Computer Notes

Simulation of Effects of
Dominance on Estimates of
Population Genetic Diversity
and Differentiation
K. V. Krutovskii, S. Y. Erofeeva,
J. E. Aagaard, and S. H. Strauss
The advent of PCR-based molecular markers has led to a rapid expansion in studies
describing the levels and distribution of
genetic variation among populations at
the DNA level. Randomly amplified polymorphic DNA (RAPD; Williams et al. 1990)
and amplified fragment length polymorphism (AFLP; Vos et al. 1995) markers are
now commonly used in population genetic
studies (e.g., Aagaard et al. 1998; Isabel et
al. 1995; Liu and Furnier 1993; Mosseler et
al. 1992; Peakall et al. 1995; Szmidt et al.
1996; Travis et al. 1996; Wu et al., in press).
However, these PCR-based markers have
limitations compared to allozymes, which
had been the prevalent means for population studies prior to the use of PCR. At
the majority of RAPD and AFLP loci the
dominant allele masks the presence of the
null allele in heterozygotes when assaying
diploid tissues (e.g., about 97%98%; Krutovskii et al. 1998), thus sampling variance
for dominant allele frequencies is typically
greater than that for codominant alleles
( Lynch and Milligan 1994). The frequencies of null and dominant alleles are
inferred from the frequency of null allele
homozygotes; the precision of their estimation thus depends on mating system assumptions and is strongly affected by the
sample size. Empirical studies have also
suggested that dominant markers can bias
estimates of genetic diversity and differentiation among populations (e.g., Isabel
et al. 1995; Szmidt et al. 1996).
Although RAPD markers have proved to
be useful for population studies, and their
gross patterns of diversity usually agree
with that of allozymes, the levels of genet-

ic variation, differentiation, and fine-scale

genetic structures often differ (e.g., Baruffi
et al. 1995; Dawson et al. 1996; Heun et al.
1994; Lanner-Herrera et al. 1996; Latta and
Mitton 1997; le Corre et al. 1997; Liu and
Furnier 1993; Peakall et al. 1995; Puterka
et al. 1993). To help assess whether these
differences are biological or a simple consequence of the dominance and biallelism
of RAPD and AFLP markers, we developed
a dominance simulation program, DOMSIM, that transforms codominant population data into a biallelic dominant dataset.
The program then estimates population
genetic statistics with which dominant
and codominant markers can be directly
compared. We use data from a widespread
North American conifer, Douglas-fir [Pseudotsuga menziesii (Mirb.) Franco], and
three California closed-cone pine species
to illustrate the programs function. The
test simulation suggests that dominant
biallelic markers, such as RAPDs, can
strongly underestimate population diversity but can still reasonably estimate population differentiation (GST), if sample
sizes are larger than about 30 individuals.

Program Functions
The program DOMSIM uses multiallelic datasets with a maximum number of six alleles per locus for which population allele
frequencies are defined. Assuming Hardy
Weinberg equilibrium and no linkage
among loci, the program generates N basic
populations (Nmax 5 20) of up to 1,000 individuals each with multilocus genotypes
that maintain the specified allele frequencies within populations. A total of S subpopulations (Smax 5 400) of n individuals
(n 5 10200) are then drawn with replacement for each of the N populations. The
sampling is done in two different ways: by
sampling subpopulations of size n with
replacement directly from the initially generated basic population, and by resampling subpopulations of size n with

replacement within the first sampled subpopulation of n individuals ( bootstrap resampling). Population genetic parameters
(HS, HT, and GST) are calculated for each
cycle of resampling in three ways. First,
for a codominant dataset, calculations are
made considering all alleles and genotypes present in the subpopulations. Second, the same subpopulations and data
are used to simulate a dominant biallelic
dataset by randomly selecting one allele
as dominant, with the rest treated as recessive to it. The synthetic null allele frequency is then calculated from the null
homozygote frequencies assuming Hardy
Weinberg equilibrium. Average parameters and their variance are calculated for
each set of S subpopulations. Gene diversity is evaluated using HS and HT, either
unmodified ( Nei 1973) or modified ( Nei
and Chesser 1983) for the sample size. Genetic differentiation is evaluated via uw
(Weir and Cockerham 1984) and GST parameters that are either unmodified ( Nei
1973), modified for the sample size ( Nei
and Chesser 1983), or modified for both
the sample size and population number
( Nei 1986). Finally, null allele frequencies
are corrected for dominance using Lynch
and Milligans (1994) equation 2a, and
their asymptotically unbiased estimate of
FST recommended for dominant markers is
also calculated following equation 14a.
Installing and Running the Program
The program DOMSIM is written in FORTRAN-77 (simulation routines) and in LabWindows CVI (interface routines). The
source code file, domsimd.f, was compiled
using Microsoft FORTRAN Power Station
Compiler version 1.0. DOMSIM runs on
IBM PCs and compatibles under MS Windows 95 and NT for 32-bit operating environments. To install the program run the
compressed self-extracting file domsimpr.exe which can be downloaded from
the web site http://www.fsl.orst.edu/tgerc/
protocol.htm. It will automatically decom-

499

press five files domsimd.f, domsim.001,

domsim.002, read.me, and setup.exe. Next,
run the setup file and follow the instructions on your screen during installation.
Run the program by either clicking the
icon or executing the program file domsim.exe. A read.me file contains additional
instructions for installing and running the
program.
Input and Output Files
The input format is an ASCII file similar to
GeneStat input files ( Lewis 1994), but
does not require population, locus, and allele names, and there should be no empty
lines. An example (sample.dat) and brief
help, which explicitly explains an input file
structure, are provided with the program.
The output file has all the parameters calculated for each resampled and bootstrap
set, their average values, and standard deviations.

Examples of Simulation Based on

Allozyme Data in Douglas-fir and
California Closed-Cone Pines
In order to facilitate comparisons between
dominant and codominant markers, and
to help understand the effects of RAPD
dominance and biallelism on our studies
of genetic diversity and differentiation in
Douglas-fir (Aagaard et al. 1998) and the
California closed-cone pines (Wu et al., in
press), we simulated dominance and biallelism in these two allozyme datasets ( Li
and Adams 1989; Wu et al., in press). The
first allozyme dataset included six populations of three races of Douglas-fir
coastal, north interior, and south interiorwith two populations per race. The
second one included four, five, and three
populations of Pinus attenuata, P. muricata,
and P. radiata, respectively. These populations are described in detail elsewhere
(Aagaard et al. 1998; Wu et al., in press).
From allozyme allele frequencies within
populations we generated simulated populations of 1,000 individuals each, and a
total of 400 subpopulations of n individuals were drawn with replacement from
each of the populations. The program also
performed 400 bootstrap resamplings using a subpopulation of size n. Population
genetic parameters (HS, HT, GST, uw, and
FST) were then calculated for each set of
400 subpopulations in the three ways described above. We varied the number of
individuals (n) within the subsamples
from 10 to 200 to bracket the range of sample sizes that might reasonably be employed in population studies, and the sam-

500 The Journal of Heredity 1999:90(4)

Figure 1. Levels of diversity and differentiation for codominant, multiallelic allozymes versus biallelic, dominant
markers, as simulated from an allozyme dataset from Douglas-fir studied with varying sample sizes. Standard
deviations (error bars) were calculated from the variance among 400 bootstrap subsamples and represent the
variance due to resampling of individuals at each level of sampling from the master population of 1,000 individuals.
The arrow shows the population sample size between 30 and 40 needed to eliminate the tendency for overestimation of population differentiation caused by dominance and biallelism.

ple size of 3050 trees per population that

was used in our RAPD studies (Aagaard et
al. 1998; Wu et al., in press). The results of
the simulations are summarized in Figures
1 and 2. The simulations showed that diversity measurements (HS and HT) were

likely to be underestimated by dominant

biallelic markers approximately twofold
regardless of sample size.
When 30 or more diploid individuals per
population were sampled, there was little
effect on differentiation estimates (GST, uw,

From the Departments of Forest Science (Aagaard, Krutovskii, and Strauss) and the College of Oceanic and
Atmospheric Sciences ( Erofeeva), Oregon State University, Corvallis, OR 97331-7501. We thank Tom Adams for
providing allozyme data and Vladislav Erofeev for help
with computer software. This work was supported in
part by NSF grants DEB 9300083 and BSR 895702 to
S.H.S. The dominance simulation program ( DOMSIM)
is available for public use and can be downloaded as
a self-extracting file domsimpr.exe from the TGERC web
site: http://www.fsl.orst.edu/tgerc/protocol.htm. Address correspondence to Dr. K. V. Krutovskii at the address above or e-mail: krutovskiik@fsl.orst.edu.
q 1999 The American Genetic Association

References
Aagaard JE, Krutovskii KV, and Strauss SH, 1998. RAPDs
and allozymes exhibit similar levels of diversity and
differentiation among populations and races of Douglas-fir. Heredity 81:6978.
Baruffi L, Damiani G, Guglielmino CR, Bandi C, Malacrida AR, and Gasperi G, 1995. Polymorphism within and
between populations of Ceratitis capitata: comparison
between RAPD and multilocus enzyme electrophoresis
data. Heredity 74:425437.
Dawson IK, Simons AJ, Waugh R, and Powell W, 1996.
Diversity and genetic differentiation among subpopulations Gliricidia sepium revealed by PCR-based assays.
Heredity 74:1018.
Heun M, Murphy JP, and Phillips TD, 1994. A comparison of RAPD and isozyme analyses for determining the
genetic relationships among Avena sterilis L. accessions. Theor Appl Genet 87:689696.
Isabel N, Beaulieu J, and Bousquet J, 1995. Complete
congruence between gene diversity estimates derived
from genotypic data at enzyme and random amplified
polymorphic DNA loci in black spruce. Proc Natl Acad
Sci USA 92:63696373.
Krutovskii KV, Vollmer SS, Sorensen FC, Adams WT,
Knapp SJ, and Strauss SH, 1998. RAPD genome maps of
Douglas-fir. J Hered 89:197205.
Lanner-Herrera C, Gustafsson M, Falt AS, and Bryngelsson T, 1996. Diversity of wild Brassica oleraceae as estimated by isozyme and RAPD analysis. Genet Resources Crop Evol 43:1323.
Figure 2. Genetic diversity (HS) and differentiation (GST; Nei 1986) values averaged over populations of each
California closed-cone pine species for codominant multiallelic allozyme and dominant biallelic markers simulated
in the samples of different sizes. Standard deviations (error bars) were calculated from the variance among 400
bootstrap subsamples simulated for each population of each species. Observed RAPD values are also shown as a
star.

and FST) in Douglas-fir. However, though

still very similar to the estimates for codominant markers, the estimates for the
simulated dominant markers began to diverge slightly but significantly downward
at large population sizes in Douglas-fir. In
the California closed-cone pines, the estimates for the simulated dominant markers
converge toward the estimates for codominant multiallelic markers at large population sizes, but were always significantly
higher (Wu et al., in press). Our simulations were in close agreement with our
empirical studies of Douglas-fir where, despite dominance and biallelism of RAPD
markers, we have found that RAPDs and
allozymes exhibit similar levels of differentiation at the population and race levels
with adequate sample sizes (Aagaard et al.

1998). However, the California closed-cone

pine allozyme data showed that the larger
sample sizes than we employed in our
RAPD study (Wu et al., in press) are desirable for a fair comparison of RAPD and
allozyme data. Finally, despite the expectation of much reduced diversity for dominant biallelic markers predicted by the
simulations, our RAPD data gave higher
estimates of diversity than did allozymes
in both Douglas-fir (Aagaard et al. 1998)
and the California closed-cone pines (Wu
et al., in press). This suggests that RAPD
markers may have much higher intrinsic
genetic diversity than do allozyme markers. Our results demonstrate the importance of simulations to help compare and
interpret the results of population studies
with dominant markers.

Latta RG and Mitton JB, 1997. A comparison of population differentiation across four classes of gene marker in limber pine (Pinus flexilis James). Genetics 146:
11531163.
le Corre V, Dumolin-Lape`gue S, and Kremer A, 1997.
Genetic variation at allozyme and RAPD loci in sessile
oak Quercus petraea (Matt.) Liebl.: the role of history
and geography. Mol Ecol 6:519529.
Lewis PO, 1994. GeneStat-PC 3.3. Raleigh, North Carolina: Department of Statistics, North Carolina State University.
Li P and Adams WT, 1989. Range-wide patterns of allozyme variation in Douglas-fir (Pseudotsuga menziesii).
Can J For Res 19:149161.
Liu Z and Furnier GR, 1993. Comparison of allozyme,
RFLP, and RAPD markers for revealing genetic variation
within and between trembling aspen and bigtooth aspen. Theor Appl Genet 87:97105.
Lynch M and Milligan BG, 1994. Analysis of population
genetic structure with RAPD markers. Mol Ecol 3:91
99.
Mosseler A, Egger KN, and Hughes GA, 1992. Low levels
of genetic diversity in red pine confirmed by random
amplified polymorphic DNA markers. Can J For Res 22:
13321337.
Nei M, 1973. Analysis of gene diversity in subdivided
populations. Proc Natl Acad Sci USA 70:33213323.
Nei M, 1986. Definition and estimation of fixation indices. Evolution 40:643645.

Computer Notes 501

Nei M and Chesser RK, 1983. Estimation of fixation indices and gene diversities. Ann Hum Genet 47:253259.
Peakall R, Smouse PE, and Huff DR, 1995. Evolutionary
implications of allozyme and RAPD variation in diploid
populations of dioecious buffalograss Buchloe dactyloides. Mol Ecol 4:135147.
Puterka GJ, Black IV WC, Steiner WM, and Burton RL,
1993 Genetic variation and phylogenetic relationships
among worldwide collections of the Russian wheat
aphid, Diuraphis noxia (Mordvilko), inferred from allozyme and RAPD-PCR markers. Heredity 70:604618.
Szmidt AE, Wang X, and Lu M, 1996. Empirical assessment of allozyme and RAPD variation in Pinus sylvestris
( L.) using haploid tissue analysis. Heredity 76:412420.
Travis SE, Maschinski J, and Keim P, 1996. An analysis
of genetic variation in Astragalus cremnophylax var.
cremnophylax, a critically endangered plant, using
AFLP markers. Mol Ecol 5:735745.
Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T,
Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, and
Zabeau M, 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:44074414.
Weir BS and Cockerham CC, 1984. Estimating F-statistics for the analysis of population structure. Evolution
38:13581370.
Williams JG, Kubelik AR, Livak KJ, Rafalski JA, and Tingey SV, 1990. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic
Acids Res 18:65316535.
Wu J, Krutovskii KV, and Strauss SH, in press. Nuclear
DNA diversity, population differentiation and phylogenetic relationships in the California closed-cone pines
based on RAPD and allozyme markers. Genome.
Received April 12, 1998
Accepted February 18, 1999
Corresponding Editor: Robert Angus

BOTTLENECK: A Computer
Program for Detecting
Recent Reductions in the
Effective Population Size
Using Allele Frequency Data
S. Piry, G. Luikart, and J-M.
Cornuet
BOTTLENECK (current version 1.2) is a
population genetics computer program
that conducts four tests for identifying
populations that have recently experienced a severe reduction in effective population size (Ne). Recently is defined as
within approximately the past 2Ne4Ne
generations, depending on several factors
such as the severity of the bottleneck and
the mutation rate of the loci being studied
(Cornuet and Luikart 1996). The program
runs on Windows 95y. It requires allele
frequency data obtained from one sample
of individuals (e.g., 2030 diploid individuals) and at least four polymorphic loci.
Significant deviations from population
mutation-drift equilibrium (e.g., bottlenecks) are important to detect because
equilibrium is an assumption required for

502 The Journal of Heredity 1999:90(4)

numerous analyses of population genetics

data (e.g., see Nei 1987, p. 251). Bottlenecks are important to detect in conservation biology because they can increase
the risk of population extinction. Founderflush events (i.e., short but severe bottlenecks) are important to detect because
they may play a role in some modes of
speciation [for reviews see Harrison
(1991) and Howard (1993)].

Principle
Populations that have experienced a recent reduction of their effective population size exhibit a correlative reduction of
the allele number and heterozygosity at
polymorphic loci. But the allele number is
reduced faster than the heterozygosity
(He). Thus the He becomes larger than the
heterozygosity (Heq) expected at mutationdrift equilibrium because Heq is calculated
from the allele number (and the sample
size; see Description below and Cornuet
and Luikart 1996). Note that He is calculated from allele frequencies (e.g., 1 2
Spi2, where pi is the frequency of the ith
allele). Here both the measured heterozygosity (He) and the expected equilibrium
heterozygosity (Heq) refer to heterozygosity in the sense of Neis (1987) gene diversity. Heterozygosity never refers to the
proportion of heterozygotes observed
(Ho). Thus we are not testing for an excess
of heterozyogotes (Ho . He), but rather an
excess of heterozygosity (He . Heq).
Strictly speaking, heterozygosity excess
has been demonstrated only for loci evolving under the infinite allele model ( IAM;
Kimura and Crow 1964) by Maruyama and
Fuerst (1985). If the locus evolves under
the strict one-step stepwise mutation
model (SMM; Ohta and Kimura 1973),
there can be situations where this heterozygosity excess is not observed (Cornuet
and Luikart 1996). However, few loci follow the strict SMM, and as soon as loci
depart slightly from the SMM toward the
IAM they will exhibit a heterozygosity excess as a consequence of a genetic bottleneck. When testing for bottlenecks, the
BOTTLENECK program uses both the
SMM and IAM independently, because
they represent two extreme models of mutation along a continuum of possible models (Chakraborty and Jin 1992). All loci will
follow a mutation model somewhere in-between the two extreme models.
For selectively neutral loci in a population near mutation-drift equilibrium (i.e., a
population in which Ne has remained fairly
constant in the past), there is approxi-

mately an equal probability that a locus

will show a slight heterozygosity excess or
a heterozygosity deficit. However, in recently bottlenecked populations, a majority of loci will exhibit an excess of heterozygosity ( Luikart and Cornuet 1998). To
determine if a population exhibits a significant number of loci with heterozygosity
excess, we proposed three statistical
tests: sign test, a standardized differences
test (Cornuet and Luikart 1996; Luikart
and Cornuet 1998), and a Wilcoxons
signed rank test ( Luikart et al., submitted;
Luikart 1997). We also proposed a graphical descriptor of the shape of the allele
frequency distribution (mode-shift indicator) which can differentiate between
bottlenecked and stable populations ( Luikart et al. 1998).
Interpretation of output from the sign
and standardized differences tests is thoroughly discussed in Cornuet and Luikart
(1996) and Luikart and Cornuet (1998). Interpretation of output from the graphical
descriptor is discussed in Luikart et al.
(1998). Guidelines for interpreting the output from the Wilcoxons test are less easy
to find ( Luikart 1997: chapter 4; Luikart et
al., submitted), although this test is analogous to the sign test. The Wilcoxons test
is generally the most useful of all the tests
because it is the most powerful (along
with the standardized differences test),
and robust ( like the sign test) when used
with few (,20) polymorphic loci. When
testing for bottlenecks, the null hypothesis of the Wilcoxons test is no significant
heterozygosity excess (on average across
loci). Thus the alternate hypothesis is significant heterozygosity excess (and thus
evidence of a recent bottleneck). This is a
one-tailed test that requires at least four
polymorphic loci to have any possibility
of obtaining a significant (P , .05) test result.

Description
The BOTTLENECK program computes for
each population sample and for each locus the distribution of the heterozygosity
(Heq) expected from the observed number
of alleles (k), given the sample size (n) under the assumption of mutation-drift equilibrium. This distribution is obtained
through simulating the coalescent process
of n genes under each of two possible mutation models, the IAM and the SMM. This
distribution enables the computation of the
average expected equilibrium heterozygosity (Heq) for each locus which is compared
to the HardyWeinberg heterozygosity (He,

i.e., gene diversity) in order to establish

whether there is a heterozygosity excess
or deficit at each locus. In addition, the
standard deviation (SD) of the mutationdrift equilibrium distribution of the heterozygosity is used to compute the standardized difference for each locus [(He 2
Heq)/SD]. The distribution obtained
through simulation also enables the computation of a P-value for the measured heterozygosity (He). The P-value is the probability of obtaining the measured He in a
sample (n) from an equilibrium population
that has the observed number of alleles
(k).
The way in which the coalescent process is simulated is unconventional due to
conditioning by the observed number of
alleles. The phylogeny of the n genes is
simulated as usual ( Hudson 1990). Under
the IAM, a single mutation is allocated at
a time and the resulting number of alleles
is computed. The process is repeated until
the simulation reaches the number of alleles (k) observed in the population sample. Under the SMM, a Bayesian approach
is used as explained in Cornuet and Luikart (1996). Briefly, the likelihood distribution of the parameter u (5 4Nem) given
the number of alleles (k) and the sample
size (n) is evaluated as the proportion of
iterations (in the simulation process) producing exactly k alleles for a varying set
of us. As a second step, drawing random
values of u according to the likelihood distribution, the coalescent process is simulated as usual. Only heterozygosities
found in iterations producing exactly k alleles are considered. Once all loci in a population sample have been processed the
three statistical tests are performed for
each mutation model, as explained in Cornuet and Luikart (1996), and the allele frequency distribution is graphed to determine whether a bottleneck-induced mode
shift has recently occurred. Note that a
mode shift is a transient distortion in the
distribution of allele frequencies such that
the frequency of alleles at low frequency
(frequency , 0.10) becomes lower than
the frequency of alleles in an intermediate
allele frequency class (see Luikart et al.
1998).

Input File Format

Five input data file formats are accepted
and automatically recognized by BOTTLENECK. All are text files. One is the GENEPOP computer program format (Raymond
and Rousset 1995). The second is the GENETIX computer program format ( Belkhir

et al. 1996). The other three formats concern single population data and are described in the help file of the program.

General Comments
BOTTLENECK is written in the Delphi 4 y
( Inprise Co.) computer language. The performance of BOTTLENECK has been thoroughly evaluated using simulated datasets
(Cornuet and Luikart 1996; Luikart et al.
1998) and allozyme and microsatellite datasets ( Luikart and Cornuet 1998). To
achieve reasonably high statistical power
(.0.80), we recommend typing at least 10
polymorphic loci (microsatellites or allozymes) and sampling at least 30 individuals. The standardized differences test is
recommended when using approximately
20 or more polymorphic loci (Cornuet and
Luikart 1996). For fewer than 20 loci, the
Wilcoxons test is the most appropriate
and powerful. The IAM is recommended
for allozyme data and the SMM is generally more appropriate when testing microsatellite loci (i.e., dinucleotide repeat loci)
( Luikart and Cornuet 1998). For most microsatellites, the TPM (two-phase model)
is apparently even more appropriate than
the SMM ( Di Rienzo et al. 1994; Luikart G,
unpublished data). The TPM was recently
added as an option in BOTTLENECK.
When using microsatellites we recommend the TPM with 95% single-step mutations and 5% multiple-step mutations
(and a variance among multiple steps of
approximately 12). When using the qualitative test for mode-shift distortion, we
recommend using at least 30 individuals
and 1020 polymorphic loci to avoid unreasonably high type 1 error rates (i.e., to
avoid concluding that a stable population
has been recently bottlenecked).
BOTTLENECK runs on any computer with
Windows 95 y. However, we recommend
a computer at least as fast as a pentium
PC. A fast pentium is especially recommended for analyzing datasets containing
many individuals (..30) and loci with
many alleles (e.g., . 3). Analyzing data under the SMM is far slower than analyses
assuming only the IAM. On a Pentium 166
it takes about 15 minutes to analyze a dataset of 44 individuals and 7 loci (with 2
8 alleles) when using both mutation models and 1000 simulation iterations. The
number of iterations influences the precision of the Heq estimates. A minimum of
1000 iterations is recommended. The program and example input and help files can
be obtained from the World Wide Web at
http://www.ensam.inra.fr/URLB.

From the Laboratoire de Modelisation et de Biologie

Evolutive, INRA-URLB, 488 rue de la Croix-Lavit, F-34090
Montpellier, France (Piry and Cornuet), and the Division
of Biological Sciences, University of Montana, Missoula,
Montana ( Luikart). G. Luikart is now at the Laboratoire
de Biologie des Populations dAltitude, Universite Joseph
Fourier, Grenoble, France. This work was funded by the
Institut National de la Recherche Agronomique, the Fulbright Foundation (to G.L.), and the Graduate School
of the University on Montana (to G.L.). I. Till-Bottraud
provided helpful comments. Address correspondence
to J-M. Cornuet at the address above or e-mail:
Cornuet@ensam.inra.fr.
q 1999 The American Genetic Association

References
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Chakraborty R and Jin L, 1992. Heterozygote deficiency,
population substructure and their implications in DNA
fingerprinting. Hum Genet 88:267272.
Cornuet J-M and Luikart G, 1996. Description and power analysis of two tests for detecting recent population
bottlenecks from allele frequency data. Genetics 144:
20012014.
Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin
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Harrison RG, 1991. Molecular changes at speciation.
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Howard DJ, 1993. Small populations, inbreeding, and
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can be maintained in a finite population. Genetics 49:
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Luikart G, 1997. Usefulness of molecular markers for
detecting population bottlenecks and monitoring genetic change (PhD dissertation). Missoula, Montana:
University of Montana.
Luikart G and Cornuet J-M, 1998. Empirical evaluation
of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228
237.
Luikart G, Allendorf FW, Sherwin B, and Cornuet J-M,
1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered
12:238247.
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Nei M, 1987. Molecular evolutionary genetics. New
York: Columbia University Press.
Ohta T and Kimura M, 1973. A model of mutation appropriate to estimate the number of electrophoretically
detectable alleles in a finite population. Genet Res
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Raymond M and Rousset F, 1995. GENEPOP (version
1.2): population genetics software for exact tests and
ecumenicism. J Hered 86:248249.
Received December 15, 1997
Accepted February 26, 1999
Corresponding Editor: Robert Angus

Computer Notes 503