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Isolating Mechanisms
Roger K Butlin, The University of Leeds, Leeds, UK
Isolating mechanisms are intrinsic characteristics of species that reduce or prevent
successful reproduction with members of other species. Viewed genetically, they are
characters that act as barriers to the exchange of genes between populations.
Introduction and Classification
Successful sexual reproduction requires many features of
the male and female partners to be compatible. They must
be sexually mature in the same place and at the same time,
they must recognize each other as potential mates and
coordinate their mating activity (e.g. courtship behaviour
in animals, flowering in plants or hyphal fusion in fungi).
Followingmating, the spermmust reach and recognize the
egg (in animals), the pollen tube must grow through the
style to the ovule (in plants), or nuclear migration and
dikaryon formation must occur (in fungi). Nuclear fusion
must follow and the resulting zygote must be both viable
and fertile. Finally, the second generation offspring must
also be viable and fertile. In prokaryotes, successful
conjugation or transformation is required for gene
exchange.
Within species, natural selection acts to maintain all of
these interactions and, indeed, to increase their efficiency.
However, between species the sequence may be broken or
impaired at any point and the characters involved in this
breakdown are known as reproductive isolating mechan-
isms, or simply isolating mechanisms. This terminology is
unfortunate: theword ‘mechanism’ implies something that
has been elaborated by evolution for the function of
isolation whereas reproductive isolation is probably much
more commonly an incidental effect of divergence between
populations for other reasons. For example, natural
selection may favour divergence in flowering time in two
allopatric populations of plants in response to climatic
differences. If the ranges of the populations subsequently
change so that they overlap, the flowering time difference
may result in some reproductive isolation but it certainly
did not evolve as a ‘mechanism’ to prevent successful
reproduction.
Reinforcement is the only process by which natural
selection directly favours reproductive isolation, and it is a
controversial process with limited empirical support. For
these reasons, many biologists now prefer to use the term
‘barrier to gene exchange’ because it avoids the implication
of function and focuses attention on the critical genetic
consequences. However, use of ‘isolating mechanism’ is so
widespread that it will be a long time before it is displaced
completely.
It is helpful to classify isolating mechanisms on the basis
of the possible break points in the sequence leading to
successful reproduction. The classification in Table 1 is
based on sexually reproducing animals and flowering
plants. Within these groups, some of the suggested
mechanisms are not universal: for example, animals with
external fertilization cannot show mechanical isolation.
The classification can easily be modified for sexual
reproduction in fungi or protists. An extension to
prokaryotes is more difficult although mechanisms 1 and
2 apply whatever the mode of gene exchange, as does the
requirement for offspring to be viable and capable of
further reproduction. Conjugation and transformation
require recognition and compatibility and so it is possible
to envisage mechanisms equivalent to 3–6 in Table 1.
Note that geographical barriers between populations
can prevent gene exchange but they are not included in
Table 1. Isolating mechanisms are defined as intrinsic
characteristics of organisms that prevent gene exchange
whereas geographical barriers are imposed externally.
Both external and intrinsic barriers to gene exchange can
permit evolutionary divergence, but external barriers are
often temporary.
Premating Isolation
Premating isolation may be the only barrier separating
recently evolved species pairs. For example, female spiders
in the genus Schizocosa will normally allow matings only
by males of their own species, which they identify by
substrate-transmitted vibrations (Stratton and Uetz,
1986). However, if the females are anaesthetized inter-
specific matings are possible and they generate viable and
fertile offspring. This suggests that premating isolation can
evolve more rapidly than postmating isolation and there is
evidence from Drosophila that this is a common pattern
(Coyne and Orr, 1997).
Habitat and temporal isolation (mechanisms 1 and 2 in
Table 1) may be particularly important where speciation is
sympatric since isolation may arise as an incidental
consequence of adaptation to alternative resources in the
environment, such as host plants for phytophagous insects.
The fruitfly Rhagoletis pomonella appears to be in the
process of divergence into apple- and hawthorn-associated
species. Currently, there is probably still some gene
exchange between host-associated populations but it is
Article Contents
Secondary article
. Introduction and Classification
. Premating Isolation
. Assortative Fertilization
. Postzygotic Isolation
1ENCYCLOPEDIA OF LIFE SCIENCES © 2001, John Wiley & Sons, Ltd. www.els.net
impeded by the tendency of flies tomate on the fruits of the
host tree from which they emerged, and for the peaks of
emergence of the two populations to be timed to fit the
different fruiting seasons of their hosts (Feder et al., 1997).
Both flowering time and association with habitats are
likely to be important in reproductive isolation of plant
species. A good example involving both barriers is the
partial isolation between populations of the grassAgrostis
tenuis growing on pastures contaminated with heavy
metals from mining activities and those in surrounding
grassland. The populations are spatially separated as a
result of their ecological tolerances and also isolated by
divergence in flowering timewhich has both environmental
and genetic components (McNeilly andAntonovics, 1968).
Ethological isolation has attracted a great deal of
research attention because the complex sequence of
behavioural acts leading to mating in most animals is
potentially easily disrupted, and because the characters
involved may be expected to diverge rapidly under sexual
selection (Butlin and Ritchie, 1994). This type of isolation
can be quantified relatively easily under laboratory
conditions usingmate choice experiments to detect positive
assortative mating: a tendency to mate more readily with
partners of the same species, population or phenotype.
Although they vary in design, these experiments generate
an ‘isolation index’, the frequency of interspecific matings
relative to intraspecific matings, which can be readily
compared across studies. Coyne and Orr (1997), for
example, compared many pairs of Drosophila species and
showed that the time taken to reach an isolation index of
I5 1.0, indicating complete premating isolation, is in the
region of 3 million years for allopatric species pairs but
considerably less for sympatric pairs.
Closely related species frequently differ strongly in
sexual signal characters, even when they are difficult to
separate on the basis of other phenotypic or genetic traits.
There aremany examples: closely related grasshopper, frog
and bird species typically have distinctive ‘songs’ used to
attract and stimulate mates; male cichlid fish in the
spectacular radiations in African lakes differ strikingly in
their breeding coloration; fireflies flash with species-
specific patterns; and female moths have precisely defined
pheromone blends that attract only males of their own
species. Where signals can be generated or modified
Table 1 A classification of isolating mechanisms
Mechanism Animals Plants
Premating isolation 
Interspecific pairs do not 
form
1. Ecological Pairs do not form because of 
differences in preferred habitat
Plants growing in different habitats 
do not exchange pollen
2. Allochronic Males of one species and females 
of the other are sexually active at 
differenttimes of day or year
Pollen production in one species 
does not overlap in time with 
receptivity of stigmas in the other
3. Ethological Mating signals and responses are 
incompatible
Flowers do not attract the same 
pollinators
4. Mechanical Successful copulation is prevented 
by physical incompatibility of 
the genitalia
Successful pollination is prevented 
by features of floral morphology
Postmating but prezygotic 
isolation 
Interspecific pairs form but 
fertilization does not occur
5. Gamete viability Sperm do not survive in the 
female reproductive tract
Pollen does not germinate or pollen 
tube growth is inhibited
6. Gamete recognition Sperm do not recognize the eggs 
or are incompatible with them
Pollen nuclei do not recognize or 
fuse with egg nuclei
Postzygotic isolation 
Interspecific hybrid zygotes 
are formed but have 
reduced fitness
7. Hybrid inviability Interspecific zygotes have a reduced probability of survival to 
maturity
8. Hybrid sterility Interspecific zygotes have reduced fertility
9. Hybrid breakdown Hybrids produce sterile or inviable offspring
Isolating Mechanisms
2
artificially, it has been possible to dissect the features that
contribute to reproductive isolation. Thus, both contact
pheromone blend (Coyne et al., 1994) and the temporal
characteristics of the sound produced by wing vibration
(Ritchie et al., 1999) contribute to premating reproductive
isolation between Drosophila melanogaster and D. simu-
lans. On the other hand, the unusually wide head of
Drosophila heteroneuramales is a species-specific character
that is under sexual selection but does not contribute to
isolation between D. heteroneura and its sibling species D.
silvestris (Boake et al., 1997).
Pheromones involved in recognition of compatible cells
or mycelia of opposite mating type have been described in
fungi (Casselton and Olesnicky, 1998). This type of
signalling probably underlies ‘interfertile’ versus ‘inter-
sterile’ interactions between mycelia which can be used to
define ‘breeding groups’ in some fungi. For example, the
morphologically defined basidiomycete fungus Armillaria
mellea canbe divided intomany such groups (at least five in
Europe and 10 in North America) which are likely to
represent biological species (see Brasier, 1997).
In many plants, features of floral morphology, flower
colour and scent determine the range of pollinators that
visit flowers of a particular species. If related species attract
different pollinator species, or even if individual pollina-
tors tend to move between similar flowers, interspecific
fertilization will tend to be restricted. Floral differences
between closely related species can be dramatic, just as
sexual signal differences are in animals. Two species of the
monkey flower genusMimulus differ in flower colour (pink
with yellow nectar guides versus red without nectar
guides), corolla form (wide with forward-thrust petals
versus narrowwith recurved petals), nectar volume, nectar
concentration, and anther and stigma positions (Bradshaw
et al., 1995). The first is adapted for bumblebee pollination
and the second for hummingbird pollination.Despite these
extreme differences, which almost completely prevent
hybridization in nature, the species produce vigorous and
fertile hybrids when artificially cross-pollinated.
Assortative Fertilization
Isolation that occurs betweenmating and formation of the
zygote is often referred to as ‘assortative fertilization’. It is
likely to be of great importance in organisms with external
fertilization, especially in sessile aquatic organisms that
broadcast their gametes although allochronic isolation is
also important in these cases. However, assortative
fertilization can also have a role in plant species through
differential pollen tube growth or in animal species with
internal fertilization if females mate repeatedly and store
sperm.
Howard and Gregory (1993) described a striking
example in the field crickets Allonemobius fasciatus and
A. socius. These two species form a mosaic hybrid zone in
eastern North America and patterns in the field suggest
that they are strongly reproductively isolated. However,
interspecific pairs mate readily and produce viable and
fertile offspring. The cause of isolation was a mystery until
the offspring of females that had been mated once to each
of two males was examined using genetic markers. The
results are given in Table 2. Clearly there is strong
assortative fertilization, regardless of mating order, which
will act as a substantial barrier to gene exchange in the field,
provided multiple mating is common.
Table 2 Patterns of parentage in doubly mated females (from Howard and Gregory, 1993)
f, A. fasciatus; s, A. socius.
Female – male – male
Number of females 
tested
Mean proportion of 
offspring fathered by 
first male
Mean proportion of 
offspring fathered by 
second male
Two conspecific males
f – f – f 20 0.364 0.637
s – s – s 12 0.518 0.482
Conspecific male followed by heterospecific male
f – f – s 8 0.981 0.019
s – s – f 7 0.996 0.004
Heterospecific male followed by conspecific male
f – s – f 11 0.000 1.000
s – f – s 7 0.046 0.954
Isolating Mechanisms
3
In Allonemobius, it is uncertain whether the cause of
assortative fertilization is differential sperm survival or
fertilization success but in sea urchins with external
fertilization there is good evidence that disruption of
sperm–egg recognition is a major cause of reproductive
isolation. Studies on closely related species of the genus
Echinometra show that eggs are very rarely fertilized by
heterospecific sperm even when they are applied in excess
under laboratory conditions; see Palumbi (1998) for a
review. This isolation appears to be due to a failure of
attachment by a sperm protein, bindin, to the egg surface.
The gene coding for bindin has been identified and
sequenced. It shows an unusual pattern of evolution: while
part of the molecule is strongly conserved, the remainder
hasmany amino acid substitutions between species – many
more than expected from the number of synonymous base
substitutions in the DNA sequence. This suggests diver-
gence driven by natural selection but does not identify the
source of the selection pressure. At the same time, the
bindin sequence is highly polymorphic within species and
evidence is starting to accumulate for a relationship
between bindin variation and variation in fertilization
success between pairs of urchins.
Postzygotic Isolation
Successful mating and fertilization are not enough for gene
exchange: the resulting zygote must also be able to
complete development, survive to sexual maturity and be
fertile. Inmany pairs of closely related species, it is possible
to overcome premating barriers to gene exchange in the
laboratory but the offspring produced are inviable or
sterile: there is postzygotic isolation. Frequent production
of unfit hybrids is rarely seen in nature (i.e. there is rarely
postzygotic isolation without prezygotic isolation). This
may be because prezygotic isolation evolves more quickly
or because of the inherent instability of pairs of popula-
tions that produce unfit hybrids: if they mate at random,
the rarer population produces more hybrid offspring than
the commoner one and so tends to be driven to extinction.
The exception to this generalization is the widespread
occurrence of hybrid zones where the ranges of divergent
taxa meet. Here, the constant removal of hybrids by
selection is counterbalanced by movement of individuals
into the area from the parental populations (Barton and
Hewitt, 1985).
Early research quickly identified a pattern in the fitness
of these hybrid offspring, now known as ‘Haldane’s rule’
(Haldane, 1922): in many cases only one sex is inviable or
sterile and this sex is almost always the heterogametic sex
(i.e. the sex with two different sex chromosomes: the XY
male in mammals and Drosophila, the ZW female in
butterflies and birds).
Haldane’s rule has been amply confirmed by subsequent
research (Orr, 1997),and has been shown to be an
early stage in the speciation process, by a compilation of
data on reproductive isolation in relation to genetic
distance between pairs of Drosophila species (Coyne
and Orr, 1997). Sterility and inviability of hybrid
males evolves rapidly and is followed by much slower
accumulation of female sterility or inviability. There has
been much debate about the genetic basis of Haldane’s
rule, and about the origin of postzygotic isolation in
general. It now seems likely that both result from the
accumulation of new alleles in diverging populations that
work well in the genetic environment of their own
population but are incompatible with alleles present in
other populations.
In the yellow monkey flower Mimulus guttatus various
simple genetic systems have been identified that give rise to
postzygotic isolation via either early death of hybrid
seedlings or male sterility in mature hybrid plants (Christie
andMacnair, 1987).All involve interactions among loci, as
expected. In some cases it has been possible to show that
the interaction causing sterility is a pleiotropic effect of an
allele that confers tolerance to copper contamination in the
soil. Thus, in these cases, isolation is an incidental side
effect of rapid adaptation rather than a result of long-term
divergence by genetic drift.
Postzygotic isolation need not necessarily be due to
genetic incompatibility, it may also result from reduced
competitive ability of hybrids. In someCanadian lakes, the
three-spine stickleback Gasterosteus aculeatus occurs in
two morphs: a small slender form (‘limnetic’) that feeds on
plankton in open water, and a larger, deeper bodied
form (‘benthic’) that feeds on invertebrates on the bottom
and on vegetation. Hybrids have intermediate body
form but are viable and fertile, as expected from the
very recent divergence of the parental types. However,
competition experiments show that the hybrid phenotype
performs worse than the limnetic form in open water, and
worse than the benthic form in its preferred habitat
(Hatfield and Schluter, 1999). This leads to selection
against intermediates and reduces gene exchange between
the forms.
The final class of isolating mechanism, hybrid break-
down, has been documented relatively rarely because it is
only manifest in second generation hybrids. Two races of
the grasshopper Caledia captiva in Australia provide a
well-documented example (Shaw et al., 1986). The
Moreton and Torresian races show extensive chromoso-
mal differentiation due to pericentric inversions. The F1 is
viable and fertile but the F2 (F1�F1) and backcross
(F1� parental) offspring show viability reductions of
up to 50%. This is apparently due to break-up of
coadapted gene complexes by recombination in the F1
hybrid. It represents a substantial barrier to gene exchange,
as evidencedby the narrowhybrid zonewhere the ranges of
the two taxa meet.
Isolating Mechanisms
4
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Further Reading
Dobzhansky T (1970) Genetics of the Evolutionary Process. New York:
Columbia University Press.
Eberhard W (1985) Sexual Selection and Animal Genitalia. Cambridge,
MA: Harvard University Press.
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