral study (e.g., Navarro 1999; Ferrero et al. 2009) as they variables on the photos: corona length, tepal length, are known to have little influence on nectar production corona aperture, corona diameter, style length, stigma (Wyatt et al. 1992). The nectar volume was measured diameter, tube length, ovary length, stamen length, using capillary micropipettes and the sugar concen- anther length, and stem angle (Fig. 1). All measure- tration was determined using a portable refractometer ments were taken by the image analyzer software as the percentage by weight. The amount of sugar Analysis 5.0 (Soft imaging system GmbH 1999). We produced by each flower was estimated according to also calculated the ‘‘herkogamy distance’’ (difference Cruden and Hermann (1983).