tion is described

gene pool). In the ce~se of

sexually in
the
strueture is <ilso charCJcterized by the distribution of
e~llcles into

structure of a species can vary both geoand temporally.

The classical and neutral mutation models generate

testable hypotheses and are used to explain how much
variation should exist within. natural populations and what processes are responsible for the
observed variation.

For most loci, recurrent mutation changes allelic freat such a slow rate that its effects are
On the other hand, mutation is the initial source
of all variation. This implies that once a novel mutation enters a population, other forces predominate in
determining its changes in frequency.

Genetic drift is random change in allelic frequencies

caused by random sampling of gametes that occurs in
each generation. Genetic drift produces genetic
within populations, genetic differentiation
among populations, and loss of genetic variation
within populations.

SOON AFTER MENDEL'S PRINCIPLES WERE

rediscovered, geneticists began to look not only at
the genetic makeup of individuals but also the genetic
of populations. Population genetics allows
scientists to determine whether evolution is occurring
in groups of individuals as well as the forces that cause
to evolve. In this chapter, you will learn about
in the
makeup of populations, how such
and the factors that cause these
the
in the
you will
ics of a
of mussel that is rapidly spreading through
North American

molecular

Migration, also called gene flow, involves movement of

alleles among populations. Migration can alter the
allelic frequencies of a population, and it tends to
reduce genetic divergence among populations.

selection is differential reproduction of geno

It is measured by Darwinian
which is the
reproductive success of genotypes. Natural
can produce a number of different effects on
gene pool of a population.

mating affects the genotypic frequencies

a population. Assortative mating can promote
whereas inbreeding leads to an increase
homozygosity.

Principles of population genetics can be applied to the

management of rare and endangered species. Genetic
diversity is best maintained by establishing a
tion with adequate founders, expanding the popula~
tion rapidly, avoiding inbreeding, and maintaining n
equal sex ratio and equal family size

and
Each of these four areas focuses on a different
Transmission
is concerned
processes that occur within individuals and
how genes are
from one individual to
the unit of
for transmission
individuaL In molecular
in the molecular nature of
tion is encoded within the DNA
processes of the cell translate the
the

one or
of

but the traits

concern are deterThe latter two fields

applied to groups of
are amenable to mathematical treatthe oldest and richest
in
of these areas came after
'c''"'"'"" of Mendel's work and its
implications
In
the fusion of Mendelian theis called the nco-Darwinian
Sir Ronald
221) The neo-

our
shifts away from the individual and
the cell and focuses instead on a Mendelian
A
Mendelian
is a group of
als who share a common set of genes, The genes shared
are called the
the individuals of a Mendelian
gene
To understand the
of the
process, we
the gene pool of a Mendelian
rather than the genotypes of its individual members, An
structure of a
is
of the
of the
of
of genes for the conresources and the
servation of
and

a)

b)

The advent of
DNA

and

variation within
the DNA sequence leveL Since this is the form of
variation at its most fundamental
our abilities to
cern the forces that act on this variation have increased
in recent years, These data have also
for tbe kinds of
that popuaddrcss,
mitochondrial
DNA sequence
the female
amounts of movement,
groups, and
of
DNA sequence variation in theY chromosome reveals patterns of past movements of males of a
studied
variation is found in natural popand what processes control the amount of
variation observed?
2. 'What processes are
arnong
3. How do biological characteristics
such as
system,
ture, influence the gene
To answer these
often
mathematical models
describe what
to the gene
under various conditions, An
is the set of equations that describes the influence of random
on

c)

the allele and

Figure 22.2

which we discuss later in this

note

Panaxia domimtla, the scarlet

moth.
top two moths are
normal
(BB), those in the midclle two
erozygotes (Bb), and the bottom moth is the rare

a process to its
attributes of a
essence and allow one
system in isolation. With such models we can examine
what
to the
structure of a population
when
violate one
after
another and then in combination. Once we understand
the
ofthe

seeks to understand the underlying

causes of the observed levels of genetic variation in
The field includes both an empirical side,
measuring variation in natural populations, and a theoretical or statistical aspect, which attempts to explain
the observed variation with quantitative modeling.

must first describe the gene pool of

This is done
and allelic
A

ranges between 0 and 1.

group have red
the
0.43. To calculate the
at a
we count the number of individuals with one particular genotype and divide this number by the total number of individuals in the
We clo this for each of
the genotypes at the locus. The sum of the
Ireshould be l. Consider a locus that determines the
pattern of spots in the scarlet
moth, Pw1cLXiCl dorninula
Three genotypes arc present in most popuand each genotype
a different
E. B. Ford collcctecl moths at one
in
and
Cmmd the
numbers o[ genotypes: 452 l3T3, 43
and
for a total of 497 moths. The
cics
of) are therefore

j(Bh)

452/497

0.909

43/497

0.087

2/497 = 0.00+

Total

UlOO

uc.qucuc<.-n."

at a
locus arc use-.
of certain evolutionary

processes on a

there arc three alleles

genotypes form, ancl
each to describe the gene pooL
Allelic
can he calcubtccl
from the observed numbers of different
locus or from the

we can calculate the allelic

from the

rule that we used with two

\;Ve add up the number of alleles of each
and divide
the total number
of
in the

it
the total number of alleles at that locus in the population. This method is
and
for a wick
mitochondrial genes.
method
we get
of a
Allelic

Sum of counts of all alleles

in the

Each AA individual has two A

whereas each Aa
A allele.
possesses only a
the number of A alleles in the population is
number of A.A
+
number of Aa het+ 494 l
Since every
the total number of
twice the number of inclividuor
the
allelic
are present at a
formula
to calculate allelic
p

/(A)
X

To illustrate the calculation of allelic

when more than two alleles arc present, we will use data
from a
on
variation in milkweed beetles.
Walter Eanes and his coworkers examined allelic freat a locus that codes for 1he enzvme
(PGM). Three alleles were found at this
each allele codes for a different molecular variant
of the enzyme. In one
the
numbers of genotypes were collected:
4
41
84

total number of individuals

The second method of

the step of first
demonstrated

The
lows:

l n this

0.494, and j(aa)

of the alleles are calculated

From

fol-

0.135

we calculate the allelic fre-

0.'542

j(a)

ages of the two alleles.

can be
obtained

that bas
l) of
the sum of the percentonce p is calculated, q
subtraction: 1 - p
Cf.

we have
with
th 1ec zdlclcs--i\ 1, ;V, and A 1 --at a
and we want to
detrrrninc the allelic
ucncies. Here, we usc the same

{(A')

0.323

As
add twice the
number of
that possess the allele and one
times the count of each of the
that have
the allele. We then divide by twice the number of inclividuals in the
, which represents the total
number of alleles present In the top part of tl1e equation, notice that for each allelic
we clo not add
all the
because some of the
clo not have the allele; for
in
allelic
of A 1, we do not add the number of
il.'/\ 1
in the top
of the
individuals clo not have an A allele. \;Vc can usc the
same
for
allelic
when
four or more alleles are present
1

The second method for

allelic
can be determined from the genoas follows:
l
3

alleles are A and

are
in

q
This formula assumes that the
were calculated
for each sex, so that
+
l. Be sure that you understand the
behind the gene
do
orize the formulas. If you understand
the
you will not need to remember the
equations and will be able to determine allelic
cies for any situation.

error

calculations from direct

genotype freis illustrated for a onein Box 22.1.
X-linked locus.

we
we used for autosomal loci.
female carries two
one of that
females have
all males have
To determine
the number of alleles at an X-linkecl
we multiply
females
2, then add the
number of
females and the number of hemWe next divide
the total number of
When determining the total
number of
we add twice the number of females
each female has two X-linked
to the
number of males
allele at X-llnkcd
loci).
of two alleles
and X") are determined with the

The genetic structure of a population is determined by

the total of all alleles (the gene pool). In the case of
diploid, sexually interbreeding individuals, the structure is
also characterized by the distribution of alleles into geno
types. The genetic structure can be described in terms of
allelic and genotypic frequencies. Except for rare muta
tions, individuals are born and die with the same set of
alleles; what changes genetically over time (evolves) is
hereditary makeup of a group of individuals, reproconnected in a Mendelian population.

law serves as a foundation for population

because it offers a simple
for
how the Mendelian principle of
allelic and genotypic frequencies in a
law is named after the two

a set of
statement of the law follows:

(2

X"X"
(2.

x mllnbcr of females)
of

Port 1.: In an infi

tion. free from mutation,
selection
that there are five
Part
The
of the alleles do not
time: and

AA

AS

ss

2,017

783

AC
173

sc

CC

Total

14

ll

3,002

Calculation of

f(AS)

783
3,002

14
3,002

0.261

0.0047

Calculation of Allelic
Allelic

0.134
j(A)

~ ~~~':.'-.'!~-'2:'2_~~~~~.::=_~~~~~~'::::~~~.~~~

2 X total number of individuals

0.831
f(C)

=~:_:~~~~~~.~~~~~~~~~~~~:..:::'.:::.~~~

2 x total number of individuals

0.035

Calculation of Allelic

xO 058

Part

should be
+ q" 1).
where p is
allelic

of a. The sum of the

and q is the
fre-

ln
to

)= 0 035

to

what
of a

it is) and its allele

was recessive, then short
to become more common with each generation. In time
Punnett
almost everyone in Britain should have short
believed the argument was incorrect, but he could not prove it.
was able to write a few
tl1at,
of alleles for short
and
the relative number

as the alleles are

in the absence of
if the
be

will stay the same generation after generation if no natural

selection is involved that favors one phenotype or the other
offspring. Hardy published a short paper
the relationship between genotypes and
types in
and within a few weeks a ,paper was
published by Wilhelm Weinberg
a German
of
that clearly stated the same relationJaw signaled the beginning of mod-we should note that in 1903 American
was the first to
the
between allele and genotypic h:cand vVeinherg who
in mathematical terms.
the law is sometimes called the
W E. Castle of Harvard

genotypes is

law
certain concli-
tions, or
which must be present for the law to
First, the law indicates that the
must be
If a
is limited in
chance
ratios can cause
in allelic
drift. It is true that

To illustrate random
types in humans discussed in
12. The M-N blood
type results from an
on the surface or a red blood
similar to the ABO
except that
in the M-N system docs not cause
blood transfusion. The M-N blood type is determined
one locus with two coclominant
L"'1 and L 1\ In a
of
the
M-N
= 0.835, LM/L N
and
Tf Eskimos interbreed
the
between an L"'1/LM male and an
female is equal to the
of LM/L"1 times the
1
1
of L"-' 1L"
0.835 x 0.835
0.697.
of

students

law to hold. H this were true, human

law because humans do
never

ly for

,\ second condition of the I

nmst be random."'"""''~""
bctwcl'Jl genotypes

that

hrw

skin
socioeconomic status, ;mel other
traits. However, although
traits, most humans still mate
blood types; few ol us even know what our l'A-N
types arc. The
of the
to any locus for which random
if mating is nonrandom for other loci.
Finally, for the
l;nv to work the
must he free from mutation, m
natural :;election
in detail later). Jn nrhcr

the gene pool must be closed to the addition or

subtraction of
and we are interested in how allelic
are related to

of
into the
and
two gametes at random. The genotypes that
then form after
time will he

relevant processes
must be excluded. Later we discuss these other evoluprocesses and their effect
of a
This condition

law. We see that when gametes

genOt}lJeS wiiJ occur in the nr.~n.~rt;n

and q2 (aa). These

square of the
+ q2 , and the genotypes reach
after one generation of random

law are met, the

and two results
of the alleles will not

law continue to be met. When the genotypes arc in these proportions, the
is said to be

are
theoretical distribution of genotypes does not
determined distribution.
the

tion
understood by
matpopulation, as illustrated in Table 22.2. In Table 22.2,
all
definition, random mat-

are also
\Ne see that the sum of the

(or
and Aa x AA (or
know from Mendelian

when certain conditions arc satisfied. The necessary conditions are that the
and free from
and natural selection. When these
mutation,
the
law
conch tions
that allelic
will be determined by the
p2 ,
and q2

can

Possible Combinations of A and a Gametes from

Gametic Pools for a

Male gametes
A(p)

o(q)

sidcr a
of allele /1. is p ancl the

of A and a in the gametes are also[! and q. lf

one thinks of the gametes as
in a
the random

ln sum, p2 1\i\ +

Aa+ q2 aa

l.OO

in a Randomly Mating Population for One Gene locus with Two Alleles

recmc:nc1es Contributed to the Next Generation

a Particular
AA

p AA x p AA
p2 AA x 2
2 pq Aa x
p2 AA X aa
2

q2 aa x

AA

2 pq Aa x 2 pq Aa

aa

p4

p"

~r

Aa

2 p3q

4 pq3

Aa x q aa )
aa x 2 pq Aa

2 pq3

q4

+ 2pq +

+ 2pq +

+ 2 pq +

2 pq

q2

afterward.
afterward.
between AA and Aa will occur at p2 X 2
and Aa, result in equal proportions from

random
the .,,., ....,,,,"'"
and q2 and the allelic
of the

= 2 p3q for AA

x Aa and at p2 x 2 pq = 2 p'q for Aa x AA for a total of 'I

malings. Therefore,
frequencies are 2 p3q (i.e., l/2 x 4

are still p2 ,
remain at p and q.
can thus be represtages as follows:

rare recessive condition in humans. In

albinism, affected individuals have no
which is required for normal

pA +qa

of zygotes
A and a gametes
in
p and q. The gametes unite to form
and aa zygotes in the
p2 ,
and q2 , and the
as the
of
law bold. This short
law.
law indicates that at
depend on the
This relationship between allelic
for a locus with
22.3. Several
maximum
and this maximum
of A and a are

abscissa] and q [bottom abscissa], respectively) in populations that meet the assumptions of the
law.
Any
is defined
a single vertical line such
p = 0.3 and Cf
Frequency of allele A in population (value of p)
0.5
0.3

Frequency of
aa in population (q 2 )
(J)

<J)

0..

;>,

c:

Frequency of Aa '
in population (2pq)

<J)

CJ)

0 0.5

G
c

the

<J)

and (J) when the

for that allele the rarest of the genotypes.
is also illustrated
the distribution of

:J
0"

LL

L-~-~--L--.~L-~---~~--J_--L---1---~~=-J

nonaffcctccl

for

0.5
0,7
Frequency of allele a in population (value of q)

1.0

LAP9BJL!\P9s
LAP 98/LAP 96
J_Ap96JLAP96

The Hardy-Weinberg law describes what happens to

allelic and genotypic frequencies of a large population,
when gametes fuse randomly and there is no mutation, migration, or natural selection. If these conditions
are met, allelic frequencies do not change from generation to generation, and the genotypic frequencies
stabilize after one generation in the proportions p2 ,
and q2 , where p and q equal the frequencies of
the alleles in the population.

When two alleles are present at a

law tells us that at equilibrium the
and q2 , which is the square of the
(p +
This is a
binomial
and this
of
can be
extended to any number of alleles that are sampled two at
a time into a
For
if three alleles are
equal to
present
alleles A, B, and
p, q, and r, the
of the genotypes at equilibrium
are also
the square of the allelic
(p

(A B)+
(AC) +

q+

+ rl

In the blue mussel found

the Atlantic coast of
North
three alleles are common at a locus cod. For a
for the enzyme leucine
lsland Sound
of mussels
Richard K. Koehn and colcussecllater; sec
of the three
determined that the
alleles were as follows:
LAP 9 's

p = 0.52

Li\P"c'

I[= 0.31

L.AFH

0.1'7

(0 31)2

= O.lO

LJJ,.p96/LAP94

2(0.31)(0.17)

0. l

LAP9 "/L.AP 98

= 2(0.52.)(0 17)

0.18

= (0.17) 2

0.03

J_Ap9'f/Li\P9-t

for albinism are much

1 in lOQ). When an allele is rare,
of that allele are in
and in
this case recessive
often are very rare.

q2

r2

The square of the allelic

can be used in the
of the genosame way to estimate the
types when four or more alleles are present at a locus.

in which
females are XX and males are XY. If alleles are
females may be
For
cies are the same as those for autosomal loci:
, and q2 (X 13 X13 ). In
however, the freof the genotypes are p
and q
same as the frequencies of the alleles in the
For this reason, recessive X-linked traits are more fre~
quent among males than among females. To illustrate this
concept, consider
color
which is an
X-linked recessive trait. vVe
ferent defective alleles cause
but for now let's lump them
the color blindness allele varies among human ethnic
groups; the frequency among African Americans is 0.039.
At equilibrium, the expected
of color blind
males in this group is q = 0.039, but the
color blind females is
q2 (0.039) 2 = 0.0015.
When random mating occurs within a
the
equilibrium
frequencies are reached in one gen~
eration. However, if the alleles are X--linkecl and the sexes
differ in allelic
the
are
over several
receive their
chromosome from their mother
whereas females receive an X chromosome from both the
mother and the father.
the
of an
X~ linked allele in males is the same
of that
allele in their
the average of that in mothers and fathers.
oscillate
the allelic
in the tvvo
back and forth each
and the difference in allelic
between the sexes is reduced
half each generation, as shown in
22.4. Once the allelic
cies of the males and females are
the

'""""'''orh to
of an
an initial of 1 .0 in females and 0 in males.

p j(M)

0,50

1,0
OJ

iJ:1 0,8

p and (1
we can

0,6
0,4

test,

0.2

4
5
Generations

we
each
times the total
her of individuals counted (N), as follows:

f(jJ)
is
the chance that we would get this
c]lance alone?" rr the observed
match the
structure based
we can
to ask about vvhich of the
are
violated,
determine whether the genotypes of a population are in
we first compute the allelic
from the observed 'w'"~'"'"
not to take the square
to obtain allele fre-

test
us the
that the difference between what we observed
and what we expect under the
law is due
to chance, To illustrate this
that cocles for transferrin (a blood
backed
Three genotypes
[ound at the transferrin locus: MM,
In a population of voles
in the Northwest Territories of
Canada in 1976, l ,\!JM
53
m1cl I JJ iml i vicl ua ls
tlw genotypes are in
first calculate the ;tllelic
onr fmniliar formula:

p2

0.25

q2

77

9.3

xN
x77

38.5

53

19.3

l2

= 0,25

With observed and

we can comrmte a
value to determine the
ty that
the differences between observed and
numbers
could be the result of chance. The
(X')
we used for
is calculatrcl for

the sutn of all

We now need
Table
freeclon1. This
step is not
square
of freedom was the number of classes in
minus L 'While there are three classes there is
of freeclorn because the
have no
values, Thus p
must be estimated from the observations themselves. So
one
of freedom is lost for every
(p in
this case) that must be calculated frorn the clata, Another
of freedom is lost
for the fixeclnurnbcr of
once all but one of the classes haw been
determined, the last class has no
set

ln the

table Lmder the column lor one

ya]uc of 1
indicates a P value less than O,OL Thus the
the differences between the observed ancl
ucs
clue to chance is very low That

of

nnmhers of genotypes do not fit the

under
law.

numbers

An
law is
the calculaticin of allelic
alleles is recessive. For
albinism in humans results from an autosomal recessive
this trait is rare, but among the
Indians of
albinism is
common.
Charles M. Woolf and Frank C
visited the
1969 and observed 26 cases of albinism in a
of about 6,000
. This
than the
of albinism in
most
we have calculated the frequency of the
we cannot
determine the frequency of the gene for albinism because we cannot
between
individuals and those
for the normal allele. Recall that our cominvolves
the
number of alleles:

has

<:~lhinism,

expect
because strong social factors are at
individuals. If the conditions of the
curate.
these

for a recessive trait such as

N everthethis is

22.5
Hopi

average, carries an allele for albinism.

We should not
that this method of
allelic
of the

to discern the causes of deviations of observed

from
we will look at
the

2N

But because
albinism cannot be

equilibrium. At equilibrium, the

gous recessive genotype is q2 For albinism among
q2
and q can be obtained
root of the
of the affected
and p l

about 1900. The middle child

an autosomal recessive disorder that occurs wilh
among the Hopi Indians of Arizona.

Hardy-Weinberg principle applies to alleles defined

in a number of ways, including single nucleotide polymorphisms (SNPs), protein variants, or any other factor
that segregates like a Mendelian gene.

The genetic structure of populations can vary in space

and time. This means that the
and distribution of alleles can vary in
in
different areas or samples from the same area collected at
different times.
22.6 shows how the
of
three alleles at the locus for the enzyme leucine
in a
series
of blue mussels that inhabit the east coast of
of
and animals
distributions show clifthat have
fercnccs of this sort in the allele
of their component
variation
shows clear patterns or trends across space. \Vhen allele
in a
way across a geotranscct, we call this an allele rnrm,errv dine.

of the
, and
of the
for the enzyme leucine amino "~''"'"'''- (L~P) in the blue musseL

Often
associated with
attribute in the environment, such as
In the case of
Such clines suggest the
pattern is caused
differential selection for the alternate
and much additional work
maintained
structure of a

7.
Because of the
allele

variation in

many statistical tools for

the
of
variation. The
of total
variance into
parts. At the
can think of a fraction of
the
variance that exists within each local
tion and another fraction of the
variance that
this kind oC measure, for
about l 5 percent of the
humans is found between different

Lions.

find that

Jre close

to

prairie
each other and near

Lawrence, Kansas.
1.0

0.9

0.8

>(.)

0.7

Q)

::0

g;v

0.6

Q)

cQ)
CJ)

LL.

0.5

'1
't)

0.4

0.3

0.2

0.1
N

1970

1971

shared across
variation may also be of immense
vation. ln terms of the future evolution of a
resources of a
conservation of the
tion has to be
to the fact that there is a
ponent to

J
1972

of

of the

1973

processes because some processes increase

variation while others decrease it. The manner in which
new
arise may
variation harbored within populations. In
of a population to
over time can be influenced
how much
variation it has to draw on
should environments
For all these reasons, population
are interested in
variation,
to understand the
processes that affect
and
the effects of
human environmental disturbance that may alter it.

For many years,

were constrained
how much variation existed within natthat
and
variation exists
Genetic variation within popfor several reasons. First, it deterfor
and
clues about the relative

basis of most traits is too

to
genotypes to inchvicluals. A few traits
and alleles that behaved in a Mendelian
spot pan ems in butterflies and shell color in
provided observable
variation, but these isolated
estimate of

variation exists in most natural

as apparent
patterns of the Cuban tree snail, a species treasured for its

evidence was used

of chromosomes and their bandin the
of fruit flies.
published a
to the
of

many loci. This

was soon used to examine
variation in hundreds of
the way for modern
about the forces

varies
mation of the
rated based
alleles of

loci that arc hetercJz, 'f,OUS.

of green
from
for esterase and found
was 0.09.
for this locus would be 0.09. We would average this
with those for other loci and obtain an estifor the
Note that promisses much of the variation that is
tein
detected when the DNA sequence of the same gene is
determined because silent or synonymous nudcoticles
may vary at the DNA level but leave no trace of variation
at the
level. This means that estimates of
and
of
underestimates of the amount of total
Table

variation
from the work of
cists, which stated that most natural
tle
variation. 1f the classical model is wrong, then
what maintains so much
variation within
tions? Tn the late 1960s and
1970s, observations of

showed that
amino acid sequences from many
there was considerable variation in amino acid sequence.
Motoo Kimura
that much of the
lutionary
a
combination of random mutations and random chance
fixation of alleles. This model was also
of variation within populations, and
dictions from the model seemed to
called the neutral
the presence of exten~
sive
but proposes that this
variation is neutral with
to natural selection. This
does not mean that the
detected
elec~
have no function hut rather that the different
genotypes are
ural selection does not act on the neutral
clom processes such as mutation and
the patterns of
variation that we see in natural
The neutral mutation model proposes that
and natural selection
variation at some loci affects
eliminates variation at these loci. The neutral mutation
model had strong support that was
eroded
after full DNA sequences of alleles were available and
more complicated models were found to
better
of the data.

Genic Variation in Some Major Groups of Animals and in Plants

Mean
Number
of I~od

Others

Marine invertebrates
~---~~~-~----

-~

28

24

0.529 O.OJoa

0.150 0.010

28

0.531

OJ. 51

15

0.243 0.039

26

0.587 0.084

0.062 0.007
0.147 0.019

~----~---~------------ --~---~----~~-------~~-~

Snails
Land
Marine
Fish

Rndcnts
Plants'

18

0.437
0.175

0.150
0.083

21

0.306 0.047
0.336 0.034
0.231 0.032

0.078 0.012
0.082 0.008
0.047 0.008

19

O.H5

26

26

40
8

0.202 0.015
0.213

0.042
0.054 0.005
0.037
0.170 0.031

17

14
l.l

21
22

9
4

0464 0.064

stzmdarcl error.

macaque, and southern

seaL
mean iJacne
is 0.233 0.029

one often encounters competing

models that seek to explain the amount of variation in
natural
In the 1920s and 1
the classimodel
that there was an archetypical"wild
and that most alleles were of this sort, with a few
mutant variants in the population. In the 1960s and
1
protein electrophoresis revealed abundant
variation in natural populations, thus disproving
the classical model. The neutral mutation model proposes that the
variation detected by elecis neutral with regard to natural selection.

You use protein electrophoresis to measure

variation in mussel populations in
the iActivity, Measuring Genetic Variation,
on your CD-ROM.

restriction enzymes. You will recall

enzymes make double-stranded cuts in
7, pp. 165Most restricbase sequences
a sequence of four or six
For
the restriction
-GGATC
enzyme BamHI
c
and whenever this sequence appears in
the DNA. The
agarose

on an agarose
This variation is called restriction

and

Individual 2

Individual 1

Smaller fragments
Individual
'I

Individual
2

the DNA or

for

sequences

that two individuals differ in one or more

nucleotides at
DNA sequence and that the
differences

on a
patterns of
as shown in
ferent patterns on the
are called restriction
or RFLPs
; see
indicate that the DNA sequences of
individuals differ. RFLPs are inherited in the
same way that alleles
the RFLPs do not
any outward

their
are the
on
a
when the DNA is cut
the restriction enzyme.
RFLPs can be used to
information about how
DNA sequences differ among individuals. Such differ~
ences involve
a small
of the
the few nucleoticles
the restriction enzyme.
if we assume that restriction sites occur ranin the
which is not an unreasonable assumption because the sites are not
as traits, the
presence or absence of restriction sites can be used to
estimate the overall differences in sequence.
To illustrate the use of RFLPs for
suppose we isolate DNA from five wild mice and
a
DNA
PCR
oligonucleotide primers
of the
we cut the
with the restriction enzyme BamHl and separate the
ments
agarose
A
set of

Restriction patterns
of the three shown). Each mouse has two
carries the restriction site.
may he+/+ (has the restriction site on both chromosomes), +/-- (has the restriction site on one chromosome), or
restriction
on neither chromosome). 'vVhen the restriction site present, the DNA is broken into two
after
the restriction enzyme and separation with

with

that
be obtained is shown in
a mouse could be +/+
on both

4 have the restriction

at the nucleotide level
can be estimated from restriction site
Nucleotide
number of different

of nucleotide
human genome average around 0.0008.
an individual
nucleoticles on the two
at
about one in every 50 to l ,000 nucleotides.
One
of using RFLPs for
that this method reveals variation at
the nucleotides that make up a
a small
the restriction

a method for
all nucleotide differences that exist in a set of
DNi\ molecules.
We saw earlier that
differences that do not
or conformation. The best method for
variation is to obtain the DNA
the gene from each individuaL In the first
this
Martin Kreitman
from different fruit
of the alcogene in
he found different nucleoticles at 43
segment. Furtherwere identical at all
there were 8 eli fferent alleles
of this gene.

misses

This

harbor

estimates for different parts of

Adh gene. As is observed within most
tiona! genes, the
occurs at sites that do
not
the amino acid sequence of the
protein, and these are known as synonymous
The
level of synonymous nucleotide
is
the observed
at nucleoticles that

nonsynonymous
nucleotide
in a gene are
so 3/4 of all random mutations
be nonsynonymous, but in fact the variation one
much more
to he synonymous. For
tin Kreitman's
there were 13 synonymous
varied. If nonsynonymous mutations were
to
be seen, then we
to see 3 times this number of nonsynonymous
or 39
K.reitman found
Most nonsynonyrnous
mutations are visible to natural selection and have been
eliminated fi~om the population,
the
observed excess of synonymous

DNA
and Microsatellites. fn aclclition
to evolution of nucleotide sequences
nucleotide
variation
occurs in the nmTJ IJer of
nucleotides found within a gene. These variations are
called DNA
and
ari.se
deletions and insertions of short stretches of
DNA
nucleoticles. For
have been observed in the alcohol
fn addition to extensive variation in nucleotide sequence, Kreitman found
insertions and deletions in the 1 J
of the gene he

Number of

Nucleotides and

Estimates of Nucleotide Hei:ero,zve'ositv

for DNA Sequences
5' + 3' flank
Growth hormone gene
Alcohol
lv!itochonclrial DNi\
1 f4 gene rcglon

gene

Humans

0.002

l'ntit fly

0.006

!Iumans

0.004

urchin

0.019

33'5

U.U02

lJ
l

192
'576
789
76"7

o.n1

Exons

fntrons
Y nontranscribccl

18

U.OOl
Oi 1tH
l)!i())

I
rxamined. 1\ll of thesr were confined to introns and
of the
none was found within
exons. Insertions and deletions within exons
alter
the
so
are selected
As a
insertions and deletions arc most common in au"' v'"''"
of the DNA.
some insertions and deletions have been found in the
of certain
genes. Another class of DNA
involves variation in the number of
gene. For
her of

A
is seen in mkrosatellites
short tandem repeats or
these were
described in
8, p.
. More than 8,000 STRs
in the human genome, and their use
in humans and mice has been critical
of many genes associated with
disorders. In conservation
one often is faced
with a need to obtain information on
variation
for which there is almost no
know]gene sequences, and in
microsatellites are almost
used to
patterns of

We have looked at the many ways in which

ation can he
in natural
corne to the conclusion that
mous amounts of variation. Now it is time to return to
the
of what maintains this variation. If the popand free from mutaancl natural selection, then whatever
variation 1here
will

r-

le

and mutation,
natural
be
selection may occur. ln these circumstances, allelic f'redo
and the gene
of the
evolves in response to the
of these processes. Tn
the
sections we discuss the role of four evoluclri ft,
and natural selection--in
the allele
of
. INc also discuss the effects of nonrandom

One process that can alter the

of alleles
within a
is mutation. As we discussed
19, gene mutations consist of heritable
in the DNA that occur within a locus.
a mutation
converts one allelic form oF a gene to another. The rate
which mutations arise
is low hut varies between
loci and between
Certain genes
overall mutation rates, and many environmental
such as
and infectious
agents, may increase the number of mutations.
mutation is the source of all new
variation; new combinations of alleles may arise
but new alleles occur
as a result of
mutation.
mutation
ial on which evolution acts. Some mutations are
neutral and have no effect on the
fitness of
mutations arc detrimental and are
However, few mutations
individuals that possess
Whether a muta-

harmful or neutral mutations may become beneficial. For

after the
use of the insecthat conferred
ticicle DDT, insects with
and
many insect
evolved resistance to
DDT. Mutations are of fundamental
to the
process of evolution because
variation on which other
processes act.
In
rates of mutation arc so low that once a
mutant allele enters a
the fate of the mutation
is determined almost
nonmutational forces. To
see
this is so, we can consider a model in mutation
the
force. The mutation of i\ to a
mutation. For most genes, mutations also
occur in the reverse
C1 may mutate to
These
mutations are called reverse mutali011s, and
occur at a lower rate than forward mutations. The forward
mutation ratc~thc rate at which A mutates to C/
(A --1
with u. The reverse mutation
rate--the rate at vvhicb a mutates to 1\
bolizecl with v. Consider a
which the
of A is p and the
\Ve assume that the population
lion occurs on the alleles. ln each
a
u of all A alleles mutates to a. The actual number

Mutation per
100,000 Gametesb

Trait
(virus)

coli K12

Salmonella

(bacterium)

males

Corn

~---~-:._

To rapid

To new host range

0.001

To streptomycin resistance

0.00004
0.003
0.00007
0.0004
0.006
0.2
0.41
0.2
0.005
0.01

To phage Tl resistance
To leucine independence
To arginine independence
To tryptophan independence
To arabinose dependence
To threonine resistance
To histidine dependence
To tryptophan independ.:;nce
To penicillin resistance
To adenine independence
To inositol independence
(One inos allele, JH5202)
to yellow
bw+ to brown
e' to ebony
to
Wx to waxy
Sh to shrunken
C to colorless
Su to sugary
Pr to purple
I to i

R' tor'
Mouse

Chinese hamster somatic cell tissue culture

Humans

a+ to

0.0008-0 0.29
0.001-0 010
1.5
12
3
2
6
0.00
0.12
0.23
0.24
1.10
10.60
49.20
2.97

b 1. to brown
c+ to albino
cl+ to dilute
!n+ to leaden
Reverse mutations for above genes
To
resistance
To glutamine
Achondroplasia
Aniridia
Dystrophia myotonica

0.39
1.02

disease

0.5

Intestinal
Neurofibromatosis

Retinoblastoma
"Mutations to independence for nutritional substances are from the omummn
frequency estim~Hcs of viruses, bacteria, Nettrospora, and Chinese

1.25

0.80
0.27
0.001
O.ol4
0.6-1.3
0.3-0.'5
0.8-1.1
0.4-1
1.3

5-10
0.7--LJ
l. 7-2. T

0.5-1.2
comlition (e.g..
).
or cell counts rather than

by permission of Prentice Hall, Inc.; Upper Sa delle

of A alleles. For
consists
alleof every 10,000 A alleles
' one
mutates to a. When p
all 100,000 alleles in the
are A and free to mutate to a, so
10 A alleles should mutate to a. How10,000 alleles are A and free to
with a mutation rate of w-4
1
mutation. The decrease in the
from mutation of A -7 a is
to up; the increase in
from A +-- a is
to vq. As a result of mutation, the amount
which
i\ decreases in one
is
to the increase in A
alleles caused
reverse mutations minus the decrease in
A alleles caused
forward mutations. Since we have a forof a and a
the
of a, it is
number of alleles
to the num-

forward mutation is
ber of alleles
no further
occurs,
that forward and reverse mutations continue to take
theu

q=

H +V

When we study what happens when we violate the

assumption of the Hardy-Weinberg equilibrium of the
absence of mutation, we see that mutation is the
way in which novel genetic material can come to exist
within a species. The larger a population, the more
potential there is for a novel mutation to arise.

are not infinite in size, but

that chance factors have small effects on allelic
this case chance factors may
allelic
Random
due to chance is called random "-'V"'-'LA''Ronald Fisher and Sewall
la and 22.1b), brilliant
laid much of the theoretical foundation of the
the
of
drift

value for p is

and the

Ll

v
+v

this process of pure mutation

In a
with the ini0.9 and q 0.1 and mutation
2 X
, we can calculate the
in the first

tial allelic

vq

t!p

(2 X

0.1)

(5

-0.000043
of A decreases
1 percent. Because mutation rates are so
in allelic
clue to mutation pressure is
slow.
the
from 0.50 to
it from O.J to

in human
is
interaction of mutation pressure and natural selection.

Other processes have more

and mutation alone
of a
For
an autosomal dominant trait in humans that

consequences for the conservation of a rare or

To sec how chance can
role
structure of a
group of humans
that this
consists of
5 of whom have green eyes and 5 of whom
have brown eyes. For this
assume that eye
color determined
locus
a number
of genes control eye
and that the allele for green
eyes is recessive to brown
Bb codes for brown
eyes and b/J codes for
of the allele
for green eyes is 0.6 in the island
A
strikes tht.c
.50 percent of the
five of the inhabitants
in the storm. The five individuals who die all have brown eyes.
affects the
of
those with green eyes survive is
chance. After the
the allelic
of the green eye allele has
as a result of chance.
the same scenario, but this time with a
l ,000 individuals. As
50 percent of
has green eyes ancl 50 percent has brown
strikes the island and kills l1alf the

drift. In

not present in
is

when males
the effective

the number of

the gametes unite to

of the genotypes will
and , and the
of the allewill remain p and q. If the number of
the gametes that unite to
from the infinite

not
son is that

females and

as a group, contribute half or an genes

and
a group, contribute
of 70 females

and

the genes
contributes 1/2 x 1!Tu
number of
cl c~mv>r
alleles
present in the next
. the effective
2) ==

chance we obtain heads and l

or even
all tails. When the
this case the number of
the
error.
Mathematicians have worked out the exact
of
for
499 heads and 50 l
called binomial distribution
our purposes the
with
p of
alleles for the next
of that next

than in one with

breed
divided between males and females.
Other
differential
Lions, can further reduce the effective
of these f~Ktors result in an effcctin:
the count of individual adults in the
the dfcctivc
our
variance of llclc !
variance which:::
1

of as the amount of variaLion in

from

and p and q

the next generaindividuals. The

in these 107
is

of allelic
""''"~''"''"" me.lanogtlsil:r: Shown
quency of the /Jw 75 allele among the
in 19 consecutive
generations. Each
con.si.stccl of 16 individuals.

calculate the 95
which incH-

Generation:

are
that

in some
to
confidence limits tell us that in the next generation, 95 of the
100
should have p
the range of 0.72 to 0.88.
if
observe
a
in p greater than
say from 0.8 to
know that the
that this
will occur
drift
less than 0.05.
would con-

s-IL_.. .~-..aa.L.~~---~~

. .~~-~mhm-MLdL~~

9~~--~~~

10~. .~~~~dR~. .MB-JL-~----R

1i

tributed to

P. Buri
0

examined the
ill?

and the initial

0.5
Frequency of

i.O
allele

of the

founder effect because the

few individuals that survive the
Two

of

Consider the inhabitants of

the inhabitants to leave the island. At this time many

islanders
to America and South
the
103 individuals at
of l
to 33 in 1857. A second bottleneck
1885.
November
the adult males on the island put out in a
small boat to make contact with a
full

years, and the

Both bottlenecks had a
the
were
these events.
Tristan cla Cunha has been influenced
the form of founder
small
bottleneck effect
drift occurred in the evolu
First, founder effect took
the

vania. Between
from

and settled

the Dunkers have remained an

ou tsicle of the sect, and
their communities has
studied one of the

the red
line. These results were obtained
1.0

0.8

United
also different
German
which the Dunkers descended. Table 22.7 presents
of the allelic
the ABO blood group
locus.
among the Dunkers

0.6

q
0.4

0.2

Generation

continued to influence allelic

1729

the ABO Blood

Dunker

System

Three Human

() 38

0.03

0.59

0.593

0.036

() 023

0 ..348

0.26

0.04

0.70

0.431

0.058

0.021

OA90

007

0.64

0.455

0.095

O.CHl

0410

if the initial allele

among
observed in studies of
Selander, for

L~--L~-~--L--L-~--~-~L-~~---~~---~

0
Initial allele frequency (p 0 )

however,
chance
the new mutation will drift to fixation and
a
the gene will have evolved. Given that mutation
event, a gene will accumulate differences over
chance alone. In this way the genes of two related
such as humans and other
be
and used to estimate the
shared a common ancestor. In this way it
humans and
last shared a common
6 million years ago.
is also
debate and

in
in the same direction.
in their allelic
illustrated in

as a

29
50)

13

Est-Jh

11b!J 8

0.418

0.8-'19

0.372

0 84)

Size

0.051

0.1

0.013

o oog

0.9
0.8
0.7
0.6
0.5

OA
We
to introduce new
effect of random
to remove that
from the
if we combine these two
'Will there be a balance achieved such

0.3
0.2
0.1
0
0

models have been devoted to this

and one of the best known is the
many alleles
alleles model.
each mutation that occurs in
gcnc
a novel allele that has never been

reasonable. The
the
situation, the
forces of mutation and drift balance each
and
up with a curious kind of
state in which new
but alleles are also
In this

the evolution of allelic

would rcrnain

of mutation and
a range of values of

and mutation rates

with this rnodd

ested in the movement of genes, which may or may not

move. Movcrncnt of genes takes
or gametes
contribute tbcir genes to the gene
of the
This process is also called
Gene flow has two
dfects
introduces new alleles to the population
rare event, a
fie mutant
and not in another
alleles to other
Yariation for the
when the allelic

of

Migrants from

"'rx

IIIPx

p'v

their allelic ''"""''''"'.,

of the gene
and Pv become
in allelic
allelic
true
when other factors besides
influence allelic
A.n additional

found
in allelic

obtain

between two
vent the two
alleles.
The effrcls
tions not

in allelic

portion

or the

fcrcnce in allelic
and residents
I\
allelic lrcquencv

nccted to

(1

migrate north
spring and summer to
northern Canada.
gene flow occurs
with the result that monarch

processes alter the gene

influence the evolution of a
drift do
and

that enable a
that allow

tation
Genetic
mutation, and
tion all inf1uence the pattern and process of
arises
from natural selection.
selection is the dominant force in the evolution
traits and has
much of
variation

selection prcHluces or~:anisn1s

environment, such as this lizard
aUows it to blend in with its

A
o[
natural
is the evolution of
forms of moths in association with indus~
as industrial

form of the
this back"
areas,
extensive
with the industrial revolu~
tion in the mid-nineteenth century had killed most of the
lichens
the tree trunks with black sooL
the

nation;
the carbonc1ria
qucncy in industrial
ln rural
was
the wrbonaria
and
form
the
of the

Kettlewell demonstrated that selection affected the

Darwin described

on the average four

the most fit genotype,

fitness values.

Fitness Values ami Selection Coefficients of

Gdult
(relative number of
Selection coefficient (s

...

ilil

n w mm

?JtWEPEf

we wa a

Genotypes

16

lO

128

40

128/16
8/8

=c

"f0/l0 = 4

4/8

tm

20
40

Method

+ l/2(H')
p'

caused by selection
fi mess in this example is considered to be the
in the number of
by

for genotypes
be
fitness to the
because we
of those off-

in allelic
ural selection can be calculated
Table
10. This
of

method
overclominant. To
the genotypes
If random

associated
at a
that
on average
have effects on different
that affect fitness. Such
in the overall

W. Jn our
arc s = 0; for G 1 G 2 ,

and
selection
and
some of the genotypes survive.
The contribution of each genotype to the
to the initial
of the genotype multiits fltness. For NA 1 this p2 x W 11 . Notice that
the contributions of
three genotypes do not add up
to . We calculate the relative contributions of each genotype
each
the mean
the
The mean
of ihc
This
of the genotypes after selection.
culate the new allelic
(p') frorn the

Natural selection
At times. natural
selection eli

on the

these
relative fitness ol the
of the alleles

Cltncss to 10, we get a

each with its own effects

among fitness values lor the

genotypes. These include the 1-ollowing:

selection
after selection

W'
P'
after selection p'

p'

c(

= P' +

0/0.35

0.16/0.35
0.46

1/2(H')

0 + l/2(0.54)
0.27
1 p' ~ 1 0.27
0.73
p'
p
0.27
0.6

how several

a fitness of l, whereas the recessive

reduced
as shown here.

AA

l1a

aa

l~

1f the genotypes are

tions, the contribution of
cration the

in
genotype to the
the fitness.

AA.

Aa
x (1

aa
once stable
h;1s been reached. Case 6 results
in what looks llkc a dircctimml
the ,,l!cle that selected
on the initial

tncss
Since

of

s)

q i.

the

population
Cf'
1.
mean

AA
0.9

Aa

0.8
0.7

aa

0.6

0.5

OA
0.3
0.2
0.1

the

of a after one
Generation

value of C[
with selection.
Selection also
on the actual
of
the allele
because the relative
ions of Ao and ao individuals at various
selection can

as
have gone
discussion
effects of selection on a recessive trait to illustrate
formula for
in allelic
be
our
table n1cthod of allelic
selection. Similar derivations can be carried out
clomiancl codominant traits

not

those derivations here, but the

under chfTable
allelic

does not
in
variation.
the maintenance of
variation and
the backbone of the balanced model of

Hb-A/Hh-A genotype have

Formulas for Calculating Change in Allelic Frequency After One Generation of Selection

1 - s

1
1
(l

Selection wilh no dominance

Selection that favors the
(overclominance)

1 -- s

the
General

10.

s/2)

and

FJ!J,A!Hb~S

individuals have siekle~cell

individuals have sickle~cell
environment in
at a

results in the maintenance of

variation in the population.

Distribution of
malaria caused I:Jy

l'/asmodium j;<[c:ipnrunt

Distribution frequencies
of !Jl,S allele, percent

tion rate is l0- 6 and s

of the gene will be q
deleterious traits remain within

of
selection.
a dominant allele

the

u!s

dominant alleles
ones.

0, and the

mutation of
between selection and mutation
decrease in allelic
increase

oeeurs when
individuals mate more
than
If humans exhibited

of
may influence the
notypes for which
cleterrnined.

11

q-'

u!s

1{

lethal (s

If the
becomes

the
In very
imlividuab tossecl a coin
used

Cf

lA

cxan1

of the balance
rrmUHion ancl
gene for which the muta-

imL consider a

at low

0
l

l/4
l/4

7/16

1/S

3/S

1/16

7/16

J/32

15/32

l/16

7/16

+ l/32

l/32

15/32

1/4

4
11

+ 1/8

l/8
1116

3/8

3/8

+ 1/64 31/M
11 - (1/2)"]/2
U2

(112)"

relatives
mates. lnbreeclof the coefficient of
the

1/4

3/8
7/16
15/32

l/64

31/M

[1

1/2

the
but after further rounds the prothan that

at the expense of
of alleles A and a
of the three

means that in each

of hetand
!y between the two
the

In
ways.
effects of
processes and their
the pattern of
variation observed
over time.

tion is greater than it

estimated
there are
and
described. As

variation; i I one
decrease in
quency and can be eliminated from the
selection.
natural selection can increase
variation within

other forms of

crvndomi~

tions and of the amount. of

essential information for
there
information in conservation
argue that the central
is loss of
the
of habitat destruction can he

ogy ami
better understand the best course of action for
the

of life in our ecosystems.

zygotes:

or the
fails to grow.
isolation is
is a snowball effect in which the

of the argument that younger

on
isolation, these

the F 1 females are viable and

One can backcross

of

genotypes.
contribution of genotypes is
The effects of
of

unaffected. One
leads to an
New

of

variation should exist within natural popu~

lations and what processes
for the
tion observed.

variation is maincombination of forces and that

be heavily influenced
fixation of

between

genes appears to fit

the variation
maintained
clri ft and mutation.

tion7
the genotypes in

stantiated. In this
rium vvas inaccurate.
not
removed from

(2

slate.

X It

because both alle-

11

It

cumsrances?

we discussed

derivation ro this

mutation rate, or u
value of q vvill be q
tion becomes q lOv/llv, so q = 10/l ,
about

one
value in the chj,.
<l P value of

Pink
Yellow
Total

2)6
I

500

, calculate the

malate
Choancl each
determined wilh
of

individuals mate at random.

20
76
to Problem 22.8.
the 5 locus.
allele 5"
alleles and

type

what percentage of the

of
in

following

of range cattle
49 percent red
white (rr)
\Vhat percentage of the gametes that
of cattle in this

roan

data

Females

99%

1.%

Males

90%

10%

The difference
known to be inherited.
with the
X-linkccP

rise to tl1e
will con

color blind.
to show the trait if
either
of r

blind

of the men

of a

rancolor
of women would be

to be

of women would

to be

later!

A and a, can

of a
u

structure?
for
adult
females.

AA.
l

0.04

() 32

0.64

0.

0.87
0.10

0.01
0.45

0.45

females.
of 40 adult males and 40 adult
of allele A is 0.6 and the trp,nHn
confidence limits of the

of A if the

ncmoralis is native to
North America

genotype distribution when

genotype
not selected
What will be the allelic
lion in
altered environment/
\Yhat will he the allelic
tions'
Human individuals
autosomal gene die before
this removal of all affected
indication that

To what

one genera
of
of

II
III

0.42
0.45

0.09
0.05

be

Hb-A!Hb-A

0.88

alleles?

.00

of the

in
The mutation

the

or

\Vhat factors inllucnce the spontaneous mutation

trait'
the L ~ 1
of the

and

AlB4
192

0.128

A200

0.086
0.036
0.016

0.007

A18B

0.006

AlSO
Al90

0.089

0.013
0.007

X129

a mother bear and

cubs

XJ33,

CI05, C.l05

L159, U61

drift?

cannot locate two animals.