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Sympatric Speciation
Author(s): J. Maynard Smith
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Source: The American Naturalist, Vol. 100, No. 916 (Nov. - Dec., 1966), pp. 637-650
Published by: The University of Chicago Press for The American Society of Naturalists
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Vol. 100, No. 916
The American Naturalist
November-December, 1966
SYMPATRIC SPECIATION
J. MAYNARDSMITH
Department of Biology, The University of Sussex, Falmer, Brighton, Sussex
"One would think that it should no longer be necessary to devote much time to
this topic, but past experience permits one to predict that the issue will be
raised again at regular intervals." Mayr (1963)
I. INTRODUCTION
The problemdiscussed in this paper is whetherspeciation can occur in a
sexually reproducingspecies withouteffectivegeographicalisolation. The
is an old one. It is still alive because it cannoteasily be settled
argument
by observation;the present distributionof species is equally consistent
either with the sympatricor the allopatric theory. The crucial argument
against sympatricspeciation, admirablysummarisedby Mayr(1963), is that
no mechanismconsistentwiththe knownfacts of genetics can be suggested.
I have been led to question this argumentmainlyby the experimentalresults of Thoday and his colleagues (Thoday and Boam, 1959; Millicentand
Thoday, 1960; Thodayand Gibson, 1962). Although.Iam unable to account
forthe rapiditywithwhich Thoday and Gibson were able to establish reproductiveisolation betweentwo populationsof Drosophila melanogaster,
this series of experimentshas shownthat disruptiveselection (i.e., selection favoringextremeat the expense of average phenotypes)can producea
stable polymorphism.
At firstsight this is a puzzling finding. If alleles A and a have additive
effectson the phenotype,disruptiveselection would make AA and aa fitter
than Aa. This is the exact opposite of the situation requiredforstable
polymorphism
throughheterosis, and would lead to a populationconsisting
wholly of AA or wholly of aa individuals. The explanationlies in the
mechanismregulatingthe populationsize. If the populationformsa single
entitywhose size is regulatedto some numberN, regardless of the genotypes of its members,the conclusionthat disruptiveselection cannotmaintain polymorphism
is correct. But if the populationinhabits two subenvironmentsor "niches," the populationsize being separatelyregulatedto
numbersN1and N2in the twoniches, and if AA is fitterin one niche and aa
in the other,thena stable polymorphism
is possible, even if there is randommatingbetweenindividualsraised in the two niches. The firstpartof
this paper is concernedto establish this pointand to determinethe conditions whichmustbe satisfied. This partof the paper confirmsconclusions
reached earlier by Levene (1953), and analyzes the effectsof "habitat selection." The conditionof separate density-dependent
regulationin two
niches was in effect satisfied in Thoday's experiments,since constant
numbersof "high" and "low" parentswere selected in each generation.
637
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THE AMERICANNATURALIST
638
Polymorphismhowever is not speciation. The second part of this paper
considers whether reproductive isolation would be likely to evolve between
the two morphs. The answer to this question depends on how genes causing
reproductive isolation are supposed to act. Four possible mechanisms are
distinguished. It is concluded that a stable polymorphismcould well provide the starting point of a process of speciation.
The possibility that a stable polymorphismmightarise in an environment
which is uniformin space, but which varies fromgeneration to generation
in such a way that the relative fitnesses of differentgenotypes changes,
has been considered by Haldane and Jayakar (1963) and by Basykin (1965).
The latter author considers the conditions which must be satisfied if such a
polymorphismin a temporallyvarying-environmentis to give rise to speciation. However, this mechanism of sympatric speciation seems less likely
to occur than that considered in the present paper.
II.
STABLE POLYMORPHISMIN A HETEROGENEOUS ENVIRONMENT
The first point to be investigated is whether a stable polymorphismis
possible in. a heterogeneous environment. The assumptions which will be
made are as follows:
1) The environmentis divided into two "niches," 1 and 2, in such a way
that the density'dependent factors regulating'the population size operate independently in the two niches. The niches can be thought of as different
food plants in the case of phytophagous insects, as differenthost species
in the case of parasites, as shore and common or as lake and river in the
case of bird species, and so on. The assumption about density-dependence
implies that niche 1 will support a population of n1 adults, and niche 2 of
n2 adults. In much of what follows, it will be assumed that n1 = n2, but this
assumption is not required for the establishment of a stable polymorphism:
it has been made to simplifythe algebra.
2) Also for simplicity, generations are assumed to be separate.
3) The adults produced in the two niches forma single random-mating
population.
4) There may be a degree of "habitat selection" by females.
Allowance for habitat selection is made only in the simple case in which
n. = n2* It is then assumed that a female herself raised in niche 1 lays a
fraction 1 (1 + H) of her eggs in niche 1, and 4(1 - H) in niche 2, where
0 < H _1, the proportions being reversed in the case of females raised in
niche 2. Thus H= 0 implies no habitat selection and H = 1 complete habi-.
tat selection.
It should be emphasized that the choice by a female of a place to lay her
eggs depends not directly on her genotype but on her own upbringing. Evidence forthe occurrence of such a process is reviewed by Thorpe (1930).
Equilibrium with dominance, when n1= n2
A, a are two alleles, with fitnesses (measured as relative probability of
survival fromegg to adult) as follows:
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639
SYMPATRIC SPECIATION
Aa
1+ K
1
AA
1+ K
1
in niche 1
inniche 2
aa
1
1+k
Thus A is fullydominantin bothniches. The case of completedominance
has been chosen forfull investigationbecause thereis thenno dangerthat
any equilibria discovered will have arisen froma "concealed" overdominance; but similarresults can be reached if effectson fitnessare additive
in bothniches.
Let p1, p2 be the frequenciesof A in adults raised in niches 1 and 2, respectively,in generation0.
Then in niche 1, a fraction- (1 + H) of all eggs laid are laid by females
with gene frequenciespA: (1 -pl)a, and (1 -H) by females withgene
frequencies p2A:(1 - p2)a. All females mate at randomwith males with
gene frequencies (P1 + P2) A: 1 - I (P1 + P2) a.
Hence,
writing
(P + P2) =.SI2
(P1 - P2) = d, the zygotic frequencies
are:
AA = 2 ( + H) pS + 2(I - H) p2 S
= S(S + Hd)
Aa =2
+ H)Ip,(I
=
2S(1
=
(1
aa-
-S) + (1 -:p,)s S+
(1- H)tpj1--5)+(1-P2)S
- S) + Hd(1 - 25)
(1 + H)(1 - p1)(1 -5)
- S)(1 - S - Hd)
(I
+
-
H)(1
-
p2)( 1 -5)
Now at equilibrium, writingthe zygotic frequency of AA as [AA] and so on:
P1 = S + d =
_ 12[AA] + [Aa]1(1 + K)
12 [AA] + 2 [Aa]}(1 + K) + 2 [aa]
And substitutingand simplifying,this reduces to
S)
d2HK(1-S)+d~l+HKS(1-S)+KS(2-
I
2H(1+K)}-KS(1_S)2
=0
(1)
The equivalent equation forniche 2 is
d2Hkl-S
k~
f
S) + k.(l _ 5)2
-
}-kS
(I _: 5)2
=
2
d can be eliminated by multiplyingequation (1) by k and equation (2) by
K, and subtracting. The resultant equation can then be reduced to the form
k- K
452
_
85 + 2 + H(1-2)2
(3
2- H
Kk
If there is no habitat selection (H = 0), females laying eggs in the two
niches at random,this becomes
k-K
Kk
=252-45+1
(4)
And if there is complete habitat selection (H = 1), females always laying
eggs in the niche in which they themselves were raised, then
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THE AMERICAN NATURALIST
640
K =K8S2_12s+3
(5)
Kk
Equations (3), (4), and (5) give the mean frequency of the dominantallele
A in the adult population, S, in terms of the selective advantages k and K.
The stability of these equilibria can be deduced fromFig. 1, in which S
is plotted against (k - K)/Kk. Considering first the case in which H= 0,
3-
k-K
Kk
2H:1
0 0
:0
09
\
FIG. 1. Relation between
0
0.6
k-K
Kk
0.i
I
and S, the mean frequency
of allele A at equilibrium.
the slope of the graph is negative throughout. Suppose then that the values
of k and K are such as to maintain an equilibrium with S = S., and that the
actual gene frequency of A is S, + AS, where AS is positive. It follows
that (k - K)/Kk is too large, and hence that K is too small compared with k,
to maintain the gene frequency at this value. Now since 1 + K is the fitness of Aa and AA, and 1 + k of aa, in their respective niches, it follows
that if K is too small relative to k to maintain the frequency at SO + A Si
then the frequency will fall towards S,. In other words, the equilibrium is
stable provided that the slope in Fig. 1 is negative.
Thus when H- O if an equilibrium exists it is stable. For an equilibrium
to exist, it is sufficient that S should lie between 0 and 1, and hence that
>k
or
k(I -K)<K;
-: K
>
Kk
k(I +K)>K
If K is small, this imposes very narrow limits on k.
(6)
For example, if
K= 0.1, k must lie between 0.09 and 0.11, a condition most unlikely to be
satisfied.
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641
SYMPATRIC SPECIATION
If the selective advantages are large, the range of permissiblevalues is
muchwider. Thus the firstconditionis necessarily satisfied if K ) 1 and
k positive;thus if K = 1, a stable equilibriumexists if k > 0.5.
WhenH = 1 (completehabitatpreference),stable equilibriaexist over the
range S = 0,
k -.K
= 3 to S = 0.759
k -K
k
Kk
Kk
=
-
1.5. If
k- K
lies between-1
Kk
and - 1.5, a second, unstable equilibriumexists with S > 0.75. Thus the
conditionsfora stable equilibriumare:
k(I - 3K) < K;
k(I + 1.5 K)> K
(7)
WhenK is small, this again imposes narrowlimits on k. If K = 0.1, k
mustlie between0.087 and 0.143.
But if K ? 3 the firstconditionis necessarily satisfied if k is positive.
Thus if K = 3, a stable equilibriumexists if k > -2. The values of k and K
forwhichstable equilibriaexist are shownin Fig. 2.
1.6 -
1.6
H-O
1.2 -1.2
H=1
-
k
k
0.8 -
0.8STABLE
04
STABLE
-0.4
0.2
O.!
0.4
0. 8
0.2
0.4
K
0.6
0.8
K
FIG. 2. Values of the selective coefficients k and K for
which a stable equilibrium exists.
Equilibriumwithdominance,no
/ n2,
no habitatpreference
The equilibria foundin the last section do not depend on therebeing
equal numbersin the two niches. However,when n, / n2, allowance for
habitat selection leads to highlyintractablealgebra. But in orderto see
how the equilibrium conditions depend on the relative sizes of the two
niches, it will be sufficient to consider the case with no habitat preference
(H = 0).
Let p be the frequencyof allele A in the adult population. Then the relative frequencies of adults in the two niches in the next generation are:
Niche 1
AA
Aa
aal_44
Total
+
p2(1
2pq(1 + K)
_
q_
~~~~2
1 K(1-.q 2)
q
Niche 2
K)
p2
~
~
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2pq
2
q+k)
(1 +kA
1 ?kq2
642
THE AMERICAN NATURALIST
If the numbers of adults in the two niches are n1, n2, respectively, then
the frequency of allele A in the new adult population is
n
n, +n2
(p 2+ pq)(1
1 + K(1
+ K)
n2
(p2
n1 + n2
-q2)
+?pq)
1+ kq2
=
a
*
and this reduces to
q2
n2k(1+K)-nK
(nl + n2) Kk
(8)
An equilibrium exists provided that q lies between 0 and 1, which requires that
k {1 - K nlA < K ni
\
0,
n2 /
~~~~~~~~(9)
k(l + K)>K K,
n2
Whenn1= n2, this is equivalent to condition (6).
If the selective advantages are small, they must be nicely adjusted to the
relative sizes of the two niches if an equilibrium is to exist; and this is unn
likely to occur. But if K
> 1, the first condition will be satisfied, and
n2
an equilibrium will exist if k >
1 . Suppose, for example, a species
1 + K n2
were established in a "small" niche, 2, and that a large niche, 1, became
available, with n1/n2= 10. Then a dominant mutationadapting the species
to niche 1 would spread if K 0. 1, i.e., if it gave a 10%, selective advantage. But a dominantwith K = 0.1 would eliminate the recessive allele
* x 10; i.e., unless the recessive had a twofold
1.1
advantage in the original niche.
Conditions (9) are subsumed under the more general case considered by
Levene (1953), who gives the conditions fora stable equilibrium when there
are a numberof niches, and when the fitnesses of the three genotypes AA,
Aa and aa are differentfromone another and in differentniches. It is implicit in his conditions that, unless there is heterozygous advantage in individual niches, a stable equilibrium requires either that the selective advantages are large, or that they are nicely adjusted to the niche sizes.
completely unless k >
III. THE EVOLUTION OF REPRODUCTIVE ISOLATION
It is a characteristic of good species that they rarely interbreed even
when occupying the same area. Granted then that a stable polymorphism
can exist in a heterogeneous environment;can reproductive isolation evolve
between the two morphs?
There are fourways in which this mighthappen.
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643
SYMPATRIC SPECIATION
1. Habitat selection
If in a heterogeneousenvironment
matingtakes place withinthe "niche"perhaps because individualstend to returnto mate in the habitat in which
theywere raised (e.g., manybird species)-then the populationsfromtwo
niches, whethergeneticallydifferent
or not, will be largelyisolated. They
could, therefore,evolve into separate species exactly as in the case of
allopatricspeciation. This shouldperhapsbe regardedas a formofallopatric
speciation in whichisolation is behavioralratherthangeographic.
But even if, as mustusually be the case, the isolation betweenniches
was only partial, it would favorthe establishmentof a stable polymorphism
of the kinddiscussed in the last section; i.e., smallerselective coefficients
wouldbe requiredto maintainpolymorphism.
Suppose, however, that initially no isolation exists between the two
niches, the adults fromboth forminga single random-mating
population.
Then, once a stable polymorphism
has been established, therewill be selection in favorof habitatselection in bothsexes, forthe followingreason.
Individualswill tend to be adapted to the niche in whichtheywere raised,
will tendto
because theydid in fact survivein thatniche. Their offspring
resemblethem. Therefore,if theyhave a genotypecausing themto produce
in the same niche in whichtheywere themselvesraised, this will
offspring
increase theirfitness.
It follows that the establishmentof a stable polymorphism
may lead to
isolation by habitatselection.
2. Pleiotropism
The gene pair A, a adapting individuals to differentniches maythemselves cause assortative mating:i.e., A matingwith A and aa with aa.
This seems veryunlikely.
3. ModifierGenes
It is supposed that the original population,duringthe establishmentof
the A, a polymorphism,
had a genotype-say bb-such that matingwas
random. Matingisolation could arise by the replacementof b by B, so that
for individuals of genotypeB, there is assortative matingat the A locus.
The situationis set out in Table 1, in which+ indicates thatmatingoccurs,
TABLE
1
Mating relations between genotypes resulting fromthe modifiergene B.
+ indicates mating; - indicates no mating.
genotype
A bb
A bb
Genotype
bb
A B
aa B
+
+
+
-
aabb
+
+
_
+
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AB
+
+
+
aaB
+
+
+
THE AMERICAN NATURALIST
644
- that it does not. In matings between B and bb, it. has been assumed that
the occurrence of mating is determined by the female. The main difficulty
is to imagine how a gene B could influence mating in this way; in effect, B
is a gene which causes courting individuals to be influenced by the difference between A and a, which.bb individuals ignore.
If such genes exist, would they increase in frequency and so cause reproductive isolation?
Clearly B will increase in frequency only if individuals selecting mates with the same genotype as themselves at the A
locus have more surviving offspringthan non-selective individuals. This
will be the case if the heterozygote Aa has a lower fitness than AA or aa.
For the equilibria considered in the last section, in the absence of habitat
selection the three genotypes AA, Aa, and aa are equally fit; and therefore
there is no selective advantage in assortative mating. But in the presence
of habitat selection by females, the mean fitness of heterozygotes is less
than that of homozygotes. This may at first sight seem puzzling, since AA
and Aa were assumed to have identical phenotypes; the lower fitness of Aa
arises because heterozygotes more often find themselves in the "wrong"
niche. Therefore, if there is habitat selection, B will increase in frequency
and ultimately lead to reproductive isolation between the two niches.
4. Assortative mating genes
It is perhaps more plausible to consider an allele pair B, b which.themselves cause assortative mating, regardless of the genotype at the A locus.
The occurrence of mating is then as shown in Table 2.
TABLE 2
Mating relations when alleles B and b determine assortative
mating irrespective of the A, a locus
genotype
A
B or
a
A
B or
a
genotype
A
bb or
a
+
A
bb or
a
+
There are many ways in which genes affecting signals or behavior used
in courtship could have this effect. The problem is whether an allele pair
of this kind would become associated with the genes A, a responsible for
polymorphism,so as to give rise to two, isolated populations, one AA BB
and the other aa bb (by symmetry,theycould equally well be AA bb and aa BB).
In. the absence of habitat preference by females, I see no reason why such
an association should evolve because, as explained in the last section,
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SYMPATRIC SPECIATION
645
thereis no selective advantagein assortativemating. But if thereis habitat selection, an association would be expected to evolve because it would
lead to a rise in the mean fitnessof the population. I do not findthis argument fully convincing,and in any case it says nothingabout the rate at
whichan association would arise. Unfortunately
I have been unable to find
a general solutionforthe case in whichbothallele pairs are segregatingin
a population. Instead I have investigatednumericallya case whichI hope
is typical.
The firststep is to choose a numericallysimple equilibriumforalleles
A, a, as follows:
niche sizes equal, n, = n,
completehabitatpreference,H = 1
selective advantages, K = 5
k=
7'
5
12
It thenfollowsfromsection II thatat equilibriumthe genotypefrequencies
are as shown in Table 3. It is assumed that assortative matingforthe
allele pair B, b is complete,so that BB mates only withBB, and bb with
bb. HeterozygotesBb will be rareor absent.
TABLE 3
Equilibrium frequencies for a model in which H=
-, k=
1, K
Niche 1
eggs
AA
0.3
Aa
0.5
aa
0.2
-5 and n1 = n2.
Niche 2
adults
eggs
3.6S
3
0.2
adults
i1.6S
4
61
6
0.5
1.4
11
0.3
-
3
9
Considera populationin whichthe frequenciesof BB and bb are P and Q,
respectively, but with small departuresfromthese values for different
genotypesat the A locus, as shownin Table 4.
If' the values &3 to l6 correspondto generation0, we want to findthe
values 8'to &8'in generation1.
corresponding
In the adult male population,amongBB males the relativenumbersof AA,
Aa and aa are:
AA BB
50P +
99
AaBB ~98
-P+
AaBB
99
aa BB
50
99
11
6
11
-+&+
+1.4 'a
11
+ -64
16
9
4
9
-85
34
6
9
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THE AMERICAN NATURALIST
646
TABLE 4
Frequencies of genotypes in two niches expressed as frequencies
P and Q modified by small deviations 8.
Niche 1
Genotype
A bb
aa
l bb
Q - la4
P +&2
BB
a bb
8
+,P
Q - 8,
AA{B
Aa
Niche 2
P +,5
Q - as
Q _'a2
BB
P{+8,
P +6
Q- 83
Q- &
and hence among BB males, the frequency of allele A, is
{ BB)=
p(A
1-8
P-11
__(1
2
0.7
08
1_
11
9
9
A table can then be set up showing the numbers of different types of fe-
male, and the proportions of differentgenotypes among their offspring,part
of which is shown in Table 5.
TABLE 5
Correspondence between type of female, numberin niche, and proportionof different
kinds of offspring. Only a part of the complete set of relations is shown.
Type of female
Proportion of offspring
Number in Niche 1
p(P+ 61)
BB AA
BB Aa
6p (P+
11
i4
11
BB aa
p(A I BB)
62)
(P+
Aa
AA
2
p(a
p(A JBB)
o
BB)
2 p(aIBB)
2
0
3)
aa
p(AIBB)
p(aIBB)
Whence the numberof BB AA offspring-in niche 1 is:
3.6
(P + 31)p (A I BB) t
~~~~~3+
- -
2) p(A I BB)
(P
Substituting for p (A BB), and rememberingthat the total number of AA
offspringin niche 1 is 0.3, we have in niche 1 in generation 1:
numberof BB AA offspring
total numberof AA offspring
7.8
= +7a
8 + 5~
51
11 b 11
Similar equations
2 -
0.7
1
11
3
+0.83
+
9
4 -
1.7
9
9
6
=
1
can be obtained for 3K'to &6', of which the coefficients are:
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647
SYMPATRIC SPECIATION
31
('
(32
I3
0
0.1636
(34
+
a5
+ 0.0327
(6
-0.11636
3
(32
+ 0.4545
+ 0.5455
+0.6818
+ 0.7091
+ 0.2945
-0.1636
0
0
(5
(4.
- 0.0636
i 0.1400
+0.3818
+ 0.0889
-0.0178
-0.0889
- 0.0127
+ 0.0636
+ 0.1956
- 0.0889
- 0.0636
- 0.1889
+ 0.0378
+0.1889
+ 0.4444
+ 0.3704
+ 0.3400
+ 0.8185
+ 0.5556
+ 0.5333
86
0
0
0
- 0.1889
These equations are satisfied when all values of (3are zero; i.e., there is
an equilibrium when the frequency of allele B is the same for all genotypes
at the A locus. But this equilibrium is unstable, as can be shown by iteration, startingfroma small initial disturbance.
Taking, in generation 0, (3 = 0.01 and (2 to (6 as zero, Fig. 3 shows successive values of P1(B) and P2(B), the frequencies of allele B in niche 1
and niche 2, respectively.
P+
0.02-X
/ P(B)
'
P+OO01
10
P
P-0.01
S
~~~GENEKATfON
-
p-0.02_
t~~~~~~~~~~~~(B)
FIG. 3. Frequencies of allele B in niches 1 and 2,
aftera small disturbancefromthe initial value P.
Thus, if an initial disturbance raises the frequency of B in niche 1 above
that in niche 2, this difference is amplified in subsequent generations.
This holds whatever the initial value of P. Hence if allele B were initially
rare, but by chance were less rare in niche 1, its frequency would steadily
increase in that niche.
Therefore, increasingly individuals raised in niche 1 will tend to mate together, and similarly for those raised in niche 2. This will finally lead to
reproductive isolation between the two niches, and, since AA is fitter in
niche 1 and aa in niche 2, to the evolution of two isolated populations,
AA BB and aa bb.
Although this conclusion has been established only in a particular case,
there is no reason why it should not be generally true, provided that females
show some degree of habitat selection. But the conditions chosen-complete
habitat selection by females, an allele pair giving complete assortative
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648
THE AMERICAN NATURALIST
mating, and an allele pair with large selective differences in the two
niches-all
favor the rapid evolution of isolation. In practice, the establishment of mating isolation between two niches would be very slow, taking
hundreds rather than tens of generations.
The preceding discussion has some relevance to the origin of isolating
mechanisms in cases of allopatric speciation. If two populations, previously
isolated geographically and differingat many loci, come to occupy the same
area, there are three possible outcomes:
1) No interbreedingtakes place. This could be due either to habitat selection, or to the pleiotropic effects on mating of gene differences, usually
polygenic, which evolved in the first place as adaptations to differentgeographical conditions. In this case, either one population will become extinct, or, if sufficient ecological difference exists between them, both will
survive as distinct species in the area of overlap.
2) Mating takes place, but hybrids are inviable or sterile. This is the
classic situation in which, as Dobzhansky (1940) pointed out, we could expect to see the evolution of isolating mechanisms, in particular behavioral
ones, acting before gametes have been wasted in hybridization. Some experimental evidence (e.g., Koopman, 1950) exists that mating barriers will
evolve in these circumstances. But it is not clear whether such barriers
will usually be due to modifyinggenes, or to assortative matinggenes.
3) Mating takes place, and hybrids are at least partially viable and fertile. This is likely to lead to a rapid blurringof the genetic difference between the populations, even if the hybrids are initially of low fitness. For
example, if two populations of equal numbers mate at random, and if the
mean fitness of all hybrids (F1, F2, backcross etc.) is 0.25 that of pure-bred
individuals, then in five generations the frequency of hybrids will rise to
75 %, and in eight generations to 99.9 % of the whole population. Thus selection in favor of more viable and fertile hybridgenotypes is likely to have
a bigger effect than selection forreproductive isolation.
In practice, the situation will be more complex because the populations
will mix only in a zone of overlap into which .new pure-bredindividuals will
continually be migrating. Nevertheless, it seems likely that unless the
mean fitness of hybrids is very low, the outcome will be a single interbreeding population ratherthan reproductive isolation.
However, if the two populations differby at least one allele pair (or block
of closely linked genes) adapting them to differentniches, with selective
advantages large enough to satisfy equation 6 or 7, this would lead to a
stable polymorphismin the zone of overlap, and hence to speciation.
CONCLUSIONS
In a heterogeneous environment,it is possible for there to be a stable
polymorphismbetween alleles adapting individuals to differentecological
niches. The conditions which must be satisfied are however severe; they
are as follows:
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SYMPATRIC SPECIATION
649
factors regulatingthe population size must
1) The density-dependent
operate separately.in the two niches; this conditionwill be satisfied more
oftenthannot.
2) The selective advantages mustbe large. If thereis habitat-selection
by females, leading themto produce offspringin the niche in which-they
themselveswere raised, this will favorthe establishmentof a stable polymorphism;but even in this case, selective advantages of 307o or moreare
required.
can exist forallele
If these conditions are satisfied, a polymorphism
pairs showingdominantor additiveinheritance,even if.individualsraised in
population.
thetwo niches forma single random-mating
arises, this is* likely to be followed by the
If a stable polymorphism
evolution of reproductiveisolation between the populations in the two
an allele pair A, a,
niches. In particular,if a populationis polymorphic.for
an advantagein one ecological niche, and if a second allele
each conferring
pair B, b causes assortative mating,BB matingwith BB and bb with bb,
then,providedthatthereis some degree of habitatselection by egg-laying
females, two reproductivelyisolated populations, AA BB and aa bb (or
AA bb and aa BB) will evolve.
Thus the crucial step in sympatricspeciation is the establishmentof a
this paper is
in a heterogeneousenvironment.Whether
stable polymorphism
regardedas an argumentforor against sympatricspeciation will depend on
is thoughtto be, and this in turndepends
how likely such a polymorphism
on whethera single gene differencecan produce selective coefficients
large enoughto satisfythe necessary conditions(inequalities 6 and 7).
SUMMARY
It is shownthatin a heterogeneousenvironment
dividedintotwo"niches,"
a stable polymorphism
can exist betweentwo alleles each conferring
a selective advantagein one of the niches, even if adults forma single randommatingpopulation,provided:(1) the populationsize is separatelyregulated
in the two niches, and (2) the selective advantages are large. The conditions to be satisfied are given; it is difficultto say how oftentheywill be
satisfied.
is favoredif femalestendto lay eggs in the niche
A stable polymorphism
in which.theywere themselvesraised.
Four genetic mechanisms-habitat selection, pleiotropicgenes, modifying genes, and assortative matinggenes-which-could cause matingisolacould be the
tion are considered. It is concludedthatstable polymorphism
firststage in sympatricspeciation. The relevance of these mechanismsin
allopatricspeciation is also discussed,
LITERATURE
CITED
Basykin, A. D. 1965. On the possibility of sympatric species formation.
Bull. Mosc. Soc. Nat. Biol. Div. 70(1):161165.
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All use subject to JSTOR Terms and Conditions
650
THE AMERICAN NATURALIST
Dobzhansky, Th. 1940. Speciation as a stage in evolutionary divergence.
Amer. Natur. 74:312-321.
Haldane, J. B. S., and S. D. Jayakar. 1963. Polymorphismdue to,selection
of varyingdirection. J. Genet. 58:237-242.
Koopman, K. F. 1950. Natural selection for reproductive isolation between
Drosophila pseudoobscura and Drosophila persimilis. Evolution.
4:135-148.
Levene, H. 1953. Genetic equilibrium when more than one ecological niche
is available. Amer. Natur. 87:331-333.
Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press.
Millicent, E., and J. M. Thoday. 1961. Effects of disruptive selection IV.
Gene-flow and divergence. Heredity, 16:199-217.
Thoday, J. M., and T. B. Boam. 1959. Effects of disruptive selection II.
Polymorphismand divergence without isolation. Heredity, 13:205218.
Thoday, J. M., and J. B. Gibson. 1962. Isolation by disruptive selection.
Nature, 193:1164-1166.
Thorpe, W. H. 1930. Biological races in insects and allied groups. Biol.
Rev. 5:177-212.
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All use subject to JSTOR Terms and Conditions