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Reproductive Biology |
2Departamento de Biologia Vegetal y Ecologia, Universidad de Sevilla, Apdo-1095, 41080 Sevilla, Spain; 3Department of Systematic and Evolutionary Botany, Institute of Botany, University of Vienna, Rennweg 14, A-1030 Vienna, Austria
Received for publication February 15, 2005. Accepted for publication August 16, 2005.
ABSTRACT
We studied the relationships between self-incompatibility mechanisms and floral parameters in the genus Hypochaeris L. sect. Hypochaeris (consisting of H. glabra, H. radicata, H. arachnoidea, and H. salzmanniana). We assessed at intra- and interspecific levels (1) the self-incompatibility (SI) mechanism and its distribution among populations, (2) the relationship between SI and floral parameters, and (3) the relationship of SI to reproductive success. Hypochaeris salzmanniana is semi-incompatible, H. glabra is self-compatible, and H. arachnoidea and H. radicata are self-incompatible. Floral parameters differed among populations of H. salzmanniana: plants in self-compatible populations had fewer flowers per head, a smaller head diameter on the flower, and a shorter period of anthesis than self-incompatible populations. We also detected this pattern within a semi-compatible population of H. salzmanniana, and these differences were also found between species with different breeding mechanisms. Fruit to flower ratio in natural populations was generally high (>60%) in all species, regardless of breeding system. It is hypothesized that self-compatibility may have arisen through loss of allelic diversity at the S locus due to bottleneck events and genetic drift.
Key Words: Asteraceae • floral parameters • Hypochaeris • S alleles • sporophytic self-incompatibility • reproductive success
In flowering plants, three major systems of self-incompatibility (SI) are known: homomorphic gametophytic SI (GSI), homomorphic sporophytic SI (SSI), and heteromorphic SI (HetSI) (see review by Hiscock and Kües, 1999
). Both homomorphic systems have a genetic control, usually of one gene with multiple alleles; however, whereas in GSI the S genotype of the haploid (usually two-celled gametophyte) pollen effectively determines the SI reaction, in SSI the incompatibility reaction of the (usually three-celled gametophyte) pollen is determined by both S alleles present in the pollen parent. Moreover, whereas the S alleles are codominant in GSI (see model in Talavera et al., 2001
), in all SSI cases analyzed thus far, the S alleles have a hierarchy of dominance–recessive interactions, which often differ in the stigma and pollen grain of the same plant. A consequence of such interactions is in crosses that have an S allele common to both parents; progeny homozygous for the incompatibility gene may be produced (Williams, 1965
).
The homomorphic sporophytic self-incompatibility (SSI) mechanism was established in the Asteraceae by Gerstel (1950)
for Parthenium argentatum (Anthemideae) and by Hughes and Babcock (1950)
for Crepis foetida subsp. rhoeadifolia (Lactuceae). Since then, self-incompatibility in Asteraceae has been recorded in 40 genera (Charlesworth, 1985
). Within Lactuceae, self-incompatibility has been found in several species of Leontodon (Izuzquiza and Nieto Feliner, 1991
; Ruiz de Clavijo, 2001
) and in Crepis sancta (Cheptou et al., 2000
), Reichardia picroides (Gallego, 1983
), Hypochaeris radicata (Parker, 1975
), H. maculata (Wells, 1976
), and Stephanomeria exigua subsp. coronaria (Gottlieb, 1973
; Brauner and Gottlieb, 1987
). In addition to Asteraceae, this complex self-incompatibility mechanism is known in only five dicotyledonous families: Betulaceae, Brassicaceae, Caryophyllaceae, Convolvulaceae, and Polemoniaceae (Hiscock and Kües, 1999
).
The number of S alleles in populations of species with SSI is relatively poorly documented in the Asteraceae: six S alleles (Brennan et al., 2002
) and 7–11 (Hiscock and Tabah, 2003
; Brennan et al., 2003
) in Senecio squalidus, 6–8 in Carthamus flavescens (Imrie and Knowles, 1971
), and 16 in Centromadia pungens subsp. laevis (Friar and LaDoux, 2002
). These rather low numbers of S alleles differ from reports for species of other SSI families: Brassicaceae—e.g., 22 in Iberis amara (Bateman, 1954
), 20–30 in Brassica campestris (Nou et al., 1993
), 22 in Raphanus raphanistrum (Karron et al., 1990
), 52 in Sinapis arvensis (Stevens and Kay, 1989
); Convolvulaceae—e.g., 49 in Ipomoea trifida (Kowyama et al., 1994
, 2000
).
The occurrence of some self-compatible individuals within self-incompatible populations is relatively frequent and has been observed in Asteraceae species such as Carthamus flavescens (Imrie and Knowles, 1971
), Stephanomeria exigua subsp. coronaria (Brauner and Gottlieb, 1987
), Rutidosis leptorrhynchoides (Young et al., 2000
), and Senecio squalidus (Brennan et al., 2002
); in Brassicaceae species such as Leavenworthia crassa and L. alabamica (Lloyd, 1968a
, b; Solbrig and Rollins, 1977
), and in Convolvulaceae such as Ipomoea trifida (Kowyama et al., 1994
, 2000
; Kakeda et al., 2000
).
Occasional self-compatible individuals, in the absence of apomixis, are unlikely to persist in a population with a moderate number of alleles at the S locus if the mutated allele (Sc) is not dominant in the allelic series. However, in the family Asteraceae, the number of S alleles at the S locus may be low (Imrie and Knowles, 1971
; Hiscock and Tabah, 2003
; Brennan et al., 2003
), and in these circumstances, if the self-compatibility is inheritable and mate availability is limited, then self-compatible individuals would be selected and the population would become self-compatible. Pollen limitation is considered to be a condition favoring the breakdown of self-incompatibility (Baker, 1955
; Charlesworth and Charlesworth, 1979
).
In many SI species, some plants produce a low proportion of seeds with self-pollen. This phenomenon is known as pseudo-self-compatibility (PSC) (see Nettancourt, 1977
) or pseudo-self-fertility. In the PSC plants, cross-pollen has an earlier germination and more rapid tube growth than self-pollen, whereas plants with true self-compatibility (SC) have similar seed production following self or cross pollinations, with similar germination and growth rates of self- and cross-pollen tubes. Pseudo-self-compatibility allows some seed production following crosses between individuals that share both S alleles (Levin, 1996
).
In the Asteraceae, the self-incompatible species have, in general, bigger heads than the congeneric self-compatible ones. Gibbs et al. (1975)
, in a study of five species of Senecio, found that the three incompatible species (S. joppensis, S. aetnensis, and S. squalidus) had a larger head diameter than the self-compatible species (S. viscosus and S. vulgaris), and Parker (1975) showed that SI Hypochaeris radicata has bigger heads than SC H. glabra. This pattern has also been observed in other self-incompatibility systems, as in Eriotheca (Oliveira et al., 1992
), with late-acting self-incompatibility, Anagallis (Gibbs and Talavera, 2001
), with GSI, and also, in general, in allogamous species as opposed to their autogamous congenerics (see Levin, 2000
). But, intraspecific information is scarce on how such changes in the size of flowers or inflorescences have accompanied the change from self-incompatibility toward self-compatibility.
The present study focuses on all the species of Hypochaeris sect. Hypochaeris (H. glabra L., H. radicata L., H. arachnoidea Poir., and H. salzmanniana DC.). We address the following objectives: (1) the occurrence of SI at species and population levels, (2) whether flower number and diameter of the head and length of period of anthesis of the head vary with the degree of self-compatibility in populations of the different species, and (3) compare the pre-emergent reproductive success (fruit to flower ratio) in natural populations.
MATERIALS AND METHODS
Section Hypochaeris: species, populations and metapopulations
Hypochaeris sect. Hypochaeris contains four species, H. glabra L., H. radicata L., H. arachnoidea Poir., and H. salzmanniana DC. In phylogenetic molecular analyses (Tremestsberger et al., 2005), this section is monophyletic, with H. glabra sister to H. radicata, H. arachnoidea, and H. salzmanniana and with H. radicata sister to H. arachnoidea and H. salzmanniana.
In the Asteraceae, flowers show protandry and develop centripetally within the head. In species of Hypochaeris sect. Hypochaeris, the heads show nystinastic movements during anthesis, which lasts 3–10 days. Flowers in the head open daily late in the morning and close in the evening, allowing pollen in the anthers of the inner male-phased flowers to touch the stylar branches of the outer female-phased ones.
The differential morphological characters, ecology, and distribution of the four species of sect. Hypochaeris are shown in Table 1. Localities of the studied populations are given in Appendix. Hypochaeris salzmanniana is the most restricted species, with only eight known populations in Spain and eight in Morocco (Fig. 1). In recent molecular studies using the AFLP technique in H. salzmanniana from Spain (Tremetsberger et al., 2004
) and from Morocco (M. Ortiz et al., unpublished manuscript), the populations from Conil (pop. 1, see Fig. 1), Barbate (pop. 2), and Los Caños (pop. 3) were shown to form a metapopulation (Barbate metapopulation) that contains more than 90% of the Spanish plants (2 x 106–3 x 106 individuals). Of the other Spanish populations, three (Zahara, pop. 6; Punta Paloma, pop. 7; and Los Algarbes, pop. 8) are small and isolated, and the other two (Palmones, pop. 4 and La Linea, pop. 5) form another well-differentiated metapopulation (Bahia de Algeciras metapopulation) (Fig. 1). The Moroccan populations are structured into three groups: two small ones near Tangiers (Tanger, pop. 9 and Asilah, pop. 10) and a third consisting of six populations (pops. 11–16) that form a metapopulation (La Mamora metapopulation) containing more than 90% of the individuals of H. salzmanniana in Morocco (>107 individuals) (Fig. 1). We compared the floral parameters (number of flowers per head, diameter of the head, and duration of anthesis of the head) at an individual, population and metapopulation level.
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Self-incompatibility
In all of the hand-pollination experiments, we used plants that originated from field-collected seeds (each seed from a different mother plant) or seedlings transplanted from the field (mother plants or seedlings at least 2 m apart). Plants were cultivated in the glasshouse of the University of Seville in 2001, 2002, and 2004. The photoperiod (16 h light/8 h darkness), temperature (18–22°C), and watering (every 4 h) were controlled. Individual plants were grown in plastic pots (18 x 15 cm) in a substrate of peat and perlite (3 : 1 v/v).
Once the flowering period had begun in Hypochaeris glabra, H. radicata, and H. salzmanniana, we carried out a series of diallel crosses within populations. These comprised seven individuals of H. glabra, 12 of H. radicata, and nine of H. salzmanniana. To avoid pests or pollen contamination, all plants under treatment in the greenhouse were covered by a translucent white cloth. Most pollinations were effected by rubbing the two heads together or by rubbing a cotton-tipped swab against the inner pollen-bearing flowers and then against the stigmas of the outer ones of the same head (self-crosses) or the head of a different individual (outcrosses). This operation was repeated at least twice during the period of anthesis of the head; 2–4 (8) heads on each individual were not pollinated and used as a control. After the period of anthesis, all heads were individually bagged until fruit collection (after at least 25 days). We counted flowers and fruits with embryos and estimated fruit to flower ratio (number of flowers transformed into fruits).
In a preliminary experiment to determine whether automatically selfed heads (i.e., pre-anthesis bagged heads that were not hand-pollinated) had a different fruit to flower ratio to hand self-pollinated heads (geitonogamy), we applied a GLM (general linear model) considering the individual as a block effect. We did not detect any statistical difference between these treatments (hand self-crosses and automatic self-crosses, with heads covered with tea bags during anthesis) for the fruit to flower ratio (Ortiz et al., unpublished data). This lack of difference indicated that hand self-pollinations were unnecessary to determine self-compatibility and allowed us to subsequently study self-incompatibility in a larger number of populations and plants per population, by simply bagging pre-anthesis heads.
An individual is considered as SI when the fruit to flower ratio of its heads is null, PSC when the fruit to flower ratio of its heads is >0 and 
0.12, and as SC when the ratio is >0.12. For statistical analyses, PSC individuals were considered as SI. In this study, we used 771 individuals belonging to 57 populations (13 of H. glabra, 21 of H. radicata, 7 of H. arachnoidea, and 16 of H. salzmanniana).
Parameters of head in anthesis
We obtained head measurements from the same plants used in the self-incompatibility study (under the same growing conditions). The first heads of at least four individuals were marked and left unpollinated. For these heads, we measured the head diameter at midday (1200–1500 hours) on the second or third day of the period of anthesis, and also noted the number of days the head was open. This allowed us to relate the SC or SI status of each individual with its head characteristics. These variables were measured in 269 heads of 103 individuals of 16 populations of the four species.
Fruit to flower ratio in natural populations
Reproductive success in the wild was studied in 3–56 individuals per population, selecting, in each case, individuals both from the inner and the outer parts of the population area. All sampled individuals were chosen randomly, at least 2 m from each other. We selected the head of the main stem of each plant, and, once dry in the laboratory, we counted the number of flowers and achenes with embryos. All the Moroccan populations were sampled in the spring of 2003 and the Spanish ones during 2002 and 2003. In total, 407 individuals (43 individuals in three populations of H. glabra, 59 individuals in nine populations of H. radicata, 66 individuals in five populations of H. arachnoidea, and 185 individuals in 14 populations of H. salzmanniana) were studied.
Statistical analyses
Statistical analyses were carried out with JMP, version 4.0.1 (SAS Institute, Cary, North Carolina, USA.). Fruit to flower ratios were arcsine-square root transformed prior to analyses. To examine differences among individuals, populations (or metapopulations), and species for the number of flowers per head, head diameter, and length of the period of anthesis, we applied GLM analyses, considering the individual (nested within populations and species) as a random effect and the species and population (nested within species) as fixed effects; random effects were evaluated using the method of moments (EMS, expected mean square). A post-hoc Tukey-Kramer honestly significant difference (HSD) test was applied to detect differences in these variables among populations and species (considering for each species all the individuals of a population if there was only one population and mean values of different populations if more than one). We considered significant differences at a 5% confidence level (Bonferroni correction applied). Finally, for H. salzmanniana, we applied a principal components analysis (PCA) on correlations among number of flowers, diameter of head, and duration of anthesis.
RESULTS
Self-incompatibility
In the diallel of seven plants of Hypochaeris glabra, all the hand-pollinated heads, both selfs and crosses, as well as the nonhand-pollinated controls, produced viable fruits, with an average fruit to flower ratio per plant of 0.79–0.98 and 0.52–0.91 in hand selfs and crosses, respectively.
Every individual (N = 178) of the 13 sampled populations of H. glabra developed a high number of viable fruits in bagged heads (Table 2), with an average fruit to flower ratio >0.60 (data not shown). We conclude, therefore, that every individual in this species is self-compatible and predominantly geitonogamously self-pollinated.
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All plants (N = 79) of the seven populations of Hypochaeris arachnoidea behaved as self-incompatible (Table 2).
In Hypochaeris salzmanniana, of the nine individuals used in diallel crosses, four were self-compatible and five were self-incompatible (Fig. 3). Individual 9 had, as female and as male, the same pattern as individual 7. That is, they were the same compatibility phenotype, whereas the other three individuals (nos. 3, 6, and 8) had different compatibility phenotypes (see Fig. 3). In SC plants, the average fruit to flower ratio was 0.22–0.75 for the self-crosses, and 0.47–0.72 for outcrosses (data not shown); in SI individuals the fruit to flower ratio was 0.16–0.40 for outcrosses (data not shown).
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In the three species with self-incompatible individuals (Hypochaeris radicata, H. arachnoidea, and H. salzmanniana), a variable proportion of the individuals developed heads after selfing, bearing 1–8 fruits with embryos (Table 2). All these individuals have been considered as pseudo-self-compatible (PSC). In H. arachnoidea only one PSC individual was found in pop. 1 (7% PSC value), whereas in H. radicata we found 23 PSC individuals (of 205 plants): 11 from Spain (pops. 2, 33%; 4, 13%; 6, 25%; 7, 7%; and 9, 13%), one from Sicily (pop. 12, 20%), three from Morocco (pops. 14, 50%; and 17, 25%), and eight from Americas (pops. 18, 19%; 20, 29%; and 21, 40%). In H. salzmanniana, of 309 plants we found 26 PSC individuals: six, four, and 11 PSC individuals from Barbate (6%), Bahia de Algeciras (8%), and La Mamora (16%) metapopulations, respectively, and the rest (five individuals) from the two most northern Moroccan populations (pops. 9, 30%; and 10, 20%).
Floral parameters
Number of flowers per head
Hypochaeris arachnoidea and H. salzmanniana possess heads with the lowest number of flowers and H. radicata with the highest number (Fig. 4A). The GLM applied was significant (F102,166 = 13.57; P < 0.0001; R2 = 0.8271) as were all the effects considered (individual, population, and species; Table 3). However, the number of flowers/head was not statistically different between H. glabra and H. radicata or between H. glabra, H. salzmanniana, and H. arachnoidea (Fig. 4A).
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In Hypochaeris salzmanniana (Tukey-Kramer HSD test: q* = 3.34; 
= 0.016) we found that three SC populations of H. salzmanniana (pops. 6, 7, and 8) have a significantly lower number of flowers per head (mean ± SE = 69.30 ± 1.95) than the SI individuals from the Barbate and Bahia de Algeciras metapopulations, and of the SC populations, the individuals of the Los Algarbes population had a significantly lower number of flowers per head than the individuals from the populations at Punta Paloma and Zahara (Fig. 5A).
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= 0.016), whereas we did not find significant differences among H. arachnoidea, H. salzmanniana, and H. radicata (Fig. 4B). In Hypochaeris radicata, mean values of head diameter of the six studied populations were not significantly different, but we did find significant differences among populations and metapopulations of H. salzmanniana.
In Hypochaeris salzmanniana, the means of the three SC populations (pops. 6–8; mean ± SE = 30.97 ± 0.39) were equal and significantly lower than those for individuals from the Barbate metapopulation (mean ± SE = 38.97 ± 0.63) (regardless of whether they were SC or SI) and also the Bahia de Algeciras metapopulation (Fig. 5B).
Length of the period of anthesis of the head
In Hypochaeris glabra, 83% of the analyzed heads were in anthesis for 3 days and the remaining 17% for 4 days. Heads of the other species, in general, last longer, up to 10 days (Fig. 4C). The GLM analysis applied was significant (F102,166 = 9.84; P < 0.0001; R2 = 0.7708), as were all the effects considered (Table 3). The heads of H. glabra had a duration of anthesis much shorter than those of H. arachnoidea, H. radicata, and H. salzmanniana (Tukey-Kramer HSD test: q* = 3.36; = 0.016). In H. radicata, the mean duration of anthesis of the head did not differ significantly among the six populations, but we did find significant differences among the populations and metapopulations of H. salzmanniana (Fig. 5C) (Tukey-Kramer HSD test: q* = 4.78; = 0.016).
In Hypochaeris salzmanniana (Tukey-Kramer HSD test: q* = 3.34; = 0.016), the duration of anthesis of the heads in individuals from the three SC populations (pops. 6, 7, and 8) and SC individuals from the Barbate metapopulation had a significantly lower mean (mean ± SE = 5.39 ± 0.08) than the SI ones (mean ± SE = 7.79 ± 0.16) (Fig. 5C).
Correlation of floral parameters in Hypochaeris salzmanniana and relationship with self-compatibility
The PCA applied to the number of flowers per head, head diameter, and duration of anthesis showed that they are highly correlated (Fig. 6). PC1 accounted for 87.16% of the variance and showed high correlation with variation in the three features (Pearson correlation coefficients of 0.9118, 0.9691, and 0.9282, respectively); PC2 accounted for only 8.92% of the variance and was not strongly correlated with any of the measured variables (Pearson correlation coefficients of 0.3970, –0.0619, and –0.3259, respectively).
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Fruit to flower ratio in natural populations
The reproductive success (flowers that result in fruits, or fruit to flower ratio) of all species and almost all populations is very high (generally >0.80). At the population level, the lowest fruit to flower ratios were encountered in Tiznit (pop. 6; Morocco) for H. arachnoidea (ratio = 0.68; Fig. 7A), in Doñana (pop. 7; Spain) for H. radicata (ratio = 0.18, Fig. 7B) and in the Barbate metapopulation (pops. 1–3; Spain) for Hypochaeris salzmanniana (ratio = 0.63 on average, Fig. 7C). The GLM analysis testing differences in fruit to flower ratio among species and populations was significant (F22,329 = 7.56; P < 0.0001; R2 = 0.2912; Table 3). The mean fruit to flower ratio in the Doñana population of H. radicata and that of the Tiznit population of H. arachnoidea were statistically different from the rest of the populations in their respective species (Tukey-Kramer HSD test: q* = 3.24, = 0.05 for H. radicata and q* = 2.81, = 0.05 for H. arachnoidea). In the analysis of H. salzmanniana, statistically significant differences (Tukey-Kramer HSD test: q* = 2.88; = 0.05) were only found between the means of two large metapopulations at Barbate (mean ± SE = 0.66 ± 0.03) and La Mamora (mean ± SE = 0.84 ± 0.02). These two metapopulations had differences in patterns of fruit to flower ratio (Fig. 8): whereas in the Barbate metapopulation 39% of the plants had a ratio <0.50, in the La Mamora metapopulation only 8% of plants had a ratio <0.50.
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Self-incompatibility vs. self-compatibility
The 21 populations of Hypochaeris radicata and the seven populations of H. arachnoidea were self-incompatible, whereas the 13 populations of H. glabra were self-compatible. H. salzmanniana had varied breeding systems.
In the diallel cross series with H. radicata and H. salzmanniana, the frequency of positive or negative results that follow the crossing direction indicates that many individuals have a common allele at the S locus, and these S alleles have a different dominance patterns in the pistil and the pollen grain. This pattern is characteristic of the sporophytic self-incompatibility mechanism (SSI) as established for other Asteraceae genera such as Crepis (Hughes and Babcock, 1950
), Parthenium (Gerstel, 1950
), Senecio (Hiscock, 2000a
; Brennan et al., 2002
, 2003
; Hiscock and Tabah, 2003
), Cosmos (Crowe, 1954
), Carthamus (Imrie and Knowles, 1971
; Imrie et al., 1972
), Rutidosis (Young et al., 2000
), and Centromadia (Friar and LaDoux, 2002
).
In H. salzmanniana, of the 310 individuals from 16 populations, 197 were self-incompatible and xenogamous and 113 self-compatible and potentially geitonogamous (see Fig. 1). All the SC individuals of H. salzmanniana belonged to six populations: in three of these (Zahara, pop. 6; Punta Paloma, pop. 7; and Los Algarbes, pop. 8), the samples were comprised entirely of SC individuals (12, 29, and 20 studied individuals, respectively). However, in the other three populations (Conil, pop. 1; Barbate, pop. 2; and Los Caños, pop. 3) belonging to Barbate metapopulation, we found both SC individuals (18, 22, and 13 studied individuals, respectively) and SI (included PSC) individuals (18, 31, and 6 studied individuals, respectively) with an average percentage of SC individuals of 49% for this metapopulation. These self-compatible or partially self-compatible populations are all located in the NW periphery of the distributional area of the species (Fig. 1), and the occurrence of autogamous populations at the edge of a distribution area is a relatively frequent situation, e.g., "Baker's Law" (Baker, 1966
). However, to our knowledge, the co-occurrence of SC and SI individuals in the same population, as found in the Conil, Barbate, and Los Caños populations of H. salzmaniana, is a novel situation.
Diverse genetic models have been proposed to explain the loss of self-incompatibility in SSI systems. In Ipomoea trifida (Convolvulaceae), a species with the SSI mechanism, only one individual in a sample of 224 Central American populations was self-compatible (Kowyama et al., 1994
, 2000
; Kakeda et al., 2000
). These authors concluded that self-compatibility is due to a mutation in the S locus (Sc), and that the Sc allele is the most recessive among all the alleles in the series (49 alleles of the S locus) except for S3 (Sc > S3). Obviously, a mutation at the S locus, which produces a weakly dominant allele in a large allelic series, as described by Kowyama et al. (1994)
, should not lead to the loss of self-incompatibility in more than a few individuals in the population. This might explain why SC individuals are so infrequent in SI populations, as found here in H. radicata and H. arachnoidea or in SI populations of other species (see Introduction). Similar results were reported by Brauner and Gottlieb (1987)
in Stephanomeria exigua subsp. coronata (Asteraceae, and like Hypochaeris, tribe Lactuceae), native from Oregon (USA). Another model for loss of SI in SSI taxa was described in Brassica campestris and B. oleracea (Brassicaceae) where some mutations at loci unlinked to the S locus can cause the breakdown of self-incompatibility (Hinata et al., 1983
; Nasrallah, 1989
).
A sequence of events, can be proposed to explain the change of a population from SI to full SC: (1) a mutation of the S locus originating an allele (Sc), which is dominant over other wild Si alleles in the population (Sc > Si); (2) enhanced fitness of the self-compatible individuals and, particularly, the selfing-progeny (ScSi or ScSc) in comparison to the self-incompatible individuals and the outcrossed progeny; (3) a bottleneck event (founder effect or a decrease of the population size), which would reduce the S allele variability, with consequent diminished mate availability (for models, see Imrie et al., 1972
, and Byers and Meagher, 1992
), may favor the evolution towards self-compatibility (Baker, 1955
; Charlesworth and Charlesworth, 1979
). Similarly, diminished pollinator availability might permit genetic drift and selection to favor the mutated S allele, leading to homozygosis of this S allele (ScSc).
The results from the diallel crosses involving individuals of H. salzmanniana from Conil (pop. 1) provide an insight into the number of alleles at the S locus controlling the self-incompatibility mechanism. In the nine individuals of this diallel, we found only five different phenotypes, one represented by the four self-compatible individuals and the other four phenotypes represented by the five SI ones. Moreover, in the three semi-incompatible populations studied of Barbate metapopulation, 49% of the individuals were SC (Table 2). For this reason, allelic variation at the S locus is expected to be low, despite the fact that this metapopulation has a high number (2 x 106–3 x 106) of individuals. These H. salzmanniana populations are located in one of the windiest regions in the western Mediterranean Basin, where the pollination by insects is disrupted repeatedly during the flowering period. Therefore, SI individuals that depend on insects to fructify are in a disadvantageous position compared with SC individuals of the same population, particularly because in this species nystinastic movements during anthesis can promote spontaneous geitonogamy in all individuals in the population that have lost their SI. Perhaps, as Stebbins (1957)
stated, "flowers may resort to self-pollination when conditions become unfavorable for crossing."
Population genetic studies of H. salzmanniana using AFLP markers (Tremetsberger et al., 2004
; M. Ortiz et al., unpublished manuscript) showed that, in general, self-incompatible and semi-incompatible populations have a higher percentage of polymorphic fragments than self-compatible populations. This might indicate that self-compatible and semi-incompatible populations have suffered a bottleneck in the past that has reduced their allelic diversity, as in Senecio squalidus (Brennan et al., 2002
) or that selfing causes a loss in diversity as homozygosity increases. A low allelic diversity at the S locus has also been found in small populations of other Asteraceae such as Eupatorium resinosum (Byers, 1995
).
In the self-incompatible population samples of H. radicata, H. arachnoidea, and H. salzmanniana some individuals developed 1–8 selfed fertile fruits (fruit to flower ratio <0.12) and were labeled as pseudo-self-compatible (PSC). Again, this is relatively frequent in species with the SSI mechanism (Byers, 1995
; Hiscock, 2000a
) and was also shown in H. radicata by Picó et al. (2004)
. Reasons for PSC may be genetic, mainly due to genes not linked to the S locus, or environmental, such as a temperature rise, a long photoperiod, or plant senility (Levin, 1996
). Selfing may also be induced experimentally, e.g., by bud pollination or deposition of a weak saline solution on the stigma (Hiscock, 2000b
). Some experimental studies have indicated that PSC may have been pivotal in the transition from self-incompatibility to true self-compatibility in some groups of plants, e.g., in Phlox drummondii and P. cuspidata (Bixby and Levin, 1996
). In general, PSC can play an important role in self-incompatible species because it might be the only way to generate sexual offspring when pollinator vectors are limited and/or the population allelic diversity of the S gene is too low (Levin, 2000
).
Floral parameters associated with incompatibility
Of the four species in Hypochaeris section Hypochaeris, H. glabra is the only strictly self-compatible and geitonogamous species, and it has heads 3–4 times smaller in diameter and a period of anthesis half as long in comparison to the self-incompatible and semi-incompatible species. Because H. glabra occupies a basal position in the phylogeny of the section Hypochaeris (Tremetsberger et al., 2005
), it is possible that this species is the oldest in the section and that H. glabra lost its self-incompatibility a long time before the loss of self-incompatibility in some populations of H. salzmanniana. This could explain why all the head parameters associated to the loss of self-incompatibility are so marked in H. glabra.
It is widely documented that, in general, autogamous species have smaller flowers and remain in anthesis for a shorter time than allogamous congenerics (Stebbins, 1957
; Grant, 1971
; Levin, 2000
). This has been shown in self-compatible species in Senecio (Gibbs et al., 1975
), Anagallis (Gibbs and Talavera, 2001
), Amsinckia (Schoen et al., 1997
; Barrett, 2002
), Eriotheca (Oliveira et al., 1992
), Phlox (Bixby and Levin, 1996
), and Hypochaeris (Parker, 1975
).
Floral longevity in other species is linked to the growth of pollen tubes and ovule fertilization because these processes promote the production of growth hormones necessary for the development of fruit, but which also cause floral senescence (Crane, 1964
; Biale, 1978
; Stephenson, 1981
). This would explain why heads of SC Hypochaeris glabra and heads of the self-compatible (and geitonogamous) individuals of H. salzmanniana do not last long as those of self-incompatible species. Effectively, this parameter is an indirect measurement of a species' capacity to self.
Of the species of Hypochaeris studied here, H. salzmanniana is the only species that has statistically significant differences in the measured parameters (number of flowers, head diameter, and length of the period of anthesis of the head) among populations and individuals within populations. In general, heads of self-incompatible individuals from all populations had more flowers, a larger diameter, and remained in anthesis longer than heads of self-compatible individuals (Fig. 5). Further, we found a strong correlation among these three variables (Fig. 6).
There is little information on variation of flower parameters within the same species that may be associated with the emergence of self-compatibility from within self-incompatible populations. In Baldellia ranunculoides (Alismataceae), the subspecies ranunculoides is self-compatible and has much smaller flowers than the self-incompatible subspecies repens (Vuille, 1987
). Likewise, in Euphrasia species, French et al. (2005)
found a negative correlation between corolla size (the area of the central lower lobe) and inbreeding coefficient (FIS), which is an indirect measure of selfing. In these taxa, as in Hypochaeris species, high selfing rates are associated with small flower size.
Fruit to flower ratio in natural populations
In general, the fruit to flower ratio of all examined species of Hypochaeris is exceptionally high. This to be expected in H. glabra (fruit to flower ratio 0.96), a self-compatible and geitonogamous species, and is in accordance with results from other autogamous species (Wiens et al., 1987
; Gibbs and Talavera, 2001
). However, the ratio in H. radicata and H. arachnoidea, both self-incompatible and therefore obligatorily xenogamous, is also high, in general more than 0.7 in all populations except one. Such high fruit to flower ratios in SI species are uncommon (Wiens et al., 1987
), but have also been found in other obligately outbreeding taxa, such as Cistus ladanifer (ratio = 0.95; Talavera et al., 1993
) and Anagallis monelli (ratio = 0.80; Gibbs and Talavera, 2001
). In contrast, the fruit to flower ratio in the Doñana (Spain) population of H. radicata (ratio = 0.18) and in the Tiznit (Morocco) population of H. arachnoidea (ratio = 0.68) was significantly lower (see Fig. 7) than that of other populations of these species (further discussed later).
Hypochaeris salzmanniana also has a fairly high fruit to flower ratio (>0.60), but if we compare the two large metapopulations, La Mamora, which is completely self-incompatible, and Barbate, which is semi-incompatible (with SI and SC plants at around 50%), whilst most plants of the former had a fairly high fruit to flower ratio (only 8% of the plants have <0.50), some 39% of the plants from Barbate metapopulation had a low ratio (<0.50) (Fig. 8). This last group probably comprises the self-incompatible plants of this metapopulation and the diminished fecundity of these SI plants may be due to the consequences of bottleneck events, e.g., low S allelic diversity and restricted mate choice or early-acting inbreeding depression due to consanguineous matings. It is possible that the low fecundity of the Tiznit population of H. arachnoidea, which is in the extreme SW of the distribution of this species, and the Doñana population of H. radicata, in which a high degree of apomictic reproduction occurs (Ortiz et al., unpublished observations), is also due to a low diversity of S alleles in these populations.
Although the populations of Hypochaeris species probably originally had many S alleles with unequal frequencies, subsequent loss of alleles may have occurred in some populations due to genetic drift following bottleneck events (founder effects or a decrease of the population size). Once the number of S alleles is limited, the availability of compatible crosses will be diminished, leading to lowered fruiting success. Such a scenario has been analyzed through modeling by Byers and Meagher (1992)
. Indeed, populations with low seed set in SSI species of the Asteraceae seem to be due, in the majority of cases, to a low frequency of compatible phenotypes in the population as shown in Aster furcatus (Reinartz and Les, 1994
), Scalesia affinis (Nielsen et al., 2003
), Hymenoxis acaulis var. glabra (DeMauro, 1993
), and possibly also in Hypochaeris maculata (Wells, 1976
).
FOOTNOTES
The authors are indebted to Dr. P. E. Gibbs, Dra. M. Arista, and Dr. J. Arroyo for critically reading the manuscript; F. Guevara (Mexico), J. L. Fernández Alonso (Colombia), S. Ortiz (Spain), M. Luceño (Spain), and S. Castroviejo (Spain) for the material collected; and two anonymous reviewers, particularly reviewer two, for their valuable comments on a previous version of the manuscript. They also thank Glasshouse General Services of the University of Seville. This work was supported by a predoctoral grant to M.Á.O. from the Ministerio de Educación y Ciencia (BES-2003–1506) and a grant from the Ministerio de Educación y Ciencia (REN2002–04634-C05–03 to S.T. and REN2002–04354-C02–02 to M.A.), the Austrian Science Foundation (FWF P-15225 to T.S.) and Junta de Andalucia (group RNM-204). 
4 Author for correspondence (e-mail: aortiz{at}us.es
), fax: 34–954557059
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