TREE vol. 7, no.
12, December 1992
Interspecific hy&ridization between a
native and an invading plant species, or
two invading species, sometimes results
in a new, sexually reproducing taxon.
Several examples of such taxa have been
confirmed by recent molecular and
isozyme analyses. Further study of these
new taxa, when recognized soon after their
origin, should aim to elucidate the factors
that influence their subsequent establish-
ment and spread, thus leading to a Getter
understanding of the processes that lead to
successfulspeciation.flant hy6rids formed
following a plant invasion provide great
potential for the study of ‘evolution in
action’.
The invasion of new territories by
animals and plants following acci-
dental or deliberate introductions
by man has been much discussed
since Elton raised awareness to the
matter in his book The Ecology of
Invasions by Animals and Plants’.
Recent attention has focused
species that have successfully col-
onized new territories, factors that
promote biological invasions, the
speed with which invasions take
place and the effects of invasions
on indigenous ecosystems2”. Gen-
etic changes in colonizing popu-
lations, due to founder effects, drift
and/or selection, have also been
evaluated’-“. However, the evol-
utionary consequences of inter-
specific hybridization between
invading and native species have
remained, until recently, relatively
neglected. Recent work has high-
lighted the importance of such
interspecific hybridization in cre-
ating evolutionary novelty.
Interspecific hybridization
Despite current interest in plant
invasions, few published floras
contain exhaustive lists of species
judged to be alien (i.e. introduced
by man and now naturalized in the
wild). Hence, it is not normally
possible to determine with any
accuracy the proportion of a local
flora composed of aliens and their
hybrids. A notable exception is
State’s recent New Flora of the
Richard Abbottis at the Division of Environmental
and Evolutionary Biology, School of Biological and
Medical Science, University of St Andrews,
St Andrews, Fife, UK KY 16 9TH.
0 1992. Elsevw Science Publishers Ltd (UK)
Plant Invasions, Interspecific
Hybridization and the Evolution
of New Plant Taxa
British Isles’2, which includes
details of all species believed to
be of alien status, and further, the
hybrids that have formed from
them. Of the 2834 species treated
fully by State, 1264 are judged to
be aliens. Many of these species
are now widespread in the British
isles and can be considered as suc-
cessful invaders.
State also lists 715 hybrids, and
of those known to have been pro-
duced in the British Isles, 70 are
deemed to be products of
hybridization between native and
alien species, 21 between two alien
species, and four between an intro-
duced hybrid and a native species.
In total, approximately 7% of intro-
on duced species have been involved
in the production of interspecific
hybrids now recognized to be part
of the flora of the British Isles, while
approximately 4% of native plants
have hybridized with alien species.
Despite the lack of equivalent
detailed information for other parts
of the world, it has been estimated
that significant percentages of
many regional floras are now com-
posed of aliens 2,3f’3.It is expected
that in these areas, too, such
species should sometimes hybrid-
ize with each other or with native
species.
Most of the interspecific hybrids
found in the British Isles are highly
or completely sterile12. Neverthe-
less, some degree of fertility has
been recorded for approximately
49% of hybrids between a native
and alien species, and 62% of
hybrids between two alien species.
These values are likely to be
underestimates as the fertility of
most of the remaining hybrids has
yet to be determined.
Origin of new plant taxa
Interspecific hybridization is now
accepted as a major mechanism for
generating evolutionary novelty in
the plant kingdom’““. Recent evi-
dence has confirmed that such
hybridization can lead to: (I ) the
introgressive origin of new intra-
Richard J. Abbott
specific taxa, e.g. varieties, ecotypes
and subspecies’8~‘9; (2) the origin of
new fertile homoploid hybrid de-
rivative species2G22 (i.e. species at
the same ploidy level number as
the parents); (3) the multiple origin
of new allopolyploid species2’,24. A
precondition for (I) and (2) is that
the hybrid must exhibit some fer-
tility either as an ability to backcross
to a parent or a capacity to repro-
duce via sib-crossing or inbreeding.
If the hybrid is completely sterile
then (3) remains an option, as does
asexual reproduction.
Backcrossing to one or both par-
ents leads to the infiltration of
genes from one species to another.
Such interspecific gene flow, known
as introgression’4, will result in the
production of offspring that are
clearly referable to one of the par-
ent species, but that possess cer-
tain characters inherited from the
second species. Sometimes, these
products may become stabilized
and develop into new intraspecific
taxa. On the other hand, products
of sib-crossing and/or inbreeding of
the hybrid are more likely to
become stabilized into fertile
homoploid derivative species with a
phenotype either intermediate
between those of the parent
speciesZo or resembling an extreme
variant form of one of the parents25.
Many authors have pointed out
that backcrossing and sib-
crossing/inbreeding of the hybrid
are extremes of what is likely to be a
continuum occurring in hybridizing
populations. Consequently it has
been proposed that the stable
products of these processes, all of
which arise from some level of inter-
specific gene flow, should be treated
as stabilized introgressants26.
Stabilized introgressants
In a recent review of the evol-
utionary consequences of inter-
specific gene flow in plants,
Rieseberg and Wende126 listed 165
proposed cases of introgression, of
which 65 were considered to have
been rigorously documented. In
401
reviews TREE vol. 7, no. 12, December 1992

most cases, introgression was
viewed to have led either to an
increase in genetic diversity within
a species, broken down or rein-
forced reproductive barriers, or
resulted in the transfer or origin of
adaptations. However, in six cases
there was good evidence for the ori-
gin of a new intraspecific taxon or
ecotype, and in a further eight
examples, the origin of a new
species at the homoploid level. The
list produced by Rieseberg and
Wendel was not exhaustive, and
further examples of the origin of
new taxa via introgression
have appeared in the recent litera-
ture’9,27.Some of the best evidence
for the introgressive origin of new
plant taxa comes from studies of the
evolutionary consequences of inter-
specific hybridization involving a
parent or parents of alien origin
(Table 1). Frequently the history of
these events is known, allowing
examination of the factors which
may have favoured the spread of a
new taxon following its origin.
Recent studies on North
American sunflowers (Helianrhhus
spp~)18,21.25
and British ragworts and
groundsels (Senecio sp~.)‘~,*~are of
particular note in this respect.
Helianthus annuus occurs both in
the wild type form and as a weed
throughout much of North America.
Wild type H. annuus - the progeni-
tor of the domesticated sunflower28
- is believed to be indigenous to
the Great Plains of the Mississippi
River, but has since been intro-
duced elsewhere*‘. Following its
introduction to other parts of the
USA, it has hybridized with other
sunflower species that are either
native to the region or introduced
along with H. annuuS?O. As a conse-
quence, H. annuus has acquired
genes that may have enabled it to
adapt rapidly to the new con-
ditions it has encountered, and in
at least one case, the process has
led to the origin of a stabilized
introgressant form of H. annuus.
Morphological and cytological evi-
dence3’ suggests that the sub-
species H. annuus ssp. texanus
originated in Texas following intro-
gression of genes from native H.
debilis ssp. cucumerifolius into H.
annuus. Recent molecular evi-
dence18 supports this hypothesis,
showing that 13 of 14 populations
of H. annuus ssp. texanus sur-
veyed possessed chloroplast DNA
(cpDNA) and/or nuclear ribosomal
DNA (rDNA) markers diagnostic of
H. debilis ssp. cucumerifolius.
Helianthus annuus is believed to
have been introduced to Texas by
native North Americans; however,
historical details are lacking in
regard to the date of origin of H.
annuus ssp. texanus and its sub-
sequent spread throughout the
north-eastern part of the State. In
contrast, such information is avail-
able in regard to the recent origin
and spread in Britain of an intro-
gressant radiate form of the com-
mon groundsel, Senecio vulgaris
var. hibernicus. The radiate variant
of groundsel differs from the more
common nonradiate form, S. vul-
garis var. vulgaris, in that it pro-
duces flower heads (capitula) with
ray florets in addition to the disc
florets produced by var. vulgaris.
The difference in capitulum type
results from allelic variation for a
single gene which controls pres-
ence/absence of ray florets”.
Radiate groundsel was first col-
lected from the wild in 1832 from
wasteground in Oxford following
the reported escape in 1794 of the
alien radiate species, Senecio
squalidus (Oxford ragwort), from
the nearby Oxford Botanic Garden”
(Fig. I ). The escape of S. squalidus
occurred after its introduction to
the Garden from Sicily towards the

Table 1. Plant taxa produced following a plant invasion and subsequent interspecific hybridization”

Hybrid taxon Parent taxa Location Evidenceb Reference

Stabilized introgressants
Intraspecific taxa Helianthus annuus H. annuus* x H. debilis Texas, USA m,c,cpDNA,rDNA 18,31
ssp. texanus ssp. cucumerifolius

Senecio vulgaris S. vulgaris var. vulgaris UK m,c,as,i 19,35

var. hibernicus x S. squalidus*

Species Helianthus anomalus Texas, USA m,c,cpDNA,rDNA 25

H. deserticola H. annuus* x H. petiolaris* Texas, USA m,c,cpDNA,rDNA 25
H. paradoxus Texas, USA m,c,i,cpDNA,rDNA 21.25

Iris nelsonii I. brevicaulis*, I. fulva*, Louisiana, USA m,c,i 22

I. hexagona*

Allopolyploids
Species Senecio cambrensis S. vulgaris x S. squalidus* North Wales and m,c,as,i,rDNA 24,45
Edinburgh, UK
Spartina anglica S. alterniflora* x S. maritima UK m,c,i 42

Tragopogon mirus T. dubius* x T. porrifolius* Washington and m,c,i,rDNA 23,40,41

Idaho, USA
Tragopogon miscellus T. dubius* x T. pratensis* Washington and m,c,i,cpDNA,rDNA 23,40,41
Idaho, USA

aOnly examples confirmed by isozyme and/or molecular analysis are included.

bm, morphological; c, cytological; as, artificial synthesis; i, isozymes; cpDNA, chloroplast DNA; rRDA, nuclear ribosomal DNA.
*Invading species.

402
TREE vol. 7, no. 12, December 7992

(a) (b)

end of the 17th century32,33. Since

then, S. squalidus has spread
rapidly to many parts of the British
Isles (Fig. I ) and is now often found
growing with S. vulgaris on open,
disturbed sites, particularly in
urban areas. Hybrids (S. x baxteti),
are formed between S. vulgaris and
S. squalidus at low frequency in the
wild34, with S. vufgaris acting as the
maternal parent35. Hybrids are
highly sterile, but may backcross to
S. vulgaris.
Evidence for an introgressive ori-
gin of S. vulgaris var. hibernicus
(2n = 40) following hybridization
between S. vulgaris var. vulgaris
(2n = 40) and S. squalidus (2n = 20)
is based on: (I) the parallel spread
of S. squalidus and S. vulgaris var.
hibernicus in Britain over the past
160 years (P.C. Crisp, unpublished
PhD thesis, University of London,
1972); (2) artificial synthesis
tetraploid plants bearing a close
of w (4
resemblance to var. hibernicus fol- s. w/galis s. 5-quskius
lowing backcrossing the triploid ncwadiate radiite
(2n = 40) (2n = 20)
hybrid to var. vulgaris35; and (3) the
occurrence of an allozyme marker
allele at an intermediate frequency
in S. vulgaris var. hibernicus, which s. x bsxtefi
is absent from populations short radiate
(2n = 30)
monomorphic for S. vulgaris var.
vulgaris but present at high fre-
quency in S. squalidus’g.
As well as confirming the origin B&CCrosS S. cambrensis
short-radiate radiate
of new intraspecific introgressant (2n = c40) (2n = 60)
taxa, molecular and isozyme stud-
ies have provided strong evidence
for the recent origin in North
America of three new homoploid
Fullyradiate
hybrid species in the genus segregant
Helianthus - H. anomalus, H. (2n = 40)
vulgar/s. var. Mbemkus
deserticola and H. paradoxus -
following invasion of new places
and hybridization between H.
annuus and H. petiolaris2’,25 (Table Fig. I. (a,b) Specimens of Senecio squalidus cultivated at the Oxford Botanic Gardens Ibulk-eye in (c)I
I). Each of these three Helianthus in the late 17th century following the introduction of the species from Sicily. The material shows wide
hybrid species occupies habitats variation in leaf form as does wild material in the British Isles today. (c) Current distribution of S.
squalidus in the British Isles. (d) Postulated pathway of the origin of the stabilized introgressant S. vu/-
which differ from each other and gads var. hibernicus and the allopolyploid S. cambrensis’9,2”,~5,45 405
also from those of the parents, and
in the case of H. paradoxus there is
circumstantial evidence that the in frequency following the spread bility of a single origin, subsequent
species originated in Texas within of the parental species into open, founder effects and genetic drift),
the past 50 years. A further ex- disturbed habitats created by newly formed stabilized introgress-
ample of the hybrid origin of a fer- man. Molecular and isozyme stud- ant taxa are expected to have
tile homoploid derivative species, ies have so far failed to reveal reduced genetic diversity relative
supported by isozyme analysis, is multiple origins for any of these to the parent species, and this has
that of iris nelsonii2? produced fol- new hybrid species, despite (in been confirmed for S. vulgaris var.
lowing hybridization between /. the case of Helianthus species) hibernicu?‘, H. anomalus, H.
brevicaulis, 1. fulva and I. hexagona extensive surveys of cpDNA and desertkola and H. paradoxus25.
in southern Louisiana, USA. In this rDNA variation on both parental Allelic diversity is likely to be
particular case natural hybridiz- and derivative species. increased in the introgressant only
ation is thought to have increased For several reasons (the possi- at certain loci where different
403
reliefs
alleles in the two or more parents
become combined and sub-
sequently maintained via linkage
and/or selection in the new taxon.
Once created, the stability of the
gene complexes of a
introgressant taxon will depend
greatly on mechanisms preventing
recombination and segregation. In
the Helianthus hybrid species, and
possibly Iris nelsonii, this appears
to have been accomplished
‘recombinant speciation”7, i.e. the
establishment of a new chromo-
some arrangement following re-
combination of two or more distinct
arrangements that distinguish the
parental species. The new recom-
binant types are fertile inter se, but
at least partially sterile with both
parents.
Strong ‘internal’ reproductive
barriers between an intraspecific
introgressant taxon and its parental
taxon are unlikely to occur to the
same degree, but should not be
ruled out. In Senecio vulgaris, the
introgressant radiate taxon var.
hibernicus is only found in the
wild, as a component of stands with
nonradiate var. vulgaris. Both vari-
ants reproduce by predominant
self-fertilization’7; however,
level of intervariant crossing is such
that the two variants might be ex-
pected to have a common genetic
background and be differentiated
only by capitulum type. In fact, the
two variants also differ for certain
allozyme traits’9,36 (controlled by
genes unlinked to the locus con-
trolling capitulum type) and sev-
eral life history characters’8”9.
Consequently, it has been argued
that a ‘coadapted’ complex of
genes may have been introgressed
into S. vulgaris from S. squalidus,
and is currently maintained in var.
hibernicus due to the reduced fit-
ness of progeny produced from
crosses with var. vulgariP.
Allopolyploids
Within the last century four new
allopolyploid species have orig
inated in the wild: two in North
America (Tragopogon mirus and T.
miscellus4°,4’); and two in Britain
(Spartina anglica42 and Senecio
cambrenwY4) (Table I). In the two
Tragopogon species, each origin
followed hybridization between
Tragopogon species introduced
from Europe. In contrast, both new
404
British allopolyploids are products
of hybridization between a native
and an introduced species.
Each new allopolyploid species
was identified soon after its origin
new and thus it has been possible to
document the establishment and
spread of each species up to the
present. Isozyme evidence sug
gests there was a single origin of S.
anglica in Britain and that genetic
by diversity has remained virtually
absent in the species despite its
current wide distribution42. In con-
trast to S. anglica, the geographical
distributions of the other new
allopolyploids are much more
restricted; however, there is evi-
dence in each case that the species
are spreading4’,44, and that this has
been aided by multiple origins
of the allopolyploids following
hybridization between parental
species at different locations.
Restriction analysis of chloroplast
DNA and rDNA has revealed at
least two independent origins of T.
mirus and two origins of i7 miscel-
Ius in the Palouse region of eastern
Washington, USA”. lsozyme and
cpDNA data have identified at
least two independent origins for
the S. cambrensis, one in North Wales
and one in Edinburgh24r45.Whereas
T. miscellus, which is more abun-
dant than T. mirus, has spread to
locations beyond the range of at
least one of its diploid progeni-
tor.+, both T. mirus and S. cam-
brensis are normally found only at
sites where both parent species
occur.
Marked fluctuations in popu-
lation size are common in all three
species involving episodes of local
extinction and extensive recolon-
ization. Under such conditions, an
ability to originate in a repetitive
fashion provides insurance against
extinction, particularly during the
early phase of establishment.
Moreover, multiple origins may
increase the amount of genetic
diversity sampled from the par-
ental species, which might explain,
in part, the greater level of allelic
diversity found in T. mirus, T mis-
cellus and S. cambrensis relative to
S. anglica.
Conclusions
Recent studies have confirmed
that interspecific hybridization fol-
lowing plant invasions may some-
TREE vol. 7, no. 12, December 1992
times lead to the rapid evolution of
new plant taxa - i.e. either stabil-
ized introgressants or allopoly-
ploids. If recognized soon after
their origin, further study of these
new taxa can provide an under-
standing of the factors which influ-
ence their establishment and
spread, and thus in certain cases
the processes which lead to suc-
cessful speciation. (For a discussion
of the factors likely to affect the ori-
gin, establishment and persistence
of polyploid plants, see the recent
TREE review by Thompson and
Lumaret46.) Such material also pro-
vides model systems for the
assessment of risks associated with
hybridization and the release of
genetically engineered organisms
into the environment47. In view of
the obvious advantages that this
material holds for the study of
evolutionary processes, it can be
expected that its further analysis
will lead to significant improve-
ments to our current understanding
of how plants evolve in the wild.
Acknowledgements
I thank Clive State for providing me with a
breakdown of the number of native and
alien species included in his New Flora of
the British Isles, Serena Marner for slides of
specimens of Senecfo squalidus from the
historic collections of the Fielding-Druce
Herbarium, Chris Preston for a map of the
current distribution of S. squalidus in the
British Isles, and Christophe Thebaud for
comments on an earlier draft of the manu-
script.
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Bioscience 40, 438-442
Parasites and Sex:
Richard J. Ladle
thus may suffer from increased lev-
els of parasitic exploitation. The
Red Queen hypothesis, therefore,
relies on parasites adapting to the
most common host resistance geno-
types, thereby generating a selective
disadvantage against becoming or
remaining common that is sufficient
to outweigh the inefficiency of sex.
As Red Queen computer simu-
lations9s’2,‘3have become increasingly
sophisticated and their assumptions
more realistic (see Box I), the
hypothesis has become widely
accepted as a leading contender for
the maintenance of sex’4,‘5. The Red
Queen hypothesis predicts that
species should most frequently be
sexual when they occupy biotically
diverse (saturated) habitats, com-
pete with members of their own
species and compete by contest
rather than simply by fecund breed-
ing13. A wealth of comparative evi-
dence supports these predictions -
they appear very accurate with
respect to the ecological distribution
of asexuality3. However, they are
almost identical to the predictions of
the most convincing alternative
405