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Reproductive Biology |
Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697 USA; Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 70-275, C.P. 04510, México Distrito Federal, México; Departamento de Ecología de la Biodiversidad, Estación Regional del Noroeste, Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 1354, C.P. 83000, Hermosillo, Sonora, México; Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, California 94132 USA
Received for publication May 31, 2006. Accepted for publication May 7, 2007.
ABSTRACT
The evolution of distyly from tristyly was investigated in populations of Oxalis alpina at high elevations throughout the Sky Islands of the Sonoran Desert. Incompatibility systems in tristylous populations, where self-incompatible short-, mid-, and long-styled morphs occur in populations, vary from those typical of tristylous species in which each morph is equally capable of fertilizing ovules of the other two morphs, to breeding systems in which incompatibility relationships are asymmetric. In these populations, selection against the allele controlling expression of the mid-styled morph is likely. The degree of modification of incompatibility in the short- and long-styled morphs in 10 populations was strongly associated with fewer mid-styled morphs, supporting models predicting the effect of these modifications of incompatibility on frequency of the mid-styled morph. Self-compatibility of the mid-styled morph may be important for maintaining the frequency of this morph, depending on the level of self-pollination, self-fertilization, and the extent of inbreeding depression. Modifications of incompatibility in tristylous populations and the distribution of distylous populations of O. alpina in the Sky Island region have similar geographic components, indicating the potential importance of historical factors in the evolution of distyly from tristyly.
Key Words: distyly • heterostyly • illegitimate crosses • legitimate crosses • Oxalis alpina • self-incompatibility • Sky Islands • tristyly
Most flowering plant species are hermaphroditic, and many have the capacity for self-fertilization. Charles Darwin (1900)
first demonstrated the deleterious consequences of self-fertilization and suggested that many reproductive systems in flowering plants have evolved to promote outcrossing (matings with other individuals in the same population). Understanding the evolutionary forces that underlie modifications of plant breeding systems, which themselves may influence genetic diversity, gene flow, population structure, and the potential for speciation, is a major challenge. Heterostylous breeding systems have been useful model systems for addressing questions about breeding system evolution. In heterostylous breeding systems, two or three floral morphs occur in a population (Barrett, 1992
). Because of strong self-incompatibility, each floral morph is normally incapable of producing seed after self-fertilization. In tristyly, three floral morphs occur in populations (Fig. 1A). Flowers have three levels at which organs can occur; stamens occupy two levels, while stigmas occur in the third. Morphs differ in the levels at which stigmas and anthers occur (Fig. 1A). Compatible matings are generally those occurring between anthers and stigmas located at the same level in the flower and were termed legitimate by Darwin (1877)
. Because there are three floral morphs, there are six categories of legitimate pollinations (L x l/S, L x l/M, etc.; see Fig. 1A for explanation of cross notation) that typically produce seeds. The numerous categories of illegitimate cross- and self-pollinations (L x m/S, L x s/M, etc.) normally fail to produce seeds.
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; Lewis and Jones, 1992
). Theoretical studies have indicated that this system of genetic control leads to equal numbers of the three morphs in populations (Charlesworth, 1979
; Heuch, 1979
). In distylous species, only two morphs occur in populations (Fig. 1B); as in the case of tristyly, fertilizations that are capable of leading to seed production are normally those occurring between anthers and stigmas at the same level. Distyly is found in approximately 25 families of flowering plants (Barrett, 1992
). Tristyly is much less common and is found in only six flowering plants families (Barrett, 1993
; Thompson et al., 1996
). Distyly also occurs in four families with tristyly (Amaryllidaceae, Linaceae, Lythraceae, and Oxalidaceae) and is thought to be derived from tristyly in the Lythraceae and Oxalidaceae (Weller, 1992
).
Theoretical analyses indicate that the most obvious cause for the loss of floral morphs in a tristylous population is fitness differences among the morphs. Morph-specific fitness disadvantages may occur when pollinators discriminate among floral morphs, when one of the morphs undergoes more self-fertilization and a reduction in fitness of offspring due to inbreeding depression (Charlesworth, 1979
) or when the efficiency of pollen transfer is not symmetrical and one or two morphs suffer pollen limitation (e.g., Hodgins and Barrett, 2006
). Similarly, modifications of heterostylous incompatibility allowing production of seeds following illegitimate crosses could lead to loss of a floral morph, assuming the occurrence of illegitimate pollen flow and pollen limitation (Charlesworth, 1979
). A much less explored alternative is the loss of floral morphs in tristylous populations independent of fitness differences among the morphs. These losses may occur if patterns of pollen flow and compatibility favor the propagation of one of the morph-determining alleles or if one of these alleles is more susceptible to drift (Eckert and Barrett, 1992
).
We investigated Oxalis alpina to test whether modifications of tristylous incompatibility relationships have resulted in the evolution of distyly in a number of populations of this species (Weller, 1976a
; Charlesworth, 1979
). The importance of these modifications was suggested by observations of incompatibility from populations of O. alpina in the Sky Islands (or Madrean Archipelago), isolated mountain ranges in the Sonoran Desert that have coniferous forest at higher elevations. In typical tristylous species, including tristylous species of Oxalis from southern Mexico (Weller, 1980
), only legitimate pollinations (pollen transfer between stamens and stigmas occurring at the same level) lead to fertilization and seed set (Fig. 1A). In contrast, in the two populations investigated in the Sky Islands, incompatibility reactions were modified from the typical condition of southern Mexican species (Weller, 1976a
, 1980
). In the short- and long-styled morphs there was no differentiation of the incompatibility reactions of the two anther whorls, and the two morphs were completely intercompatible (for the long-styled morph, the L x m/S and L x l/S crosses had equivalent seed production; for the short-styled morph, the S x m/L and S x s/L crosses had equivalent seed production; Fig. 2).
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). From the perspective of male fitness, pollen from two stamen whorls of the short-styled morph, but only a single stamen whorl of the mid-styled morph is capable of fertilizing ovules of long-styled morphs (Fig. 2). Similarly, pollen from two stamen whorls of the long-styled morph, but only a single stamen whorl of the mid-styled morph is capable of fertilizing ovules of short-styled morph (Fig. 2). Unless the proportion of legitimate pollen flow (S x s/L and L x l/S crosses) is high relative to illegitimate but compatible pollen flow (S x m/L and L x m/S crosses), pollen from the short- and long-styled morphs should outcompete pollen from mid-styled morph (Weller, 1976a
). From the perspective of female fitness, pollen from only two stamen whorls, the mid-stamen whorl of the short- and long-styled morphs, is capable of fertilizing mid-ovules, while pollen from three stamen whorls is capable of fertilizing ovules of both short- and long-styled morphs (Fig. 2), an approximate 50% advantage for the short- and long-styled morphs. Hence, the hypothesis predicts an alteration in the pattern of segregation within those populations where incompatibility reactions of the short- and long-styled morphs have been modified. In populations of O. alpina there is no evidence for reduced fecundity of the mid-styled morph (Weller, 1981a
), presumably because pollinators transfer adequate pollen for full seed set. These results also indicate that it is unlikely that lower fecundity of the mid-styled morph has resulted in reduced frequency of this morph and consequent modifications of incompatibility in the short- and long-styled morphs.
The consequences of loss of incompatibility differentiation for the evolution of distyly were modeled by Deborah Charlesworth (1979)
. With relatively high levels of selfing and inbreeding depression, a modifier that resulted in loss of incompatibility differentiation usually resulted in loss of the mid-morph. Self-pollination of the mid-morph was considered more likely because stigmas are located between the two anther whorls (Charlesworth, 1979
). Pollen limitation increased the likelihood of loss of the mid-morph. In contrast, when legitimate pollen flow was high (e.g., fewer L x mS and S x mL pollinations), retention of the mid-morph was more likely. Charlesworth (1979)
suggested that the ability of mid-level pollen to function in the L x m/S and S x m/L crosses should be accompanied by a corresponding failure of M x m/S and M x m/L crosses.
In this paper, we describe variation in incompatibility among 13 Sky Island populations of O. alpina and determine how these differences are associated with style-morph variation. In particular, we test the hypothesis that modifications of illegitimate crosses of the short- and long-styled morphs are responsible for the reduction in frequency of the mid-styled morph and evolution of distyly, as predicted from earlier studies (Weller, 1976a
, 1986
; Charlesworth, 1979
). Self-compatibility was investigated because of the possibility that greater selfing of the mid-styled morph relative to the short- and long-styled morphs, and expression of inbreeding depression in the progeny of mid-styled individuals, could select against this morph (Charlesworth, 1979
). Seed production of the M x m/S and M x m/L crosses was related to the degree of incompatibility modification to determine whether loss of incompatibility differentiation is associated with reductions of fecundity for legitimate crosses of the mid-styled morph, as predicted by Charlesworth (1979)
. The overall goal of this study was to determine how the mid-styled morph in populations of O. alpina could be lost, despite apparent frequency-dependent advantage resulting from the tristylous breeding system.
MATERIALS AND METHODS
Study species
Oxalis alpina (Rose) Knuth (section Ionoxalis) is a widespread species ranging from Guatemala to the southwestern United States (Denton, 1973
). This scapose species grows from a small bulb in response to summer rains. Sessile bulblets are formed in the leaf axils in populations from the Sky Island region. Cytogeographic studies, which have shown that the haploid chromosome number varies from 7 to 42, suggest that O. alpina is not monophyletic (Weller and Denton, 1976
). In contrast, populations in the Sky Island region of Arizona, New Mexico, and Sonora are likely to be monophyletic based on similar morphology, uniform tetraploidy (Weller and Denton, 1976
), and production of viable hybrid seed (Weller, 1978
).
Style-morph representation
We surveyed 18 tristylous populations and six distylous populations for style-morph representation in 2001–2004. Populations were defined physically as an area where plants occurred in a spatially contiguous distribution, usually in moister canyons, separated from other populations by intervening unsuitable habitat (usually dry ridges). In the field, we defined flowering individuals by their physical separation from neighboring plants; spatially distinct flowering individuals might represent ramets of the same genet, although neighboring plants often had different style morphs, indicating that clonal growth in O. alpina may be limited. In three tristylous populations, style-morph frequencies were estimated from nonflowering bulbs collected in the field and grown in the greenhouse. Several populations sampled in 1977–1979 were also sampled in 2001, 2003, or 2004. We sampled a single population for style-morph frequencies in most mountain ranges, although more intensive sampling of some mountain ranges was carried out in earlier studies (Weller, 1979
). G tests for heterogeneity of style-morph representation were carried out for 1977–1979 to identify fluctuations in morph frequencies likely to result from sampling, and for all sampling years (including surveys in 2001–2004) to determine the likelihood of changes in morph representation that had occurred over the longer time interval. Equality of morph representation among years was investigated using G tests. Samples sizes averaged 387 (range 116–1723) for distylous populations and 395 (range 55–1004) for tristylous populations. Sample sizes varied among populations in part because of variation in total population size.
Incompatibility relationships in populations of O. alpina
We collected bulbs from 13 tristylous and one distylous population in Arizona, New Mexico, and Sonora for investigation of incompatibility relationships. The distylous population was included in the crossing study to confirm incompatibility results obtained for other distylous populations throughout the range of O. alpina (Weller, 1976a
). We attempted to analyze incompatibility relationships in at least one population of O. alpina from each mountain range in the Sonoran Sky Islands. A few inaccessible populations or populations with inadequate population sizes (Sierra Los Pinitos, Sierra El Tigre, Sierra La Madera) were not included in the study. Bulbs were sampled throughout each population to minimize the chance that genets were represented more than once. Bulbs were planted in a soilless mix at the University of California Irvine greenhouse. All crosses were made during the summer months when O. alpina responds to water and grows actively. To assess the status of incompatibility in populations, we used approximately 10 individuals of each style morph as seed parents in crosses and an equal or larger number of plants as male parents. In each tristylous population, there were six legitimate crosses (Fig. 1A), 12 illegitimate crosses (crosses between individuals where anthers and stigmas occur at different levels), and six illegitimate self-pollinations (both anther whorls of each morph used for self-pollinations). For each individual used as a maternal plant, two to five crosses per category were carried out, yielding a minimum of 750 crosses per tristylous population. Control flowers (tagged but not pollinated) were used to monitor any background pollination. There was virtually no evidence that potential insect pollinators gained access to the greenhouse, and data from control crosses are not presented. Capsules were collected 13–15 d following pollination, before explosive dehiscence. The average number of viable seeds per capsule was used as a measure of incompatibility following a cross.
Statistical analysis of crossing results
Preplanned comparisons (SAS Institute, 1989
) were used to test whether the S x m/L and L x m/S crosses had the same level of compatibility as legitimate crosses with short- and long-styled morphs as female parents (S x s/L, S x s/M, L x l/S, L x l/M). Loss of incompatibility differentiation between the mid- and long-anther whorls of the short-styled morph and the short- and mid-anther whorls of the long-styled morph was indicated when the preplanned contrast was not significant; a significant contrast indicated either partial or no modification of incompatibility differentiation. The contrast between these legitimate and illegitimate crosses is critical because of previous work indicating that high compatibility of the S x m/L and L x m/S crosses is likely to favor loss of the mid-styled morph (Weller, 1976a
; Charlesworth, 1979
). Preplanned contrasts were also used to determine whether the S x m/L and L x m/S crosses had greater seed set than the remaining illegitimate crosses (S x l/M, S x m/S, S x l/S, M x l/S, M x s/L, M x s/M, M x l/M, L x s/M, L x m/L, L x s/L). Lack of significance indicated that incompatibility of the S x m/L and L x m/S crosses was similar to the other illegitimate cross categories; a significant value for the contrast indicated some loss of incompatibility differentiation for the S x m/L and L x m/S crosses. Results from the two preplanned contrasts for each population were used to characterize tristylous incompatibility populations as having (1) retained ancestral tristylous incompatibility (contrast of four legitimate and two illegitimate crosses significant; contrast of S x m/L and L x m/S crosses with remaining 10 illegitimate crosses insignificant), (2) partial loss of incompatibility differentiation (contrast of four legitimate and two illegitimate crosses significant; contrast of S x m/L and L x m/S crosses with remaining 10 illegitimate crosses also significant), or (3) complete loss of incompatibility differentiation (contrast of four legitimate and two illegitimate crosses insignificant; contrast of S x m/L and L x m/S crosses with remaining 10 illegitimate crosses significant).
All legitimate crosses were compared using Tukey's post hoc tests (SAS Institute, 1989
) to detect potential differences in viable seeds per capsule and especially modifications of mid-morph fecundity. Seed production following self-fertilization was also compared using post hoc analyses to determine whether some morphs, particularly the mid-styled morph, have evolved detectable self-compatibility. Values of seed production for all cross categories were tested for deviation from zero using t tests. Potential differences in mid self-compatibility were compared for populations where incompatibility differentiation was absent, partial, or complete with a one-way ANOVA on untransformed seed production data. All statistical analyses were carried out using SAS version 9.1 (SAS Institute, 2002–2003
).
Loss of incompatibility differentiation and fecundity of the M x m/S and M x m/L crosses
We used regression to investigate the relationship between relative seed production of the legitimate M x m/S and M x m/L crosses to loss of incompatibility differentiation. Relative seed production of the M x m/S and M x m/L crosses was calculated by dividing the value for each of these crosses by the average value for seeds per capsule for the legitimate crosses with short- and long-styled morphs as seed parents. This analysis was carried out for all 13 tristylous populations.
Loss of incompatibility differentiation and frequency of the mid-morph
The potential effect of the degree of incompatibility differentiation in the short- and long-styled morphs on the frequency of the mid-styled morph in populations was investigated by dividing the mean number of seeds per capsule for the L x m/S cross by the mean number of seeds per capsule for the L x l/S cross. This ratio approaches 1 as the incompatibility between the L stigma and style and the m/S pollen is lost. Similarly, S x m/L values were divided by S x s/L values. A value indicating the overall extent of incompatibility differentiation was obtained for each population by averaging values for the short- and long-styled morphs, with higher values indicating greater loss of incompatibility differentiation. Regression of mid-frequencies against these values was used to determine whether loss of incompatibility differentiation is associated with reduced mid-frequency. Only those populations with field surveys of style-morph frequencies were used in this analysis.
RESULTS
Style-morph frequencies
In the Sky Island region, distyly is apparently restricted to populations of O. alpina occurring in neighboring mountain ranges in Arizona (Table 1, Fig. 3) and the Chiricahua Mts., where distylous populations occur at the northern end of the range and tristylous populations at the southern end of the range (Weller, 1979
). Distylous populations had equal numbers of short- and long-styled style morphs (defined as isoplethic by Heuch, 1979
) in four of the six populations surveyed in 2001–2004 (Table 1). Among distylous populations, the greatest deviations from isoplethy occurred in the Sierra Ancha Mts., the most northern Arizona mountain range where O. alpina is found. In this mountain range style morphs were found in large patches, possibly because of clonal growth. While tristylous populations in Sonora were more likely to have equal numbers of short-, mid-, and long-styled morphs, style-morph frequencies deviated greatly from isoplethy in the more northern tristylous populations (Table 1). Populations in the Chiricahua Mts. (Morse Canyon, Fly Peak, South Fork Canyon, and Greenhouse Trail), near the Black River, and in the Pinos Altos Mts. had reduced frequencies of mid-styled morphs. Excesses of the long-styled morph were characteristic of anisoplethic populations (Table 1).
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Incompatibility relationships
Seed production following crosses within a distylous population from the Santa Catalina Mts. (voucher 706) was high for legitimate crosses (L x l/S, L x m/S, S x s/L, and S x m/L in a distylous species; Fig. 1A) and very low for illegitimate crosses and selfs (Fig. 4A). In preplanned comparisons, there were no differences in seed production between the L x l/S and S x s/L crosses vs. the L x m/S and S x m/L crosses (F = 0, df = 1, P = 0.99). Post hoc comparisons indicated that short- and long-styled morphs produced similar numbers of seeds (F = 1.76, df = 3, 37, P = 0.17; Fig. 4A). Based on preplanned comparisons, seed production was much higher for the S x m/L and L x m/S crosses than for illegitimate crosses (S x m/S, S x l/S, L x m/L and L x s/L in a distylous species), in which seed production did not deviate significantly from zero (F = 16.63, df = 1, P < 0.0001; Fig. 4A). Seed production following self-pollinations did not deviate significantly from zero.
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Partial loss of incompatibility differentiation occurs in a third group of populations scattered throughout the Sky Islands (Fig. 4B, White Mts., Arizona, 713; Fig. 4F, Miller Canyon, Huachuca Mts., Arizona, 702; Fig. 4G, Sierra San Jose, Sonora, 959; Fig. 4I, Sierra La Elenita, Sonora 956; Fig. 4M, Sierra Buenos Aires, Sonora, 961; Fig. 4N, Sierra La Purica, Sonora, 968). In these populations, the S x m/L and L x m/S crosses produced significantly less seed than the legitimate crossing categories (Table 2a; contrasts of four legitimate vs. two illegitimate crosses were significant) but produced significantly more seed than the other categories of illegitimate crosses (Table 2b; contrasts of seed production for the S x m/L and L x m/S crosses vs. the remaining illegitimate cross categories were significant). The extent of modification varied widely among these populations with partially modified incompatibility differentiation. Populations with partially modified incompatibility located in the White Mts. and Sierra San Jose (Fig. 4B, 4G) closely resembled nearby populations where differentiation of incompatibility was complete (Pinos Altos Mts. and Chiricahua Mts; Fig. 4C, 4D, respectively), while in several Sonoran populations (Sierras La Elenita, Buenos Aires, and La Purica; Fig. 4I, 4M, and 4N, respectively), modifications of incompatibility were slight, and incompatibility relationships were similar to those Sonoran populations with unmodified tristylous incompatibility relationships. Overall, loss of incompatibility differentiation was most apparent in northern populations of O. alpina located in Arizona and New Mexico (Fig. 3).
Variation in self-incompatibility in populations of O. alpina
Self-compatibility varied substantially among populations of O. alpina, with a tendency for mid-styled morphs to have greater self-compatibility than the short- or long-styled morphs, especially in those populations with partial or complete loss of incompatibility differentiation (Table 2d; Fig. 4A–N). Significant post hoc contrasts indicated higher self-compatibility of the mid-styled vs. short- and long-styled morphs for Morse Canyon, Chiricahua Mts. (727), Sierra San Jose (959), and the Pinos Altos Mts. (971), populations where modification of incompatibility differentiation is either complete (727, 971) or nearly complete (959). Mid-styled morphs from all four populations with complete loss of incompatibility differentiation had significant seed production following selfing (Fig. 4C–E and 4L). Three of six populations with partial loss of incompatibility differentiation had significant self-compatibility in the mid-styled morph (Fig. 4B, 4G, and 4M), and one of three populations possessing full incompatibility differentiation had significant seed production following selfing of mid-styled morphs (Fig. 4K). When self-compatibility of the mid-styled morph, measured as the average of seed production for the M x l/M and M x s/M self-fertilizations, was compared for populations with unmodified, partially modified, and fully modified incompatibility, there were no significant differences (F = 0.30; df = 2, 10, P = 0.7464). There appeared to be little correlation between seed production of the M x l/M and M x s/M self-pollinations within mid-styled individuals (Fig. 4).
Modification of fecundity of the M x m/S and M x m/L crosses
Loss of incompatibility differentiation was associated with modification of seed production of the legitimate M x m/S cross, as indicated by a significant regression of relative fecundity of the M x m/S cross (seed production of M x m/S divided by the average fecundity of legitimate crosses of the short- and long-styled morphs) against a measure of loss of incompatibility differentiation (F = 8.26; df = 1, 11; P = 0.015; Fig. 5). Populations with the most pronounced loss of incompatibility differentiation of the short- and long-styled morphs had the lowest relative seed production for the M x m/S cross (Table 2c). This trend was most apparent in populations from the White, Pinos Altos, Chiricahua (Morse Canyon), and Animas Mts. The relationship of M x m/L relative fecundity to incompatibility modification was not significant (F = 1.96, df = 1, 11; P = 0.189).
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Variation in incompatibility relationships in O. alpina and selection against the mid-allele
Incompatibility relationships in O. alpina show remarkable diversity over short geographic distances, and differences among populations in the extent of incompatibility differentiation between the stamen whorls of the short- and long-styled morphs were strongly related to the frequency of mid-styled morphs. Loss of incompatibility differentiation is expected to result in selection against the mid allele (Fig. 2) (Weller, 1976a
, 1986
; Charlesworth, 1979
), and in populations of O. alpina from the Sky Islands, the mid-styled morph occurs in significantly lower frequencies in populations with greater seed production for S x m/L and L x m/S crosses (Fig. 4). Reduction in frequency of the mid-styled morph most likely results from modifications of incompatibility in the short- and long-styled morphs, rather than from reduced fitness of the mid-styled morph because in previous studies (Weller, 1981a
), no differences in seed production were detected among morphs in the field. In most populations with modified incompatibility, the S x m/L and L x m/S crosses had similar seed production, although in several cases (e.g., Sierras Los Ajos, Buenos Aires, and La Purica; Fig. 4D) the fecundity was substantially greater for the L x m/S cross than for the S x m/L cross. The regression of mid-morph frequency against incompatibility modification assumes that each population represents an independent data point, although we do not know the phylogeographic history of these populations.
Geographic patterns to breeding system modification in O. alpina
Oxalis alpina was probably continuously distributed throughout the Sky Island region during the Pleistocene pluvial period because packrat–midden studies confirm that coniferous forests occurred at lower elevations during this period (Van Devender, 1977
; Van Devender and Spaulding, 1979
). Isolation of O. alpina to separate mountain ranges probably occurred following the Pleistocene, when drying caused the retreat of forests and species like O. alpina to higher elevations. The current distribution of distylous and tristylous populations could have been established before isolation of O. alpina populations or after populations became disjunct on isolated mountain ranges at the end of the pluvial period. The restriction of distylous populations of O. alpina to mountain ranges in the northwestern part of the Sky Islands (Fig. 3) may indicate that a single transition to distyly occurred in this region, prior to isolation of populations by post-Pleistocene drying. Populations throughout the Sky Islands have probably been genetically isolated from one another because drying occurred at the end of the Pleistocene pluvial period. Several studies of other organisms in this region (e.g., Aquilegia, Strand et al., 1996
; jumping spiders, Masta, 2000
) have used phylogeographic approaches and concluded that gene flow is limited between these isolated mountain ranges. Phylogeographic information would be useful for determining how many transitions to distyly have occurred in populations of O. alpina in the Sky Islands region.
The concentration of distylous populations in the northwestern part of the Sky Islands suggests that environmental differences may be important in explaining modifications of heterostylous reproductive systems in O. alpina. Despite the geographic pattern of breeding system variation, however, no obvious environmental gradients or differences in pollinators are associated with the transition to distyly (Weller, 1981b
; F. Baena [Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México], C. Domínguez, J. Fornoni, F. Molina-Freaner, S. Weller, unpublished observations). At present, we do not know why modifications of incompatibility are more common in the northern Sky Island populations of O. alpina.
Changes in style-morph frequencies over time
Comparisons of style-morph frequencies over a 24–26 yr period indicate apparent stability in the frequency of the mid-morph, with the exception of several populations from the Chiricahua Mts., as well as a population from the White Mts., where the frequency of the mid-morph declined significantly. Full or partial loss of incompatibility differentiation is characteristic of these populations, indicating that modified incompatibility relationships may have resulted in decline of the mid-morph. Distylous populations fluctuated less in style-morph frequencies over the sampling interval, with the exception of the Sierra Ancha population, where clonal growth appears to predominate and leads to substantial differences in style-morph representation, depending on the area sampled (S. Weller, C. Domínguez, and F. Molina-Freaner, unpublished observations).
Fitness of the mid-morph
Charlesworth (1979)
suggested that in populations with modified incompatibility of the short- and long-styled morphs, the ability of mid-level pollen from these morphs to function on long and short stigmas would be inversely associated with function on mid stigmas. Reduction in fertility of the M x m/S cross in populations of O. alpina with loss of incompatibility differentiation is consistent with previous observations (Weller, 1976a
), although there is no apparent loss of function of mid-level pollen from the long-styled morph on mid stigmas. High levels of natural pollination (Weller, 1981a
), as well as excesses of the long-styled morph serving as pollen donor to the mid-styled morph, may explain the absence of differences in seed production between the morphs of O. alpina despite low seed production following M x m/S crosses.
Differences in seed production of the M x m/S and M x m/L crosses also explain the results of direct tests for the effects of loss of incompatibility modification on mid-styled morph frequency. Progeny raised from naturally pollinated plants in Chiricahua populations were expected to show deficits of the mid-styled morph because of pollen competition that favored the short- and long-styled morphs (Weller, 1986
). Contrary to this prediction, mid-styled morph excesses were found, particularly in the progeny of mid-styled morphs, which produced almost no short-styled morphs in their offspring (Weller, 1986
). This unexpected result can now be understood in light of reduced seed production following the M x m/S cross in the Morse Canyon population in the Chiricahua Mts. (Fig. 4). Because the S allele is epistatic to the M allele (Weller, 1976b
), if the M x m/S cross produces few seeds, most mid-styled offspring will result from M x m/L crosses, and the M allele is more likely to be expressed in these progeny. Of the four populations with complete loss of incompatibility differentiation (Chiricahua, Los Ajos, Animas, and Pinos Altos), the M x m/S cross had low seed production in all but the Los Ajos population. Because rejection of pollen from short-styled morph parents would increase the frequency of mid-styled morphs in the progeny of mid-styled morphs, this mechanism may have been favored in mid-styled morphs that are under negative selection as a result of incompatibility modifications in short- and long-styled morphs.
Significant self-fertility was observed for a number of populations, and half of these cases involved self-fertility of the mid-styled morph. Self-fertility of the mid-styled morph might result in selection against this morph, depending on the selfing rate and the extent of inbreeding depression (Charlesworth, 1979
). Alternatively, self-fertility of the mid-styled morph might be advantageous in the face of modifications of incompatibility in short-styled and long-styled morphs that place mid-styled morphs at a disadvantage during outcrossing. Assuming that inbreeding depression was minimal, selfing would favor the mid-styled morph because of the occurrence of only mid- and long-styled morphs among progeny derived from selfing. Preliminary data suggest that self-pollination of mid-styled morphs is substantial (F. Baena, C. Domínguez, J. Fornoni, F. Molina-Freaner, S. Weller, unpublished observations), although the degree of natural self-fertilization of mid-styled morphs is unknown. We are investigating selfing rates and the extent of inbreeding depression in populations of O. alpina.
Distribution of breeding systems in Oxalis section Ionoxalis
The distribution of tristylous and distylous populations in the Sky Island mirrors the overall distribution of heterostyly in section Ionoxalis, with tristylous species found in southern Mexico and distylous species found more commonly in northern Mexico and the United States. Within section Ionoxalis, most tristylous species are diploid and have restricted ranges, while distylous species have broader distributions and higher ploidy levels, an overall pattern suggesting that distyly is derived from tristyly (Weller and Denton, 1976
). Within O. alpina, which occurs from Guatemala to New Mexico, ploidy levels are diverse, but they are not correlated with the distribution of distylous and tristylous breeding systems. In the Sky Islands region, all populations have the same ploidy level (n = 14). The closest populations outside of Sonora and Chihuahua with the same chromosome number as the Sky Islands populations occur in distylous populations in central Mexico. North of the Sky Islands region in New Mexico, populations of O. alpina are hexaploid (n = 21) and distylous. At present, the evolutionary relationships among populations of O. alpina throughout its range are poorly understood, although breeding-system lability within O. alpina is largely confined to the Sky Islands region. Additional studies, particularly those that model the effects of all modifications of self-incompatibility (J. Fornoni, C. Domínguez, F. Molina-Freaner, and S. Weller, unpublished data) and investigate the extent of self-pollination, self-fertilization, and inbreeding depression in progeny of mid-styled morphs, will be particularly useful for understanding the dynamics of style-morph representation in populations of O. alpina.
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1 The authors thank W. Yang, R. Basile, and Y. Alliman for plant care; A. Vuong, L. Duong, and A. Andres for help with the crossing program; A. Sakai for reading the manuscript and for her help in the greenhouse; S. Barrett for comments on the manuscript; T. van Devender, P. Jenkins, and R. Felger for advice on field sites; L. Portillo and R. Jaime for showing them populations of O. alpina in the Sierra Los Ajos; H. Aguayo, B. Brown, and C. Varela for access to field sites; the U. S. Forest Service for permits; and R. Pérez Ishiwara for assistance in the field. This research was supported by grants from the University of California Institute for Mexico and the United States (UC MEXUS), CONACYT (47858-Q), the National Autonomous University of Mexico (PAPIIT IN217 803), and the University of California at Irvine. 
6 Author for correspondence (e-mail: sgweller{at}uci.edu
)
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