Columnar Cacti

90 downloads 0 Views 6MB Size Report
Theodore H. Fleming and Alfonso Valiente- Banuet. p. cm. Includes ... Fleming, Theodore H. 11. ..... MiUon, J. B., Y.B. Linhart, B. K. Sturgeon, and J. L. Harnrick.
Columnar Cacti and Their Mutualists Evolution, Ecology, and Conservation :

EOITEO By:.......

THEODORE H. FLEMING ANO

ALForso

f:>

--

\t"\~ - --

:

~"

VALIENTE- BANUET

We dedica te this book to two scientists who have made major contributions to our understanding

of the evolution of Mexico's columnar cacti:

Dra. Helia Bravo-Hollis and Dr.Arthur C. Gibson

The University of Arizona Press @ 2002 The Arizona Board of Regents First printing All rights reserved i§This book is printed on acid-free, archival-quality Manufactured

paper.

in the United States of America

07 06 05 04 03 02

6

543

2

Frontispiece photo by Theodore H. Fleming.

LIBRARY OF CONGRESS CATALOGING-IN-PUBLlCATION

Columnar

DATA

cacti and their mutualists : evolution, ecology, and conservation Theodore H. Fleming and Alfonso Valiente- Banuet. p. cm. Includes bibliographical references and index. ISBN 0-8165-2204-9 (cloth: alk. paper)

1. Cactus-Southwest,

New.

2. Cactus-Mexico.

4. Mutualism (Biology)-Southwest, 6. Mutualism (Biology)-South

New.

3. Cactus-South

5. Mutualism

America. 1. Fleming, Theodore H. QK495.C11 C64 2002 583'.56-dc21

I edited by

America.

(Biology)-Mexico. 11. Valiente-Banuet,

2002003840 British Library Cataloguing-in-Publication

Data

A catalogue record for this book is available from the British Library.

Alfonso.

:

CHAPTER

6

:.......

T

H

Carnegiea

Tissue gigantea

Cereus repandus Echinocereus Lophocereus

engelmannii schottii

L. schottii J. L. HAMRICK

Melocactus Opuntia

curvispinus basilaris

O. spinosissima

THEODORE H. FLEMING

Pachycereus

JAFET M. NASSAR

pringlei

P.pringlei P.pringlei Pereskia guamacho

Introduction

- 122

Pilosocereus

lanuginosus

Stenocereus

griseus

S. thurberi

The availability of molecular genetic markers during the past 30 years has significantly increased our ability to describe genetic diversity within and among populations of a wide variety of plant taxa. The most comprehensive and widely available procedure used to identify single-gene genetic diversity is isozyme electrophoresis, which identifies and quantifies genetic variation at enzymatic loci. To date, approximately 2,750 speciesof seed plants have been the subject of"állozyme" studies. This robust database has állowed generalizations to be made concerning the influence of life history and ecologicálcharacteristics of species on the amount and distribution of allozyme variation (e.g., Brown, 1979;Hamrick et al., 1979;Hamrick and Godt, 1989). Specificálly,reviews of the plant allozyme literature have demonstrated that long-lived,woody specieswith large geographic ranges and outcrossing breeding systems have significantly more allozyme genetic diversity than do species with other combinations of traits (Hamrick and Godt, 1989, 1996). These species álso have much lessgenetic differentiation among their populations than is true of specieswith more limited gene flow potential (Hamrick and Godt, 1989, 1996). However, even though the number of plant állozyme studies will soon surpass 3,000,there are groups of plant species that are significantlyunderrepresented. One such group is the Cactaceae. To our knowledge, of the approximately 97 genera and 1,400 speciesof cacti found in !h~Western Hemisphere (Mabberley, 1997), only 11 genera and 13 species have been studied electrophoretically (Table 6.1). In contrast, more than 60 speciesof the genus Pinus have been analyzed for allozyme diversity. There are several reasons why the Cactaceae are poorly represented in the plant population-genetics literature. First, the studies are strongly biased towards north temperate species.Asa result, such speciesas cacti, which occur predominantly from Mexico to South America, are generally less thoroughly studied. Second, species of

~"'-...

Listing of Allozyrne Studies of Cactus Species Speeies

JOHN D. NASON

_Or/

TABLE 6.1

-

Genetic Diversity in Columnar Cacti

¡

Weberbauerocereus weberbaueri

flower buds seedlings stem stem flowerbuds seedlings stem stem flowerbuds, seedlings flower buds flowerbuds leaves seedlings seedlings flower buds flowerbuds, seedlings

Number of Populations

Number of Loei

16 14 6 8 21 18 1 2 1

30 17 7" 18 31 19 1 13 8

9 19 17 10 15 20 1

24 24 19 23 18 31 12

Reference Hamrick et al. (unpubl. data) Nassar et al. (unpubl. data) Neel et al. (1996)

Parker and Hamrick (1992) Nason et al. (unpubl. data) Nassar et al. (forthcoming a) Sternberg et al. (1977) Hamrick and Godt (1997) Murawski et al. (1994) Fleming et al. (1998)

Hamrick et al. (unpubl. data) Nassar et al. (forthcoming b) Nassar et al. (unpubl. data) Nassar et al. (unpubl. data) Hamrick et al. Sahley (1996)

a Number of enzyme systems. Loci were not identified.

arid habitats, as a group are underrepresented in the plant allozyme literature. Very fewof the ecologicaldominants of arid lands have been the subject of genetic diversity studies. In contrast, there are more than 150 studies of tropical tree species. Finally,many potential investigators have hesitated to undertake studies of the Cactaceaebecause of the generally held belief that the mucilaginous cactus tissue makes enzyme extraction difficult, if not impossible. In this chapter, our chief objective is to review what is known concerning allozymegenetic variation in the Cactaceae,particularly columnar cacti.Wedispel the myth that it is difficult to electrophoretically analyze extracts from cactus tissue for allozymeloci.Wecompare the results of the fewexistingcactus allozymestudies with results obtained from reviews of the extensiveplant allozymeliterature to determine whether the levelsand distribution of genetic diversity in cactus species are consistent with their life history traits.

Electrophoretic Procedures We have found that cactus species require no special handling or extraction procedures to obtain well resolved isozymebands. In fact, severalcactus specieshave given excellentband resolution. Generally,the handling and extraction procedures that our

1

123

nAMRlCK

~

ET AL.

laboratory has developed for a variety of gymnosperm and angiosperm speeies have also worked well for cactus speeies. We have used a variety of cactus tissue with varying results (Table 6.1). Best expression and resolution is typically obtained from greenhouse-grown seedlings. We usually try to use seedlings that are at least one centimeter in height but have also used both larger and smaller seedlings with success. Plower-bud tissue produces nearly equal expression and resolution to that of seedlings. Adult stem tissue has not worked as well for some enzyme systems but provides good results for other enzyme systems and loci.

banding patterns. Kephart (1990) also discusses a variety of electrophoretic buffers and stains that work well for plants.

Measures of Genetic Diversity Genetic diversity can be estimated at three levels:within speeies,within populations, and among populations. Within-speeies measures are estimated from pooled (over all populations sampled) values and are not confounded by partitioning of genetic diversitywithin and among populations. In contrast, genetic diversitywithin populations is a function of total genetic diversity within the species as well as the proportion of this total that occurs within populations. In this chapter, speciesvalues are subscripted by "s" and within-population values are subscripted by "p:' Severalparameters are typicallyused to measure the levelsand distribution of genetic diversity within speeies and populations and among populations. Each measure is informative but some are composite measures that incorporate information from other parameters. Genetic diversity measures used in this chapter include:

PIELD COLLECTING When collecting cactus tissue in the field, we have used two approaches for its preservation and transportation. We have had success collecting flower buds and stem tissue, plaeing the tissue in a cooler with ice and transporting it directly to the lab within two or three days. Some loss of expression has occasionally been experienced, but this is a successful technique when dealing with limited samples (Le., those that can be collected during a one- or two-day period) from a geographically restricted area. In our experience, flower buds preserve better than stem tissue, perhaps because their removal from the plant is less traumatic to the tissue. When the sampling period is extended, as in sampling for geographic surveys of allozyme variation, we collect flower buds, place them on ice, and within 36-48 hours transfer the buds to a liquid-nitrogen container. When it is necessary to keep track of samples from individual plants, we wrap the buds (or cross-sections ofbuds) in aluminum foil and individually mark each sample. Several wrapped buds are then placed in net bags tied to nylon fishing line and are irnmersed in a container of liquid nitrogen. Once frozen, tissues should not be allowed to thaw. Air transport can be accomplished with a dry liquid-nitrogen carrier or the samples can be placed on dry ice.

P = the proportion of polymorphic loci (Le.,loei with more than one allele). AP = the mean number of alleles per polymorphic locus. Ae =lI'I.p/= the effectivenumber of allelesat a locus, where p¡ is the frequency of the ith allele.This paramet~r is calculatedfor each locus and is usuallyaveragedover allloei (monomorphic and polymorphic). Values of Ae are influenced by P,Ap, and the evennessof allelefrequencies. Ha

ENZYME EXTRACTION

Enzyme extraction can be accomplished using protocols developed for other plant materials (see Kephart, 1990). Using flower-bud or stem tissue, we crush the material to afine powder under liquid nitrogen with a mortar and pestle. Pine ocean sand may be added to improve grinding of the plant tissue. An extraction buffer is then added to the powder to make a slurry. We have had good results with the extraction buffer of Mitton et al. (1979), which was developed for coniferous speeies. The buffer of Wendel and Parks (1982) also works well for so me speeies (e.g., Lophocereus schottii). Kephart (1990) and Wendel and Weeden (1989) provide thorough reviews of available extraction buffers. The slurry that results is then filtered through a patch of Miracloth and the liquid is absorbed on filter-paper wicks. Wicks can be used immediately or stored in a -70°C freezer with no loss of enzyme expression. Standard electrophoretic procedures and enzyme stains are then applied to resolve allozyme

124

Genetic Diversity in Columnar Cacti

= observed

heterozygosity. This parameter is calculated directly from observed genotype frequeneies at each locus and is averaged over allloei. The parameter is of limited value as a comparative statistic between speeies because it is affected by inbreeding and other evolutionary processes that may be unique to the speeies or population.

He = 1- 'I.p/ = the expected proportion of heterozygousloei per individual. Referred to as genetic diversity or genic diversity, this parameter is calculated for each locus and is averaged across monomorphic (Le., He = O) and polymorphic loei. It is a composite measure that summarizes genetic diversity at a locus. It is influenced by P,Ap, and allele frequeneies at each locus and is the most commonly used index of genetic diversity for allozyme data. HT = 1 - 'I.p/ = the total genetic diversity at polymorphic loei, where p¡ is the mean frequency of the ith allele pooled across all populations in a study.

Hs = the mean genetic diversitywithin populations for polymorphic loei.

~

125

J.J..M.¿...J.J.,J.I ,.,~

LJ.

.M.L.

LTeneilí.:

UI'v't:I;'H}

.~ GST= (HT - HS)/HT = the proportion of total genetic diversity that occurs among populations. Values of GSTare usually averaged over all polymorphic loci to estimate population divergence for the species. PIS = (He - Ho)/He = the proportional deviation at each locus of observed from exP P pected heterozygosity within populations. Values of PIScan be averaged over all polymorphic loci.

Genetic Diversity in Cactus Species

vUt.-H

TABLE 6.2 Leve1s of Overall

A more complete discussion of these parameters and their use can be found in Berg and Hamrick (1997).

"H vV"UiUUU¡

Genetic

Diversity

for Nine Species

of Cactia

Species

Ps(%)

APs

Aes

Hes

Carnegieagigantea Cereusrepandus wphocereus schottii Melocactuscurvispinus pachycereuspringlei Pereskiaguamacho Pilosocereuslanuginosus Stenocereusgriseus S. thurberi

93.3 94.1 90.3 89.5 91.7 89.5 91.3 100.0 83.8

2.79 3.69 3.00 3.82 3.14 3.53 3.52 3.50 3.42

1.20 1.47 1.39 1.21 1.38 1.45 1.43 1.35 1.33

0.129 0.242 0.214 0.145 0.212 0.239 0.274 0.812 0.201

a P, = proportion of polymorphic loei; AP, = number of alleles per polymorphic locus; Ae, = effective number alleles; He, = expected proportion of loei heterozygous per individual = genetic diversity.

of

VARIATIONWITHIN SPECIES Allozyme studies with sufficient populations and loci are available for seven species of columnar cacti and for two other cactus species, Melocactus curvispinus and Pereskia guamacho (Table 6.2). Stenocereus griseus has the highest proportion of polymorphic loci (Ps = 100%), whereas Stenocereus thurberi has the lowest (83.8%). The number of aneles per polymorphic locus ranges from 2.79 for Carnegiea gigantea to 3.82 for M. curvispinus. Genetic diversity (HeS>also varies among species, with C. gigantea having the lowest value (0.129) and Pilosocereuslanuginosus the highest (0.274). It is interesting that autotetraploid species, Pachycereus pringlei and Pilosocereus lanuginosus, maintain approximately the same levels of genetic diversity as diploid species. .

repandus, Pereskia guamacho, and Stenocereus griseus are significantly different from

zero (P < 0.01). An excess of homozygosity within a population can be due to at least two causes: inbreeding and population subdivision. For predominantly outcrossing species such as the cacti discussed here, self-fertilization is unlikely but biparental inbreeding between related individuals can occur, especially if seed dispersal is local. In addition, if there is population substructure (Le., a Wahlund effect), there would also be an apparent deficiency of heterozygotes. To obtain adequate sample sizes for these cactus species, rather large spatial areas were often sampled. It is ther~fore possible that some population genetic structure exists within the sampled areas, giving rise to the apparent deficiency of heterozygotes observed for so me of these species. Three of these cacti-Pachycereus pringlei, Pilosocereus lanuginosus, and Weberbauerocereus weberbaueri-are autotetraploid species with apparent tetrasomic inheritance patterns. As a result, individuals have four copies of aneles at each locus.

The relatively low genetic diversity in Carnegiea gigantea is due to the presence of a common anele (p > 0.95) at 17 of its 28 polymorphic loci. Melocactus curvispinus and Stenocereus griseus also have low Hes values relative to their Ps and APs values for the same reason. This conclusion is supported by the lower HT values for these three species relative to the other five species (Table 6.3). VARIATIONWITHIN POPULATIONS

TABLE6.3 Distribution of Genetic Diversity among Populations of Nine Species of Cactia

Data at the within-population level are available for ten cactus species. A single population was sampled for Weberbauerocereus weberbaueri and as a result, estimates of

~

~~a

genetic diversity for this species may not be representative of the species. Mean values of PP range from 45.3% for Melocactus curvispinus to 75.1 % for Pilosocereus lanuginosus (Table 6.4). Weberbauerocereus weberbaueri has the highest mean number of alleles per polymorphic locus (2.88) and M. curvispinus has the least

Carnegieagigantea Cereusrepandus Lophocereusschottii Melocactuscurvispinus Pachycereuspringlei Pereskiaguamacho Pilosocereus lanuginosus Stenocereusgriseus S. thurberi

(2.17). This trend is also seen for H ep: W weberbaueri=0.257 whereas M. curvispinus = 0.098. Where valid comparisons can be made (Le., diploid species), Ho values are somewhat lower than Hep values, indicating a deficit of heterozygous individuals relative to Hardy- Weinberg expectations. Mean PIS values of six of the seven diploid species have a deficiency of heterozygotes (positive PIS values), whereas Lophocereus schottii has a very small heterozygote excess (Table 6.3). The PIS values for Cereus

~ 0.125 0.228

0.237 0.166 0.231 0.261 0.267 0.177 0.239

0.158 0.112 0.213 0.215

0.252 0.152 0.201

a HT = total genetic diversity at polymorphic loei; Hs portion

of total genetic

diversity

~

0.139 0.277

due to differences

= mean among

within-population populations;

~

0.075 0.126 0.242 0.189 0.076 0.112 0.043 0.092 0.128

FIS

0.057 0.182 -0.003 0.377

_b

0.180

_b

0.145 0.036

genetic diversity; GST =pro-

= inbreeding

coeffieient

within

popuiations. b Autotetraploid species.

126

127

L

(

.1.1r\.J.vUH\

r

el

AL.

This do es not affect most of the population-level genetic diversity parameters. Observed heterozygosity is considerably elevated, however. For example, for a diploid species with two equally frequent alleles at a locus (p = q = 0.5), 50% of the individuals should be heterozygous. For a species with tetrasomic inheritance, in contrast, 94.4% of the individuals should be heterozygous (Le., have at least two alleles at a locus).

~ -

Species Lophocereus schottu pachycereus pringlei Stenocereus thurberi

53.7 72.3 49.5 45.3 62.1 63.4 76.1

2.20 2.44 2.33 2.17 2.50 2.42 2.69

1.19 1.38 1.25 1.16 1.37 1.37 1.41

Stenocereusgriseus

56.7

2.36

1.30

S. thurberi Weberbauerocereus weberbaueri

62.4 66.6

2.36 2.88

1.30 1.24

0.110 0.179 0.142 0.067 _b 0.170 _b 0.145 0.157 _b

0.116 0.205 0.144 0.098 0.200 0.202 0.253 0.161 0.169 0.257

a

= proportion of polymorphic lod; APp = number of alleles per polymorphic locus; Aep = effective number of alleles; Ho = observed proportion ofIod polymorphic per individual; Hep = expected proportion ofIoci het-

P

erozygous

per individual

= genetic

diveristy.

b Autotetraploidspedes;thus eachindividualis heterozygousfor most of the polymorphicloci. 128

93.3 73.3 70.8 83.9

3.09 3.00 3.04

2.79 2.59 2.82 2.92

0.197 0.220 0.214

Baja Sonora California 0.129 0.178 0.200 0.160

0.205 0.062 0.097

Sonora 0.075 0.082 0.062 0.059

VS. SONORA

POPULATIONS

netic diversity parameters (Ps' APs and Hes' Table 6.5) for these four species. Much of the additional genetic diversity in the Baja California populations is due to the presence of severallow-frequency alleles that are absent from the Sonora populations. Such genetic differences may indicate that the Baja California populations are ancestral to the Sonora populations, but such interpretations are difficult to verify when based only on genetic diversity measures. There is also more genetic differentiation among the Baja California populations for Lophocereus schottii and Stenocereus thurberi. As discussed above, much of the variation among L. schottii populations in Baja California is due to sampling across its two subspecies. Genetic differentiation among Baja California populations of S. thurberi is nearly 65% greater than genetic differentiation among populations of S. thurberi from Sonora. Fleming et al. (2001) have shown that when S. thurberi occurs with Pachycereus pringlei, it is predominantly bird- and insect pollinated but where P. pringlei is absent, S. thurberi is more frequently visited by the bat Leptonycteris curasoae. In Baja California, S. thurberi is sympatric with P. pringlei throughout its range, whereas in northern Sonora, P. pringlei is absent. Thus the higher genetic differentiation among the Baja California populations of S. thurberi may be due to more extensive pollination by less vagile insects. In much of its Sonora range, S. thurberi is pollinated by the more widely foraging L. curasoae, leading to the possibility of greater gene exchange among its populations (Fleming et aL, unpub~. data) and less genetic differentiation.

6.4

Cereus repandus Lophocereusschottii Melocactuscurvispinus Pachycereus pringlei Pereskiaguamacho Pilosocereus lanuginosus

Carnegieagigantea

Baja Baja Sonora California Sonora California

GST

The geographic distribution of three of the columnar cacti from northern Mexico and the southwestern United States allows comparisons among Sonora and Baja California populations of these species. Genetic diversity in the Baja California populations is generally higher than that seen in the Sonora populations for all of the ge-

Levels ofWithin-Population Genetic Diversity for Ten Species of Cactia H ep

76.7 91.7 80.6

BAJA CALIFORNIA

species (Cereus repandus, Melocactus curvispinus, Pereskia guamacho, Pilosocereus lanuginosus and Stenocereus griseus) is consistent with this interpretation. Although these five species were sampled from approximately the same geographic locations, the bee-pollinated Pereskia guamacho and the hummingbird-pollinated M. curvi-

Ho

Baja California

H es

spinus have somewhat higher GSTvalues (0.112 and 0.189, respectively) than the strictly bat-pollinated S. griseus (0.092), C. repandus (0.126), and Pilosocereus lanuginosus (0.043) (see Table 6.3).

Sonora populations. The remainder is predominantly due to variation among its Baja California populations (Table 6.5). There are two named subspecies of L. schottii in Baja California and our collections included both subspecies. Even taking these considerations into account, L. schottii has a somewhat higher GSTvalue for its Sonora populations than do the other three Sonora species (Table 6.5). This result may be due to low pollen flow among geographically separated populations of L. schottii. This species is predominantly pollinated by the mutualistic moth, Upiga virescens (Fleming and Holland, 1998; Holland and Fleming, 1999), which may have limited long-distance dispersal abilities. The other three Sonora cactus species are pollinated by a combination of birds, bats, and insects and may have a greater potential for pollen flow. Genetic differentiation among populations of five Venezuelan cactus

A ep

'-\.¡.~~~

e Tables 6.2 and 6.3 for definition of symbols.

has a relatively high GSTvalue (0.242). A significant portion of the among-population variation in L. schottii (38.8%) is due to variation between its Baja California and

APP

'--'~.,""."."

AP s

PS(%)

Interpopulation genetic variation is quite low for the majority of the nine cactus species with adequate data (Table 6.3). The exception is Lophocereus schottii, which

PP (%)

."

TABLE 6.5

Carnegiea gigantea.

TABLE

.L/~I"."¡~~")

Levels of Genetic Diversity within Sonora and Baja California Populations of Four Species of Columnar Cactia

VARIATIONAMONG POPULATIONS

Species

\Jt:ltt:tH...

L

129

HAMRICK

T

ET AL.

TABLE 6.6

only geographical regions that have been partially studied are Sonora and Baja California in Mexico and northern Venezuela. Thus columnar cacti in central and southern Mexico, Central America, Andean South America, and the Caribbean are largely unstudied. The existing studies demonstrate that cactus species, on average, maintain

Comparisons of the Mean Levels of Genetic Diversity for Cactus Species with Other Plant Species with Similar Life-History Traitsa Group Al! plant speciesb Long-lived woody plantsb Animal-pollinated,outcrossing woody plantsb Cactus species

Ps{O/o) 51.3 65.0 63.2 91.5

APs

Hes

HT

GST

2.89 2.88 2.87

0.150

0.224

0.228

0.177

0.253

0.084

0.211

0.268

0.099

3.38

0.211

0.222

0.120

high levels of genetic diversity. These cacti differ from many other long-lived woody species with animal-poIlinated breeding systems in that an exceptionally high proportion of their loci are polymorphic and that these polymorphic loci have more alleles. However, overalI genetic diversity at polymorphic loci (HT) is lower than the mean for other plants, indicating that a high proportion of the polymorphic loci of these cacti have a very common alIele and one or a few rare alIeles. Most of the genetic diversity within cactus species resides within their populations. There was some indication that predominantly insect-poIlinated species have

aSee Tables 6.2 and 6.4 for definition of symbols. b From Harnrick et al. (1992).

Comparisons

Genetic Diversity in Co/umnar Cacti

more genetic differentiation among their populations than predominantly batpoIlinated species. Additional studies are, however, needed before such generalizations can be stated with confidence.

with Other Plant Species

The nine cactus species with sufficient population samples generalIy have high leveIs of genetic diversity relative to the mean for other plant species (Table 6.6). The proportion of polymorphic loci (Ps) is much higher than that of the average plant species. The number of alIeIes at polymorphic loci (AP.) and mean genetic diversity (Hes) are also higher than the mean for other plant species. Interestingly, total genetic diversity at polymorphic loci (HT) is nearly equal to that of the average plant species. Cactus species also have a low proportion of their total genetic diversity among their populations (GST) relative to other types of plants.

Resumen Los estudios de diversidad genética en especies de cactus son sorprendentemente pocos considerando su importancia ecológica en regiones áridas del hemisferio occidental. De acuerdo a nuestro conocimiento, solo existen estimaciones de niveles de diversidad genetica para diez especies de cactus. Las únicas regiones geográficas que han sido parcialmente estudiadas son Sonora y Baja California en México, y el norte de Venezuela. Por tanto, las especies de cactus columnar en el centro y sur de México, America Central, los Andes de Sur America y el Caribe permanecen sin ser estudiadas. Los estudios existentes demuestran que las especies de cactus, en promedio, mantienen niveles altos de diversidad genética. Estas especies de cactus parecen diferir de otras especies de plantas leñosas de larga vida polinizadas por animales, en las cuales existe una proporción excepcionalmente alta de loci polimórficos, los cuales tienen más alelos. Sin embargo,

ReIative to plants that share many of their life-history traits-Iong-lived woody plants and woody plants with animal-poIlinated, predominantly outcrossing breeding systems-the nine cactus species discussed here have higher proportions of polymorphic loci and more alIeIes per polymorphic locus and equivalent Hes values. The mean HT value for the cacti is somewhat lower than the mean HT for other woody plants. Apparently, a high proportion of the polymorphic loci of these cacti have a single very common alIeIe and one or more reIatively rare alIeles. The mean GSTvalue for these cacti is somewhat higher than the means for other woody plants (predominantly wind-poIlinated) and for animal-poIlinated, outcross-

la diversidad genética total en locus polimórficos (HT) es menor que el promedio para otras plantas indicando que una alta proporción de loci polimorficos de estos cactus se caracterizan por tener un alelo muy común y pocos alelos raros. La mayor parte de la diversidad genética en especies de cactus reside dentro de las poblaciones. Se encontraron indicios de que especies polinizadas predominantemente por insectos tienen más diferenciación gen ética entre sus poblaciones qué las especies polinizadas predominantemente por murciélagos. Se necesitan más estudios adicionales antes de poder generalizar en estas conclusiones.

ing woody species. However, if Lophocereus schottii is removed from the analysis (see above), the mean GSTvalue for the other eight species is 0.105, only slightly higher than that of other animal-poIlinated woody species.

Surnmary

ACKNOWLEDGMENTS

Studies of genetic diversity within cactus species are surprisingly few, considering their ecological importance in the arid lands of the Western Hemisphere. Data estimating genetic diversity within and among populations exist for only ten cactus species. The

We thank Mindy Burke for technical assistance in the lab, Mary Harris for assistance with the field collections, and Mary Jo Godt for searching the allozyme database for cactus

130

131

j

nAMRICK

T

ET AL.

species. Portions of this work were supported by NSF Grant DEB9420254 to J.L.H. and J.D.N and an NSF supplernental grant to T.H.F. and J.M.N.

Genetic Diversity in Columnar Cacti

Sternberg, L., 1.P.Ting, and Z. Hanscorn. 1977. Polyrnorphism of rnicrobody rnalate dehydrogenase in Opuntia basilaris. Plant Physiology 59:329-30. Wendel, J. F., and C. R. Parks. 1982. Genetic control of isozyme variation in Camellina japonica L.Journal of Heredity 73: 197-204.

REFERENCES

Wendel, J. F., and N. F. Weeden. 1989. Visualízation and interpretation of plant isozyrnes. In Isozymes in Plant Biology, ed. D. E. Soltis and P. S. Soltis, 5-41. PortIand, Ore.: Dioscorides Press.

Berg, E. E., and J. L. Harnrick. 1997. Quantification of genetic diversity at allozyrne loci. Canadian Journal ofForest Research 27:415-24. Brown, A.H.D. 1979. Enzyrne polyrnorphisrn in plant populations. Theoretical Population Biology 15: 1-42. Flerning, T. H., and J. N. Holland. 1998. The evolution of oblígate rnutualisrns: the senita and senita rnoth. Oecologia 114:368-78. Flerning, T. H., S. Maurice, and J. L. Harnrick. 1998. Geographic variation in the breeding systern and the evolutionary stability of trioecy in Pachycereus pringlei (Cactaceae). Evolutionary Ecology 12:279-89. Flerning, T. H., C. T. Sahley, J. N. Holland, 1.Nason, and J. L. Harnrick. 2001. Sonoran Desert colurnnar cacti and the evolution of generalízed pollination systerns. Ecological Monographs 71:511-30. Harnrick, J. L., and M.J.W. Godt. 1989. Allozyrne diversity in plant species. In Plant Population Genetics, Breeding and Genetic Resources, ed. A.H.D. Brown, M. T. Clegg, A. L. Kahler, and B. S. Weir, 43-63. Sunderland, Mass.: Sinauer. -.

1996. Effects of lífe history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society of London: Biological Sciences 351: 1291-98. -. 1997. Genetic diversity in Opuntia spinosissim, a rare and endangered Florida Keys cactus. Final Report, Florida Nature Conservancy. Harnrick, J. L., M.J.W. Godt, and S. L. Sherrnan-Broyles. 1992. Factors influencing levels of genetic diversity in woody plant species. New Forests 6:95-124. Harnrick, J. L., Y.B. Linhart, and J. B. MiUon. 1979. Relationships between lífe history characteristics and electrophoretically detectable genetic variation in plants. Annual Review of Ecology and Systematics 10:173-200. Holland, N., and T. H. Flerning. 1999. Mutualistic interactions between Upiga virescens (Pyralidae), a pollination seed-consurner, and Lophocereus schottii (Cactaceae). Ecology 80: 2074-84.

Kephart, S. R. 1990. Starch gel electrophoresis of plant isozymes: a cornparative analysis of techniques. American Journal of Botany 77:693-712. Mabberley, D. J. 1997. The Plant Book. 2nd ed. London: Carnbridge University Press. MiUon, J. B., Y. B. Linhart, B. K. Sturgeon, and J. L. Harnrick. 1979. Allozyrne polyrnorphism detected in mature needle tissue of ponderosa pine, Pinus ponderosaLaws.JournalofHeredity 70:86-89.

Murawski, D.A., T. H. Fleming, K. RitIand, and J. L. Harnrick. 1994.Mating systern of Pachycereus pringlei: an autotetraploid cactus. Heredity 72:86-94. Nassar, J. M., J. L. Harnrick, and T. H. Flerning. 2001. Genetic variation and population structure of the rnixed-rnating cactus, Melocactus curvispinus (Cactaceae). Heredity 87:69-79. -. Forthcorning. Allozyrne diversity and population genetic structure of the leafy cactus, Pereskia guamacho (Cactaceae). American Journal of Botany. Neel, M. c., J. Clegg, and N. N. Ellstrand. 1996. Isozyme variation in Echinocereus engelmannii varo munzii (Cactaceae). Conservation Biology 10:622-31. Parker, K. c., and J. L. Harnrick. 1992. Genetic diversity and donal structure in a colurnnar cactus, Lophocereus schottii. American Journal of Botany 79:86-96. Sahley, C. T. 1996. Bat and hurnmingbird pollination of an autotetraploid colurnnar cactus, Weberbauerocereus weberbaueri (Cactaceae). American Journal of Botany 83: 1329-36. 132

~

133