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Population Biology |
Departamento de Ecología Evolutiva, Instituto de Ecología, Apartado postal 70-275, C.U., Universidad Nacional Autónoma de Mexico, CP 04510, D.F., Mexico
Received for publication July 5, 2002. Accepted for publication December 5, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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= 0.083), although gene flow estimates (Nm) varied among groups of populations: southern populations had the lowest levels of genetic differentiation, suggesting high levels of gene flow; northern populations had greater levels of genetic differentiation ( = 0.115), suggesting low gene flow among them. The patterns and inferences of the genetic structure of the population at the molecular level is consistent with variation in floral traits and pollinator visitation rates across the range of the species.
Key Words: Agavaceae • Agave lechuguilla • Chihuahuan desert • gene flow • population differentiation • population genetics
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, b
; Handel, 1983
; Schoen and Clegg, 1985
; Hamrick and Godt, 1989
; Hamrick and Loveless, 1989
; Eguiarte et al., 1993
). Additionally, reproductive ecology can influence the amount of gene flow among populations, their effective population sizes, and the potential for natural selection to occur (Hamrick and Godt, 1989
; Hamrick and Loveless, 1989
; Eguiarte et al., 1993
; Parra et al., 1993
; Slatkin, 1994
). On the other hand, genetic structure affects the evolution of reproductive traits, which in turn depends upon the availability of useful genetic variation and on effective population sizes (Hedrick, 1983
; Parra et al., 1993
). Although the literature on plant reproductive ecology and genetic structures is vast, few studies have explicitly studied the joint variation of reproductive ecology and genetic structure geographically (i.e., Schoen, 1982a
, b
; Ohara et al., 1996
; Wong and Sun, 1999
).
Studies that examine differences in the reproductive ecology and genetic structure of several populations with contrasting environmental conditions serve to corroborate predictions about the effect of variation in ecological characteristics or selfing-outcrossing rates on molecular genetic diversity. For instance, Schoen (1982a
, b
) studied Gilia achilleifolia in California and found correlations between pollinator identity, reproductive biology traits, outcrossing rates, and levels of genetic variation among several populations. Similar patterns were found in Trillium kamtschaticum by Ohara et al. (1996)
, in which variation in the breeding system and genetic diversity of populations is related to the abundance of different pollinators in distinct areas on the island of Hokkaido, Japan.
We studied the relationship between reproductive ecology and genetic structure in several populations of Agave lechuguilla along a latitudinal gradient in the Mexican portion of the Chihuahuan desert. The reproductive ecology of the species was reported in a separate paper (Silva-Montellano and Eguiarte, 2003
). This work demonstrated that along a latitudinal gradient, floral traits of the species clearly vary: southern populations have long, tubular, pale flowers, which produce large amounts of diluted nectar and are intensively visited by nocturnal and diurnal pollinators. In contrast, northern populations have shorter, more open reddish flowers, which produce smaller quantities of concentrated nectar and are less intensely visited (Cadaval, 1999
; Silva-Montellano, 2001
). The efficiency of fruit production is also higher in southern than in northern populations (Silva-Montellano and Eguiarte, 2003
). Here we analyze the genetic structure of A. lechuguilla along its distributional range and investigate possible correlations between interpopulation differences in floral biology and differences in levels of genetic variation, inbreeding, and differentiation among populations. Because flowers are less frequently visited in the north, we expected to see higher levels of inbreeding and greater genetic differentiation in northern populations than in southern ones.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) is one of the most abundant Agave species. This small century plant is abundant throughout the Chihuahuan desert. Silva-Montellano and Eguiarte (2003)
and Cadaval (1999)
describe the general characteristics and floral biology of A. lechuguilla.
Studied populations
We studied 11 populations along a latitudinal gradient that extends through most of the Mexican portion of the Chihuahuan desert (Table 1). These populations did not statistically differ in density of rosettes and inflorescences as described in detail in Silva-Montellano and Eguiarte (2003)
. Samples for genetic analyses were collected from June to September in 1996. Forty different individuals were collected in each population from an area of approximately 2 ha. To avoid repeatedly sampling members of clones, we collected tissues from individuals that were more than 2 m apart (see Trame et al., 1995
). We sampled the younger expanded leaf of each rosette and collected a small portion from the base of the rosette. Samples were transported in liquid N2 and stored at –80°C until used.
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; Martínez-Palacios et al., 1999
). Samples were mechanically disrupted with an electric drill, using 15–20 drops of the extraction buffer described in Aguirre-Planter et al. (2000)
. Extracts were absorbed in 12 x 1.5 mm paper wicks and stored at –80°C. Allozymes were run in 12% starch gels for 7 h at 60 mA, using buffer system 8 of Soltis et al. (1983)
with gel buffer at pH 7.6. We analyzed 10 enzymes, giving a total of 13 loci: phosphoglucose isomerase (PGI, E.C. [Enzyme Commission number] 5.3.1.9, two loci), glutamate oxaloacetate transaminase (GOT, E.C. 2.6.1.1, one locus), leucine aminopeptidase (LAP, E.C. 3.4.11.1, one locus), esterase (EST, E.C. 3.1.1.1, one locus), diaphorase (DIA, E.C. 1.6.4.3, two loci), malic enzyme (ME, E.C.1.1.1.40, one locus), phosphoglucomutase (PGM, E.C. 2.7.5.1, two loci), acid phosphatase (ACPH, E.C.3.1.3.2, one locus), anodic peroxidase (APX, E.C. 1.11.1.7, one locus), and cathodic peroxidase (CPX, E.C. 1.11.1.7, one locus). Staining procedures correspond to those of Soltis et al. (1983)
, with minor modifications available from the authors.
The fastest loci and alleles were scored as 1, the second 2, and so on, following genetic interpretations of the closely related species, Agave victoriae-reginae (Martínez-Palacios et al., 1999
) for the nine loci common to both species. One population of A. victoriae-reginae (population 7 from Martínez-Palacios et al., 1999
) was used in the analysis both as an outgroup (see below) and for comparison of the loci and alleles, including the 13 loci of the present study.
Statistical analyses
Most of the statistical genetic analyses were done using TFPGA (Miller, 1997
), unless indicated otherwise. We obtained the allelic frequencies for each locus, and from these frequencies, we calculated the proportion of polymorphic alleles (P), the observed (Ho) and expected (He) heterozygosities, the average number of alleles per locus (A) and the effective number of alleles (Ae) (Hedrick, 1983
). To analyze the deviations from Hardy-Weinberg equilibrium, we estimated the fixation index (f) for each locus from each population with BIOSYS (Swofford and Selander, 1989
), using a 
2 test to evaluate if deviations were different from zero (Li and Horvitz, 1953
). Clinal variation of expected and observed heterozygosities per locus and fixation index per locus along the latitudinal gradient were tested using regression for repeated measures of Y (Sokal and Rohlf, 1995
), which includes an ANOVA for differences among populations.
Wright's F statistics were obtained following Weir and Cockerham (1984
; F, f, and , equivalent to FIT, FIS, and FST, respectively) procedures. Single locus values for each index were tested if different from zero using 2 tests (Li and Horvitz, 1953
; Workman and Niswander, 1970
) and averaged by means of a jackknife procedure (Weir, 1990
). Confidence intervals of 95% for each statistic were obtained from 1000 bootstrap samples. Nm was aproximated from using Crow and Aoki's (1984)
formula.
We used a Mantel test (Manly, 1987
) to assess the model of isolation by distance using the genetic distance for pairs of populations (Nei, 1978
) and geographic distance among these populations. The Nei's genetic distance was also employed to obtain a UPGMA phenogram, after 1000 bootstrap samples.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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(=FST) was relatively small (0.083), but it was significantly different from zero, indicating low but significant genetic differentiation among populations. As a consequence, F (=FIT) was significantly positive (0.179).
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We detected no genetic differentiation among populations in the southern populations ( = 0.009, not different from zero, according to the 95% confidence interval), but central populations had a significant amount of differentiation ( = 0.059, different from zero, 95% CI) and an even greater differentiation among the northern ones ( = 0.115, different from zero, 95% CI).
The single locus estimates of the mean number of migrants per generation (Nm) was always higher than one (Table 2; average Nm = 2.28), suggesting that gene flow is probably an important force in A. lechuguilla. Considering each of our geographic regions separately, Nm declined from south to north. The mean Nm was 12.23 in the south, suggesting high levels of gene flow among populations, 2.23 in the central populations, and 1.08 in the northern ones.
Allelic frequencies along the latitudinal gradient and distribution of rare alleles
The most common allele in each locus was plotted as a function of population latitude. In most cases, we were not able to detect clear patterns in the changes of allelic frequencies. Only two loci (GOT, 3 and APX, 1) had marginally significant (P 
0.05) latitudinal increases or decreases in allelic frequencies (not shown).
Rare alleles (with an allelic frequency less than 0.05 within a given population) were more abundant in some populations (Fig. 3; 1, 6, M, 7, and 8), than in others (2, 3, 4, 5, 9, and 10). The frequency of rare alleles is negatively related to gene flow (Slatkin, 1985
; Slatkin and Barton, 1989
). Hence, the low amount of private alleles (alleles detected in only one population; one at population 8, locus DIA1-3) is congruent with the overall low and high gene flow estimated previously.
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).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Hamrick et al., 1992
; i.e., average of long-lived perennial outcrossers at the species level He = 0.211, N = 51; and at the population level He = 0.163, N = 66). Similarly high levels of He were also reported in the closely related but more geographically restricted species A. victoriae-reginae (Martínez-Palacios et al., 1999
; He range 0.21–0.41) and in species of the A. deserti complex, using RAPDs (Navarro-Quezada, 1999
; Gonzalez Chauvet, 2000
; He range 0.12–0.26). Our prediction that southern populations would harbor greater genetic diversity than northern ones was met to some extent because southern populations had higher He levels, although the change along the latitudinal gradient was not significant.
The presence of similarly high levels of genetic variation in A. victoriae-reginae and in A. lechuguilla, despite the more restricted geographic range and smaller population sizes of A. victoriae-reginae, suggests that Agave species may harbor particularly high levels of genetic variation compared to other long-lived desert perennials (Martínez-Palacios et al., 1999
; Silva-Montellano, 2001
). Long-lived desert perennials have variable levels of genetic variation, ranging from very low, as in the palm Washingtonia filifera (McClenaghan and Beauchamp, 1986
) to quite high, as in the cactus Echinocereus engelmannii (Neel et al., 1996
) and other Cactaceae (Harmick et al., 2002
), as well as in species of different families analyzed by Schuster et al. (1994
; average He = 0.173). Nevertheless, the high levels of genetic variation in wild Agave species is not typical of all desert plants (see Comes and Abbot, 1999
). In contrast, domesticated Agave species harbor very low levels of genetic variation (Colunga-GarcíaMarín et al., 1999
; Gil-Vega et al., 2001
).
Fixation indices and inbreeding within populations
Our data revealed a latitudinal trend in the deviation of genotypic frequencies from Hardy-Weinberg equilibrium. Latitude accounted for 20% of the variance in the regression of heterozygosity across latitude, decreasing from south to north. Populations in the south (1–3) had an excess of heterozygous individuals, whereas populations in the central section (4–6, including M) had genotypic frequencies near Hardy-Weinberg equilibrium and those in the north had an excess of homozygous individuals. This pattern is consistent with the higher rates of pollinator visitation and greater fruit set in the south (Silva-Montellano and Eguiarte, 2003). Lower rates of pollinator visitation may explain the lower efficiencies in fruit production and higher levels of homozygosity in northern populations. The excess of heterozygous individuals in the south could be generated by several different mechanisms (Hedrick, 1983
; Waser, 1987
). The most important of these is probably heterosis: more heterozygous individuals could mean greater vigor and survival (Linhart et al., 1981
; Eguiarte et al., 1992
). This idea is consistent with the fact that A. lechuguilla is a long-lived perennial (Eguiarte et al., 2000
).
The low levels of genetic differentiation in the southern populations suggest very high levels of gene flow and behavior as a single panmictic population. In these very large populations, natural selection favoring the heterozygous individuals would be more efficient (Eguiarte, 1990
; Parra et al., 1993
). Meanwhile, in the north the situation is the reverse; populations are more isolated and show great genetic distance. Flowers in northern populations receive fewer pollinator visits and apparently generate inbreeding by geitonogamous self-pollination among flowers within a given inflorescence or by moving pollen among the different inflorescences in the same genet (Silva-Montellano, 2001
). If we assume that all of the inbreeding in the northern populations (7–10) is due to self-pollination, the outcrossing rate can be approximated as f = 1 – t/1 + t (Haldane, 1924
; Hedrick, 1983
). Using this equation yields a t value of 0.467, which suggests that about half of all seeds are produced by self-pollination. The finding that outcrossing is higher in the southern populations and lower in the north was supported by a subsequent series of controlled pollination experiments and genetic analyses of outcrossing-rates between the two most contrasting populations (Silva-Montellano, 2001
).
Genetic differentiation
We were able to detect genetic differentiation in populations of A. lechuguilla along a latitudinal transect in the Chihuahuan desert. The pattern of population differentiation along this transect was congruent with patterns of morphological and reproductive differentiation found in a previous study (Silva-Montellano, 2001
; Silva-Montellano and Eguiarte, 2003
). The average (0.083) found in A. lechuguilla was significantly different from zero and was lower than the value for Agave victoriae-reginae ( = 0.236). The latter species is found only in 10 very localized populations in a relatively small area of the central Chihuahuan desert. These differences in may be caused by the large population sizes and wide distribution of A. lechuguilla. On the other hand, low levels of interpopulation genetic differentiation were detected in A. deserti ( in this species complex ranged from 0.08 to 0.13, Navarro-Quezada, 1999
; Gonzalez Chauvet, 2000
). Agave deserti is relatively abundant and widespread in the Sonoran desert. We also found strong patterns of differentiation between northern and southern populations. Southern populations of A. lechuguilla were genetically similar, central populations were more differentiated (mostly due to the M population), whereas northern populations were highly differentiated. This phenomenon can be explained by differences in pollinator abundance and in taxa across the gradient. Pollinators seem to be less abundant and to have a more restricted range of movement in the north than in the south (Silva-Montellano, 2001
; Silva-Montellano and Eguiarte, 2003
). The movements of more abundant and more mobile pollinators would generate greater genetic connectivity among southern than among northern populations.
The UPGMA analysis suggests that the more primitive populations may be those in the north (in particular population 10). Although we are aware that some other evolutionary process may account for the observed patterns (i.e., intense genetic drift or introgression from other Agave species in some of the northern populations), our interpretation is worth considering, because it suggests a contrast to the traditional view that the Agave species originated in central Mexico, and then migrated to the north (i.e., Alvarez de Zayas, 1989
). If our interpretation is correct, then A. lechuguilla seems to have originated in the north and more recently colonized the south. A similar pattern was detected using RAPDs in the A. deserti complex of the Sonoran desert, comprising several subspecies of A. deserti and of A. cerulata and A. subsimplex (Navarro-Quezada, 1999
; Gonzalez Chauvet, 2000
). If this scenario is correct, then the traits of the southern populations (larger flowers and higher outcrossing) are derived. An alternative hypothesis is that the increment in aridity to the north (Ortega, 1995
) has led to a decline in nocturnal pollinators in the north (Silva-Montellano, 2001
). Hence, the southern population may represent the ancestral traits before the changes occurred. In that way, northern populations have had more time to adapt to diurnal pollinators with a consequent increase in inbreeding and genetic differentiation among them. In support of this second point, while the common pollination syndrome for genus Agave is considered to be chiropterophily (Schaffer and Schaffer, 1977
; Howell, 1979
; Howell and Roth, 1981
), we have evidence that the pollination syndrome in northern populations could be evolving toward diurnal pollination (Silva-Montellano and Eguiarte, 2003
). Unfortunately, the present information of biogeography and phylogeny of the genus Agave is not enough to help solve this point (see Eguiarte et al., 2000
). We need more detailed experiments and observations in the field to corroborate these interpretations, along with analyses of molecular evolution and population genetics of the Marginateae group of the Agave species.
In conclusion, our study of Agave lechuguilla (considering both this paper and Silva-Montellano and Eguiarte, 2003
) clearly demonstrates that differences in pollinators not only affect the reproductive efficiency of plant populations, but also determine their genetic structure. As we already mentioned, few studies have attempted this joint approach using ecologic-genetic markers over a wide geographic range to unravel the evolutionary ecology of plant species, despite its huge potential.
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FOOTNOTES |
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2 Author for reprint requests (asilva{at}miranda.ecologia.unam.mx
)
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