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Dioecious plant species divide reproductive function among individuals, with pollen production restricted to males, and seed and fruit production restricted to females. Reported sex ratios in tropical trees are generally male-biased; hence the proportion of seed-producing individuals in a population is usually < 50% (Queenborough et al. 2007a). As a result, given equal population densities, populations of dioecious species will have fewer seed-producing individuals than their cosexual (i.e. hermaphroditic or monoecious) counterparts. To maintain per capita growth rates that are equal to their cosexual counterparts, female individuals in dioecious populations must exhibit some fitness advantages, which might include: higher fecundity (although without increased dispersal this results in a ‘seed shadow handicap’ whereby offspring are concentrated in the proximity of a smaller number of maternal plants (Heilbuth et al. 2001)), earlier ages of reproduction, more frequent reproduction or higher quality offspring (with higher rates of survivorship or greater longevity). Indeed, one recent study has detected higher abundances of dioecious than non-dioecious species among 97 woody species in a Brazilian Atlantic rain forest (Vamosi 2006).
In pure females, selection may be relaxed on those primary or secondary traits that promote male fitness in cosexual individuals. Consequently, resources that are allocated to traits that enhance male function (e.g. anther and pollen production or flowers that are sufficiently attractive, long-lived or rewarding to ensure multiple pollinator visits per flower) may be reallocated towards traits that promote female function (e.g. seed quantity or quality). In other words, relative to cosexual plants, females of dioecious species may invest more resources in seed or fruit production simply by reallocating their reproductive effort. Sex-specific allocation of resources among floral traits – presumably the result of sex-specific selection – has been observed within many species that are polymorphic for sex. For example, in many gynodioecious species, females produce larger, more or higher-quality seeds than cosexuals (Caruso et al. 2003; Ramula & Mutikainen 2003; Shykoff et al. 2003; Koelewijn & Van Damme 2005; Chang 2006). Similarly, in many dioecious species, males produce larger or more rewarding flowers than females, presumably because males benefit (via pollen dispersal) more from higher attractiveness than females (which do not require many visits per flower to achieve full seed set) (cf. Bell 1985; Geber et al. 1999; Vamosi & Otto 2002; Humeau et al. 2003; Mitchell & Diggle 2005). Inter-specific investigations of the evolutionary reallocation of resources towards increasing seed size or quality in dioecious species relative to their hermaphroditic counterparts, however, are rare; we are aware of only one other study (Vamosi et al. 2008).
Assuming that dioecious species coexist with cosexual species through mechanisms of compensation, it should then be possible to quantify this compensation relative to cosexual species. If n‘female’ cosexual individuals invest r resources in seed production, then n/2 female dioecious individuals would be predicted to invest 2r resources. In terms of seed number, this would be double the number. In terms of seed quality, it is more difficult to quantify the resources necessary to ensure that each seed produced has a higher chance of survival because of interactions with abiotic factors (Poorter & Rose 2005). We might predict that seeds of dioecious species would be between 50% and 100% heavier, depending on the relationship between individual seed mass and the expected individual fitness of the ensuing seedling (Moles & Westoby 2004).
However, there are other mechanisms of species coexistence that may particularly aid dioecious species to persist. For example, the lower number of dioecious females may benefit from a frequency-dependent advantage (Janzen 1971; Connell 1971; Chesson 2000), or dioecious species may out-compete cosexual species in other aspects of niche-space, such as regeneration, pollination or seed dispersal (e.g. Grubb 1977; Vamosi et al. 2007). Alternatively, stochastic processes and dispersal limitation may enable the coexistence of hundreds of species, irrespective of differences in breeding system or any other species trait (Hubbell 2001).
For several reasons, tropical rain forests provide a particularly rich opportunity in which to test the mechanisms that promote the persistence of dioecious species and to detect ecological and/or evolutionary correlates of dioecy. First, due to the high species richness of tropical rain forests, it is possible to compare seed quality and population densities of a taxonomically diverse array of sympatric plant species that differ in breeding system. Secondly, the high diversity of species representing a range of growth forms (e.g. trees, shrubs and lianas) and breeding systems (Bullock 1985; Matallana et al. 2005; Queenborough et al. 2007a) allows one to explore rigorously the relationship between breeding system and reproductive performance by examining it independently within each of these plant guilds. Thirdly, dioecious and cosexual species and clades have diverged from common ancestors numerous times in tropical floras, resulting in a high local proportion of dioecious species compared to the global proportion of 6% (e.g. Bawa 1980; Renner & Ricklefs 1995; Vamosi & Vamosi 2004). Lastly, the repeated evolutionary divergence in breeding system permits one to test predictions concerning the joint evolution of breeding system with morphological traits such as individual seed mass and ecological traits such as the abundances of individuals of different size or age classes.
In this study, we tested for two compensatory fitness or demographic advantages in dioecious species compared to co-occurring hermaphroditic and monoecious species: (i) higher individual seed mass and (ii) higher densities of established individuals.
In addition to comparing dioecious species to those with cosexual flowers, we compared dioecious and monoecious species. Monoecious species serve as a control because, similar to dioecious species, they produce unisexual flowers (within individuals) but they do not suffer the disadvantage of having fewer seed-producing individuals (Heilbuth et al. 2001). We therefore predicted that dioecious species should produce larger seeds or persist at higher density than both monoecious and hermaphroditic species, but that monoecious and hermaphroditic species should not differ consistently with respect to these attributes. First, we tested for phylogenetic dependence in both the dependent and independent variables in order to determine whether we needed to control statistically for non-independence of trait states among closely related species. Secondly, we used a phylogenetically corrected generalized linear modelling approach to ask whether the evolutionary divergence in breeding system between closely related, sympatric species (i.e. divergence between dioecious, monoecious and hermaphroditic species) is associated with either a change in seed size or adult population density as predicted by the arguments above. Specifically, we predicted that dioecious species would have higher individual seed mass and higher densities of adults. In addition, we controlled for the potentially confounding effects of the well-known associations between seed size and growth form (e.g. trees, shrubs, lianas and herbs) by conducting analyses both within and across growth forms.
Because of the well-documented interspecific trade-offs between seed size and other traits (e.g. seed number, mean individual longevity, and growth rate (Swaine & Whitmore 1988; Moles & Westoby 2006; Baraloto & Forget 2007; Rees & Venable 2007)) and given the positive correlations between seed size and plant height (Leishman et al. 2000; Moles et al. 2004; Wright et al. 2007), several components of life history are likely to evolve jointly with seed size, even within growth forms. Moreover, traits such as growth rate and maximum plant height may be strongly correlated with wood density due to the constraints wood density places on the movement of water and on structural support. Indeed, wood-specific gravity (WSG) is a good correlate of longevity and life-history strategy among Neotropical trees (Chave et al. 2006). Thus, we sought to isolate and measure the relationship between breeding system and seed size by including WSG as a covariate in our analyses as a proxy for longevity.
Although seed size has primarily been contrasted between functional groups (such as shade-tolerators and light-demanders, represented in our study by wood-specific gravity), the within-group range of seed size is often much larger (Grubb 1998). Within functional groups, a basic trade-off exists between seed size and seedling survival: in species that produce larger seeds the resulting seedlings have a higher tendency to survive. This relationship is often modified by factors such as tolerance of hazards, and competition with established plants and other seedlings (summarized in Coomes & Grubb 2003). Breeding system is a relatively un-examined aspect of variation in seed-size that may subtly modify these well-established relationships.
Finally, to assess the generality of our results, we compare the patterns observed in our analysis of an Ecuadorian rain forest flora with those from a Peruvian rain forest with comparable floristic, ecological and taxonomical diversity that was subject to similar analyses by Vamosi et al. (2008). We extend their work by examining the taxonomic composition of and the species abundance within the two forests, as well as frequency distributions of seed size, to understand the potential differences in results between the sites.
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In this article, we surveyed species in a highly diverse tropical forest in Ecuador in order to (i) examine associations between seed size, breeding system, growth form and regeneration strategy and (ii) test specific predictions concerning the evolutionary and ecological consequences of dioecy. Our results were not entirely consistent with those of previous studies. Ibarra-Manriquez & Oyama (1992) found no difference in seed mass between breeding systems; Carpenter et al. (2003) found bigger seeds in dioecious species (in ‘larger tree species’); Matallana et al. (2005) found that dioecy was disproportionately represented among the 43 most abundant woody plant species relative to the remainder of the flora; Vamosi (2006) found a marginally higher density of dioecious species than non-dioecious species; and Vamosi et al. (2008) found bigger seeds in dioecious than in cosexual species in certain growth forms. First, we did not find that dioecious species produce heavier seeds than hermaphroditic species, in lianas, shrubs or trees. We did find that monoecious species produce heavier seeds than dioecious and hermaphroditic species in lianas, but lighter seeds in shrubs and trees. Secondly, although our analyses corroborated the positive relationship between seed size and WSG (which is, in turn, positively correlated with longevity (Chave et al. 2006)), we found no significant interaction between WSG and breeding system. We found no difference between the WSG of shrubs and trees, but within both of these growth forms life-history strategy varies enormously, so the absence of a significant difference between them is unsurprising.
There is a strong phylogenetic signal in the distributions of seed mass, breeding system and growth form. All three traits are highly phylogenetically conserved, with λ values significantly different from 0 and very close to 1. This is as expected (see also Vamosi et al. 2003). By contrast, species abundances were distributed at random with respect to phylogenetic relatedness. Although there is no reason from an evolutionary perspective to expect that species abundances would appear to be phylogenetically conserved, if adult densities were determined by traits that were strongly correlated with dioecy, and if the persistence of dioecious species required that they maintain higher population densities, then abundances could be strongly correlated with breeding system, appearing to ‘co-evolve’ with dioecy when examined on a phylogenetic tree. In contrast to our prediction that dioecious species should exhibit evidence of a demographic advantage that compensates for the lower proportion of seed-bearing individuals, we found no evidence for this kind of joint change in breeding system and abundance.
differences between yasuní and tambopata
Here, we compare our results with those from another diverse Neotropical forest in the Tambopata Wildlife Reserve of Peru (Vamosi et al. 2008). In that study, the authors found evidence for the association between seed size and breeding system described above and, as in this study, the association varied according to growth form (Fig. 1): Dioecious lianas and shrubs, but not trees, were found to have larger seeds. What are the differences between these two forests that might explain these patterns? And why is the predicted pattern of larger seed size in dioecious species not found among the tree species at either site?
The distribution of seed size in the two communities is different (Figs 2 and 3). There are many more smaller-seeded shrubs at Tambopata than Yasuní. The species that make up the forest communities from which seed size was sampled are also different (although half of the 15 largest-seeded species in each flora belong to the same four families: Arecaceae, Chrysobalanaceae, Fabaceae and Lecythidaceae; Table 4). For instance, Cecropia contributes six species to the Yasuní data set, all of which are dioecious and have seeds < 0.005 g. There are no Cecropia species among the sampled species from Tambopata. Conversely, monoecious figs contribute 15 species to the Tambopata data, and have seeds < 1.6 mm3, whereas there is only one Ficus present in the Yasuní data.
Table 4. A comparison of the 15 largest-seeded species in Yasuní, Ecuador (current study) and Tambopata, Peru (Vamosi et al. 2008). Note that the units are different for the two floras. Code abbreviations: BS = breeding system, GF = growth form. The same four families (in bold) are disproportionately represented among the largest-seeded species in both floras
|Yasuní, Ecuador|| || || || || ||Mass (mg)|
|Tambopata, Peru|| || || || || ||Volume (mm3)|
| ||Icacinaceae||Casimirella||ampla||H||Liana||61 645.5|
other potential compensatory fitness advantages of dioecious species
Although we found limited evidence of an increase in seed size associated with an evolutionary divergence between cosexuality and dioecy, the amount of variation in seed mass explained by breeding system, growth form and WSG was low (R2 < 0.10 in most models, Tables 2 and 4), hence other mechanisms are likely to confer fitness advantages and enable dioecious species to persist in the face of competition with cosexual species. These mechanisms may include higher fecundity, higher rates of offspring recruitment, more frequent reproduction or higher quality offspring (with higher rates of survivorship). In most cases, such advantages are assumptions in models investigating the evolutionary ecology of dioecious lineages (e.g. Charlesworth & Charlesworth 1978; Heilbuth et al. 2001; Barot & Gignoux 2004; Vamosi et al. 2007). It is likely that, in most cases, a combination of traits will be involved. This prediction is based on two large-scale patterns reported for dioecious lineages. First, despite the relative rarity of dioecy among angiosperms, there are well-documented associations between dioecy and a number of ecological/life-history traits (reviewed by Renner & Ricklefs 1995), including a tropical distribution (Bawa 1980; Vamosi et al. 2003), fleshy fruits (Givnish 1980), plain flowers (Bawa 1980) and woody and climbing growth forms (Freeman et al. 1980; Vamosi et al. 2008). Secondly, focusing on the evolutionary success (i.e. relative species richness, scaled to that of its non-dioecious sister group) of dioecious lineages, Vamosi & Vamosi (2004) demonstrated that lineages that possessed three or four of the aforementioned correlates were more common and tended to have higher evolutionary success than those with two or fewer traits. Furthermore, particular combinations of traits (e.g. woody lineages with plain flowers but dry fruits) had higher evolutionary success than lineages with the same number of correlated traits, but in different combinations (e.g. woody lineages with fleshy fruits but showy flowers). Therefore, it is plausible that, for example, large seed size (and/or some associated but unstudied trait[s]) may compensate for some of the disadvantages of dioecy in certain forests (e.g. Carpenter et al. 2003; Vamosi et al. 2008), but not in other forests (e.g. the current study). Although there is evidence that differences in ecological traits do aid in the co-existence of many hundreds of species (Engelbrecht et al. 2007; John et al. 2007; Kraft et al. 2008), frequency-dependence (Queenborough et al. 2007b; Comita & Hubbell 2009), neutral population dynamics and dispersal limitation (Hubbell 2001) suggest that these differences are not necessarily essential.
In conclusion we have found no evidence of greater seed mass in dioecious species compared to their cosexual counterparts in the forest at Yasuní. Because trees and shrubs are longer-lived than herbs and therefore have more reproductive episodes over which to maximize fecundity, and due to physical and physiological constraints of the environment, an evolutionary increase in seed size associated with a change in breeding system may be less likely to occur in woody species (Vamosi et al. 2008). Other fitness advantages, such as lower rates of inbreeding, increased seed production, greater dispersal distances (Vamosi et al. 2007) and elevated seedling survival (e.g. through the production of better-defended seeds) may represent alternative life-history adaptations that enable dioecious tropical tree populations to persist.
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Fig. S1. Weighted mean seed size for Yasuní species.
Fig. S2. Mean abundance of Yasuní species by breeding system.
Table S1. Seed mass by growth form and breeding system in Yasuní species.
Table S2. Effect of seed mass on abundance in Yasuní species.
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Please note: Wiley Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.