Factors Affecting Intrafruit Pattern of Ovule Abortion and Seed Production in Hormathophylla Spinosa

Plant Syst. Evol. 239: 215–229 (2003) DOI 10.1007/s00606-003-0009-y Factors affecting intrafruit pattern of ovule abortion and seed production in Hormathophylla spinosa (Cruciferae) J. M. Go´mez and R. Zamora Departamento de Biologıá Animal y Ecologıá, Facultad de Ciencias, Universidad de Granada, Granada, Spain Received April 29, 2002; accepted January 30, 2003 Published online: July 31, 2003 Ó Springer-Verlag 2003 Abstract. We investigated the pattern of intrafruit Key words: Cruciferae, Hormathophylla spinosa, seed production in Hormathophylla spinosa (Cru- intrafruit seed position, ovule abortion, seed- ciferae) over a 7-yr period. H. spinosa fruit have ovule ratio, sibling rivalry. two chambers, each chamber containing two ovules, and usually situate perpendicular to the infructescence axis with one chamber above the other. The percentage of ovules ripening to seeds Introduction is usually lower than 50%. In addition, we found Only a fraction of the ovules per fruit become a consistent position-dependence in seed ripening seeds in the most plant species (Casper and probability, since more than 90% of the ripe Wiens 1981; Casper 1984, 1988; Lee 1988; seeds are arranged in the lower chamber of the Stephenson 1992). Several main non-exclusive fruit. This pattern of seed production is not produced by the direct or indirect effect of seed predispersal factors account for most of this predators, by pollen limitation or by nonrandom loss in reproductive potential, outstanding the fertilizations. By contrast, fruit removal experi- effect of pollen, resource, seed predators and ments showed that sibling rivalry can partially fruit architecture (Willson and Burley 1983; explain the seed production pattern, be the cause Haig and Westoby 1988; Lee 1988; Charles- of the reduction in the seed number from the worth 1989; Diggle 1995, 1997). uppermost threshold of 50%. Moreover, experi- Pollen availability (‘‘pollen limitation’’) or mental manipulations of fruit orientation suggest incompatibility (‘‘self-incompatibility system’’) that the position-dependence in seed production cause many ovules remain unfertilized in is the cause but not the effect of seed ripening. several plant species, decreasing seed number We presume that some architectural effect is per fruit (Haig and Westoby 1988, Barrett producing a significant increase in the ripening 1988a, Vander Kloet 1991, Stephenson 1992, probability of the ovules arranged in the lower chamber, causing thus the observed pattern in the Burd 1994). Furthermore, fertilized ovules can intrafruit seed production in H. spinosa and abort during development because of inbreed- severely constraining the maximum number of ing depression (Wiens et al. 1989, Husband and seeds per fruit to two. Schemske 1996), which is specially harmful in 216 J. M. Go´mez and R. Zamora: Intrafruit pattern of seed production in Hormathophylla spinosa selfing species with a mixed mating system, due This plurality of causes governing seed to the random joining of genetically similar number per fruit dramatically difficults the gametes after endogamous pollination which analysis of the exact mechanisms shaping seed causes the expression of deleterious recessive production in many plant species, and claims alleles, which has been described as ‘‘muta- for integrative studies which consider the tional load’’ (Charlesworth and Charlesworth combination of several factors working at the 1987; Charlesworth 1989; Wiens et al. 1987, same time (Marshall and Folsom 1992, Camp- 1989; Fuss and Sedgley 1991; Vander Kloet bell and Halama 1993). Despite of this, most 1991; Byers 1995; Rigney 1995). Inbreeding studies have assumed that each limiting factor depression, however, can also occur in out- usually acts independently on seed production crossing species, if there is a high probability of (Casper and Niesenbaum 1993). In the present fertilization by mates genetically more similar study, we investigate the potential causes of the than expected by random (Barrett 1998b). observed intrafruit patterns of seed produc- Resource limitation, whether nutrients or tion in Hormathophylla spinosa (L.) Ku¨ pfer water, contributes to the loss of some ovules (Cruciferae), a Mediterranean high-mountain per fruit both directly by decreasing the ability stunted shrub. H. spinosa bears many (up to of fertilized ovules to ripe to seed (Bierzych- 8000) small (2–3 mm diameter), white to pink, udek 1981, McDade 1983, Willson and Burley actinomorphic flowers consistently displaying 1983, Gorchov and Estabrook 1987, Lee 1988, four ovules (Go´mez and Zamora 1992). These Stephenson 1992), as well as indirectly by flowers are visited by more than 70 species of increasing the competition between the embry- insects belonging to 16 families and five orders, os arranged in the same ovary, which has been though the ant Proformica longiseta is the described as ‘‘sibling rivalry’’ (Kress 1981; predominant pollinator (Go´mez and Zamora Uma Shaanker et al. 1988; Ganeshaiah and 1992, 1999). In addition, this plant species is Uma Shaanker 1988; Arathi et al. 1996, 1999; also pollinated by wind in high-altitude pop- Cheplick 1996). Moreover, not only number ulations (Go´mez and Zamora 1996). H. spin- but also pattern of intrafruit seed production osa appears to be self-incompatible when are usually affected by resources, since severe pollinated with pollen coming from the same stress can encourage seeds to ripen in positions flower, and does not produce seeds by spon- offering greater access to resources (Lee 1988, taneous autogamy, in spite of more than 10% Ehrleń 1992, Ho 1992). Similarly, seed preda- of the flowers have pollen grains on the stigma tors reduced seed number per fruit in many before opening (Go´mez and Zamora 1996). plant species directly by consuming ripe seeds, Nevertheless, this crucifer can produce some and indirectly by increasing the probability of seeds by geitonogamy, although experimental abortion of the seeds arranged in the same geitonogamous hand-pollinations produce a fruit than the attacked ones (Ellison and significantly lower amount of seeds per fruit Thompson 1987, Anderssen 1988). Finally, than that of xenogamous pollinations (Go´mez according to the ‘‘architectural effects hypoth- and Zamora 1996). Although its flowers can esis’’, the pattern of seed production can also produce up to 4 seeds, they usually set 2 ripe be provoked in some plants by intrinsic seeds (Go´mez and Zamora 1992). This occurs factors limiting the ripening of ovules located despite the seed production per fruit is not in some positions (Diggle 1995). The proxi- pollen limited in this crucifer (Go´mez and mate causes of these architectural effects are Zamora 1996), and it is not affected by selective still unknown (Diggle 1997), although cum- exclusions of main pollinators (Go´mez and mulating evidence is showing that it can have Zamora 1992). The specific objectives of this important effect on the observed pattern of study are to 1) describe the intrafruit pattern of seed production (Medrano et al. 2000 and seed production, comparing the level of ovule references therein). fertilization with the level of seed maturation J. M. Go´mez and R. Zamora: Intrafruit pattern of seed production in Hormathophylla spinosa 217 and quantifying the level of seed abortion per chamber, as well as a left and a right placenta fruit, 2) quantify the temporal (3 years) and (Fig. 1). spatial (3 populations, 80 plants) variability in After pollination, the ovules can be fertilized this reproductive component, and 3) experi- setting ripe seeds, fertilized but aborting during mentally investigate the potential causes pro- development or remain unfertilized. A ripe seed is voking this observed pattern in seed uniformily brown and the embryos and full cotyledons are totally developed. On the contrary, an production. aborted seed is invariably dark brown, with shrivelled cotyledons and embryo. The size of Materials and methods aborted seeds was highly variable, depending on H. spinosa fruit structure. The H. spinosa fruit has the moment of the development occurring the two carpels and two placentas, but is secondarily abortion. Ovules aborted immediately after fertil- divided into two chambers by means of a thin ization (Type I Aborted Seed) are much smaller membrane called the septum (see Hill and Lord than ovules aborted later in the development (Type 1987), each chamber containing two ovules. Thus, II Aborted Seed). Finally, virgin ovules are consis- in each chamber, there is one ovule belonging to tently the same creamy white color, lanceolate in one of the two placentas. The four ovules are shape and of a far smaller size than aborted or ripe symmetrically arranged at the same distance from seeds. the style and the stigma, as well as from the Ripe seeds are depredated within the fruit by a vascular tissue that feeds the fruit. However, when weevil seed predator, Ceutorhynchus sp. nov. (Cur- beginning to ripe, fruit orientation shifts to situate culionidae), which completes its development with- perpendicular to the infructescence axis and with in the fruit (Go´mez and Zamora 1994). one chamber above the other, maintaining both Study area and plant populations. The study placentas at the same distance from the ground. was carried out in the Sierra Nevada (Granada Thus, in a ripe fruit, there is an upper and a lower province, SE Spain). We selected three populations Fig. 1. Schematic representation of a H. spinosa fruit. A Longitudinal view showing a chamber with two seeds and the screem dividing

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