Measuring Fitness and Natural Selection in Wild Plant Populations

Annual Reviews
Measuring Fitness and Natural Selection in Wild Plant Populations

Author(s): Richard B. Primack and Hyesoon Kang
Source: Annual Review of Ecology and Systematics, Vol. 20 (1989), pp. 367-396
Published by: Annual Reviews
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Annu. Rev. Ecol. Syst. 1989. 20:367-96
Copyright ? 1989 by Annual Reviews Inc. All rights reserved
MEASURING FITNESS AND

NATURAL SELECTIONIN WILD
PLANT POPULATIONS
Richard B. Primack and Hyesoon Kang

Biology Department, Boston University, 2 CummingtonStreet, Boston, Massachu-
setts 02215
INTRODUCTION
A fundamentalproblemin plant populationbiology and evolutionaryecology
is determiningthe extent to which naturalselection changes the gene pool of
populations in the wild. While the measurementof naturalselection in the
wild has recently been treatedextensively by Endler(36) the special problems
and advantages of studying plant species have not been specifically consid-
ered. This review examines the methods and pitfalls of measuring natural
selection in plants and suggests promising areas for future research.
This review follows the definition of Endler (36) that natural selection is a
process that occurs when threeconditions are met: First, phenotypicvariation
exists among individualswithin a populationin some character.Second, part
of this phenotypic variationis independentof environmentaleffects and can
be tranismittedgenetically from a parentto its offspring. And third, variation
among individuals in the character affects survival and reproductionand
ultimately affects fitness, the relative numberof offspring contributedto the
next generation by particularindividuals or genotypes. If these three state-
ments are true, then the frequency distributionof the characterwill change
from one generation to the next.
367
0066-4162/89/1120-0367$02.00
368 PRIMACK & KANG
ADVANTAGES AND DISADVANTAGES OF PLANTS IN

EVOLUTIONARYSTUDIES
Plants have a numberof significantadvantagesfor studies of naturalselection
in the wild. First, plants are sessile and so are particularlyamenable to
demographic studies of growth, survival, and reproduction(51). Second,
plants can be readily grown in controlled conditions, in both the laboratory
and the field, to separate genetic and environmentalcomponents of pheno-
type. Further,many plants can be cloned, using standard,simple horticultural
techniquesto producegenetically identicalreplicates.These cloned plantscan
then be exposed to different factors of naturalselection in different environ-
ments, yielding much more informationaboutnaturalselection than would be
possible in nonmodular organisms. And lastly, plants provide an ex-
ceptionally diverse arrayof sexual systems thatcan be used to test hypotheses
relating to differential fitness and naturalselection.
Plants also have attributesthat create general difficulties for investigations
of natural selection in the wild. The first problem is the great phenotypic
plasticity of plants, by which the same genotype can have radicallydifferent
phenotypes in contrasting environments (62, 119, 145). The result is that
considerablecareful work is needed to separatethe genetic component from
the phenotype. Second, even determiningthe extent of an individualgenotype
(a genet) can be a problem in many perennial plants that can produce new
physiologically independentunits (ramets)throughthe process of vegetative
reproduction (51). Many perennial plants have rhizomes or other mod-
ifications that can producenew individualsat some distancefrom the original
parentplant (51). Fallen leaves, branches,and even tree trunksmay be able to
take root and form new ramets. Once the connections between these plants
decay, isozyme techniquesmay be requiredto determinewhich rametsin the
population belong to a particulargenotype (130). Consequently, measuring
the fitness of individualsmay be problematicif the individualitself is difficult
to identify, particularlywhen it is very long-lived. Third, in most temperate
and many tropical species, the seeds do not germinateright away but remain
dormantin the soil (8a, 41a). This seed dormancycan last for months, years,
or even decades before the seeds finally germinate or die. Calculating the
fitness of an individualor a genotype is difficult if the dynamicsof this critical
stage in the life cycle are unknown(108, 117b). And fourth, while studentsof
animal populationscan sometimes establish the parentageof new individuals
by observing mating, birth, and parentalcare (15, 47, 156), studentsof plant
populations cannot easily infer the maternaland paternalidentity of newly
appearing seedlings (93). Consequently, while plant population biologists
assume that an individual plant that produces many pollen grains and seeds
contributes more offspring to the next generation than does a plant that
NATURALSELECTION
IN PLANTS 369
producesfew pollen grains and seeds, this assumptionremainsto be proven.

In summary, while certain stages in the life cycle can be studied in detail,
measurementof lifetime fitness is difficult to determine completely.
QUANTITATIVEGENETICS
The heritability of numerous plant charactershas been studied under con-
trolled conditions. Many life-historyand morphologicaltraitsrelatingto plant
fitness show continuousvariation,suggesting that they are polygenic (20, 40,
55a, 68, 69, 96, 97). Some charactersare controlled by a single gene (46,
55a). The genetic dissection of certain quantitative characters into their
component Mendelian factors now appearsto be possible in plants using the
techniques of molecular biology (32, 94, 103). The quantitative genetic
parametersof heritabilityand genetic correlationhave been used to predictthe
magnitudeand direction of the response to naturalselection of one trait or a
set of such traits. One way of estimatingthe heritabilityof a certaintraitis to
calculate for the trait the coefficient of regression of offspring on parents
(116, 138). Sib analysis is anothermethodwhich involves growing half-sib or
full-sib families of seedlings which share a common maternaland/orpaternal
parent. For example, in a paternalhalf-sib experiment,pollen from different
paternalplants will be used to produceseeds on each maternalplant, and the
resultingseedlings evaluatedfor theirtraits. Sib analysis has also been used to
partitionphenotypicvarianceinto genetic and environmentalcomponents(85,
86, 95, 123, 154). These techniquesestimate the additivegenetic component
of the phenotypic variation. Regression and sib analysis, however, may
overestimatethe actual heritabilitydue to both nonadditivegenetic variance
and common environmentalvariance(40). In general, paternalhalf-sib analy-
sis and the regression of offspring on paternalparent are the most reliable
methods because they minimize maternaleffects (40, 123). Growing clonal
materialacross a range of environmentsis also an effective way to estimate
environmental influences on phenotype (131), but this method misses the
crucial juvenile phase and is not as effective at estimating genotype X
environmentcomponents.
While the population may contain considerable genetic variability from
various sources, only the additive genetic variation in the population can
respond to natural selection. According to Fisher's FundamentalTheorem
(41), the amount of additive genetic variance for the traits relating to plant
fitness is predicted to be low. Considerablerecent attentionhas focused on
fitness components,charactersthat measuresuccess at some stage in the total
life cycle, such as seedling survival, leaf area, total numbers of seeds pro-
duced and seed size. Many botanists and zoologists have provided evidence
for low narrow-senseheritabilityof these fitness components(18, 47, 85, 95,
370 PRIMACK & KANG
99). The estimated heritabilitiesfor most fitness components are quite vari-
able among populations (12, 95) or between closely related species (99),
suggesting that generalizationsare not easy to make. Further,if the popula-
tion is neargenetic equilibriumthen the additivegenetic variancewill begin to
approachzero (53).
Most quantitativegenetic studies on plants have been conducted under
controlled environments,such as greenhouseor common garden, using crop
or cultivatedplant species. In contrast,relatively little work has been done on
wild species in naturalconditions(95, 123). Estimatesof heritabilityobtained
from controlledconditionsmay have limited applicabilityto the very different
growing conditions in the field. In particular,while the purpose of using
controlled conditions is to eliminate or minimize environmentalheterogene-
ity, in the field environmentalheterogeneitymay be the majordeterminantof
the phenotype (43, 51, 52). While measurementsin the greenhousemay tend
to overestimate heritability of many characters(96, 107), comparisons of
mean charactervalues for naturaland greenhouse populations suggest that
field results provide an approximateestimate of genetic variationfor certain
less plastic characters(89, 150). To resolve this question, experiments are
requiredin which heritabilityis measuredboth in the field and undera range
of controlled conditions.
In natural populations, the assumptions necessary for getting a precise
estimation of the quantitativegenetic parametersare difficult to meet com-
pletely (95, 96, 97). However, carefully designed field experiments can
overcome these difficulties to a certain extent, using the same methods
employed under controlled conditions. For example, sample size can be
increased to improve the statistical power. Potential inbreedingand assorta-
tive mating can be checked by careful, controlled matings of the study
organism, or at least can be taken into account. Maternal effects can be
eliminated by using paternalhalf-sib-families. One particularfeatureof con-
ducting quantitativegenetic studies in the field is the high initial mortalityof
seedlings, which means that seedling survival itself becomes an important
characterof study (122, 123).
The magnitudeof genetic correlationsamong traits can also be estimated
from the covariance/variancematrices of traits involved (40, 69, 154). Pat-
terns of genetic correlationsamong fitness componentscan stronglyinfluence
the role of natural selection (4, 97). If fitness components are genetically
positively relatedto each other, then naturalselection can rapidlychange gene
frequencies in a population. On the other hand, if fitness components are
negatively related, the ability of naturalselection to change gene frequencies
will be constrained.On a theoreticalbasis, significantlynegativerelationships
between fitness components have been proposed. These consequently have
been interpretedas indirectevidence for the presence of antagonisticgenetic
IN PLANTS
NATURALSELECTION 371
relationshipsor trade-offsbetween genes (4, 40, 114, 131). There is evidence

for negative genetic relationships between fitness components, especially
between seed size and seed number(105-107, 132) and betweenjuvenile and
adult characters (110). However, positive or neutral genetic relationships
between fitness componentshave also been found in many plant species (12,
95, 154), and these patternsmay be sensitive to environmentalconditions(65,
132). These results make us doubt the ubiquitous presence and general
significance of negative genetic relationshipsbetween most pairs of fitness
traits. The implicationsof both positive and negative correlationsneed to be
considered in the context of environmentsin which the species occur and the
traits involved (12, 105a). The relationshipbetween phenotypic correlations
and genetic correlationsis a particularlycrucial evolutionaryproblemrequir-
ing furtherstudy both in the field and in terms of its theoreticalimplications
(4, 19, 95, 107).
PHENOTYPICPLASTICITY
Phenotypic plasticity can generate a convergent phenotype from different
genotypes or can allow the same genotype to have different phenotypes in
contrastingenvironments(13, 62, 119). Phenotypicplasticity is investigated
when plants are grown underdifferentcontrolledenvironmentsor in different
naturalenvironmentsthroughthe use of reciprocaltransplants.The magnitude
of plastic response underdifferentenvironmentsis measuredby using coeffi-
cients of variation (18, 82, 83, 107) or variances (80, 131). Phenotypic
plasticity can occur in almost any featureof plant growth and developmentin
response to environmentalconditions. The pattern of plastic response can
differ among closely related species, among populations, and even among
individuals in a population (182, 83, 107, 119, 120). In studies involving
quantitativegenetics or measuringnaturalselection, an interactionbetween
genotypes and the local environmentis frequentlydetected, indicating that
microsite effects can overwhelmgenotypic effects (23, 123, 127). Phenotypic
plasticity is often explained as an adaptivephenomenonin a given environ-
ment mainly because of the sessile habit and modularstructureof plants (13,
119, 145). Considering the enormous range of plastic responses in various
traits, especially in such traits as numberand size of seeds traditionallyused
as major components of fitness, phenotypic plasticity surely cannot be dis-
missed as unimportantin an attempt to measure naturalselection.
Since the plastic response appears to be generally adaptive in a given
environment,plasticity itself may be a majortargetof naturalselection (121,
150b, 161). It is possible that a genetic system controlling the degree of
phenotypic plasticity may be distinct from that controllingthe genotype (13,
120, 131). In a study on several strainsof Phlox (Polemoniaceae),means for
372 PRIMACK& KANG
morphological and life-history characterswere measured across a range of

environmentalgradientsand comparedwith the amountas well as the direc-
tion of plastic response (120). The genotypic values (equivalentto the char-
acter means across environments)were not concordantwith the patternsof
plastic response, suggesting that the mean and the plasticity of a traitcan be
controlled independentlyof each other. However, studies on other species
have indicatedthatthe mean and patternof plasticity of a traitwere drivenby
the same force (80). While the results so far indicate that plasticity may be
controlled by a genetic system, the natureof this genetic system is not yet
entirely clear. The significance of phenotypicplasticity to differentialfitness
and naturalselection will be better appreciatedonce the genetic and physi-
ological basis of plasticity is more fully known.
MATERNAL EFFECTS
If performancefor a single or a set of traits is significantly different among
maternalfamilies, as opposed to paternalfamilies, it will indicatethat mater-
nal effects are operating on the progeny (84). Maternaleffects have been
detected in plants when a complete diallel matingdesign is used (85, 86, 112,
123, 154). Maternaleffects are frequentlydetected in seed size variation(7,
86), in the rate of germinationof seeds and the establishmentand growth of
seedlings, particularlyin competitive situations (111, 116, 117, 123, 138,
139). The head startthroughthe variationof seed size and seed qualitycan be
a great advantage in subsequentlife stages because the success of the later
stages of life cycle often depends upon the size hierarchyestablishedin early
stages (51, 112). In general, maternaleffects tend to become weakeras plants
age (123, 154). Certainmaternaleffects, on the other hand, can persist over
one or more generations (2, 133).
Three types of maternaleffects have been distinguished in plants (112).
First, cytoplasmic inheritancethroughplastids, chloroplasts, and mitochon-
dria can occur in plants (24, 133) and is independentof meiotic recombina-
tion. Second, the double fertilizationprocess in flowering plantsresults in the
productionof triploidendospermtissue that surroundsthe embryo. Since this
tissue develops from two maternal nuclei and one paternal nucleus, the
maternalparentmay have greatercontrolon the initial offspringbehaviorthan
does the paternalparent(155). And third,the maternalgenotype and maternal
environmentsare both known to affect offspring performance.For example,
maternalplants growing in favorable conditions produce bigger seeds; this
results in advantages in germination and/or establishmentof the offspring
simply because they have more resourcesin the seed and subsequentseedling.
Therefore the response to selection must take into account maternaleffects
from various sources.
NATURAL SELECTIONIN PLANTS 373
Quantitativegenetics experimentsmust consider the variance from mater-

nal effects (particularlywhen heritabilityestimates are derivedfrom maternal
half-sib analysis) or else the results may be overestimatesbecause maternal
effects increase the similarity between mother and offspring phenotypes.
Controlling maternal effects is the main reason for using paternal half-sib
analysis to calculate heritability.Since maternaleffects are definitely impor-
tant in seedling survival and subsequentplant growth, the appropriatedesign
for studies of fitness involves performing diallel crosses under standard
conditions and then transplantingthe seeds back into their environmentand
following their subsequentfate. Using such a design with the perennialgrass
Anthoxanthumodoratum, weak but significant genetic effects were detected
for seed germinationand seedling survivorship,in contrastwith strong mater-
nal effects and microsite effects indicative of differential plasticity even
among siblings (123).
RANGE OF CHARACTERSSHOWING GENETIC

VARIATION
Genetic variability can occur in morphological, physiological, anatomical,
biochemical, and phenological charactersexpressed at every stage in the life
cycle. The most detailed studies of genetic variabilitycome from crop plants
that have been studied extensively because of their economic value. For
example, plant breeding programsfor apples are directed at cold hardiness,
winter chilling requirements,season of flowering, durationof the juvenile
period, spur types on which the fruit are borne, fruit size, fruit shape, fruit
ribbing, season of fruitripening, fruitcolor, fruitflesh color, degree of russet
on the fruit, fruit flavor, disease resistance, pest resistance, and rootstock
quality (14). As a generalrule, these breedingprogramshave shown thatplant
species contain a large range of genetic variationfor charactersnot directly
correlatedwith total yield; this conclusion is in general agreement with the
results of breeding programswith animals (40).
Several sets of charactershave received particularattentionin the last few
years. First of all, allozymes have become importantas genetic markersand
as indicatorsof the level of heterozygosity. Geneticists have confirmed that
allozymes variable within populations are usually, though not always, in-
heritedin a Mendelianmanner(35a, 48). Second, the biochemical ecology of
plants has proved to be of basic importancein understandinghow plants are
able to resist attack by insects, other pests, and diseases. In general these
results have confirmed that genetic control over the quantities and types of
plant metabolites is similar to other types of quantitativegenetic characters
(10, 88).
Plants are now being examined simultaneouslyin the field for a wide range
374 PRIMACK& KANG
of fitness componentsin orderto see how they eventuallycorrelatewith plant

fecundity and survival (95). These investigationsinclude seedling characters
(date of germination, size of cotyledons, height of cotyledons), juvenile
characters (height and leaf area at certain dates after germination), adult
characters(date of first flowering, total numbersof flowers produced,number
of fruits and seeds produced, seed size, vegetative size of plant at maturity)
and survivalto each stage (12, 95, 110). In generalit appearsthatthese fitness
components have a low heritabilityin comparisonwith many other classes of
characters (95, 96). Such studies of multiple characters may eventually
identify which specific charactersare the targets of selection (66, 69a).
MEASURING FITNESS
Female Fitness
Fitness is estimatedby the relativenumberof offspringin the next generation,
a function of success in growth, survival, and reproduction. Traditional
studies of plant fitness have focused on seed production.Plants that produce
more seeds are assumed to have a greaterfitness than plants which produce
fewer seeds. This assumptionhas not been fully examined for three reasons.
First, seed productionis primarilya component of female fitness, not total
fitness which includes both seed and pollen production (77). The female
fitness of a plant is measuredas the numberof offspringin the next generation
that came from its fertilized ovules. Second, following seeds from one
generationto the next is difficult undernaturalconditions. Plantsthatproduce
relatively few seeds may have seeds of higher quality than do plants that
produce many seeds, and consequently the plants with low fecundity may
actually leave more offspring in futuregenerations.Third, seeds may remain
in the soil for years or even decades before germinating. Some of the
seedlings emerging in one year may have been producedby plants that died
many years in the past. The basic problemis that it is virtuallyimpossible to
markthe seeds while they are on the parentplant and to identify the parentsof
newly emerging seedlings. An alternativeapproachinvolves collecting the
seeds from parent plants and planting them into seed-free soil at fixed
positions in the naturalenvironment, and then monitoringthe germination,
survival, and fecundity of the resultingplants (122, 123). While such studies
are certainly an improvementin estimating female fitness, the stage of seed
dispersal is still missed and the seeds are in a more-or-less altered soil
environment,ratherthan in the naturalsoil at normalseed densities. Several
investigatorshave addressedthis problemby trying to develop techniquesto
label seeds and seedlings (108, 137). The most promisingtechniquecurrently
available involves the use of allozymic markersto establish parent-offspring
relationships of seedlings. Only one published study has applied this tech-
nique to the study of seedlings (93); this study is discussed in detail later.
Male Fitness
The total fitness of a plant has traditionallybeen estimated by counting the
relative number of seeds that it produced. However, fitness is equally de-
termined by success as a male parent in fertilizing ovules (77). The male
fitness of a plant is measuredas the numberof offspringin the next generation
that the plant sired with its pollen. Simple quantitativemethodscan be used to
estimate male fitness by assuming that plants which produce more pollen-
bearing flowers fertilize more ovules in the populationthan do plants which
producefewer pollen-bearingflowers (77, 100, 109). This estimationis only
true if all flowers produce equal amounts of pollen, the pollen is dispersed
evenly, and the pollen grains are equivalentin their ability to fertilize ovules.
This is probably a great oversimplificationsince certain individualshave an
enchanced ability relative to others to fertilize ovules in controlled crosses
(11, 81, 115, 125, 126). Consequently,the assumptionthat male fitness and
female fitness are directlycorrelatedin hermaphroditicplantsmay not be true.
Another method for estimating male fitness involves careful observations
of pollinatormovement from plantto plant and inferencesthat such pollinator
movement involves the transfer of pollen and subsequent fertilization of
ovules. However, in experimentalpopulations, such observationsappearto
be only weakly correlatedwith actualpollen transport(50, 124). The problem
appearsto be that pollen attachmentonto the pollinatorbody and subsequent
deposition onto the stigma is an erratic, irregularprocess, and pollen parents
may differ in their ability to fertilize ovules (50). Further, pollen may be
carriedon the body of the pollinatorduringmany visits to many plantsbefore
being deposited onto a stigma. Fluorescentdyes and powdershave been used
to follow pollen movements and in some systems seem to show a good
correlation with pollen movement (153). However, in other studies, dyed
pollen movement did not necessarily correlatewith fertilizationin the target
plant (50).
Isozyme markers have proved valuable in determining the paternity of
seeds collected from genetically known maternalplants in both naturaland
experimentalpopulations (Figure 1) (33, 34, 81, 92, 125, 126, 142). These
studies have clearly documenteda key aspect of male fitness and have also
shown that there is a differential ability of plants to fertilize ovules. These
studies have generally assumed that plants that fertilize more ovules leave
more offspring in the next generation than do plants that fertilize fewer
ovules. Since these studies, however, have not followed the subsequent
germinationand establishmentof seedlings in wild populations,this assump-
tion has yet to be evaluated. Experimentsare now needed to determineif the
376 PRIMACK & KANG
a.~~~~~~~~~~~~~ e
e~~~~~~~~
e
e 9 se g ge 09
2< 0 2
2 ci~~~~e
_ ~~~c 9 @ d
9 ~
e e~~~~~~~~
a.Pstoso aeaneaepat.b Lie extn fofeae pattohe mlswt
Figure]I Mating structurefor a Chamaeliriumpopulationin 1981 using isozyme markers(92).

a. Positions of male and female plants. b. Lines extend from female plants to the males with
which they mated, based on analysis of isozyme markers.
offspring sired by the successful male plants are as vigorous in natureas the
offspring of male plants that fertilized fewer ovules.
Plant charactersrelatedto male fitness may be affected by sexual selection
in a way comparableto animals(141, 143, 159). Sexual selection resultsfrom
the differential reproductivesuccess of individuals of the same sex and is
generally consideredto be a special form of naturalselection (36, 143, 159).
The primary requisite for sexual selection to operate on male fitness com-
ponents is the presence of additive genetic variation of traits related to
competitionfor mates and mate choice. In animals, high heritabilitiesfor such
male fitness components as body size and vocalization have been reported
(54, 91). In plants, genetic componentshave also been documentedfor such

charactersas pollen productionper flower (29), pollen grain size (140), and
pollen tube growthrate (64). In orderfor sexual selection to contributeto the
total plant fitness, the effect of genes expressed in the gametophyticphase
should not be antagonisticto those expressedat sporophyticphase (71). Some
indication of the positive, persistent effects of gametophytic selection on
survival or growth traits at sporophytic stage has been provided (71, 129,
160). Otherstudies have found negative effects or no effects (86, 135). Many
questions on the topic of sexual selection are open, especially regarding
evolutionaryadvantagesof sexual polymorphismscommon in plants and the
relative importance of natural and sexual selection for the total fitness of
plants (159).
Variation among plants in male fitness characters may often be over-
whelmed by the enormousvariationin the numberof flowers per plant. Many
studies have documented that pollinators are disproportionatelyattractedto
plants with larger inflorescences and numbers of flowers per plant (9, 25,
158). For example, in plantationsof wind-pollinatedspruce trees, the trees
that produce the most pollen cones tend to fertilize the most ovules (125,
126). Also, the ability of a plant to fertilize other plants and so act as a male
parentmay depend upon neighborhoodeffects because plants are most likely
to fertilize neighboringplants (Figures 2, 3) (76, 93). These spatialeffects of
nearest-neighborfertilizationscan dramaticallyinfluence measures of repro-
ductive success and estimates of gender (28, 162). Such effects of neighbor-
hood and plant size appear to be particularlyimportantif male fitness and
female fitness do not vary in parallel fashion.
0.35
e 0.3 I
U) A
0.25 I
X) 0.2 A
o 0.15 x
a A
o 0
E 0.1 go
0
Q.
2 0.05 X
x 'x
O X
0 10000 20000 30000 40000 50000 60000

Number of Male Cones Produced
Figure 2 Estimatedproportionof seeds sired by spruceclones differingin male cone production

(125). Estimates obtainedfrom the seeds of cones 585 (closed circles), 594 (open circles), 648
(closed squares), 650 (open squares), 667 (closed triangles), 694 (open triangles), and 716
(crosses).
378 PRIMACK & KANG
.12
- - pollen
n --- - seed
ad .pollen/seed .... combined
u
z
w
C3
. 04-
IL
* 5 10 15 20 25 s0 35
OISPERSAL OISTANCE Cm)
Figure 3 Frequency distributionprofiles comparing ~pollen dispersal,----seed dis-

persal, and ...cumulative male dispersal(pollen and seeds) from isozyme analysis of naturally
occurring Chamaeliriumseedlings (93).
Case Study-Direct Measurementsof Male and Female

Contributionsto Seedling Production in a Wild Population
Only one published study that we are aware of has actually spannedthe gap
from adults to established seedlings in a wild plant population. This unique
study by Meagher & Thompson (93) determinedthe percentageof seedlings
naturallyestablishing in a population of wild lilies, Chamaeliriumluteum.
The populationof reproductivelymatureindividualswas comparativelysmall
so that the population could be comprehensively sampled. The potential
parent pairs were consequently limited in numbers. Because the species is
also dioecious, the number of possible parents was furtherrestricted. The
population was sufficiently isolated that gene flow from neighboring pop-
ulationscould be discounted. Over the eight years of the study, the population
contained 281 seed-producingfemale plants and 634 flowering male plants.
These adults plus a total of 571 naturallyoccurringseedlings were evaluated
for eleven electrophoretic marker loci. The pool of possible parents was
considered to be those plants in flower one or two years prior to seed
emergence, since seed viability in the laboratorywas less thantwo years. The
most likely maternalparent was identified for 418 seedlings and the most
likely paternalparent for 313 seedlings. For 283 of the 571 seedlings, the
procedureallowed both most likely parentsto be identified. The most surpris-
ing result is that the number of seedlings produced is unrelatedto the fruit
production of female plants and the flower productionof male plants. The
correlationsare even negative, thoughnot significantlyso. Consequently,the
critical index of fitness is whetheror not a plant reproduces,while the actual
numbersof seeds and pollen grains producedare not useful predictorsof the
number of offspring produced.
NATURALSELECTION
IN PLANTS 379
This unique study by Meagher & Thompson (93) also hints at the limita-
tions of isozyme analysis. First, parentagecould be assigned to only about
half of the seedlings in a comparatively small, isolated population of a
dioecious species. In largerpopulationsof hermaphroditespecies with some
gene flow, the ability to assign parentage would require a much greater
numberof polymorphicloci. Second, the study only considered the pool of
possible parents to be those plants that flowered one or two years prior to
seedling emergence. However, if seed viability in the soil were longer than
two years, which is true for many plant species, then the analysis presented
might have to be recalculated.And third, since these plants are long-lived and
reproduce many times, and the seedlings themselves were not followed to
adulthood, lifetime fitness values of individual plants were not measured;
only some components of fitness were estimated.
NATURAL SELECTIONIN WILD POPULATIONS

One approachto determiningthe significance of naturalselection is to search
for nonrandomchanges in gene frequencies over time and on a local scale.
While such studies are potentiallyvaluable demonstrationsof evolution, they
may not necessarily reveal the phenotypiccharacterson which naturalselec-
tion is operating. Also, other mechanisms, such as gene flow, can cause
apparent changes from random patterns (36, 74). The following are
approachesthat have been used to provide evidence of naturalselection:
1. Populationsof wild grasses have been examined for the distributionof
allozyme polymorphismsin relation to an environmentalmosaic. In several
studies a significant, nonrandom association of particularallozymes with
certain microsite types suggested that genetic differentiationhad occurred
through the process of naturalselection (for example, 49, 101, 117b).
2. In a population of annuals, plants producing abundant seeds were
compared genetically with plants producing only a few seeds to see if the
charactersassociated with high seed productioncould be identified (43). No
genetic differences were found between large and small plants. In general, it
appears that any plant that has reached reproductivematurityis genetically
suited to its environment,with environmentalheterogeneitydeterminingthe
exact numberof seeds produced(52, 136) or, alternatively,thatselection is of
low intensity.
3. Naturalselection may act on the level of heterozygosity, changing the
gene frequenciesof the next generation.A higher-than-expectedfrequencyof
heterozygote seeds in numeroustree species provides such evidence of selec-
tion against homozygote progeny (70). Heterozygous individuals have also
often been considered to have higher growth rates than homozygous in-
dividuals (98) and by implication to have a higher fecundity;however, this
380 PRIMACK & KANG
view has recently been questioned through the use of more sophisticated
statistical techniques (16). In one study, heterozygotes appearedto have an
increased rate of survival in comparison to homozygotes (14a).
4. Naturalselection is often inferredwhen phenotypiccharactersare corre-
lated with survival and fecundity. Recently, multivariateregression tech-
niques have been developed by Lande & Arnold (69a) as a tool to identify the
targets of selection, to quantify the selective intensity, and to infer potential
selective agents. These techniquesappearto be useful in describingphenotyp-
ic selection in naturalpopulations(17a, 66, 117B, 144). The significance of
these techniques to naturalselection, however, requires a knowledge of the
genetic basis for phenotypic variation and also meeting certain statistical
assumptions related to regression analysis (97, 117b).
5. A species growing along a strong environmentalgradientis frequently
found to have individualsthat are physiologically or morphologicallyadapted
to their local site (reviewed in 55a). For example, on a local scale, individual
grass plants growing on a mine site grow better in soil contaminatedwith
heavy metals than do individualsin a nearbyuncontaminatedfield (5, 157a).
Other well-documented examples include adaptation to calcareous soils
(133a) and serpentinesoils (67a). Species with a wide geographicaldistribu-
tion often have populations adaptedto local climatic conditions (55a, 147,
148).
Phenotypic Selection on Fruit Characters and Dispersal
Seed dispersalcould be a process duringwhich naturalselection operatesto a
significant degree, affecting characteristicsof fruits (39, 59, 90, 134). Plants
with some fruit characterthat allows them to disperse more of their seeds to
good sites for germination and establishment will presumably leave more
offspring into futuregenerations.The existence of genetic variationfor a wide
range of fruitcharactershas been demonstratedby the breedersof commercial
fruit crops (61).
Detailed population studies of animal-dispersedfruit are consistent in
showing that within populations, plants with large fruit crops disperse more
seeds than do plants with small fruit crops (27, 55, 58, 99a). Intraspecific
variation in fruit charactershas only a limited effect on seed dispersal. For
example, in the Panamaniannutmeg Virola surinamensis(Myristicaceae), a
species with large seeds surroundedby a fleshy aril and dispersedby birds and
monkeys (58, 60), the proportionof fruits taken was negatively correlated
with seed size and positively correlatedwith the ratio of aril weight to seed
weight in only one of three years. Such results suggest that selective pressure
on these fruit traits is rather weak. In one of the three years, a negative
correlationexisted between the proportionof seeds dispersedand the number
of fruits on neighboringtrees; this shows that local effects can also have a
significant impact on seed dispersal. In Osyris quadripartita(Santalaceae),a

hemiparasiticshrubwith bird-dispersedfruitthat grows in Spain (55), 96% of
the variationin the numberof seeds dispersedis accountedfor by the number
of fruits producedper plant, while only 0.2% of the variationis explained by
interindividualdifferences in fruit characters, such as size and nutritional
content. These results all suggest that the overridingfactor determiningthe
numberof seeds dispersedis the numberof seeds producedby the plant, and
this may be largely determined by environmental factors. The effect of
intraspecific variation in fruit quality with some genetic basis is relatively
minor in comparison.In addition, many fruit charactersare developmentally,
phenologically, and pleiotropically linked to other reproductiveand vegeta-
tive characterson the plant, furtherconstrainingthe abilityof naturalselection
to change individual characters(106).
Case Study: Disruptive Phenotypic Selection in Impatiens

pallida
Many studies have documentedthe existence of phenotypic selection acting
on one characterat a single phase in the life-cycle of a particularpopulation.
Whetherthis selection is acting uniformlythroughoutthe populationand how
it affects both survivorshipand fecundity are rarelyaddressed.Several recent
studies have shown that the level of natural selection may be extremely
localized (66, 89, 123). For example, Stewart & Schoen (144) examined
phenotypic selection at 24 locations randomlydistributedwithin a 30 m x 40
m area containing a population of the annual Impatienspallida (Balsami-
naceae). A sample of 64 naturally occurring seedlings were studied per
location. Life-historycharacters,such as cotyledon area, plant size at various
dates, and date of first flowering were examined in relation to survivorship
and fecundity at each location. The surprisingresult was that the directionof
phenotypic selection was inconsistentat differentlocalities separatedby only
a few meters. For example, cotyledon area showed a significant positive
correlationwith fecundityat four localities, but a significantnegative correla-
tion at two other localities, and no correlation at the remaining eighteen
localities. Two key environmentalvariables-soil moisture levels and light
intensities-had a greater impact on survivorshipthan on fecundity.
This study (Stewart & Schoen-144) dramaticallyillustratesthe potential
complexity of naturalselection in the wild, since both viability selection and
fecundity selection influence overall phenotypicselection. And yet, since the
patterns of viability and fecundity selection are generally unrelated in this
study, the overall influence of phenotypic selection is difficult to predict if
only one phase in the life-cycle is studied. In particular,strong, fluctuating
phenotypic selection acting on a very local scale that is well within the
dispersaldistanceof the seeds may minimize the ability of naturalselection to
382 PRIMACK& KANG
change gene frequenciesacrossthe population.The abilityof naturalselection

to affect this system may be furtherminimized since most if not all of the
variation in these life-history charactersappearsto be under environmental
rather than genetic control (95). However, genetic differentiation in this
species has been found in relation to a strong environmentalgradient at a
different field site (1 18).
TransplantStudies
A valuable technique for examining the importanceof naturalselection in
adaptinglocal plant populationsto their environmentis the reciprocaltrans-
plant experiment. This technique involves comparing the performance of
resident individuals against that of alien individuals (members of the same
species from other populations)within a particularenvironment. If resident
individuals consistently outperformthe alien individualsin terms of growth,
survival, and fecundity, then this can be accepted as evidence for natural
selection and evolutionary adaptationto local conditions. While common
garden and greenhouse experiments may be used to demonstrate genetic
differences, these artificialenvironmentswill probablynot have some of the
key environmentalcomponents that affect plant performance(6, 55a, 74a).
Only in the field can the performanceof genotypesbe appropriatelyevaluated
for the relative contributions of genetic and environmentalfactors to the
observed phenotypic variation.
The use of reciprocaltransplantsto measurethe degree of local adaptation
has a long history in plant ecology (147, 148). These studies have confirmed
the ubiquity of naturalselection in adaptingpopulationsto extreme environ-
ments. One of the best-known and most detailed examples of such ex-
periments comes from research by Clausen, Keck, & Hiesey on races of
yarrow, Achillea millefolium (Compositae), cinquefoil, Potentilla glandulo-
sum (Rosaceae) and other species, along an altitudinalgradientin California
(20-22, 57). The basic research methodology involved cloning plants col-
lected from extreme and intermediatepoints in the species' altitudinalrange
and reciprocallytransplantingthe resultingplants back into gardensat each of
the habitats. Seedlings were also used for certainstudies. Both environmental
and genetic differences were found to play an importantrole in plant height,
survival, and timing of flowering. Residentplantstransplantedback into their
own environmentusually performedbetter than alien plants. Hybridization
studies demonstratedthatthere was quantitativegenetic variationboth among
and within populationsfor leaf and flower characters,as well as life-history
characterssuch as survival, growth, and phenology (57).
Many additional studies using reciprocal transplantsof cloned material
have investigated a wide range of species and environmentalagents, such as
metal tolerance(5), calcium contentin the soil (133a), andcompetitiveability

(149). However, transplantresearchnow often utilizes reciprocaltransplants
of seeds and seedlings (6, 118, 122, 123). Since the survival rate duringthe
period of seedling establishmentis quite low, this period may be a critical
time for naturalselection to operateif there is a genetic componentto survival
(27a, 89, 117b, 123). By using seeds and seedlings as the startingpoint for
the reciprocal transplant, the entire life-cycle can be studied, and fitness
differentialsamong genotypes can be expressedprecisely as differencesin the
finite rate of increase (27a, 75). Also, these classic studies by Clausen, Keck,
& Hiesey (20, 21, 22) involved populationsthat were morphologicallyquite
distinct and growing in radically differentenvironments.With such environ-
mentaldifferences, ecological adaptationcan probablybe demonstratedwith-
out consideringall of the complexities of experimentaldesign associatedwith
quantitativegenetics. Currentresearch often involves reciprocal transplants
among populations that are growing near to one anotherbut in contrasting
habitats.To detect the influence of naturalselection in responseto such subtle
and complex gradients, techniquesof experimentaldesign obviously must be
more sensitive. Lastly, in these classic studies, cloned material was trans-
planted into experimentalgardensat each field site. Such a methodology will
minimize within-siteenvironmentalheterogeneityand maximize the power of
the experimentto discern genetic differences among populations. However,
since researchersare now often concernedabout the degree to which genetic
variabilityis expressedin nature,many currentexperimentsinvolve reciproc-
al transplantsof seeds or seedlings directly into the undisturbedenvironment,
with the position carefully noted for later monitoring (6, 118, 123).
Case Study: Reciprocal Transplantsof Phlox drummondii

Among the most detailed transplantexperiments are those involving Phlox
drummondii (Polemoniaceae), a winter annual of Texas which grows in
discrete populationsthathave differentiatedphenotypicallyuntil they are now
considered as varieties (38). Schmidt& Levin (122) tested the hypothesisthat
natural selection has adapted each variety to its local environmentalong a
moisture gradient. Seeds collected from each of eight populations were
reciprocally sown into a planting scheme at each site. Experimentalseeds
were planted in narrow strips of seed-free sand runningthroughthe natural
vegetation so that the seeds would be exposed to the naturalenvironmentand
also that the experimental seeds could be distinguished from the naturally
occurring seeds in the seed bank. In comparison with plants coming from
resident seeds transplantedinto their own sites, plants from alien seeds have
an average of only 72% of the survivorshipand 71% of the fecundity, giving
them a calculated average rate of population increase of only 51% of the
384 PRIMACK& KANG
residents. These results appear to provide convincing evidence of natural

selection acting to adapt plants to their local environment.
This experiment on Phlox drummondiiby Levin & Bulinska-Radomska
(75) was extended to test the hypotheses that plants produced by either
interpopulationhybridizationor inbreedingwill have a different survivorship
and fecundity from resident plants. Plants from different populations were
grown in the greenhouse and hybridized between populations while other
plants were self-pollinated for one or two generations in the greenhouse.
Seeds obtainedfrom these treatmentsas well as field-collected residentseeds
were planted back into the field and evaluated for prereproductivesurvivor-
ship, fecundity, and estimated fitness calculated as the finite rate of popula-
tion increase. The results showed that hybrids had better average estimated
fitness than did residentplants. The plants self-pollinatedfor one generation,
and the open-pollinatedplants were indistinguishablein performance,while
the plants that were selfed for two generationshad a lower average estimated
fitness than that of resident plants.
These two studies of Phlox are excellent in terms of studying most of the
life cycle of the plant, growing plants in their natural environment, and
calculating estimated fitness differences in terms of the rates of population
increase. They are among the best studies to date of measuring fitness and
local adaptationin reciprocaltransplantexperiments. However, the results of
these fine studies could be improved and extended in several ways.
1. The seeds used in the first study were apparentlycollected from the
different field sites. The seeds in the second experiment were produced on
plants growing either in the field or in the greenhouse. The environmentof
seed maturationmay have played a greater role in seed germination and
subsequentseedling survival than did genetic differences among populations
(1 12). Ideally, the experimentshould have used seeds producedunderone set
of conditions, either in the greenhouse or in a common garden.
2. The first experiment showed that on the average resident plants did
betterthan aliens. However, in the majorityof cases the residentplants were
not the best plants at their own site in terms of the finite rate of population
increase; they were merely above average. This result suggests that while
residentsare well adaptedto theirown site, certainalien plantsoutperformthe
natives themselves. These results are difficult to explain if naturalselection is
in operation, and they need to be examined further.In additionto the mean,
perhaps the variance in performanceshould be considered as well.
3. These studies did not include measurementsof either seed dispersal or
post-dispersal germination. Fecundity was used as an approximationof fit-
ness. However, as discussed above, this assumption has not actually been
tested. This experiment could have been extended to study the transplants
over two or more generations to test the predictionsof population increase
based on this one-generationexperiment.
4. In anotherstudy, by Schwaegerle & Bazzaz (127), many of these same

populations were shown to be differentiatedgenetically in response to en-
vironmentalfactors, such as moisture, light, soils, and competition. Howev-
er, this genetic variationhad no simple relationshipto the environmentsof the
plants. The moisturegradientin particulardid not appearto be the dominant
selective force, as originally proposed. At this point, the major selective
agents at each site remain unknown. In addition, most of the quantitative
genetic variation as well as isozymic variationin this species occurs within
ratherthan between populations(128), indicatingthatpopulationsmay not be
uniquely adapted to their particularlocal environments.
GENETIC DRIFT
Gene frequency changes can also occur in populationsas a result of genetic

drift, as well as naturalselection. In plant populations, genetic drift may be
particularlysignificant due to the combinationof weak selection coefficients
and small, effective populationsize. While we can all recollect huge fields of
particularspecies in flower, the majorityof plant species probablyoccur as
scattered individuals or clumps. This effect of clumping will be enhanced
since most pollinatormovementtends to be between neighboringplants (76),
most seedlings establish near their maternalparent(93), and many plants are
obligately or facultatively self-pollinated. While gene flow may tend to
reduce the importanceof genetic drift, investigationsof actual gene flow in
natural populations are still limited (73, 74, 76). The available evidence
suggests that the naturallevel of gene flow may be highly variable, minimiz-
ing its impact on genetic drift (74).
Estimates of effective population size in plants are relatively few. The
potential numberof neighboringparentsthat would fertilize the ovules of a
target plant was estimated for 25 species (73). In 15 of these species, the
numberof potentialfathersin the populationis less than 150 plants. Because
of the leptokurtic nature of pollen dispersal, these figures are probably
inaccurateto some degree.
The great variability in size and fecundity among individuals in plant
populations can also decrease the effective number of individuals in the
population (43, 72). It is not unusualto find numerousplants that either are
not reproducingor are producingonly a small numberof seeds each, and a
few large plants that produce huge numbersof seeds. Since the large plants
may producethe overwhelmingmajorityof seeds in the population,the basic
models of genetic drift may have to be alteredto accomodatethe skewness in
plant fecundity (56). For example, in populations of 34 annual species,
variation in plant fecundity had a stronger effect on genetic drift than did
386 PRIMACK& KANG
randomgamete samplingerror(56). In many plantpopulations,the numberof

breedingindividualsmay give a quite false estimateof the truepopulationsize
and an extreme underestimateof the importanceof genetic drift.
These results all suggest that genetic drift may be of great importancein
determining the gene frequencies of the majority of plant species. Many
populationbiologists interestedin naturaland sexual selection are investigat-
ing small populationsbecause of the relative ease of assigning parentageto
seeds and seedlings. However, it is exactly in these small populations that
genetic drift may overwhelm the influence of naturalselection.
SOMATIC MUTATION
Mutations in the somatic cells of long-lived plants may result in genetic
variabilitywithin plants and increasedgenetic variabilityamong plantswithin
the population(67). Generalmodels of the populationgenetics and evolution
of higher animals may not represent the complete picture in long-lived
organismssuch as perennialplantswith numerousmeristemsin which there is
no sequesteringof a germ line, as in vertebrates(42, 130, 157). The apical
meristemof a shoot tip contains a clusterof cells thathave divided mitotically
large numbersof times to produce all of the cells of the stem, the leaves, the
buds, and the flowers and fruit. During these repeated mitotic divisions a
possibility exists that a cell in the apical meristem or one of the buds
undergoes a mutation (46). Many distinct types of such somatic mutations
have been identified in plants and are well known horticulturally(46). If this
mutantcell is in a favorableposition within the apical meristem, it may divide
mitotically and give rise to large numbers of descendant cells within the
shoot. Also, if the mutation confers some physiological or biochemical
advantageon these cells, they may divide more rapidlythan the other apical
cells and be representedby an increasingpercentageof the shoot's cells over
time (42, 157). If this process occurs throughoutthe plant, then individual
shoots of the plantwill begin to diverge genetically as a resultof these somatic
mutations. This genetic variability within individuals should increase over
time and be particularly evident in long-lived plants, such as trees and
clonally spreadingplants (67, 70). Such somatic mutationsmay increase the
phenotypic variability of the population and increase the response of the
population to naturalselection.
While somatic mutationcan arise from randommutation, it can also result
from inducible changes in the nuclearDNA caused by specific environmental
factors (26) as well as by ionizing radiation (104). Such genetic changes
include transpositions,translocations, amplifications, and deletions, and in
general the rate of such mutationsis relatedto the extent of stress on the plant
(87, 152). The genomic changes are often permanentand can be transmitted
throughmeiosis and mitosis from one generationto the next (26). The most
NATURALSELECTION
IN PLANTS 387
extensively studied plant species for this phenomenonare flax, tobacco, and
maize (26, 30, 31, 87). In flax, controlledenvironmentsof excellent or poor
growing conditions can result in permanentgenetic changes in plant height
and weight at maturity, the number of hairs on the fruit, the mobility of
isozyme bands, the total amountof nuclearDNA, andfor the numberof genes
coding for repetitivesequences in the genome, in particulargenes coding for
ribosomal RNA (26). Consequently, the extreme environmentalconditions
which are probably importantin naturalselection may have the secondary
effect of inducing greatergenetic variabilitythroughhigher somatic mutation
rates.
While these theoriesof somatic mutationand naturalselection are primarily
concernedwith the nucleargenome, DNA also exists in chloroplastsand other
plant plastids. In 86% of angiospermgenera surveyedto date, the inheritance
of chloroplastDNA occurs strictlythroughthe maternalline, while in 14%of
the genera, chloroplastDNA is inheritedfrom both the maternaland paternal
parents(24). Genetic variabilityoccurs in chloroplastDNA both among and
within species (8, 44, 102, 146, 151) and even occurs within individualtrees
(45). While somatic mutation of chloroplast DNA might be an important
source of heritablevariation,evaluatingits significance at the presenttime is
difficult due to the limited number of studies.
Somatic mutation has been hypothesized to be particularlysignificant in
allowing long-lived plants such as trees and clonally spreading plants to
evolve genetic defenses against insect pests with much shorterlife cycles (3,
157). Those branches (or ramets) with somatic mutations that confer pest-
resistance will grow better and produce more seeds than branches with no
pest-resistance,particularlyduringtimes of high pest populations.This argu-
ment could be extended to include inducible, random somatic mutations
(152). For example, branches that are defoliated by pests may come under
physiological stress, which might induce a higher rate of somatic mutation.
This high rate of mutationmight continueto producemore genetic variability
within an individual plant until a new genetic form is produced that has
pest-resistanceand can grow in the presence of the pests. As the shoot began
to grow more vigorously the mutationrate would then returnto its previously
low level. It should be pointedout thatwhile the theoryof long-lived plants as
genetic mosaics is an exciting new developmentin plant populationbiology,
the field evidence from wild populations is very limited (35, 67, 78, 130).
Antolin & Strobeck (3) and Gill (42) outline a series of predictions and
experimentalprocedureswhich could be used to test the theory.
CONCLUSIONS
The most convincing evidence for naturalselection in wild plant populations
comes from transplantstudies of clonal material which show that residents
388 PRIMACK& KANG
grow better then aliens. These experiments have involved comparisons of

extreme environments that presumably impose radically different selective
pressures on each population. In such circumstances, adaptationto local
environmentscan be demonstratedwithout worryingexcessively about such
subtle effects as acclimationand maternaleffects. However, the source of the
genetic variation in these experiments is not completely known. While no
evidence is available, it is possible that randomor inducible somatic muta-
tions are responsible for a least some of the adaptive genetic variation,
particularly in long-lived plants. Other reciprocal transplant experiments
comparing less extreme environments have sometimes failed to find that
residentplants are better adaptedto their own environmentthan other plants.
Such results are less easy to interpretbut suggest that the genetic variability
and phenotypic plasticity within each population are sufficient for many
plants in each population to survive and reproducein the normal range of
environments that the species occupies. It is only in the extreme environ-
ments, perhaps at the edge of the species' range, that natural selection
becomes strong enough to cause a measurablegenetic change in the popula-
tion (74a, 84a). Anotherpossibility to explain such negative results is thatthe
experimentwas not carriedout for a long enough time and thatsooner or later,
during some unusual environmentalcondition, the residents will show their
superiority.
Transplantexperimentsneed to be carriedout using either seeds or seed-
lings so that survival, growth, and a reproductiveschedule can be measured
and selective coefficients calculated. Many such transplantexperimentsusing
bulk samples of seeds collected from the field and maternalhalf-sibships of
seeds have confoundedmaternaleffects and genetic effects so that the results
are difficult to interpret. Whenever possible, the correct methodology in-
volves producing seeds under controlled conditions using diallel crosses to
separatematernal,paternal,genetic, and environmentaleffects. However, in
long-lived and in many clonally spreadingplants, such experimentsmay have
to be carriedout over many years. One crucial test of adaptationthat has not
been tried is reciprocal transplantexperimentsof annual species lasting for
two or more generations,to see if the initial advantagesof certainpopulations
persist. The genetic adaptationsnoted in certain reciprocal transplantex-
periments might come throughweak selection coefficients acting over many
generations on genetic variability against a dominating backgroundof en-
vironmentalheterogeneity.
Plant biologists have attemptedto estimate fitness componentsby various
means, but the assumptionsbehind these estimations have never been fully
evaluated, even though they often seem eminently logical. The following
conclusions should be kept in mind in investigations of fitness in plant
populations:
1. Plants that are visited more often by pollinatorsor that produce more
pollen do not necessarily have enhancedabilities as male parentsin compari-
son with other plants. The most effective method at the present time for
assessing male reproductivesuccess is isozyme analysis (34, 92, 125, 126).
2. Variationin charactersrelatedto fruit quality does not explain much of
the variationamong plants in the numberof fruitsdispersed.The total number
of fruits produced is the most importantindicator of the number of fruits
dispersed.
3. Experimentsare requiredto test the widespreadassumptionthat plants
which produce more seeds (and fertilize more ovules) leave more offspring
into the next generationthan do plants that producefewer seeds (and fertilize
fewer ovules).
4. Thereis often no generalrelationshipbetween survivorshipand fecundi-
ty, and consequently the overall effects of natural selection cannot be es-
timated if only one of them is measured (144).
Since virtuallyall publishedstudies examine only one partof the life of the
plant, the precise role of natural selection in wild plant populations also
remains generally unquantifiedat the present time. More studies are now
beginning to consider the complete life cycle of the plant. Perhapsone of the
few truisms is that if a plant does not survive to the flowering state it cannot
leave any offspring in the next generation(93). Anotherapparenttruthis that
substantialphenotypicand genetic variabilityis generally maintainedin most
naturalplant populations.
The single greatestproblemfaced by plant evolutionarybiology is that it is
extremely difficult to determinethe parentageof new seedlings appearingin
the population using present techniques. Isozyme analysis has been used
successfully in small populations to determine seedling parentage. In large
populationsand populationsin which there is some gene flow, determination
of seedling parentageusing isozyme analysis will requirea largernumberof
genetic markersthan is currentlyavailable. Because of the laboriousnatureof
isozyme work, the monomorphic nature of many loci and the statistical
problems of interpretation(17), field studies using isozymes to determine
relatedness have been very limited (93). An exciting new development in
zoology thatmay eventuallybe used to determinethe parentageof seedlings is
DNA fingerprinting(15, 63, 156). Unique combinations of markers can
identify individuals and give unequivocal answers in human paternitycases
(63). However, estimation of relatedness using DNA fingerprintingfaces
statisticalconstraintssimilarto those in isozyme analysis (79). These statisti-
cal problems may be particularlysevere in field studies of seedlings where
neitherparentis known. The basic techniquesof DNA fingerprintingappear
to be applicableto plant material(1 13). Assuming thatsuch techniquescan be
used in plants, measurementsof fitness components could be validated by
390 PRIMACK & KANG
comparisonswith directdeterminationsof lifetime fitness. Then plantpopula-

tion biology would be poised to enter anotherphase of rapid progress.
ACKNOWLEDGMENTS
The ideas in this paperwere developed with the supportof a National Science
Foundation grant (DEB 82-14108). Helpful comments on the manuscript
were provided by Pamela Hall, Scott Williams, Janis Antonovics, Norman
Ellstrand, John Silander, Miao Shili, Peter Del Tredici, Thomas Meagher,
Daniel Schoen, and John Endler.
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Measuring Fitness and Natural Selection in Wild Plant Populations

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Measuring Fitness and Natural Selection in Wild Plant Populations

MEASURING FITNESS AND

Richard B. Primack and Hyesoon Kang

ADVANTAGES AND DISADVANTAGES OF PLANTS IN

producesfew pollen grains and seeds, this assumptionremainsto be proven.

relationshipsor trade-offsbetween genes (4, 40, 114, 131). There is evidence

morphological and life-history characterswere measured across a range of

Quantitativegenetics experimentsmust consider the variance from mater-

RANGE OF CHARACTERSSHOWING GENETIC

of fitness componentsin orderto see how they eventuallycorrelatewith plant

a.Pstoso aeaneaepat.b Lie extn fofeae pattohe mlswt

Figure]I Mating structurefor a Chamaeliriumpopulationin 1981 using isozyme markers(92).

(54, 91). In plants, genetic componentshave also been documentedfor such

0 10000 20000 30000 40000 50000 60000

Figure 2 Estimatedproportionof seeds sired by spruceclones differingin male cone production

OISPERSAL OISTANCE Cm)

Figure 3 Frequency distributionprofiles comparing ~pollen dispersal,----seed dis-

Case Study-Direct Measurementsof Male and Female

NATURAL SELECTIONIN WILD POPULATIONS

significant impact on seed dispersal. In Osyris quadripartita(Santalaceae),a

Case Study: Disruptive Phenotypic Selection in Impatiens

change gene frequenciesacrossthe population.The abilityof naturalselection

metal tolerance(5), calcium contentin the soil (133a), andcompetitiveability

Case Study: Reciprocal Transplantsof Phlox drummondii

residents. These results appear to provide convincing evidence of natural

4. In anotherstudy, by Schwaegerle & Bazzaz (127), many of these same

Gene frequency changes can also occur in populationsas a result of genetic

randomgamete samplingerror(56). In many plantpopulations,the numberof

grow better then aliens. These experiments have involved comparisons of

comparisonswith directdeterminationsof lifetime fitness. Then plantpopula-

genetic and phenotypic correlations. 33. Ellstrand,N. C. 1984. Multiple paterni-

J. B. 1979. Relationships between life development, physiological constraints

breedingon fitness in Phlox. Am. J. Bot. ferentiation and life-cycle stages of

Tanksley, S. D. 1988. Resolution of pallida (Balsaminaceae), a selfing an-

Correlationand path coefficient analysis plications of phenotypic plasticity in

rapidly evolving pests. In A New Ecolo- Choice in Plants. Princeton,NJ: Prince-

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