Biological Conservation 89 (1999) 143±152

Rapid displacement of native species by invasive species: e€ects of

hybridization
Gary R. Huxel*
Department of Environmental Science and Policy and Institute of Theoretical Dynamics, University of California, Davis, CA 95616, USA

Received 23 March 1998; received in revised form 24 October 1998; accepted 4 November 1998

Abstract
The introduction of non-native populations can lead to the competitive exclusion (displacement) of native populations. This has
been hypothesized to be further exacerbated by the potential of hybridization, which can dilute or genetically assimilate the native
genotype leaving no ``pure'' natives. With relatively moderate to high rates of immigration, the loss of the native species can be
rapid with or without hybridization. Using single-locus, two-allele models, I ®nd that species replacement can occur very rapidly
and the time to displacement decreases rapidly with increasing immigration and selection di€erential. Immigration and selection act
in two di€erent ways: increasing immigration results in displacement by overwhelming the native; whereas increasing the selection
di€erential in favor of the invader leads to displacement via genetic assimilation. The implications of these results are the need for
more empirical studies on the immigration patterns of invasive species and their potential for interbreeding with natives. # 1999
Elsevier Science Ltd. All rights reserved.
Keywords: Introgression; Species displacement; Hybridization; Genetic assimilation; Invading species

1. Introduction taxa or extinction of the native taxa. Although theore-

Hybridization is a common phenomenon in plants,
birds, ®sh, and many other taxa (Mayr, 1942; Grant,
1981; Harrison, 1990; Grant and Grant, 1992, 1996;
Dowling and DeMarais, 1993; Levin et al., 1996; Rhy-
mer and Simberlo€, 1996; Williamson, 1996; Arnold,
1997). Yet in studying the displacement of native species
by invading species the potential for interbreeding
between an invading species and a native species is often
ignored or understated. It has been suggested that
interbreeding increases the threat of extinction for a
number of species due to hybridization introgression
(Levin et al., 1996; Rhymer and Simberlo€, 1996). For
example, ``pure'' native Pecos pup®sh may no longer
exist due to introgression with an introduced bait ®sh,
the sheepshead minnow (Echelle and Connor, 1989).
Conditions under which hybridization is expected to
increase or decrease the rate of species displacement has
not been explicitly examined. In cases where related
taxa are able to interbreed, introductions may lead to
the introduced taxa dying out, coexistence, new hybrid
* Tel.: +1-530-752-5162; fax: +1-530-752-3350; e-mail: grhuxel@
ucdavis.edu.
0006-3207/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved.
PII: S0006-3207(98)00153-0
tical studies have addressed the introduction of new
alleles into populations (i.e. the third phase of Wright's
shifting balance theory), few have focused on the dis-
placement of native taxa (alleles). Here, I use single
locus, two-allele (one native and one non-native) to
examine the in¯uence of interbreeding with invading
taxa on native taxa.
Historically, geographical isolation has been a major
factor in limiting the impacts of hybridization and
introgression. Today, however, taxa are being brought
into contact with related taxa from which they have
been isolated through many anthropogenic pathways
(Carlton, 1979, 1989; Carlton and Geller, 1993; Wil-
liamson, 1996). For example, the movement of ballast
water throughout the world is increasing the opportu-
nities for closely related taxa to interbreed leading to
homogenization of near-shore marine communities
worldwide and the widespread loss of species (Carlton,
1979, 1989, 1996; Carlton and Geller, 1993). Similar
large distance (inter-regional), short time scale immi-
gration occurs with the introduction of nurse stocks of
plants and the incidental movement of herbivores and
parasitoids (Heywood, 1989). Furthermore, introduc-
tion of bird species has been extremely widespread
144 G.R. Huxel / Biological Conservation 89 (1999) 143±152
throughout the world (Moulton and Pimm, 1986;
Moulton, 1993; Case, 1996). Human-mediated intro-
ductions can be frequent and re-occurring, greatly
increasing immigration rates (Carlton and Geller, 1993).
In the absence of hybridization the interaction
between the native and introduced species is essentially
a competitive one between species that are similar in
many aspects of their ecology and life histories. Assum-
ing a homogeneous environment, without interbreeding,
the species with the greater ®tness (e.g. better compe-
titor or higher reproductive rate) will dominate at equi-
librium. Switching from discussing individuals, I now
focus on interactions between native and non-native
genotypes. If immigration rates are very low and given
no (or a weak) selection advantage to the invader, then
one would expect that Allee or stochastic e€ects may
lead quickly to elimination of the invader as its popula-
tion density remains low. At very high rates of immi-
gration, Kondrashov (1992) has shown that
immigration e€ects alone in the absence of interbreed-
ing can cause the loss of the native species. Alter-
natively, large ®tness di€erentials, alone, lead to the
®xation of a favored genotype, therefore the relatively
slow process of selection acting without immigration
can be quickened by increasing the ®tness di€erential.
For example, intermediate genotypes can be made lethal
for a population with a large, but ®nite, population size
so that the inferior parental genotype is rapidly lost
(Kondrashov, 1992).
In the presence of hybridization, one would expect
costs associated with genetic assimilation and/or bene-
®ts of infusion of new genes into one or both parental
taxa. However, hybrids can be fertile yet reproductively
isolated from adults for various reasons including ferti-
lity selection (allopolyploidy, translocation hetero-
zygosity, recombination speciation, species-speci®c
di€erences in mitochrondial DNA) and pre-mating fac-
tors (behavioural changes, reproductive phenology,
niche separation). Interbreeding may also allow rare
genotypes to become established and then increase as
backcrosses with the non-native parental taxa or inter-
breeding between hybrids occurs. This of course, is
simple in the single locus models used here, but is more
complicated in real situations involving multiloci (see
below). Large selection advantages for non-native
alleles should result in more rapid displacement of
native alleles with hybridization than without.
While studies have shown that lowering the ®tness of
hybrids can result in displacement (Kondrashov, 1992),
the question remains as to whether the rate of species
displacement increases or decreases with increased
interbreeding between an invading genotype and a
native genotype. Genotypic displacement occurs when a
native species becomes extinct and is replaced by an
invading species. By ®tness, I mean the relative compe-
titive ability expressed as the number of viable o€spring
produced compared with the number produced by other
genotypes. Thus, the interesting question in terms of the
conservation of species, and the main question of this
paper, is whether hybridization enhances or impedes the
rate of species displacement and whether this phenom-
enon is a€ected by introgression. I address this question
using single locus, two-allele models with varying
degrees of interbreeding. Additionally, I examined the
in¯uence of varying the ®tness of the heterozygote from
underdominance to overdominance in a system that
exhibits introgression.
2. Model descriptions and analyses
Let us consider two populations with non-over-
lapping generations. One population is native and has a
®xed allele at a given locus (BB) and the other is non-
native with a di€erent ®xed allele at the same locus
(AA). Non-native individuals can migrate into the
native habitat but the opposite in not allowed. This may
represent stocking programs or other human-mediated
dispersal so that immigration rates can be much greater
than otherwise found in natural systems. The popula-
tion is assumed to follow Hardy±Weinberg proportions
with selection immediately following immigration. This
assumes no mutation, large populations and random
mating. Furthermore, any competitive di€erences are
accounted for in ®tness di€erentials. In the model, the
population size is in®nite and ®xation of AA is said to
occur when its frequency is greater than 0.99. Four
cases of post mating isolation are modeled: (1) lethal
heterozygotes; (2) sterile hybrids; (3) hybrids with
backcross sterility and (4) introgression. A ®fth case was
examined which also involves introgression, but the ®t-
ness of the heterozygote is varied from underdominance
to overdominance. The frequency of AA, pAA, (the
introduced genotype) at time (t ‡ 1):
p0AA ˆ pAA …1 ÿ m† ‡ m; …1†
where m is the migration rate. This assumes that
migrating individuals each replace one resident indivi-
dual proportionally (no preference for displacement of
any genotype by immigrants). Fitness of the native spe-
cies was assumed to be 1 in all models for mathematical
and interpretive ease.
Most theoretical studies have focussed on equilibrium
analyses of introduced alleles, but I was most interested
in the time to displacement. The time frame of dis-
placement has important conservation consequences
due to human-mediated immigration rates and the lack
of taxonomic work in many systems (Carleton and
Geller, 1993; Geller et al., 1997). Thus I allowed the
systems to run assuming a large population of constant
size from one generation to the next until displacement
 G.R. Huxel / Biological Conservation 89 (1999) 143±152 145

occurred or 500 generations had elapsed. I used the

range of values for ®tness (!AA Юtness of AA in the
®rst four cases or !AB Юtness of AB in the last case)
from 0 to 4.0 with step increases of 0.1 and m from 0 to
1.0 with step increases of 0.1. The initial community is
comprised only of natives (pBB ˆ 1).

2.1. Lethal heterozygotes

I simpli®ed the analyses by only following the intro-

duced species in this case. If pAA is the frequency of the
introduced genotype in the generation after selection
and if no interbreeding can occur then

p0AA ˆ !AA p2AA =b!AA …p2AA ‡ m† ‡ !AB ……1 ÿ pAA †2 ÿ m†c

…2†

where !AA is the ®tness of the ``pure'' invader genotype,

pAA is the frequency of the ``pure'' invader genotype, m
is the migration rate and !BB is the ®tness of the native
genotype. This is the baseline case for the discussion,
which is essentially a competitive situation where the
species have remained reproductively isolated.
Fixation of the invader genotype (pAA ˆ 1) always
occurred when both immigration and !AA were at
moderate levels [Fig. 1(a)]. Fixation also occurred when
the invader had a disadvantage in ®tness (!AA < 1). For
example, when !AA > 0:20, ®xation occurred whenever
immigration was greater than 0.30. Under the condition
of no immigration (m ˆ 0:0) the invader genotype is
always lost. An interesting dynamic happens at m ˆ 0:1
Fig. 1. The no interbreeding case; (a) time to extinction and (b) fre-
which is below the critical immigration rate for which a quency of AA. These patterns hold for the sterile hybrid and back-
species cannot successfully replace another without cross sterility cases as well.
selection when !AA ˆ 1 (Crow et al., 1990; Kondra-
shov, 1992). As predicted with m at this level, at and greater population sizes than the native species and in
below !AA of 2.0 the pAA slowly approaches 0.07 so that the absence of introgression may displace the native.
®xation does not occur in 500 generations, but increas- This seems to be occurring in the introduction of brook
ing !AA to 2.1 leads to ®xation in just 33 generations. trout (Salvelinus fontinalis) into the habitat of native
This is typical of the dynamics with no hybridization bull trout (S. con¯uentus) in the Columbia and Klamath
where there exists a sharp boundary between rapid and River drainages (Leary et al., 1993).
no ®xation with 500 generations (eventually however
®xation will always occur with one way migration and 2.2. Hybrid sterility
!AA > 1). The frequency of AA after 500 generations
was always less than 0.25 when ®xation did not occur Next I examine the extreme case of hybridization
and was usually less than 0.10 [Fig. 1(b)]. When ®xation without introgression in which the hybrids are sterile
occurred it always did so in less than 33 generations and (!AB ˆ 0), but are part of the t ‡ 1 generation. The
as both !AA and m increased, this time to ®xation was equation for the frequency of AA (pAA) is the similar to
reduced to less than 10 generations. Eq. (2), however to maintain a constant population size,
The case of no interbreeding demonstrates that dis- pAA at time t ‡ 1 one must account for the loss of
placement is greatly in¯uenced by immigration and dif- hybrid individuals each generation. Therefore I assumed
ferences in relative ®tness. Time to displacement, when that the two parental lineages produce sucient num-
it occurred, was extremely rapid and decreased as m and bers of o€spring so that the population size is constant
!AA increased. Immigration rates may be increased by from one generation to the next and do so at their
human activities; examples of this are found in stocking respective proportions after selection. For example, if
programs, in which the introduced species may have pAA ˆ 0:40 and pBB ˆ 0:60 (®tness of all genotypes is set
146 G.R. Huxel / Biological Conservation 89 (1999) 143±152
to 1 and m is set to zero for this example), random
mating results in pAA ˆ 0:16, pAB ˆ 0:48, and
pBB ˆ 0:36. As the heterozygotes are sterile, the fre-
quency of A for contribution to the following genera-
tion is 0.32/(0.32+0.72) or 0.307. Thus, the only
di€erence between this model and the no interbreeding
case is that some reproductive e€ort is spent on the
hybrids which do not reproduce.
The pattern of the rate of species displacement found
in this case was similar to the no interbreeding case (see
Fig. 1). The di€erence was that the transitions were
steeper, that is, when ®xation did not occur, pAA was
lower. In many instances the invader genotype did not
become established even at high rates of immigration
(but low AA ®tness values). The number of generations
to species displacement, when it did occur, was the same
as the no interbreeding case. The frequency of the native
(pBB) only slowly decreased with m and !AA until the
steep transition to displacement. The frequency of
hybrid (pAB) remained low while AA was low and were
lost with the native.
The results show that hybridization with sterile
hybrids has little e€ect on species displacement as com-
pared to the no interbreeding case. This result is depen-
dent upon the surviving ``pure'' individuals having great
enough fecundity to maintain a consistent population
size. If fecundity of these individuals cannot maintain a
consistent population size then they are likely to become
extinct, which is a real possibility for populations that
start with small numbers of individuals. Once the
extinction of natives and hybrids has occurred, the
invader may then become established. Furthermore, this
case demonstrates that even when the invader is at low
density, small increases in immigration or ®tness of the
invader can lead to rapid displacement.
2.3. Hybridization with backcross sterility
In this case the hybrids are fertile yet have become
reproductively isolated from the two parental lineages
(which can interbreed). This can be modeled by the fol-
lowing:
p0AA ˆ !AA fag=‰!AA fag ‡ !AB fbg ‡ !BB fcgŠ
p0AB ˆ !AB fbg=‰!AA fag ‡ !AB fbg ‡ !BB fcgŠ
p0BB ˆ !BB fcg=‰!AA fag ‡ !AB fbg ‡ !BB fcgŠ
a ˆ …p2AA ‡ p2AB =4†…1 ÿ m†
b ˆ …2pAA pBB ‡ p2AB =2†…1 ÿ m†
c ˆ …p2BB ‡ p2AB =4†…1 ÿ m†; …
where a, b and c are the total contributions to the next
generation from each genotype for AA, AB and BB,
respectively; pAA is the frequency of the ``pure'' invader;
pAB is the frequency of the hybrid; and pBB is the fre-
quency of the ``pure'' native. Compared to the ®rst two
cases, the time to displacement is faster at low immi-
gration and at low !AA values, slower otherwise.
From the perspective of invading species with a low
immigration rate, this is favorable compared to a case
where no interbreeding occurs or the hybrids are sterile.
At low invasion numbers, the invader may su€er from
the Allee e€ect, which can be molli®ed by interbreeding
with the native species. In the one locusÐtwo-allele
model, even if introgression does not occur, breeding
among hybrids produces a signi®cant number of ``pure''
invaders. In the sterile hybrid model, all reproductive
e€ort with natives is lost, e€ectively reducing the popu-
lation size of the invaders. At high immigration rates,
sheer numbers alone can overcome the Allee e€ect.
2.4. Introgression
This is the standard Hardy±Weinberg scenario with
selection giving Eq. (3), but now
a ˆ …p2AA ‡ p2AA =4 ‡ pAA pAB =2†…1 ÿ m† ‡ m
b ˆ …2pAA pBB ‡ p2 =2 ‡ pAA pAB =2 ‡ pBB pAB =2†…1 ÿ m†
c ˆ …p2BB ‡ p2AB =4 ‡ pBB pAB =2†…1 ÿ m†
Using this model, I performed two analyses. In the ®rst,
in this section, I varied !AA as in the earlier two cases
and in the second, Section 2.5, I varied !AB to examine
the e€ects of hybrid ®tness. In the former, !AB and !BB
were set to 1 and in the latter, !AA and !BB were set to
1. Hybrid vigor can occur whenever hybrids are pro-
duced, sterile hybrids may thrive by vegetative growth
and reproductively isolated hybrids may also have
increased ®tness. For demonstrative purposes, I chose
only to model sexual reproduction in Section 2.5.
As with all other cases, ®xation occurs over a wide
range of m and !AA values [Fig. 2(a)]. However, in this
case ®xation does not occur when !AA < 0:50, but does
occur when m50:05 and !AA > 0:90. Thus, ®xation can
arise at lower levels of immigration, but displacement is
restricted to conditions when the relative ®tness of the
native is low. Comparing time to ®xation, the introgres-
sion model takes longer than the previous three models,
but the di€erences are relatively small. The frequency of
AA is also much greater when ®xation does not occur in
this case compared to the others [Fig. 2(b)]. Because of
high frequencies of hybrids, pBB was much lower in this
case than the previous models [Fig. 2(c)]. As m and !AA
3†
values (as well as pAA) increased, pAB became greater
than pBB [Fig. 2(d)]. The hybrid increased as m and !AA
increased until the native was driven to low frequencies
and then both pAB and pBB went extinct.
In the case of introgression, the rate of species dis-
placement is faster at low levels of immigration, but
 G.R. Huxel / Biological Conservation 89 (1999) 143±152
Fig. 2. The introgression case; (a) time to extinction; (b) frequency of AA; (c) frequency of AB; and (d) frequency of BB.
slower at lower values of relative ®tness of the invader
when compared to the no interbreeding case [Figs. 1(a)
and 2(a)]. Owning to a lower frequency of the native
genotype and increased frequency of the hybrid, the
native is more susceptible to demographic or environ-
mental stochasticity as well as genetic assimilation by
the invader. The presence of large numbers of hybrids
may also arise at points of contact between species at
the limits of their ranges creating hybrid zones. As an
example, introgression seems to be playing a role in the
loss of the ``pure'' native red deer in Scotland (Aber-
nethy, 1994). In this system a hybrid zone was created
and it is in disequilibrium so that the zone is shifting,
resulting in a decrease of the native red deer range.
Displacement occurs at lower values of !AA for
immigration rates greater than 0.05 in comparison of
the introgression case with the hybridization with back-
cross sterility case. Similarly, the hybridization with
backcross sterility case is intermediate in terms of the
frequency of the three genotypes. The native has a lower
frequency when it persists compared to all other cases.
The other two genotypes have greater frequencies com-
147
pared to the ®rst two cases, but they have lower fre-
quencies compared to the introgression case.
2.5. Heterozygote ®tness
At values of !AB < 1 (underdominance), the species
displacement of the native is enhanced [Fig. 3(a) and
(b)]. However, when !AB > 1 (overdominance), this was
greatly reduced and complete displacement did not
occur at any level of m when !AB > 2:1. As pAB
increased with !AB , pBB was driven to <0.13 at low m,
decreasing to pBB < 0:02 at m > 0:40 [Fig. 3(c) and (d)].
The hybrid also became dominant over the ``pure''
invader as pAA decreased and !AB increased at all levels
of m [Fig. 3(b)]. These results may be an artifact of the
single locus models in which hybrids interbreeding
among themselves or with either parental genotype
can produce ``pure'' parental genotypes (see below).
This may not occur given a large number of interacting
loci.
The loss of the ``pure'' native due to genetic assimila-
tion can be hastened by hybrid vigor (overdominance)
148 G.R. Huxel / Biological Conservation 89 (1999) 143±152
Fig. 3. The introgression with underdominance and overdominance: (a) time to extinction; (b) frequency of AA; (c) frequency of AB; and (d) fre-
quency of BB.
whether introgression occurs or the hybrids are repro-
ductively isolated from the parental lineages. Though
complete displacement may be reduced as the relative
®tness of the hybrid increases, the frequency of the
native decreases (above a threshold) and approaches
zero when the rate of immigration is high [Fig. 3(a)].
As an illustration, the introduction of Spartina alter-
ni¯ora into the British Isles shows aspects of hybrid
sterility, hybridization without backcrossing and hybrid
vigor. In plants (and other organisms), hybrids may be
reproductively isolated from the parental lineages due to
polyploidy. When this occurs and the new species shows
hybrid vigor, both ``pure'' species may be displaced.
This can be seen in the case of S. anglica (Thompson,
1991). The introduction of S. alterni¯ora, a native of the
North American Atlantic coast, into the British Isles
lead to its hybridizing with S. maritima, a European
native, producing S.  townsendii which was sterile.
Subsequently a chromosome doubling occurred in S. 
townsendii producing S. anglica, which was fertile but
reproductively isolated from the parental lineages. This
new species has since displaced both ``pure'' species and
the sterile hybrid and become a dominant plant extend-
ing much further down into the tidal zone while the
original hybrid has not spread (Thompson, 1991).
3. Discussion
The results suggest that displacement of native taxa
by non-native taxa can occur very rapidly [e.g. less than
®ve generations; see Fig. 2(a)]. Given the number of
cryptic species and the high rates of human-mediated
species introductions, extinctions may be on the increase
from the e€ects of hybridization alone.
The results of the models are dependent on a number
of factors implicitly assumed in the model. These
include: (i) that the ®tness of AA and AB can have a
large range of values; (ii) migration rates can be extre-
mely high; (iii) a single locus can infer large relative ®t-
ness di€erences; and (iv) mating is random. Below I
brie¯y discuss each of these.
 G.R. Huxel / Biological Conservation 89 (1999) 143±152
3.1. Fitness of AA and AB
The range of values of ®tness for AA used in this
study may seem fairly extreme, however in the context
of an invading species these values may not be extreme.
Invading species that are transported across large barriers
may have the advantage of escaping from predators,
parasites and competitors (Elton, 1958). Essentially
species can land in ``enemy free space''. This may explain
some of the diculty in developing general theories con-
cerning which species will successfully invade which
community (RejmaÂnek, 1995; Reichard and Hamilton,
1997). Competition, predation and parasitism (or a
combination of some or all) may drive a species into a
narrow niche in its native range, once released from this
the species may become more common in its new habi-
tat. Additionally, a species that is rare in its native
habitat may become more common with increasing
amount of favorable habitat in its new range. New
habitat can include prey species with which they have
no previous evolutionary contact so that no defenses are
encountered. Conversely, a species may ®nd increased
competition, predation and parasitism and less favor-
able habitat in the new region lowering its ®tness.
One of the potential consequences of hybridization is
that the hybrid may be able to invade territory that its
parental species cannot, thus the total population size
may be increased due to new resource availability.
Spartina anglica's occupation of lower regions of the
intertidal zone is an example that is consistent with this
scenario (Thompson, 1991). A possible limitation to the
model is that it does not allow for hybrids to reproduce
vegetatively. Sterile hybrids may expand their range and
spread via vegetative growth, but there is no evidence
for this.
As to the relative ®tness of hybrids, there are only a
limited number of documented cases of overdominance.
Endler (1986) lists only six examples. However, this may
be due to the lack of solid data testing for this phe-
nomenon, but with improving genetic techniques this
will become easier to test. Blossey and NoÈtzold (1995)
suggested that the evolution of increased competitive
ability can result from shifts in resource allocation pat-
terns due to selective forces in the new habitat. This may
lead to rapid changes in relative ®tness of the invader
and any hybrids. In a test of this hypothesis, Blossey
and Kamil (1996) found that introduced Lythrum sali-
caria (purple loosestrife) grew better in identical condi-
tions than it did in its native range. Similarly, Strong
(pers. comm.) has found that introduced Spartina alter-
ni¯ora populations in Washington State grows rapidly,
but has lost many of its defenses to herbivores. Levin et
al. (1996) further suggested that hybrids might perform
best under conditions not favored by either parent.
Similarly, Floate et al. (1993) found that herbivory has
greatest in hybrid zones relative to ``pure'' zones.
149
3.2. Migration
The movement of coastal marine species via ship
fouling, incidental passengers and ballast water has
been occurring for many of years, with most the move-
ment in terms of ballast water occurring recently (Carl-
ton, 1979, 1989; Carlton and Geller, 1993). With many
species in the marine environment yet undescribed, the
impact of species displacement may be highly sig-
ni®cant. Many marine taxa are widely distributed and
geographically distinct. Terrestrial systems have also
been subjected to introduction rates that are occurring
at three or more orders of magnitude greater than the
major paleontological invasions such as the Great
American Interchange (Williamson, 1996).
In addition to human-mediated transportation, chan-
ging global climate can also signi®cantly increase
migration rates. For marine systems, near-shore tem-
perature is a major limiting factor in species distribu-
tions; increased temperatures in these systems will
facilitate dispersal. For example, the interaction
between Mytilus galloprovinicialis and M. trossolus may
be further complicated by warming of northern Paci®c
waters allowing M. galloprovinicialis to spread north-
ward (Suchanek et al., 1998).
Migration and ®tness may also be altered by di€er-
ences in gamete production and fertility. The invading
species may genetically ``swamp'' the native by produ-
cing large numbers of gametes (i.e. pollen or sperm by
males) and increased fertility in the expanded range.
Many rare plant populations contain few individuals
(Levin et al., 1996). Low population size results in
increased susceptibility for rare species to genetic
assimilation and species displacement due to inter-
breeding. This is an important factor of animal species
as well. For example, introgression has been cited as a
substantial contributing factor for three (the Tecopa
pup®sh, Cyprinodon nevadensis; the Amista gambusia,
Gambusia amistadensis; and the longjaw cisco, Cor-
egonus alpenae) of the 13 species that have become
extinct since the creation of the Endangered Species Act
(Rhymer and Simberlo€, 1996).
An increasing source of migration of large numbers of
individuals is the introduction of biological control
agents and genetically engineered genes (Howarth, 1991;
Klinger and Ellstrand, 1994; Simberlo€ and Stiling,
1996). Crop plants are a large source of engineered
genes and the spread of these genes into wild popula-
tions has been documented in several cases (Klinger and
Ellstrand, 1994; Bergelson et al., 1998). Bergelson et al.
(1998) recently demonstrated that engineered genes in
crop plants may have greater risks of spread than wild-
type genes in weedy forms. Additionally, many biologi-
cal control agents have very narrow range of hosts,
however, hybrids between these non-native species and
natives may allow for a broadening of hosts or host
150 G.R. Huxel / Biological Conservation 89 (1999) 143±152
switching by the hybrids. This potential hybridization is
usually not considered when selecting for biological
control agents. One the above mentioned species that
became extinct after the creation of the Endangered
Species Act, Gambusia amistadensis, was in part due to
two conspeci®cs, G. anis and G. holbrooki, introduced
for biological control of mosquitos. Additionally, other
endangered or vunerable Gambusia species hybridize
with the mosquito®sh, G. anis (Minckley et al., 1991).
3.3. Number of loci
In many cases of hybridization, the species may not
be sister species so that segregation between many loci
can frequently occur during recombination. Segregation
can in¯uence interactions between genes and lead to
hybrids being phenotypically closer to one of the par-
ents. In a study of gene interactions in hybrid specia-
tion, Rieseberg et al. (1996) found that selection to a
large extent has governed past hybrid species forma-
tions. They also stated that nonrandom rates of intro-
gression and signi®cant associations among unlinked
genetic markers of three synthesized hybrid lineages
implied that interactions between coadapted parental
speices' genes constrain the genomic composition of
hybrid species. In many cases, reduced hybrid fertility
or sterility is due to unfavorable genomic interactions.
However, successful origin of new species via hybridi-
zation implies that this is not always the case. The
selection process will weed out unfavorable combina-
tions while favorable ones are preserved creating new
genotypes (or possibly new species) or introducing new
alleles into one or both of the parental species.
In a theoretical study of relative roles of migration
and selection in the introduction of new alleles, Kon-
drashov (1992) compared a single locus system with a
model using an in®nite number of loci. He found that
both migration and selection were important factors
and that the coexistence of genotypes is more likely to
occur with in®nite loci. Yet in both model systems, dis-
placement occurs even in the extreme case of lethal
hybrids. While Kondrashov (1992) examined models of
extreme numbers of loci, either one or in®nite, most
systems will involve an intermediate number of loci.
Crow et al. (1990) found in models of two to nine loci
that with interbreeding, ®xation of the invading geno-
type could occur at high rates of two-way migration (the
more conservative case compared to one-way migra-
tion) and moderate rates of ®tness of the invader. The
critical migration rate for the ®xation of the non-native
genotype for ! ˆ 1 increases to 0.5 in the in®nite loci
case, up from 0.18 in the single locus model. However,
for presence of the non-native alleles, the migration rate
could be several orders of magnitude lower (0.005 in
the case of a triple dominate genotype in a three loci
model).
Furthermore, introgression may lead to the develop-
ment of a hybrid swarm consisting of a large number of
hybrid types due to large numbers of loci. The intro-
gression between the native Pecos pup®sh (Cyprinodon
pecosensis) and the introduced sheepheads minnow (C.
variegatus) generated a hybrid swarm. C. variegatus was
introduced, by sport ®shers, as a bait®sh. Within 5 years
of introduction of the sheepheads minnow, the native
had been excluded from approximately half its original
range and all remaining individuals were hybrids
(Echelle and Connor, 1989). Thus, multiple loci seem to
enhance the number of hybrid types and genetic mixing
and have sped the diminution of the ``pure'' native
types. Also, large numbers of loci essentially reduce the
probability of a ``pure'' individual of either parental
lineage from being produced by two hybrid individuals,
an event that is common in the single-locus models.
Displacement holds, in model systems, for the in®nite
loci case and may exaggerate the in¯uence of introgres-
sion due to the large number of potential hybrid com-
binations. Thus, one would expect that genetic
assimilation would be more common with increased,
but ®nite, numbers of loci, preserving some of the
natives' alleles in the hybrids (however unfavorable
genomic interactions will limit the number of hybrid
types; Rieseberg et al., 1996). One then can assume that
the selection di€erences among genotypes are dependent
upon a relatively small number of loci. Given even a
small number of loci, a greater number of hybrid types
will be produced than in the single locus model and the
likelihood that one will be able to outcompete both the
native and the non-native is increased. Without intro-
gression these hybrids may quickly form a new species
as the hybrids are reproductively isolated, but with
introgression this may be slowed as backcrosses with
parental lineages occurs.
3.4. Mating
While my models assume random mating, non-ran-
dom mating can greatly in¯uence the results. In the case
of the Pecos pup®sh, female mate preference for males
of other species may have played a role in the rapidity
of the spread of exotic genotype and the loss of the
``pure'' native (Echelle and Connor, 1989). In the case
of the introduction of brook trout into the Columbia
and Klamath Rivers, the lack of introgression created
an advantage for the more numerous introduced species
(Leary et al., 1993). However for species invading a new
habitat, mating is likely to occur with any potential
mates.
Species that are most at risk to hybridization are ones
that have external fertilization (e.g. as broadcast
spawning marine invertebrates and outcrossing plants).
Wind pollined taxa such as oaks have high rates of
introgression. Hybridization is more likely in groups
 G.R. Huxel / Biological Conservation 89 (1999) 143±152
that have extended breeding cycles (Rhymer and Sim-
berlo€, 1996).
Associated with random mating is the assumption of
large population size that does not vary. This has con-
sequences, as discussed above, in the sterile hybrid
model and for newly evolved species and/or hybrids that
have slightly di€erent ecological requirements. In the
latter, the carrying capacity of the system may be
increased. Further, habitat segregation and selection
have been found to limit random mating in studies of
two or three patches (Holt, 1987; Holt and Gaines,
1992) and in metapopulations (Levins, 1969; Hedrick
and Gilpin, 1997; Peacock and Smith, 1997).
4. Conclusions
Hybridization with introgression can exacerbate spe-
cies displacement rates under the assumptions of the
models presented here. Hybridization with sterile o€-
spring seems to have little e€ect on displacement.
Introgression enhances displacement at low immigra-
tion rates, but impedes it when the native has a large
selective advantage and at higher rates of immigration.
However, because of increased frequency of hybrids
with introgression, the native is still heavily impacted
and its likelihood of extinction is greatly increased.
Varying the ®tness of the hybrid demonstrated that at
low !AB , displacement is enhanced and at greater values
of !AB , displacement is impeded. But again, because the
increased frequency of hybrids, the native species is
susceptible to genetic assimilation or extinction. This is
especially important because the taxa that are most
threatened by introgression and hybridization have low
population sizes and restricted ranges (Levin et al.,
1996). This includes the potential loss of genetic integ-
rity of native populations through selective stocking of
non-native individuals (LargiadeÁr and Scholl, 1996).
As Kondrashov (1992) pointed out, both immigration
and selection are important in species displacement. For
invasive species, both can play important roles when
immigration occurs from long distances at frequent
intervals leaving ``enemies'' behind (or new niche space
is available) and maintained at a high rate of immigra-
tion. Because of rapidity of species displacement under
conditions of high ! and m, limiting opportunity for
species invasions is critical. The loss of natve species due
to a closely related introduced species may not just be a
simple ecological or evolutionary trade-o€. Further
extinctions due to unrelated species result in a greater
loss of genetic information as some genetic information
of the native is assimilated into the invader. In the
models presented here, the invader always becomes
established and increases in frequency when immigra-
tion is greater than zero. Given the rate of species
movement by human activity one can expect immigra-
151
tion rates to be increasing. Albuquerque et al. (1996)
found that species that are sympatric may have greater
barriers to interbreeding than species (or populations)
that have evolved allopatically. These results suggest
that more empirical studies need to be carried out to
examine the genetic structure of populations that are
being invaded and determine whether hybridization and
introgression are possible. Additionally, the information
on the relative ®tness provides better predictive power.
This information will allow for predictions of whether
displacement is likely. However, due to the rapidity of
displacement under many conditions of the models, it is
best to prevent biological invasions from occurring
when possible.
Acknowledgements
I would like to thank Dan Simberlo€, Bernd Blossey,
Susan Harrison, Alan Hastings, Kevin McCann,
Donald Strong, Alisa Swann, David Cutler, Amy Wolf
and two anonymous reviewers for suggestions, com-
ments and references. Support for this work was pro-
vided by a NSF Research Training Grant (BIR-960226)
and a NSF Population Biology Grant (DEB-9629236).
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