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Division of Forest, Nature and Landscape Research, Catholic University of Leuven, Celestijnenlaan 200 E, B-3001 Leuven, Belgium; Research Institute for Nature and Forest, Kliniekstraat 25, B-1070 Brussels, Belgium
Received for publication February 21, 2006. Accepted for publication November 16, 2006.
ABSTRACT
In distylous, self-incompatible plants, clonal propagation, unbalanced floral morph frequencies, and reduced population size can interfere with the functioning of distyly by compromising legitimate intermorph pollinations, resulting in reduced reproductive output. Here, we examined the mating system and the impact of mate availability, population size, and spatial aggregation of morphs on reproductive output in the distylous, clonal, aquatic plant Hottonia palustris. Controlled pollinations under greenhouse conditions detected no spontaneous selfing without the action of a pollen vector (autonomous autogamy) and demonstrated very low fruit and seed development after self-pollination. Intermorph (legitimate) crossings resulted in high reproductive output in both floral morphs (long- and short-styled individuals), whereas intramorph (illegitimate) crossings decreased fruit and seed development by more than 50%, indicating that the species has partial intramorph-incompatibility. In natural populations, small population size and increasing deviation of floral morph frequencies negatively affected reproductive outcome. Individuals of the majority morph type developed significantly fewer fruit and seeds than individuals of the minority morph type. This rapid decline in fecundity was symmetrical, indicating that regardless of which morph was in the majority, the same patterns of negative frequency-dependent mating occurred. Increasing spatial isolation between compatible morphs significantly reduced fruit and seed set in both morphs similarly. This study provides clear indications of frequency- and context-dependent mating in natural populations of a distylous plant species.
Key Words: clonal propagation • frequency-dependent selection • heterostyly • Hottonia palustris • legitimate vs • illegitimate pollination • morph bias • pollen dispersal
Heterostylous breeding systems have evolved independently in 25 angiosperm families (Ganders, 1979
; Lloyd and Webb, 1992
). Heterostyly is a genetically controlled floral polymorphism exhibited by species having two (distyly) or three (tristyly) floral morphs that differ in the relative position of their stigmas and anthers (herkogamy). Theory suggests that disassortative pollen transfer between flowers, i.e., greater transfer between flowers of different morphs ("legitimate" transfer) than between flowers of the same morph ("illegitimate" transfer, see Barrett, 1990
), evolved to promote efficient pollen exchange between individuals (Lloyd and Webb, 1992
). Additionally, physiological barriers for self- and intramorph fertilization developed as a means to prevent selfing and the deleterious effects of inbreeding (Ganders, 1979
; Richards, 1986
; Barrett, 1988
). Both mechanisms usually lead to an equal morph ratio in equilibrium (isoplethy; Finney, 1952
), as a result of frequency-dependent selection (Heuch, 1979
; Clark et al., 1988
).
Reproductive success in self-incompatible heterostylous species is closely tied to rates of legitimate pollen transfer, so reductions in population size and/or unbalanced morph frequencies are expected to provoke sizeable decreases in seed output due to different reasons. First, small populations may fail to attract sufficient pollinators, resulting in limited pollen deposition and consequently lower fruit and seed production (e.g., Kéry et al., 2000
; Jacquemyn et al., 2002
, 2003
; Brys et al., 2003
, 2004
; Ashman et al., 2004
). Second, in polymorphic populations, sexual reproduction may also depend on morph frequencies (e.g., McCauley and Brock, 1998
; Thompson et al., 2003
). In largely morph-biased populations, one should expect that plants of the majority morph have fewer legitimate pollen donors from which pollen can received and fewer legitimate pollen recipients to which pollen can be exported, i.e., negative frequency-dependent mating. Such a shortage of legitimate pollen for flowers of the dominant morph may result in reduced fruit and seed set, and consequently lower overall reproductive output of the population. In this context, clonal growth may conflict with the benefits of exposing more floral displays (number of inflorescences), because it can result in strongly morph-biased populations and consequently frequency-dependent mating. Moreover, clusters of inflorescences resulting from vegetative propagation may, on the one hand, enhance limited pollen deposition (due to the preclusion of efficient pollen transfer resulting from herkogamy) (e.g., Harder and Barrett, 1996
), and, on the other, increase pollen discounting if geitonogamous pollen transfer occurs within or between inflorescences of the same genet. The latter may greatly reduce siring success if self-pollination triggers processes that compromise a pollen grain's chance of producing a viable seed, such as self-incompatibility (e.g., Harder and Barrett, 1996
).
In species with a rigid mating system, strong mating incompatibility should be particularly disadvantageous if populations have extreme size fluctuations and/or occupy ephemeral habitats. Under such circumstances, weak (or cryptic) incompatibility may assure progeny production during mate or pollinator scarcity (e.g., Barrett and Cruzan, 1994
; Eckert and Allen, 1997
). Hence, the strength of the incompatibility system in heterostylous plants may be determined, on the one hand, by the relative importance of avoiding self- and intramorph mating and, on the other, by fertility assurance and the likelihood of reproductive failure (e.g., Barrett and Cruzan, 1994
).
Many species in the Primulaceae are distylous, and in several studies on different Primula species, such as Primula elatior (Jacquemyn et al., 2002
), P. veris (Brys et al., 2003
; Kéry et al., 2003
), and P. vulgaris (Endels et al., 2002
; Brys et al., 2004
), reported indications of a morph bias effect on reproduction. However, none of these studies clearly unraveled the separate effects of morph bias and population size because both factors were strongly and negatively correlated.
In this study, we investigated the effects of population size, morph bias, and spatial distribution of compatible mates on sexual reproduction in natural populations of the distylous, aquatic, clonal herb Hottonia palustris L. (Primulaceae). Natural populations of this species are composed of two floral morphs that differ in style length. Populations were selected to disassociate population size and morph bias. To study the strength of the dimorphic incompatibility system and to unravel observed patterns of reproductive outcome in the field, we performed experimental hand-pollinations under greenhouse conditions.
More specifically, we tested the following hypotheses: (1) Do fruit and seed set differ following experimental selfing, illegitimate intramorph crossings, and legitimate intermorph crossings? (2) Do increasing unbalanced morph frequencies reduce reproductive success, and if so is there a negative frequency-dependent advantage to the rare morph? (3) Do the effects of population size and dominance in morph type on reproductive outcome interact, and if so can this be related to morph type? (4) Do increasing spatial isolation of inflorescences from compatible mating partners reduce reproductive outcome?
MATERIALS AND METHODS
Study species and site
Hottonia palustris, the water violet, is a distylous, herbaceous, perennial herb of shallow, stagnant to slow-flowing freshwater systems (Haslam, 1978
). This species is a widely distributed plant throughout lowlands of western Europe and northern Asia (Hegi, 1927
). Although the species prefers open, sunny, freshwater systems, it can also occur in the understory vegetation of wetland forests (Brock et al., 1989
). As in many aquatic herbs, H. palustris is dispersed by seeds and rhizomes and has a prolific capacity for clonal growth (Brock et al., 1989
). As a result, even large populations can have unbalanced floral morph ratios or contain only a single morph, similar to other heterostylous aquatic plants (e.g., Eckert and Barrett, 1995
; Shibayama and Kadano, 2003). If rosettes become generative, they develop one main 15–50 cm tall inflorescence, which produces up to 40 light-pink flowers. Although flowers are visited by a wide range of insect pollinators, such as several species of the Syrphidae and Empididae, our observations suggest that most pollinators are members of the Apidae (mostly honey bees and bumble bees). Hottonia palustris flowers from mid-May to mid-June and have a heteromorphic incompatibility mechanism (Ganders, 1979
). Moreover, it is a distylous species in which the flower morphs differ reciprocally in the heights of the stigmas and anthers, i.e., reciprocal herkogamy (Lloyd and Webb, 1992
). Long-styled flowers have their stigma placed outside the corolla tube and anthers placed within the tube, whereas short-styled flowers have their stigma concealed in the corolla tube and anthers protrude slightly beyond the corolla tube. Fruits ripen at the beginning of July, are 3–5 mm long, and contain up to 100 brown seeds.
The study was conducted near Ghent (northern Belgium, see Fig. 1), where H. palustris occurs in ditches and ponds.
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Treatments were conducted on 108 individuals obtained from two large populations (N > 1000) with relatively balanced morph frequencies. To ensure that the target plants were different genets, we selected individuals that grew at least 5 m from each other. In May 2004, 27 plants of each floral morph type were randomly selected per population and transplanted into concrete tanks in a greenhouse to exclude pollinators and prevent predation. Nine individuals were selected for each combination of population, treatment, and morph, for which six flowers were experimentally pollinated per plant. Per individual, only one pollination treatment was applied in order to prevent resource reallocation between developing fruits and thus, to avoid overestimation of the effects (reviewed in Knight et al., 2006
). Additionally, three flowers per plant were left unmanipulated to examine the possibility of autonomous self-pollination. The remaining unmanipulated flowers were used as pollen donors for the different experimental pollinations. Pollen for the inter- and intramorph crosses was obtained from at least five individuals and was mixed before deposition. Pollen was deposited evenly onto the whole stigmatic surface with brushes, resulting in an excess of pollen on stigmas.
Fruits were counted and collected when they were fully grown (mid-June). For each fruit, the number of seeds and number of ovules were counted, and fruit to flower and seed to ovule ratios were calculated.
The impacts of population size, floral morph ratios, and distance to the nearest legitimate mating partner on reproduction
To investigate the effects of population size and floral morph ratios on fruit and seed production, we selected 25 populations that were at least 250 m from other populations during spring 2004. For each population, population size was determined as the number of inflorescences (flowering shoots), which ranged from 1 to c. 2000. Hottonia palustris has one inflorescence per ramet, and all ramets are attached to rhizomes anchored to the sediment. This estimate of population size was used because we were unable to determine the number of genets due to vegetative propagation. This measure best reflects the maximum number of mates and the amount of pollen available for fertilization in any single year. Furthermore, the number of long- and short-styled inflorescences was counted in each population. Morph bias was then calculated as the difference in the number of long- and short-styled inflorescences, divided by the total number of inflorescences. Consequently, this value varies from –1 (only long-styled individuals present) to 0 (both morph types in equal frequencies) to 1 (only short-styled individuals present). The study populations were selected so that the absolute value of morph bias was not correlated with population size (rp = –0.340; N = 25; P = 0.197).
In each of the 25 study populations, 30 inflorescences (15 per floral morph type, if possible) were randomly selected and individually labeled with water-resistant tags. During May 2004, we recorded the morph and number of flowers for each selected inflorescence. When fruits were fully grown (mid-June), all locations were visited again to count the initiated fruits per inflorescence. At the same time, a maximum of five mature, unopened fruits were collected per inflorescence to determine the average number of seeds per fruit. If the total number of fruits per inflorescence exceeded five, total seed set per inflorescence was calculated as the average number of seeds per fruit multiplied by the total number of fruits per inflorescence. Consequently, four components of reproductive success were determined: (1) number of fruits per inflorescence, (2) proportion of flowers that developed into fruits, (3) number of seeds per fruit, and (4) total number of seeds per inflorescence.
To study the impact of the spatial distribution of morphs on reproduction, four populations were selected from the described sample of 25 populations. These populations were large (N > 250), had a relative equal balance in floral morph frequencies (morph ratio ranging between 1 : 1 and 2 : 3), and were characterized by a variable dispersion of morphs. Within these four populations, we measured the distance from the selected inflorescences to the nearest inflorescence belonging to the opposite floral morph and the same four components of reproductive success were determined.
Statistical analysis
Based on the hierarchical data structure (plants within populations and fruits within plants), we performed generalized linear mixed model analysis (GLMM) to test for the effects of controlled pollination treatments and morph (long- vs. short-styled) (fixed effects) on the number of ovules per flower, the proportion of fruits per flower, and the proportion of seeds per ovule (dependent variables). Plant and population were included as a random (categorical) variable to correct for random population and maternal effects.
The GLMM was also applied to test for effects of population size, floral morph bias, morph type, and intermorph distance on fruits per flower, seeds per fruit, and seeds per inflorescence in natural populations. In these analyses, population size, morph bias, and distance to the nearest mating partner were included as continuous covariates, whereas morph (long- vs. short-styled) was included as a categorical variable. Finally, population was entered as a random (categorical) variable to incorporate random effects and thus to avoid pseudoreplication.
A first analysis examined the overall impacts of population size, morph bias and morph on reproductive outcome. In this model, a quadratic function of morph bias was entered as a fixed factor, because negative frequency-dependence should result in optimal reproductive success at an equilibrium floral morph ratio (morph bias = 0) and decreased reproductive outcome at both sides of the 1 : 1 floral morph ratio. These analyses considered the number of fruits per flower and of seeds per fruit and per inflorescence as dependent variables, with population size, morph bias, (morph bias)2, and morph as fixed explanatory factors.
In a second analysis, we examined whether distance to the nearest mating partner affected reproductive output in four large and morph-balanced populations. This analysis considered the distance to the nearest inflorescence of the opposite morph, the morph (long- vs. short-styled), and their interactions as fixed explanatory factors and the numbers of fruits per flower and seeds per fruit and per inflorescence as dependent variables.
All statistical analyses were performed using the SAS 9.1 (SAS Institute, 2005
) statistical package. We used the MIXED procedure to analyze the mixed generalized linear model of normal distributed data (Littell et al., 2002
) and the GLIMMIX procedure for dependent variables with Poisson or binomial distributions. The latter analysis considered the log link function for Poisson variables and logit link function for dichotomous variables (proportional data) (SAS Institute, 2005
). All analyses were conducted using a backward elimination procedure to obtain the final model, in which significance of terms and the overall AIC of the model were used as a criterion for model selection. The Kenward–Rogers approximation was used to determine appropriate denominator degrees of freedom (Littell et al., 2002
).
RESULTS
Maternal fertility following selfing and outcrossing
In controlled pollinations, proportional fruit and seed set in H. palustris depended significantly on pollination treatment and the interaction between pollination treatment and morph (Table 1; Fig. 2). In general, total number of ovules per flower did not differ significantly between morphs, populations, and pollination treatment (P > 0.05). Fruit development after intermorph pollination did not differ significantly between the short- and long-styled individuals and was, respectively, 87.5% and 85.6% (Fig. 2a). Similarly, development of ovules into seeds did not differ significantly after intermorph pollination and was on average 61.1% and 70.5% in short- and long-styled individuals, respectively (Fig. 2b). Self-incompatibility was strong and not significantly different between morphs because it resulted on average in less than 5% fruit set and 3.5% seed development when flowers were pollinated with pollen of the same inflorescence (Fig. 2a, b). In contrast, illegitimate intramorph crossings resulted in intermediate fruit and seed set between the selfing and intermorph crossing treatments and differed significantly between morphs, as indicated by the significant interaction between pollination treatment and morph (Table 1; Fig. 2a, b). Intramorph crossing resulted in lower fruit set for short- (25.9%) vs. long-styled individuals (56.3%) and differed significantly from fruit set in the other pollination treatments (Fig. 2a). Furthermore, short-styled individuals set fewer seeds (13.1%) than the long-styled individuals (26.7%) (Fig. 2b). Finally, unmanipulated flowers produced no fruits.
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Maternal fertility after selfing and crossing
Unlike the vast majority of heterostylous species, which have strong intramorph-incompatibility (Ganders, 1979
; Richards, 1986
), distyly in H. palustris is apparently not associated with strict physiological incompatibility in both morphs. A rigid mating system imposed by strong self-incompatibility would be particularly disadvantageous for species subject to large population fluctuations and/or occupying ephemeral habitats. Under such circumstances, weak (or cryptic) intramorph-incompatibility permits a flexible mating strategy that leads to the production of legitimate progeny during mate or pollinator abundance and to the production of at least some illegitimate seed production during mate or pollinator scarcity (Becerra and Lloyd, 1992
; Cruzan and Barrett, 1993
). In this context, Barrett and Cruzan (1994)
suggested that such incompatibility systems operate in a quantitative manner, depending on the local pollen environment. When large pollen loads are deposited, intense pollen competition excludes illegitimate matings, whereas with smaller pollen loads, seeds can be produced by illegitimate pollen, too (Barrett and Cruzan, 1994
). Such leaky self-incompatibility systems are more likely to occur in animal-pollinated species, that are subject to wide fluctuations in population size and thus mate availability. The population biology of H. palustris may have contributed to the evolution of the observed weak heteromorphic incompatibility system. Like many aquatic plants (e.g., Cruzan and Barrett, 1993
; Eckert and Allen, 1997
; Shibayama and Kadono, 2003
; Wang et al., 2004), the water violet occupies ephemeral habitats (ponds or rivulets that periodically dry up), which are associated with strong population size fluctuations (Brock et al., 1989
; R. Brys and H. Jacquemyn, unpublished data).
The results of the hand-pollination experiment further revealed very poor fruit set and almost no seed production after selfing (geitonogamy) for both morphs. This strong reproductive difference between cross- (both legitimate and illegitimate pollinations) and self-pollination may evolve as a strategy to avoid inbreeding depression (e.g., Barrett and Cruzan, 1994
; Eckert and Barrett, 1994
).
Maternal fertility and population size
In natural H. palustris populations, all measures of maternal fertility decreased significantly with decreasing population size. Given that the water violet cannot reproduce sexually via autonomous selfing, the observed fruit and seed production levels resulted only from active pollen transfer by pollinators. The latter suggests reduced pollen transfer in small populations, probably as a result of unreliable pollinator services, a form of Allee effect (Groom, 1998
).
On the other hand, our observations revealed that fruit and seed production in large and morph-balanced populations equal those resulting from supplemental hand-pollinations. This observation supports Darwin's cross-pollination hypothesis, in which the reciprocal placement of stigmas and anthers (reciprocal herkogamy) promotes efficient pollen transfer (legitimate crossing) in distylous species via pollen segregation on pollinators' bodies and disassortative pollen dispersal between morphs (e.g., Wolfe and Barrett, 1989
; Kohn and Barrett, 1992
). In contrast, low seed production of inflorescences in both long- and short-styled monomorphic water violet populations suggests that intramorph pollinations may, however, occur in extreme unbalanced situations.
Spatial distribution of mating types and frequency-dependent mating
As expected, skewed morph frequencies and increasing spatial isolation of morph types in relation to their compatible mating type clearly reduced reproductive success in H. palustris. Very low fruit set was observed when morphs were more than 10 m apart, suggesting that transfer of compatible pollen mainly occurs within a few meters from the pollen donor. This is in accordance with field observations of foraging pollinators within H. palustris populations (R. Brys and H. Jacquemyn, unpublished results), which typically move between nearby flowering inflorescences. The significant and steep decline in fertility with distance, both in long- and short-styled individuals, parallels observations of pollen dispersal in other animal-pollinated plants. For instance, Ishihama et al. (2003)
reported that in the related Primula sieboldii, the mean pollen-transfer distance was 7.23 m. Similarly, Wang et al. (2004) showed an even stronger decline in maternal fertility with increasing distance to the nearby mating partner in the distylous, self-incompatible Nymphoides peltata (Wang et al., 2005).
The evolutionary maintenance of sexual polymorphisms, such as distyly, is usually ensured by frequency-dependent selection during mating (Clark et al., 1988
). Provided that there are no inherent fitness differences among morphs (differences that are expressed independent of the morph composition of the population), negative frequency-dependent selection during sexual reproduction should result in equal morph frequencies at equilibrium (Heuch, 1979
). The rate at which populations will reach equilibrium will, however, depend on several factors such as the life-history of the plant, the extent of clonal growth, the number of loci controlling the mating type, outcrossing rate, and the ratio between random and disassortative mating (e.g., Eckert and Barrett, 1992
; Eckert et al., 1996
). In the studied water violet populations, inflorescences belonging to the majority morph indeed had substantial reductions for all measured aspects of reproductive success, especially in largely unbalanced populations. Neither the number of flowers nor ovules per flower differed between long- and short-styled inflorescences, so this reproductive difference between morphs indicates negative frequency-dependent mating in unbalanced populations, resulting in a reproductive advantage to the rare morph. Additionally, the rapid decline in fruit and seed set with increasing unbalance of morph frequencies was symmetrical, suggesting that regardless of which floral morph was in majority, the same pattern of negative frequency-dependent reproduction occurred. This finding is surprising based on the outcome of the hand-pollination experiment. Indeed, short-styled individuals were shown to produce significantly fewer fruits and seeds after illegitimate-pollination compared to long-styled individuals. Although the latter supports the expectation that short-styled individuals should be more sensitive to the negative impact of a morph bias effect, this tendency was neither confirmed by asymmetry in reproductive outcome in long- vs. short-styled-biased populations (not even in monomorphic populations) nor in agreement with our observation of a similar decline in female reproductive success with distance to the opposite morph type in both long- and short-styled individuals.
A possible explanation for these seemingly contradicting observations might be found in the floral pollination mechanism of distylous species, in which reciprocal herkogamy precludes efficient intramorph pollen transfer. Harder and Barrett (1996)
indeed demonstrated that herkogamy clearly limited pollen transfer in experimentally created monomorphic populations of Eichornia paniculata, even after frequent visitation of pollinating bees (also see Kohn and Barrett, 1992
). Furthermore, Ganders (1979)
and Piper and Charlesworth (1986)
suggested that intramorph pollination in distylous species results primarily from geitonogamous self-pollination. This might be also the case in H. palustris, especially given its pronounced clonal propagation and the local foraging of bees within H. palustris populations. Nevertheless, substantial illegitimate intramorph-pollination is likely (especially in the monomorphic populations) because the hand-pollination experiment revealed that it can result in different fruit and seed production by long- and short-styled individuals. Because we did not observe such indications in the morph-biased populations, the question remains: does reciprocal herkogamy in H. palustris promote sufficient disassortative mating to explain the observed reproductive patterns, or does it act in combination with other processes, such as, morph-specific differences in legitimate pollen transfer (e.g., Massinga et al., 2005
)? Unfortunately, the present data do not allow tests of such hypotheses. Therefore, future work should consider pollinator behavior and pollen transfer patterns, together with determination of clone sizes based on genetic markers.
Although, the impact of unbalanced floral morph ratios on reproductive outcome has been rarely reported in natural populations of heterostylous plants (but see Eckert et al., 1996
; Thompson et al., 2003
; Barrett et al., 2004
; Wang et al., 2005
), our study clearly illustrates frequency- and context-dependent mating in natural populations of a distylous species. Such aggravated reproductive reduction in the majority morph, with an increasing unbalance of morph frequencies in natural populations, is in accordance with earlier indications of a morph bias effect in some Primula species, such as the distylous P. elatior (Jacquemyn et al., 2002
) and P. veris (Brys et al., 2003
). Both studies reported that reproductive output was more variable among plants when population size and mate (morph) availability decreased, indicating increased uncertainty of successful legitimate pollen transfer between individuals. Similarly in the distylous Primula vulgaris, individuals of the common floral morph also experienced significantly reduced fecundity compared to individuals of the minority morph, suggesting the occurrence of similar negative frequency-dependent reproductive patterns (Brys et al., 2004
).
FOOTNOTES
1 The authors thank D. Bogaert, F. van den Boscche, and L. Martens for their useful help by locating the studied populations, D. Bauwens and F. Hendrickx for statistical help, and two anonymous referees for their constructive comments on an earlier draft of this manuscript. This study was supported by the Flemish Fund for Scientific Research. 
2 Author for correspondence (e-mail: Rein.Brys{at}inbo.be
)
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= long-styled individuals (continuous line); dotted line is the regression line of the population mean. See 