Interciencia
ISSN: 0378-1844
[email protected]
Asociación Interciencia
Venezuela
Pérez, Julio E.; Alfonsi, Carmen; Nirchio, Mauro; Salazar, Sinatra K.
Bioinvaders: the acquisition of new genetic variation
Interciencia, vol. 33, núm. 12, diciembre, 2008, pp. 935-940
Asociación Interciencia
Caracas, Venezuela
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Bioinvaders: The acquisition of new genetic variation
Julio E. Pérez, Carmen Alfonsi, Mauro Nirchio and Sinatra K. Salazar
SUMMARY
Given that the introduction of organisms into a new environment usually occurs in low numbers, reducing genetic diversity
(the so-called bottleneck effect), and that selection further decreases diversity beyond that caused by the bottleneck, then how
do some alien species, if their genetic variation is low under
new conditions, succeed in evolving rapidly, becoming invasive
and expanding their ranges? In this paper a series of mecha-
nisms that allow the introduced population to acquire new genetic variations are considered. Various possible roles of epigenetic adaptation, hybridization, adaptive mutations, transposons,
endosymbiosis, somatic mutations, and mitotic recombination
are postulated as sources of new genetic variations. The roles
of purging and biotic regulation in the successful invasions of
some species is also analyzed.
Introduction
exotic species are apparently
not genetically adapted to
their new environment (Pérez
et al., 2006a, b).
In the biology of invasions
it is usually assumed that loss
of genetic variation due to the
low numbers of exotic organ­
isms introduced reduces the
capacity, called adaptive po­
tential or evolvability (Houle,
1992), of small populations to
evolve in response to new en­
vironmental conditions (Reed
and Frankham 2003; Pérez et
al., 2006a, b).
It is commonly assumed
that preserving genetic diver­
sity is absolutely necessary for
species to continue to adapt
genetically in a changing en­
vironment. The introduction
of alien species, however, pro­
duces a population bottleneck
because the number of initial
colonists is small, and a harm­
ful situation is likely to occur
due to inbreeding and genetic
drift, factors that would con­
tribute to the extinction of the
invaders. During the intro­
duction of aliens, bottlenecks
reduce diversity in neutral
genes, and selection decreases
diversity beyond that caused
by the bottleneck. Loss of ge­
netic variation is determined
by the effective minimum (or
founder) population size (Ne)
and the growth rate of the
population. As indicated by
Dlugosch and Parker (2008),
lower Ne and/or null growth
rate lead to the loss of al­
leles, particularly those that
are rare. Furthermore, several
Then, how are some alien
species so successful in ex­
panding their ranges under
new conditions, evolving rap­
idly, and becoming invasive, if
their genetic variation is low?
Is it because genetic varia­
tion is not necessary? Spiel­
man et al. (2004) answered
this question, comparing av­
erage heterozygosity in 170
threatened taxa with that in
taxonomically related nonthreatened species. Heterozy­
gosity was lower in threatened
taxa in 77% of comparisons,
KEYWORDS / Biotic Regulation / Endosymbiosis / Epigenetics / Purge /
Received: 02/18/2008. Modified: 10/15/2008. Accepted: 10/23/2008.
Julio E. Pérez. Ph.D. in Bio­
logy, University of Southamp­
ton, UK. Professor, Instituto
Oceanográfico de Venezuela,
Universidad de Oriente (IOVUDO), Venezuela. Address:
Laboratorio de Genética, Ins­
DEC 2008, VOL. 33 Nº 12
tituto Oceanográfico de Vene­
zuela, Universidad de Oriente,
Cumaná, Venezuela. e-mail:
[email protected]
Carmen Alfonsi. Dr. in Zoology.
Universidad Central de Vene­
zuela. Professor, IOV-UDO,
Venezuela.
Mauro Nirchio. M.Sc. in Marine
Sciences, UDO, Venezuela.
Professor, Escuela de Ciencias
0378-1844/08/12/935-06 $ 3.00/0
Aplicadas del Mar (ECAMUDO), Venezuela.
Sinatra K. Salazar. MSc. in Ma­
rine Sciences. UDO, Venezue­
la. Professor, ECAM-UDO,
Venezuela.
935
BIOINVASORES: ADQUISICIÓN DE NUEVA VARIACIÓN GENÉTICA
Julio E. Pérez, Carmen Alfonsi, Mauro Nirchio y Sinatra K. Salazar
RESUMEN
La introducción de organismos a un nuevo ambiente generalmente ocurre en escaso número de individuos, lo cual determina
el llamado “cuello de botella”, reduciendo la variación genética, mientras que la selección reduce aún más esta variación.
Entonces, ¿Cómo estos exóticos son exitosos, expanden su rango de distribución bajo nuevas condiciones, evolucionan rápidamente y se convierten en invasores, si su variación genética es
baja? En el presente trabajo, se consideran una serie de mecan-
ismos que permitirían a las poblaciones introducidas adquirir
nueva variación genética. Las adaptaciones epigenéticas, la hibridización, las mutaciones adaptativas, los transposones, la endosimbiosis, las mutaciones somáticas y recombinaciones mitóticas son postuladas como fuentes de nueva variación. Además se
analiza el papel de la purificación y la regulación biótica en la
invasión exitosa de algunas especies.
BIOINVASORES: AQUISIÇÃO DE NOVA VARIAÇÃO GENÉTICA
Julio E. Pérez, Carmen Alfonsi, Mauro Nirchio e Sinatra K. Salazar
RESUMO
A introdução de organismos a um novo ambiente geralmente
ocorre em escasso número de indivíduos, o qual determina o
chamado “efeito gargalo”, reduzindo a variação genética, enquanto que a seleção reduz ainda mais esta variação. Como,
então, podem estes exóticos ser bem sucedidos, expandir sua
faixa de distribuição sob novas condições, evolucionar rapidamente e se converter em invasores, se sua variação genética
é baixa? No presente trabalho, é considerada uma série de
a highly significant depar­
ture from the predictions of
the hypothesis of no genetic
impact.
Genetic va r iation has
been exa m ined using mo­
lecular markers to measure
the amount of genetic diver­
sity in invasive populations.
Molecular genetic markers
appea r to be poor indica­
tors of heritable variation in
adaptative traits (McKay and
Latta, 2002). Recent analyses
(Bensch et al., 2006) have
questioned the usefulness of
heterozygosity estimates as
measures of the inbreeding
coefficient (f) and confirm
that f and heterozygosity are
poorly correlated in a wild
and highly inbred Scandina­
vian wolf population (Canis
lupus). Never theless, they
recommend that management
programs of endangered pop­
ulations include estimates of
both f and heterozygosity, as
they may contribute comple­
mentary information about
population viability.
More research is required
to establish the genetic ba­
sis of traits related to the
establishment and spread of
936
invasive species, traits that
are probably under polygen­
ic control and significantly
inf luenced by the environ­
ment. T hese t ra its ca n not
be a na lyzed wit h protein
and DNA markers, although
mapping of quantitative traits
loci (QTL) affecting fitness
may be possible (Sakai et
al., 2001, McKay and Latta,
2002). QTL mapping analy­
sis methods and associated
computer programs provide
tools that allow evolutionary
studies on the genetic basis
of multiple tra it va r iation
(Zeng, 2005).
On occasion, t he d im i­
nution of genetic variation
seems to have contributed
to successful invasions, as
occurred in the invasion of
North America by the Ar­
gentine ant (Linepithema hu­
mile). Studies using micro­
satellite markers have shown
that the Argentine ant popu­
lations introduced in Califor­
nia possess only about 50%
of the alleles a nd 1/3 the
expected heterozygosity of
native populations. The intro­
duced population is geneti­
cally homogeneous over large
mecanismos que permitiriam às populações introduzidas adquirirem nova variação genética. As adaptações epigenéticas,
a hibridização, as mutações adaptativas, os transposões, a endossimbiose, as mutações somáticas e recombinações mitóticas
são postuladas como fontes de nova variação. Além disso, se
analisa o papel da purificação e a regulação biótica na invasão
bem sucedida de algumas espécies.
distances (up to 1000km),
whereas native populations
maintain their genetic struc­
ture over tens to hundreds of
meters (Tsutsui et al., 2000;
Tsutsui and Case, 2001). In
their indigenous range, L.
humile populations consist of
colonies that contain multiple
nesting sites, each colony
territory being aggressively
defended against other Ar­
gentine ant colonies. In con­
trast, virtually all Argentine
ants in California belong to
the same supercolony. The
success of this invasion has
been interpreted as result­
ing from the diminution in
intraspecies aggression and
subsequent supercolony for­
mation, probably due to a
reduction of recognition al­
leles that prevent individuals
from discr im inating nest­
mates from non-nestmates
based on genetic similarity
(Tsutsui et al., 2000, 2003;
Tsutsui and Case, 2001).
Furthermore, the inappro­
priate application of some ap­
proaches to invasion process­
es, such as reductionism and
the central dogma of biology
(information f lows in only
one direction: DNA is tran­
scribed into RNA, and RNA
is translated into protein; no
reverse flow of information
takes place) has delayed the
understanding of the inva­
sive process. In reductionism,
it is emphasized that genes
make sense only within the
context of whole organisms,
and that more goes into the
making of the whole organ­
ism than just its genes. Singh
(2003) commented that clas­
sical experimental population
genetics dealing with genetic
polymorphism and estima­
tion of selection coefficients
on a gene-by-gene basis is
coming to an end, and a new
era of interdisciplinary and
interactive biology focusing
on dynam ic relationships
among genes, organisms, and
environment has begun. On
the other hand, evidence that
genes do not remain unaffect­
ed by environmental influenc­
es has been accumulating in
the findings of molecular ge­
netics. Epigenetic inheritance
is just one possible mode of
reverse information flow from
the environment to the ge­
nome (Kardong, 2003).
DEC 2008, VOL. 33 Nº 12
Figure 1. Genetic variation in the introduced populations due to bottleneck,
and possible increase in the invasive population. Symbols represent the ge­
netic variation in the populations.
Ways to Increase Genetic
Variation
Although an increase or
decrease in fitness in a popu­
lation depends mainly on the
size and the distribution of
mutational effects, there are
several other mechanisms that
would allow the introduced
organisms not only to increase
their genetic variation, but
also to adapt to new environ­
ments (Figure 1).
Propagule pressure and
hybridization
Hybridization is recognized
as an important success factor
subsequent to the introduc­
tion of alien species (Facon
et al., 2005; Rieseberg et al.,
2003). Due to hybridization
between individuals from dif­
ferent propagules, introduced
populations will occasionally
have a larger genetic variation
than native populations of the
same species (Dupont et al.,
2003, Kolbe et al., 2004).
Hybridization is a genomic
creativity mechanism known
to make species more likely
to be successful in invading
novel ecosystems. Supporting
evidence is found in sunflow­
ers (Reiseberg et al., 2003) for
the viewpoint that hybridiza­
tion is a powerful evolutionary
force that creates opportunities
for adaptive evolution and fa­
cilitates ecological divergence.
Species found in the most ex­
treme habitats are ancient hy­
brids. Most trait differences in
ancient hybrids could be recre­
ated by complementary gene
action in synthetic hybrids and
were favored by selection. Hy­
bridization provides genetic
variation in hundreds or thou­
sands of genes in a single gen­
eration, given a mechanism
for large and rapid adaptive
transitions such as the coloni­
zation of discrete and divergent
ecological niches (Reiseberg et
al., 2003).
Frankham (2005) indicat­
ed that propagule pressure
(that includes the number of
individuals introduced and
the number of release events,
sometimes from different
sources) will produce invasive
species less genetically poor
than expected, and partially
explain the successful invasion
of some species. Several au­
thors (Lockwood et al., 2005;
Kelly et al., 2006; Dlugosch
and Parker, 2008; Ficetola et
al., 2008; Marrs et al. 2008)
indicated that among factors
that determine introduction
DEC 2008, VOL. 33 Nº 12
success, propagule pressure is
emerging as a single consis­
tent correlate of establishment
success.
On t he ot her ha nd, a l­
t hough hybr id ization in­
creases genetic va r iation
and successful invasions, in
many cases it does not ex­
plain several successful inva­
sions in which only a single
inoculation occurred. Three
examples cited by Pérez et
al., (2006a, b) in Venezuela
are: the tilapia, Oreochromis
mossa m bicus, int roduced
in 1959, after three or four
bottlenecks; the marine alga
Kappaphicus alvarezii, intro­
duced in 1996 (Rincones and
Rubio, 1999) expanded its
range to most of the north­
eastern coast of Venezuela
( Ba r r ios, 20 05); a nd t he
bullfrog, Rana catesbiana,
int roduced as one or two
couples in the Venezuelan
Andes (Ojasti et al., 2001).
Epigenetic changes and
phenotypic plasticity
The possibility that epige­
netic changes in gene func­
tions would allow invaders to
become established must be
considered in the short term.
It is very important to keep
in mind that possible adapta­
tive changes due to epigenetic
changes could, in some cases,
also be interpreted as evi­
dence for phenotypic plasticity
induced by variation in the
environment.
Waddington (1953) coined
the term “epigenetics” to re­
fer to processes by which
her itable modifications in
gene function occur, but are
not due to cha nges in the
base sequence of the DNA
of t he orga n ism. T he se ­
quence remains unaltered;
only the environment of me­
chanical, nutritional, chemi­
cal, and biotic factors such
as the presence of predators
is modified and affects the
phenotypic expression. The
term could also be defined
as the analysis of the normal
non-genetic processes that
influence the characteristics
of the phenotype during the
lifetime of the organism, his­
torical inf luences included
(Kardong, 2003).
Esteller (2005) suggested
that it is possible to lump
within the scope of the enig­
matic term “epigenetics” all
the heritable changes in gene
expression patterns that are
based on factors other than
straightforward DNA sequenc­
es. The mechanisms control­
ling epigenetics are very com­
plex.
On the other hand, pheno­
typic plasticity is the ability
of a single genotype to al­
ter its phenotype in response
to environmental conditions
(Nussey et al., 2005). Theo­
retical and laboratory research
suggest that phenotype plastic­
ity can evolve under selection.
Nussey et al. (2005) demon­
strated for the first time that
this is also true in the wild,
and presented evidence from a
Dutch population of great tits
(Parus major) for variation
in individual plasticity in the
timing of reproduction. They
also showed that this variation
is heritable. They have shown
that this plasticity is truly ad­
vantageous and should thus
become more common with
natural selection.
Hereunder, two examples
of adaptation are given, one
due (according to the authors)
to epigenetic change and the
other to phenotypic plasticity:
If two species of rotifers
(Brachionus calyciflorus and
Karatella tropica) are placed
in an environment with their
natural predator, another ro­
tifer of the genus Asplanchna, they will grow protective
spine-like projections. In this
case, biotic information from
the environment (epigenomic
influence) initiates gene ac­
tion. In rotifers, spine produc­
tion might be energetically
expensive, or interfere with
some other aspect of life, so
preprogramming spines ge­
netically and expressing them
before a predator threatens
may be disadvantageous (Kar­
dong, 2003). When predators
threaten rotifers, epigenomic
cues activate genes that in
turn produce protective spines;
these epigenomic influences
937
(predator) have already been
assimilated into the genome
of each, a consequence of fast
evolution. Thus assimilated
and preprogrammed into the
genome, these epigenomic in­
fluences help explain the char­
acter of the phenotype, but are
not themselves an independent
cause of the phenotype (Kar­
dong, 2003).
An example of phenotypic
plasticity has been illustrated
by Meimberg et al. (2006)
explaining the introduction
and successful invasion of
the ba rbed goatgrass, Aegilops triuncialis, from both
the Mediterranean Basin and
Asia into California, despite
their genomic uniformity. Al­
though the authors initially
suspected that the recent in­
vasive spread of this grass
would have resulted from the
recombination of genotype
from multiple introductions,
results suggested that this
had not occurred. Molecular
data indicate that the two in­
troductions are composed of
highly uniform populations.
The capacity of A. triuncialis
to expand its range in Cali­
fornia despite this strong ge­
netic bottleneck suggests that
phenotypic plasticity may be
important for adaptation in
this species.
In conclusion, although in
epigenomic changes there is
a gene alteration that allows
a response to environmental
changes, and in phenotypic
plasticity the answer seems
to be based on the amplitude
of the gene action, both pro­
cesses increase the chance
that an introduced organism
could become an invasor, and
the processes are difficult to
separate.
Dynamics of mutational
effects, adaptive mutation,
and hypermutation
Very few mutations im­
prove the adaptation ability
of an organism, and the great
majority are harmful. In a
recent study Silander et al.
(2007) argue that the muta­
tional effects are dynamic
and not fixed, and that the
938
same mutation occurring in
a poorly adapted individual
is more likely to be bene­
ficial than if it occurs in a
well adapted one. Accord­
ing to Betancourt (2007),
the study of Silander et al.
(2007) suggests that very
small populations (as occur­
ring in bioinvasions), which
tend to accumulate harmful
mutations, will be protected
from the endless accumula­
tion of more harmful muta­
tions by an increasing rate of
beneficial ones. In their work,
Silander et al. (2007) found
that some low-fitness viruses
were able to maintain or even
improve their fitness. Sanjuan
and Elena, 2006) suggested
that mutations might behave
differently in viruses than
in more complex organisms.
The results of Silander et al.
(2007) are consistent with
what has been found in some
studies with more complex or­
ganisms (Betancourt 2007).
The basis of genetics and
t he Ne o -Da r wi n ia n T he ­
or y of evolut ion suggest
that gene mutation occurs
at random and is indepen­
dent of the environment in
which the organism lives.
The discovery of ‘adaptive’
mutation in bacteria shook
the dogma by suggesting the
existence of a new kind of
mutation, one that differed
from spontaneous mutation.
‘Adaptive mutation’ refers
to a collection of processes
in wh ich cells respond to
g row t h-l im iting envi ron­
ments by producing com­
pensatory mutants that grow
well, appa rently violating
fundamental pr inciples of
evolution (Hastings et al.,
2004). In general, this kind
of mutation appea rs to be
induced by stress (Rosen­
berg a nd Hastings, 20 0 4)
and may speed evolution and
invasions. Both the mutation
mechanisms and their con­
trol by stress have remained
elusive. However, Ponder et
al. (2005) provide evidence
that the molecular basis for
stress-induced mutagenesis
in an Escherichia coli model
is error-prone DNA doublestrand break repair.
Denver et al. (2004) have
suggested that a cellula r
stress response in eukaryotes
might provoke hypermuta­
tion in Caenorhabditis elegans. Most of these muta­
tions would surely prove to
be harmful or neutral, but in
isolated cases adaptive mu­
tations would occur, allow­
ing some rare individuals in
stressed populations to flour­
ish (Rosenberg and Hastings,
2004). Undoubtedly, inva­
sion is a stress condition, and
lends support to the idea that
evolution might be hastened
under stress.
Endosymbiosis
Endosymbiosis basically in­
volves the fusion of the entire
genomes of two organisms
and overlaps with horizontal
gene transfer. Syvanen (1994)
considered these to be one
part of the larger phenom­
enon of cross-species gene
transfer, which involves, in
addition to endosymbiotic fu­
sion, the insertion of smaller
genetic regions, including
single genes or even parts of
genes. The mechanisms of
transfer will likely involve a
virus, direct transformation,
conjugation, or another as yet
to be investigated means.
Endosymbiosis is an evolu­
tionary change arising from
the interaction of different
species at the level of the ge­
nomes. As suggested by Ryan
(2006), endosymbiotic virus­
es might offer novel genetic
and genomic complexity that
would make invasion of new
environments more successful.
The most familiar example
of viral-eukaryotic symbiosis
occurs in the parasitoid wasppolydnaviruses interactions,
in which the virus carries the
essential genes required to
suppress the immune system
of the lepidopteran host of the
wasp (Wren et al., 2006). In
many such examples, the viral
genome has been integrated
into the wasp genome. It is
becoming clear that endosym­
biotic unions of viruses and
hosts are far from unusual and
have influenced the evolution
of life throughout most, if not
all biodiversity (Ryan, 2006).
Roossink (Frank P. Ryan, per­
sonal communication) exam­
ined symbiotic viruses that
made grasses more resistant
to drought conditions.
Once viruses enter a ge­
nome, their capacity for evo­
lutionary innovation remains
persistently active and can
interact with newly arrived
exogenous vir uses or with
other genetic components and
regulatory mechanisms, thus
increasing evolutionary plas­
ticity (Lower et al., 1996, cit­
ed by Frank P. Ryan 2006).
Hotopp et al. (2007) found
what seems to be the entire
genome of a parasitic bac­
terium, Wolbachia pipientis,
inserted in the genome of the
fruit fly, Drosophila ananassae. The discovery suggests
that the bacter ial genome
must have provided some sort
of evolutionary advantage to
its host. This species is a ma­
ternally inherited endosymbi­
ont that infects a wide range
of arthropods, including at
least 20% of insect species,
as well as filarial nematodes.
It is present in developing
gametes and passes from one
female to another through in­
fected ova, providing circum­
stances conducive to heritable
transfer of bacterial genes to
the eukaryotic hosts.
Chisholm et al. (1996)
showed that the rhizoids of
the giant alga Caulerpa taxifolia function as roots. Ex­
amination of the rhizoids re­
vealed that the outer surface
is coated with a mixture of
bacteria; the cytoplasm con­
tains large numbers of rodshaped bacteria with the abil­
ity to take up inorganic phos­
phorous and organic nitrogen
from substrata and translocate
nutrient products to the pho­
toassimilatory organs. The
endosymbiosis explains the
alga´s ability to proliferate in
oligotrophic waters.
Transposons
Small packages of DNA
can splice into other sequenc­
es and provide fortuitous op­
portunities for evolutionary
innovations. Transposons
DEC 2008, VOL. 33 Nº 12
seem to appear suddenly in a
genome, copying, cutting and
pasting themselves throughout
its chromosomes (Pennisi,
2007). Transposable elements
might be responsible for some
genomic rearrangements that
could provide an important
substrate for adaptation dur­
ing invasion (Lee, 2002).
Kalenda r et al . (20 0 0)
found in specimens of the
wild ancestor of cultivated
barley (Hordeum spontaneum)
collected in Evolution Can­
yon, Mount Carmel, Israel,
from various microclimates,
that a particular type of ret­
rotransposon, called BARE-1,
is up to th ree times more
abundant in ba rley plants
growing at the canyon rim
than those growing near the
bottom of the canyon. This
suggests that plants at higher
elevations gain more and lose
fewer copies than plants far­
ther down. The authors spec­
ulate that a larger genome,
achieved through the ample
presence of retrotransposons,
may help plants deal with
the more stressful high and
dry areas of the canyon, by
influencing the physiological
machinery that enables the
plant to seek or retain water.
Retrotransposons are a prin­
cipal component of most eu­
karyotic genomes, representing
~40% of the human genome
and 50-80% of some grass
genomes. They are usually
transcriptionally silent but can
be activated under certain sit­
uations of stress. Despite their
considerable contribution to
genome structure, their impact
on the expression of adjacent
genes is not well understood
(Kashkush et al., 2002).
Somatic mutations and mitotic recombination
In the species that mainly
reproduce asexually by frag­
mentation, such as the alga K.
alvarezii, genetic variation can
arise through somatic muta­
tions and mitotic recombina­
tion that can occur through
branch (ramet) replication
and would increase the ge­
netic variation within a clone.
Chapman et al. (2000) re­
veal variable levels of genetic
variation in the clonal weedy
species Pilosella officinarum
(Asteraceae) of New Zealand,
introduced from Europe in the
late 19th century. Somatic re­
combination and somatic mu­
tations contribute to increased
genetic variation and partially
explain why this species is
such a successful invader in
New Zealand.
RNA
Small regulatory RNAs
(microRNAs; siRNAs and
piRNA) can exert regulation
at the transcriptional level,
by affecting chromatin struc­
ture (epigenetic regulation),
or post-transcriptionally, by
affecting mRNA stability
or translation. Animals and
plants have hundreds of dis­
tinct microRNA genes whose
developmental regulatory roles
are most clearly evident in the
small RNAs, as confirmed
by genetic studies in model
organisms (Ambros and Chen,
2007).
Phylogenetic studies sug­
gest that microRNA-based
gene regulation emerged early
during the evolution of both
plants and animals, and in­
dicate that it played a role
in adaptative diversification.
Many microRNAs and their
target interactions appear to
be rapidly evolving, suggesting
an ongoing potential for mi­
croRNAs to drive animal and
plant diversity. Now, one of
the many immediate challeng­
es is to elucidate how small
RNAs mediate the epigenetic
regulation of gene expression
(Ambros and Chen, 2007).
Other Mechanisms
Among several other
mechanisms that increase the
chances of introduced species
becoming invasive, biotic reg­
ulation and purge (Figure 1)
are next examined in detail.
Biotic regulation
Another explanation for
the successful introduction of
some species is given by the
biotic regulation concept (Gor­
DEC 2008, VOL. 33 Nº 12
shkov et al. (2004); www.
biotic-regulation.pl.ru/bre-vers.
htm). According to this con­
cept, species of the natural
ecological community have
collectively evolved restrictions
on their functioning that serve
to stabilize the community as
a whole. Invasive species do
not carry genetic informa­
tion about ecological restric­
tions (Makarieva et al., 2004).
Exotic organisms can be a
source of perturbation acting,
in an uncorrelated manner
with the other organisms, to
prevent the community from
efficiently controlling envi­
ronmental conditions. If this
effect is strong enough, the
local environment of such a
community will begin to dete­
riorate. As soon as the degree
of deterioration becomes sig­
nificant, all inhabitants of the
local ecological community
will lose competitiveness and
alien species will encounter
at least the same conditions as
the other species.
Purge
Often the offspring pro­
duced by the mating of close
relatives are less fit than that
produced by mating of unre­
lated individuals (i.e., inbreed­
ing depression, ID). This is a
common situation in bioinva­
sion, due to the low number
of introduced exotics. This
loss of fitness has been ex­
plained by the increased prob­
ability of expressing deleteri­
ous recessive alleles in the
inbred offspring (the “partial
dominance” model). If most
inbreeding depression is due
to deleterious recessive alleles,
it is possible that the severity
of inbreeding depression can
be diminished if natural se­
lection can purge such alleles
from the population during
inbreeding (Swindell and Bou­
zat, 2006). The influence of
inbreeding on fitness-related
traits in endangered species
and other organisms appears
to be variable over popula­
tions, traits, and environment.
Leeberg and Firmin (2008)
indicate that although purg­
ing is an important process in
many small populations, the
literature contains a diversity
of responses.
An interesting case of in­
breeding, apparently with­
out consequences in fertility,
occurs in the Chillingham
cattle that live in isolation in
a park in northern England.
Although they have been in­
bred for at least 300 years,
the herd remains as fertile as
ever (Visscher et al., 2001),
despite a population crash in
1947 that left only eight bulls
and five cows. DNA analyses
show that the 49-strong herd
is almost a clonal organism,
a fact unprecedented in mam­
mals. Visscher et al. (2001)
indicate that their findings
support the theory that while
inbreeding is on average bad
for a population, it can oc­
casionally result in a viable
population. When combined
with selection, inbreeding may
purge deleterious alleles. This
successful purging probably
happens infrequently, as previ­
ous research suggests that in­
breeding usually does weaken
a population.
At present the herd is fe­
ral, but there may have been
some human help in the gene
purging during domestica­
tion. Hall, cited by E. Young
(2001), indicated that during
domestication genes that tol­
erate inbreeding are selected.
If genes that promote toler­
ance of inbreeding do exist,
tracking them down may be
important for the successful
breeding of small numbers
of endangered species in the
future.
Acknowledgements
The authors thank Frank P.
Ryan, Sheffield South West
Primary Care Trust, Sheffield,
UK, for calling our attention
to the role of endosymbiosis
in bioinvasions.
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