Homoploid hybrid speciation in action
Author(s): Richard J. Abbott, Matthew J. Hegarty, Simon J. Hiscock and Adrian C.
Brennan
Source: Taxon, Vol. 59, No. 5 (October 2010), pp. 1375-1386
Published by: International Association for Plant Taxonomy (IAPT)
Stable URL: http://www.jstor.org/stable/20774035
Accessed: 20-03-2017 12:48 UTC
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TAXON 59 (5) October 2010: 1375-1386 Abbott & al. Homoploid hybrid speciation
Homoploid hybrid speciation in action
Richard J. Abbott,1 Matthew J. Hegarty,2 Simon J. Hiscock3 & Adrian C. Brennan1
1 School of Biology, University of St Andrews, St Andrews, Fife, KYI 6 9TH, U.K.
2 Institute of Biological, Environmental & Rural Sciences, Aberystwyth University, Penglais, Aberystwyth, Ceredigion, SY23 3DA, U.K.
3 School of Biological Sciences, University of Bristol, Bristol, Somerset, BS8 1UG, U.K.
Author for correspondence: Richard J. Abbott, rja@st-andrews.ac.uk
Abstract Homoploid hybrid speciation is the origin of a hybrid species without change in chromosome number. Although
currently thought to be a rare form of speciation, especially relative to the more common allopolyploid hybrid speciation, it is
feasible that many examples of homoploid hybrid species will be discovered in the future now that genetic resources are readily
available for testing their occurrence. In this review, we focus on the speed of homoploid hybrid speciation, the importance of
ecological and spatial isolation in the process, and the nature of genetic changes that occur in a new hybrid during its origin and
establishment in the wild. With reference mainly to the extensive work carried out on homoploid hybrid species of Helianthus,
and to our own work on the very recently originated diploid hybrid species Senecio squalidus, we review evidence showing:
(1) that new fertile homoploid hybrid species can originate very quickly, although a longer period is likely to be required before
the species becomes fully stabilized both genomically and phenotypically; (2) ecological divergence of the hybrid species from
its parents is key to successful establishment, and that this can occur even in the absence of post-zygotic isolation caused by
chromosomal and/or genetic sterility barriers; (3) transgressive changes in phenotypic traits and gene expression are of great
importance in adapting homoploid hybrid species to habitats that are ecologically and spatially divergent from those of the
parents; (4) adaptive differences distinguishing a homoploid hybrid species from its parental species are likely to be maintained
in the face of parental gene flow, and evolve in concert across populations representing multiple origins of the species; (5) in the
absence of parental gene flow, i.e., under conditions of geographical isolation, rapid genetic divergence of the hybrid species
is likely to be enhanced due to the combined effects of founder events, genetic drift and selection.
Keywords ecological divergence; gene flow; homoploid hybrid species; hybridization; speciation; transgressive gene
expression
INTRODUCTION
Homoploid hybrid speciation is the origin of a hybrid spe
cies without change in chromosome number. It contrasts with
the more frequent allopolyploid hybrid speciation in which
there is whole genome duplication with diploid chromosome
numbers of the two parent species being summed in the hybrid
species. In his book Plant Speciation, Grant (1981) described
two ways in which a homoploid hybrid species could originate
without loss of sexual reproduction. The first of these required
the hybrid species to be isolated from its parents by a chro
mosomal or genie sterility barrier and because of the genetic
mechanisms involved was named "recombinational specia
tion". The second required the hybrid to be isolated by what
Grant termed an external isolating mechanism, such as habitat,
ethological (behavioural) or geographical (spatial) isolation.
Whereas Grant devoted one chapter of his book to describe the
process of recombinational speciation, he devoted only a sec
tion of one chapter to homoploid hybrid speciation that relied on
external isolating mechanisms. Thus, although it may not have
been Grant's intention, his greater focus on recombinational
speciation tended to promote a perception that recombinational
homoploid hybrid speciation was more important than eco
logical or spatial isolation between the hybrid and its parents.
However, subsequent reviews of the incidence and process of
homoploid hybrid speciation in plants by Rieseberg (1997) and
Gross & Rieseberg (2005) have made clear that ecological and
spatial isolation are vital to the successful origin and establish
ment of a homoploid hybrid species and can enable the proc
ess to occur even in the absence of intrinsic isolation due to
chromosomal or genie sterility barriers (Buerkle & al, 2000).
Indeed, homoploid hybrid speciation is unlikely to occur unless
there is at least some ecological and spatial isolation between
the hybrid and its parent species (Buerkle & al, 2000).
The most extensive and detailed empirical work conducted
on the process of homoploid hybrid speciation is that on three
diploid hybrid species of sunflower (Helianthus), which origi
nated in North America following hybridization between
K annum and H. petiolaris (Rieseberg, 1991). The three spe
cies?H. anomalus, H. deserticola and H. paradoxus?are
estimated to have originated between 60,000 to 200,000 years
ago and are reproductively isolated from their two parents by
chromosomal and ecological barriers (Rieseberg & al, 2003).
Each of these hybrid species occurs in a habitat that is dis
tinct from the two other hybrid species and from each parent
species (Gross & Rieseberg, 2005). Thus, whereas the parent
species, H. annum and H. petiolaris, occur on mesic clay and
drier sandy soils, respectively, the hybrid species, H. anomalus,
H. deserticola and H. paradoxus, are restricted to active sand
dune, arid desert, and desert salt marsh habitats, respectively.
Another classic example of homoploid hybrid speciation often
cited in the literature concerns the origin of Iris nelsonii. This
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Abbott & al. Homoploid hybrid speciation TAXON 59 (5) October 2010: 1375-1386
example is particularly intriguing in that three rather than two
different diploid Iris species are thought to be involved as par
ents in its origin. Again, there is evidence that this species is
reproductively isolated from its putative parents by ecological
barriers (Arnold & al, 1990), and the species is thought to have
originated relatively recently, possibly following a breakdown
of ecological barriers between its parent species due to hu
man activities. However, there remains a question mark over
whether Iris nelsonii is indeed a diploid hybrid species as the
genetic evidence (Arnold, 1993) is not yet conclusive on this
point.
In addition to these examples, there is a growing list of
other recorded homoploid hybrid species, including cases in
animals (fish, insects and birds) and fungi, as well as in plants
(Gross & Rieseberg, 2005; Mallet, 2007). Although homo
ploid hybrid speciation is still regarded as rare, particularly in
comparison to allopolyploid speciation in plants, it is nonethe
less an important mechanism and further examples of species
originating by this process are likely to be discovered now
that genetic resources are widely available for testing their
occurrence.
In this review, we shall focus on how quickly the process
of homoploid hybrid speciation takes to complete and secondly
on the nature of changes that occur in the hybrid during the
process. Nolte & Tautz (2010) have recently emphasized the
need to focus on genetic changes occurring in the initial stages
of hybrid speciation, so as to obtain a more complete under
standing of the process. Where relevant, we shall discuss recent
work we have conducted on the diploid (In = 20) hybrid species
Senecio squalidus (Oxford ragwort; Asteraceae). This species
is of special interest in that it represents a unique example of
recent ecogeographic homoploid hybrid speciation facilitated
by spatial isolation following human-mediated introduction of
material from a hybrid zone between S. aethnensis and S. chry
santhemifolius on Mount Etna, Sicily, to the Oxford Botanic
Garden in Britain (Abbott & al, 2000; Harris, 2002; James
& Abbott, 2005). This new species is highly invasive and has
rapidly spread through a large part of Britain and into Ireland
Table 1. Characteristics of Senecio squalidus and Helianthus hybrid species relevant to their origin and establishment.
S. squalidus H. anomalus H deserticola H paradoxus
Parent species
Age (years)
Number of origins
Invasiveness
S. aethnensis and
S. chrysanthemifolius
200-300
Once
H annuus and
H. petiolaris
116,000-160,000
Possibly three times
Highly invasive?spread Non-invasive?only few
throughout much of British populations known
Isles
H annuus and
H. petiolaris
63,000-170,000
More than once
Non-invasive?only few
populations known
H annuus
and H petiolaris
75,000-208,000
Once
Non-invasive?only few
populations known
Annual to short-lived
perennial
Life cycle
Mating system
Reproductive isolation from parent species
Outcrossing?strong
self-incompatibility
Spatial Allopatric to parents;
native to Britain & Ireland
-2000 km from parents on
Mount Etna, Sicily
Annual
Outcrossing
Parapatric to parents in
Utah & Arizona, U.S.A.
Annual
Outcrossing
Paraptric and allopatric to
parents in Arizona, Nevada
& Utah, U.S.A.; allopatric
populations are geographi
cally close to parent species
Annual
Outcrossing
Parapatric to parents in New
Mexico & Texas, U.S.A.
Ecological
Intrinsic
Grows in temperate cli
mate?possibly intermedi
ate to that of parents
Reduced fitness in F2 hy
brids indicates some genie
incompatibilities
Adapted to active sand dune Adapted to arid desert
habitat?an extreme habitat habitat?an extreme habitat
relative to parent habitats relative to parent habitats
Predominantly
chromosomal
Predominantly
chromosomal
Adapted to desert salt marsh
habitat?an extreme habitat
relative to parent habitats;
flowers later than parent
species
Predominantly
chromosomal
Information on Helianthus species was extracted from Schwarzbach & Rieseberg (2002), Welch & Rieseberg (2002), Gross & al. (2003), Gross &
Rieseberg (2005), Lai & al. (2005).
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TAXON 59 (5) October 2010: 1375-1386 Abbott & al. Homoploid hybrid speciation
since its origin (Abbott & al, 2009). Senecio squalidus and its
parental species, S. aethnensis and S. chrysanthemifolius, are
all self-incompatible (SI) (Abbott & Forbes, 1993; Hiscock,
2000), but are highly interfertile without disruption of SI func
tion in hybrids (Chapman & al, 2005; Brennan & al, unpub.).
Thus, advanced-generation synthetic hybrids can be produced
by controlled crossing experiments (Hegarty & al, 2009). Con
sequently, it is feasible to study genetic and phenotypic changes
that occur among synthetic hybrids following a cross, and to
make comparisons between these hybrids across generations
and between S. squalidus and its two parents. Because of its
very recent origin, S. squalidus represents a fascinating case
study of ecogeographic homoploid hybrid speciation 'in action'.
A comparison of similarities and differences between S. squal
idus and Helianthus hybrid species that are relevant to their
origins and establishment in the wild is provided in Table 1.
DEFINITION OF HOMOPLOID HYBRID
SPECIES
Before embarking on a discussion of the process of hybrid
speciation, it is important to define what homoploid hybrid
species are. We follow Rieseberg (1997) in basing our defini
tion on Mayr's biological species concept (Mayr, 1942), which
despite its shortcomings (see for example Mallet, 2008) re
mains the most widely accepted of the various species concepts
recognized (Coyne & Orr, 2004). Thus, we define homoploid
hybrid species as groups of interbreeding natural populations
of homoploid hybrid origin that are reproductively isolated
from other groups of interbreeding populations including those
representing the parent species. Reproductive isolation between
the hybrid species and other species may involve any combina
tion of pre- and/or post-zygotic breeding barriers. It is worth
noting that our definition is unaffected by the relative portions
of each parent species' genome present in a hybrid species.
Thus, some hybrid species that are reproductively isolated from
their parents may have originated as a result of only a few genes
being introgressed from one species to another (Jiggins & al,
2008), whereas in other hybrid species reproductive isolation
might, in part, be based on recombination of large portions of
the genomes of each parent species (Rieseberg & al, 2003). It
is often considered that a test of the biological species concept
is that species will maintain their integrity in sympatry (Coyne
& Orr, 2004), which for many allopatric species cannot be
determined unless transplant experiments are undertaken (Ab
bott & al, 2008; Sobel & al, 2010). However, as Sobel & al.
(2010) point out, if allopatric species are adapted to their local
environments, then they are ecologically as well as geographi
cally isolated from each other, and are expected to be mutually
excluded from each other's habitats. Thus, we propose that
even hybrid lineages that originated and became established in
geographical isolation from their parents, as for example was
the case for Senecio squalidus (see above), can legitimately be
regarded as homoploid hybrid species in the absence of strong
postzygotic barriers, if they are ecologically as well as geo
graphically isolated from their parents.
THE PROCESS OF HOMOPLOID HYBRID
SPECIATION
Speed of origin. ? Some of the earliest work on homo
ploid hybrid speciation investigated whether it was possible to
generate synthetic, fertile and viable homoploid hybrids that
were intersterile with both parents, thus providing a test of the
recombinational model of hybrid speciation. Stebbins (1957)
and Grant (1966a,b) showed that this could be achieved in the
plant genera Elymus and Gilia, respectively, and because they
generated such hybrids within a few generations of the original
cross, it seemed that homoploid hybrid speciation could be
a very rapid form of speciation in the wild. Confirmation of
this hypothesis has come from what is undoubtedly the most
thorough and detailed attempt to re-synthesise artificially an
existing homoploid hybrid species, namely Helianthus anoma
lus, from a cross between H. annum and H. petiolaris (Riese
berg & al, 1996). By modifying the pattern of backcrossing
and intercrossing of hybrids in each generation, three different
fertile hybrid lineages were produced by the F5 generation that
were partially intersterile with both parent species. Remark
ably, these advanced-generation hybrids were morphologically
and genetically similar to each other and to the wild form of
H. anomalus, and contrasted with the wide morphological and
genetic variation that was present among the earlier-generation
hybrids.
All three of the above studies have several features in
common. Plants were raised under controlled glasshouse con
ditions, and in each case ?x hybrids were highly sterile. Selec
tion was imposed either intentionally or unintentionally for
the most fertile plants to act as parents of the next generation,
although in no instance was there selection for plants showing
intersterility with parental species. Rather, the latter evolved
as a side-effect during the experiment. It was concluded that in
each case the origin of intersterility between fertile advanced
generation hybrids and parent species was due to recombination
of chromosomal rearrangements and/or genie sterility factors
that distinguished the parent species. Thus, the results of these
experiments supported the hypothesis that recombinational
speciation is a mechanism that can lead to the rapid origin of
a new homoploid hybrid species.
Computer simulation studies of the conditions that pro
mote homoploid hybrid speciation have also indicated that the
process is rapid (McCarthy & al, 1995; Buerkle & al, 2000).
Moreover, a study of the rate of speciation of H. anomalus
based on the size of parental species chromosomal blocks in
the hybrid species, suggested that//, anomalus originated in the
wild in less than 60 generations (Ungerer & al, 1998). However,
a more recent analysis of the rate of genome stabilization in
all three homoploid hybrid species of Helianthus, suggests that
the process may take much longer to complete than previously
thought (Buerkle & Rieseberg, 2008). Buerkle & Rieseberg
(2008) concluded from their analysis that although "segregating
factors that contribute to initial ecological or intrinsic isolation
may become stabilized quickly. The remainder of the genome
likely becomes stabilized over a longer time interval, with re
combination and drift dictating the contributions of the parental
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Abbott & al. Homoploid hybrid speciation TAXON 59 (5) October 2010: 1375-1386
genomes." This seems to mark an important advance in fully
understanding homoploid hybrid speciation in that in many
cases it might be expected that during the initial stages of the
process the entity recognised as a new hybrid species might
be phenotypically and genetically highly variable, but over the
course of many further generations becomes more stable in
form as it becomes less variable in phenotype and genotype.
Only three homoploid hybrid species are known to have
originated in the very recent past, thus enabling their origin and
establishment in the wild to be assessed as an ongoing proc
ess. These are Senecio squalidus, which originated in Britain
within the past 200 to 300 years (Harris, 2002; James & Abbott
2005), the 'Lonicera fruit fly' (a Rhagoletis hybrid species)
thought to have originated in North America in the last 250
years (Schwarz & al, 2005), and the 'invasive sculpin' (a Cot
tus hybrid species) first reported in 1992 in riverine habitats of
the Rhine drainage in the Netherlands and Germany (Nolte &
al, 2005). It is notable that leaf shape in S. squalidus is highly
variable ranging from highly dissected to serrate (Fig. 1).
This variation is not as extreme as that observed between the
highly dissected and entire leaf shapes of the parent species,
S. chrysanthemifolius and S. aethnensis, respectively (Fig. 1),
but indicates that S. squalidus may be at an early stage in its
eventual stabilization and that over time might become less
variable in form.
Ecological divergence during homoploid hybrid specia
tion. ? The successful production by Rieseberg & al. (1996)
of synthetic hybrids that resembled both morphologically and
genomically the wild homoploid hybrid species, H. anomalus,
was highly informative of the pattern and pace of structural
genomic and genetic changes that can occur during recombina
tional hybrid speciation. It was concluded from this study that
selection in the glasshouse for increased fertility in a hybrid
lineage could produce a recombined genome very similar in
structure to that of a wild homoploid hybrid species. However,
the study did not take into account the importance of ecological
divergence during homoploid hybrid speciation and the type of
genetic changes that can bring this about.
Although it has been noted that all homoploid hybrid spe
cies appear to be ecologically divergent from their progenitors
(Gross & Rieseberg, 2005), it is seldom clear whether such
divergence originated at the time of origin of a species and
was crucial to the process, or whether it evolved after the hy
brid species formed and became established as a stable entity.
Only in situations where the process is studied 'in action', i.e.,
in the wild where a new homoploid hybrid species has been
discovered immediately following its origin, or in experiments
where newly produced hybrid offspring of the progenitors of a
homoploid hybrid species are examined, is it likely to be pos
sible to test the hypothesis that ecological divergence arises
during homoploid hybrid speciation and is an essential feature
of the process. The best experimental evidence available on this
currently comes from studies on sunflowers.
Two similar experiments have been conducted on the
origin of ecological divergence in the homoploid hybrid spe
cies, H. paradoxus and H. deserticola. In each case, seedlings
of one of the hybrid species and its two parents, H. annuus
and H. petiolaris, together with seedlings of a large family of
second-generation backcrossed (BC2) plants, derived from a
cross between the two parental species, were planted in the
habitat of the hybrid species. Thus in the case of H. paradoxus
the experiment was conducted in a natural saltmarsh (Lexer
& al, 2003b), while for H. deserticola it was conducted in an
arid 'desert floor' habitat (Gross & al, 2004). In both studies,
it was shown that the hybrid species exhibited particular traits
of adaptive significance in the hybrid species' habitat that were
not exhibited by either parent species. Most importantly, it
was shown that variation in these traits among BC2 individuals
overlapped that exhibited by the hybrid species, and that the
strength of phenotypic selection acting on these traits would
move the BC2 population toward the hybrid species phenotype.
These results are consistent with the hypothesis that transgres
sive segregation in the offspring of hybrids between these two
particular parental species can quickly generate morphological,
anatomical, life history and physiological traits that enable
some offspring to occupy habitats very different from those
of the parents. Thus, the parental species are excluded from
these novel habitats and the hybrid species becomes established
because it is ecologically and spatially isolated from its parents
and, therefore, reproductively isolated from them.
In the case of H. paradoxus, further analysis of the BC2
family isolated several quantitative trait loci (QTLs) affecting
mineral uptake traits, while other QTLs were shown to affect
survival (Lexer & al, 2003a). Some of the mineral uptake QTLs
mapped to the same genomic locations of QTLs for survivor
ship, including a candidate salt tolerance gene that was later
found to map to the location of a QTL affecting mineral uptake
(Lexer & al, 2004). In this and other studies of homoploid
hybrid species of Helianthus (Rieseberg & al, 2003), it has
been shown that many of the QTLs that combine to influence
a trait of adaptive significance in the hybrid species normally
show effects in opposing directions. When traits exhibit this
kind of genetic architecture in parent species, segregation of
parental QTL alleles after hybridization produces variable and
transgressive trait phenotypes among hybrid offspring with the
potential for rapid evolution (Rieseberg & al, 2003). Rieseberg
& al. (2003) were able to demonstrate that complementary gene
action created extreme phenotypes in synthetic hybrids that
matched those of wild hybrids and, most importantly, showed
that the combinations of parental chromosomal segments that
occurred in the ancient hybrids were the same as those required
to generate synthetic hybrids of similar extreme phenotype.
These studies clearly demonstrate the vital role of ecological
divergence and selection as part of the initial stages of homo
ploid hybrid speciation.
Although the genomes of sunflower homoploid hybrid
species comprise large portions of the genomes of each par
ent species (Rieseberg & al, 2003), it is also true that in other
homoploid hybrid species ecological divergence and reproduc
tive isolation from parent species can be dependent on only a
few genes introgressed from one parent to the other (Jiggins &
al, 2008). Thus, in the butterfly genus Heliconius, the homo
ploid hybrid species, H. heurippa, has a wing colour pattern
causing assortative mating and, in turn, reproductive isolation
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TAXON 59 (5) October 2010: 1375-1386 Abbott & al. Homoploid hybrid speciation
from its parent species, H. melpomene and H. cydno (Jiggins
& al, 2008). A colour pattern very similar to that of H. heu
rippa is easily recreated in synthetic hybrids between the same
parent species by combining a few genes of major effect in
the hybrids that encode the discrete wing colour patterns of
the parent species. The colour pattern that closely matches
that of H. heurippa is only expressed against a H. cydno ge
netic background and was obtained after three generations of
backcrossing synthetic hybrids to this species (Mavarez & al,
2006). Jiggins & al. (2008) predict that in cases such as this
where only a few introgressed genes are required to produce
a new homoploid hybrid species, it will be difficult to identify
the species as hybrid unless the introgressed 'speciation genes'
are themselves examined directly. This is because, at other
loci, the hybrid species might not differ genetically from the
introgressed parent.
Fig. 1. Top panel, Leaf shape variation between Senecio chrysanthemifolius (first row), S. squalidus (second row) and S. aethnensis (third row).
The centre-most primary stem leaf of glasshouse-grown plants was sampled soon after flowering had started. Leaf perimeter to area ratios were
measured for 32 to 45 individuals per species and leaves representing the 0.05,0.25,0.50,0.75, and 0.95 quantiles are presented. Bottom panel,
Leaf shape variation among a sample of individuals from a large population of S. squalidus in Edinburgh, Scotland.
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Abbott & al. Homoploid hybrid speciation TAXON 59 (5) October 2010: 1375-1386
The findings of the butterfly work fit the genie view of
speciation (Wu, 2001), which states that reproductive isola
tion between species is controlled by a moderate number of
individual genes rather than the entire genome. It is likely that
the butterfly example represents one extreme of a continuum
in relative proportions of each parent's genome represented
in a homoploid hybrid species and required for ecological di
vergence and reproductive isolation (Jiggins & al, 2008). The
other extreme is represented by sunflower homoploid hybrid
species where ecological divergence and reproductive isolation
is based on a combination of many different blocks of genome
derived from each parent species.
Multiple origins. ? When ecological divergence is an
important driver of speciation it is possible that new species
might originate recurrently (Schluter, 2000,2009), and there is
evidence that this may have occurred in at least four homoploid
hybrid species?Argyranthemum sundingii (Brochmann & al,
2000; Borgen & al, 2003), Helianthus anomalus (Schwarzbach
& Rieseberg, 2002), K deserticola (Gross & al, 2003) and
Pinus densata (X.-R. Wang & al, 2001; Song & al, 2003),
although Gross & Rieseberg (2005) point out that the evidence
in support is not yet full-proof for any of these examples. If
a homoploid hybrid species has originated more than once, it
raises the issue of whether the differently originated lineages
will evolve independently of each other or in concert thereafter.
A study on H. deserticola by Gross & Rieseberg (2007) sug
gests that populations of this species representing different ori
gins of the species have evolved mainly in concert as some loci
show "putative selected sweeps across the species range with
the same allele fixed in each population". Whether concerted
evolution of this type is true for all homoploid hybrid species
that have originated recurrently remains to be demonstrated.
Changes in quantitative traits. ? Detailed comparative
quantitative genetic surveys of hybrid and parental phenotypes
are informative about the particular adaptations that distinguish
new hybrids from parents and guide associated searches for
candidate hybrid speciation genes. The transplant studies in
vestigating survivorship and other quantitative traits (QTs) in
parental and progenitor hybrid species of Helianthus described
above have provided much information on key transgressive
hybrid traits enabling adaptation to novel habitats (Lexer &
al, 2003a,b; Gross & al, 2004) and similar studies of hybrid
species from other genera are required to confirm the gener
ality of these findings. In this respect, two recent studies on
Pinus densata are of interest. Pinus densata is a homoploid
hybrid species (X.-R. Wang & al, 2001), which is ecologically
divergent from its progenitors, P. tabulaeformis and .P. yunnan
ensis, and occurs only at high altitude (2700-4200 m) on the
Qinghai-Tibetan Plateau, whereas P. tabulaeformis is restricted
to elevations between 100 and 2600 m in northern China, while
P. yunnanensis is mainly found in southwest China at altitudes
below 2700 m. Gao & al. (2009) and Ma & al. (2010) have dem
onstrated that P. densata exhibits several physiological traits,
not shown by either parent, which are likely to confer increased
drought tolerance for growth in its arid high-altitude habitat.
In Senecio, we have begun an analysis of adaptive diver
gence in S. squalidus by investigating twenty uncorrelated
morphological, developmental and physiological quantitative
traits (QTs) in this species, its parents, and hybrids from Mount
Etna (Brennan & al, 2009 and in prep.). A principal component
analysis (PCA) of the data collected showed that Senecio aethn
ensis and S. chrysanthemifolius were distinguished by the first
principal component (PCI), which accounted for 23.4% of the
total variance, with hybrid plants exhibiting a range of interme
diate PCI values. Senecio squalidus also exhibited intermediate
PCI values, although in general these were much closer to those
of S. chysanthemifolius than to S. aethnensis. However, there
was also an indication that S. squalidus individuals were distinct
from Sicilian plants due to some having larger PC2 values. As
part of this study, quantitative differentiation between species
(Qst) was also estimated for individual trait values, and for PCI
and PC2 values from the principal component analysis (Brennan
& al, in prep.). A significantly positive Qst value for PCI was
observed between S. aethnensis and S. chrysanthemifolius, and
between S. aethnensis and S. squalidus, but not between S. chry
santhemifolius and S. squalidus, confirming that S. squalidus is
most phenotypically similar to S. chrysanthemifolius. Patterns
of between-species Qst estimates for individual quantitative
traits varied widely, but could be placed into one of three broad
categories. Thus for 14 of the 20 traits measured S. squalidus
was most similar to S. chrysanthemifolius, while for three traits
it was most similar to S. aethnensis, and for the remaining
three traits the parents were more similar to each other than to
S. squalidus. One of these latter three traits, plant height at first
flowering, was significantly shorter in S. squalidus compared
to its parents, i.e., was transgressively expressed in the hybrid.
It remains to be established whether any of these differ
ences recorded between S. squalidus and its parental species are
adaptive, and transplant studies are required to determine this
and, in general, how adapted S. squalidus is to the 'British en
vironment' relative to its parents. Interestingly, an independent
reciprocal transplant investigation conducted on S. squalidus in
Britain recently found evidence for rapid local adaptation related
to population latitude for drought and temperature stress toler
ance and flowering time traits, thus showing that adaptation to
the British environment is an ongoing process in this relatively
young homoploid hybrid species (Allan & Pannell, 2009).
Effects of interspecific gene flow. ? Where post-zygotic
reproductive isolation is relatively weak between a homoploid
hybrid species and its parents, it is likely that extensive gene
flow will occur in areas of species overlap and have important
consequences on the genetic structure of the hybrid species.
In fact, this is suggested by a recent study by Scascitelli & al.
(2010) on gene flow between a stabilized introgressant ofH. an
num (H. annum subsp. texanus) and its two parents, H. annum
and H. debilis. Based on a survey of simple sequence repeat
(SSR) variation at 88 loci across these taxa, it was evident that
considerable bidirectional introgression had occurred between
these taxa, which are sympatric in parts of their range. Despite
the presence of a single putative hybrid incompatibility locus
exhibiting strong asymmetric introgression, patterns of differ
entiation across chromosomes indicated that genetic islands of
differentiation were smaller than 1 cM and were not associated
with chromosomal rearrangements in the hybrid.
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TAXON 59 (5) October 2010: 1375-1386 Abbott & al. Homoploid hybrid speciation
Even if strong postzygotic breeding barriers are present
between a homoploid hybrid species and its parents, it is con
ceivable that gene flow might have an effect on the level of ge
netic divergence in areas of sympatry. This is suggested by the
findings of recent studies investigating gene flow between the
species H. annuus and H. petiolaris, which are postzygotically
isolated from each other by strong chromosomal incompatibili
ties, but which nonetheless have acted as the parents of three
homoploid hybrid species. Yatabe & al. (2007) and Strasburg &
al. (2009) found that the genomes of these two species exhibit
extensive ongoing introgression even close to chromosomal
breakpoints. Of further interest is the study by Gross & Riese
berg (2007), which investigated selective sweeps in H. deser
ticola across 96 expressed sequence tag-based microsatellite
loci. This study identified one population that was genetically
more similar to its parents H. annuus and H. petiolaris than
were three other populations of H. deserticola investigated. It
was argued that this similarity could have been caused by inter
specific hybridization resulting in the transfer of new parental
alleles into this particular population of H. deserticola. Inter
estingly, selective sweeps at two loci were unique to the same
population, suggesting that it might have experienced adaptive
introgression from its parent species. Thus, it seems that oppor
tunities for introgression with parents could be a potent force in
shaping genetic differentiation in established homoploid hybrid
species, but that these hybrid species will nonetheless maintain
their ecogeographic distinctiveness, perhaps at the level of just
a few important defining genetic differences.
Genetic divergence in the absence of gene flow. ? The
homoploid hybrid species, S. squalidus, is unique among homo
ploid hybrid species in that it is known to have originated in
geographic isolation from its parent species (James & Abbott,
2005). Thus, gene flow from its parents was not a complicat
ing factor during its origin or in its subsequent establishment
and evolution. Instead, founder effects occurring during the
introduction of hybrid material to Britain, complemented by
the effects of genetic drift and selection during the origin and
establishment of the new hybrid species, are likely to have had
a significant effect on its genetic structure. Two comparative
genetic diversity studies of S. squalidus, its parents, and hybrids
from the hybrid zone on Mount Etna, have shown that S. squal
idus is of mixed ancestry between S. chrysanthemifolius and
S. aethnensis (James & Abbott, 2005; Brennan & al, in prep.).
In addition, these studies have found that S. squalidus contains
less genetic diversity, both in terms of number of alleles per
locus and expected heterozygosity, than either of its parent
species. Additional investigations of allelic diversity at the nor
mally highly polymorphic S locus that controls SI have also
found just 7 alleles in S. squalidus relative to at least 24 alleles
in each of its parental species (Brennan & al, 2006; Brennan,
Harris & Hiscock, unpub. results). Because all of these stud
ies found considerable genetic diversity among hybrid plants
from the hybrid zone on Mount Etna, it is highly likely that
S. squalidus passed through a genetic bottleneck during the
introduction of hybrid material to Britain and the origin of the
hybrid species from this material.
Of particular note from our previous genetic surveys was
the finding that S. squalidus plants formed a well-defined ge
netically distinct cluster from its parent species and hybrids
from Mount Etna. This was first made clear by a survey of
variation of RAPD markers that distinguished the two parent
species (James & Abbott, 2005) (Fig. 2). Thus S. squalidus
is more highly differentiated from S. aethnensis and S. chry
santhemifolius than are plants from the hybrid zone on Mount
S. chrysanthemifolius O Hybrids A S. aethnensis X S. squalidus
Fig. 2. Plot of individual scores against the first two axes extracted from a principal coordinate analysis of RAPD variation among individuals of
Senecio chrysanthemifolius, S. aethnensis and hybrids from the hybrid zone on Mount Etna, Sicily, and of S. squalidus from six British popula
tions. Individuals of S. squalidus form a cluster that is distinct from individuals representing its parent species and hybrids on Mount Etna. (From
James & Abbott, 2005; reproduced with permission of John Wiley & Sons Inc.)
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Abbott & al. Homoploid hybrid speciation TAXON 59 (5) October 2010: 1375-1386
Etna. An analysis of allele sharing in a survey of 13 SSRs, six
allozymes and three indels (102 alleles in total, Brennan & al,
in prep.) showed that while hybrid Senecio on Mount Etna con
tained more unique alleles than S. squalidus relative to parental
Senecio species (11 versus 5), many more alleles are shared be
tween the hybrid plants and both parents than between S. squal
idus and its parents (62 versus 35). Furthermore, allele fre
quency differences were found to be significantly smaller when
comparisons were made between Mount Etna hybrid Senecio
and parental Senecio, than between S. squalidus and parental
Senecio (Brennan & al, in prep.). Thus, both allele sharing
and allele frequency differences in S. squalidus compared to
parents and Sicilian hybrids contributed to the overall genetic
differentiation observed for S. squalidus. Together, these results
suggest that genetic differentiation during homoploid hybrid
speciation is enhanced and hastened by physical barriers to
ongoing introgression. Further investigations to quantify and
distinguish the influences of founder effects and selection on
genetic diversity during this speciation event using computer
simulation and high-throughput gene-space sequencing meth
ods are currently being conducted in our laboratories. In addi
tion, transplant experiments that compare the relative fitness
of S. squalidus and its parent species in Britain are required to
assess the adaptive significance of genetic changes identified in
this new hybrid species. Such experiments will show whether
geographical isolation caused by adaptation of S. squalidus to
the British environment was of major importance in the origin
of the species (see Sobel & al, 2010).
Changes in gene expression. ? The combination of two
divergent genomes within a single hybrid nucleus can result
in rapid genomic change in homoploid hybrid species caused
by recombination (Rieseberg & al, 1995), and activation and
proliferation of transposable elements (Ungerer & al, 2006;
Kawakami & al, 2010). In addition, it can lead to the genera
tion of novel patterns of gene expression, which could give
rise to transgressive phenotypes that are of adaptive signifi
cance. Gene expression which is not merely a combination of
that observed in the parental species is commonly referred to
as "non-additive", and has been observed extensively in allo
polyploid hybrids such as Arabidopsis suecica (J. Wang & al,
2006), and Senecio cambrensis (Hegarty & al, 2006, 2008).
Non-additive gene expression can arise due to factors such
as novel interactions between gene regulators, changes in the
epigenetic regulation of gene expression and variation in gene
copy number (reviewed in Hegarty & Hiscock, 2008). Many
of these factors are also likely to play a role in mediating gene
expression in homoploid hybrids. Indeed, a recent microarray
expression study in homoploid hybrid sunflowers (Lai & al,
2006) demonstrated non-additive gene expression in a wild
homoploid hybrid adapted to a habitat which neither parent
can tolerate. In this study, gene expression was compared be
tween the hybrid Helianthus deserticola and its parental species
H. annum and H. petiolaris. Lai & al. (2006) identified 154
genes differentially expressed between the hybrid and H. an
num and 174 between the hybrid and H. petiolaris. Whilst this
study did not attempt to assess deviation from the parental mid
point value (MPV) as is now commonplace for studies of non
additive gene expression, 58 genes were identified as showing
'transgressive' expression?that is, expression levels which
are not merely non-additive but which lie significantly out
side the expression range of either parent. This 'transgressive'
group was shown to over-represent transport-related genes (i.e.,
S. aethnensis
F1 synthetic
F2 synthetic
F3 synthetic
F4 synthetic
F5 synthetic
S. chrysanth.
Down-regulated in F1 Up-regulated in F1
Fig. 3. Non-additive patterns of gene expression in early generation resynthesized Senecio squalidus. Hierarchical clustering (based on similar
ity of expression pattern) of 986 cDNA clones showing non-additive gene expression in the Fj synthetic hybrid relative to the parental midpoint.
Red coloration indicates up-regulation whilst blue denotes down-regulation (relative to a derived baseline for each clone). A majority of clones
affected in the Fj hybrid (690 of the 986 clones) display similar expression patterns in both the F2 and F3 generations, but return to a more additive
expression pattern in the F4 and F5 hybrids. (From Hegarty & al, 2009; reproduced with permission of John Wiley & Sons Inc.)
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TAXON 59 (5) October 2010: 1375-1386 Abbott & al. Homoploid hybrid speciation
protein transporters of potassium, sodium and chloride ions),
which could explain the phenotypic divergence that enables
H. deserticola to survive in an arid environment that neither of
its parents can tolerate. Non-additive gene expression in hybrid
plants, therefore, may represent a source of phenotypic novelty
upon which selection may act.
The work of Lai & al. (2006) used a microarray platform
comprised solely of cDNA clones from tissues subjected to a
variety of environmental stresses (e.g., salt or drought stress).
Because hybridization may theoretically affect the expres
sion of genes that are not involved in stress responses (i.e.,
'housekeeping' genes), these results do not give a genome
wide picture of changes to gene expression associated with
homoploid hybrid speciation. In addition, because Lai & al.
(2006) focussed on an established hybrid species, their results
do not provide information on the timing of gene-expression
change after hybrid formation. To further explore gene expres
sion changes associated with homoploid hybrid speciation, we
used custom cDNA microarrays to compare gene expression
in wild U.K. Senecio squalidus to its progenitors, S. aethnensis
and S. chrysanthemifolius. We also recreated the hybrid under
glasshouse conditions and produced ?i~?5 generations of hy
brids via randomised mating and compared these to their pa
rental plants in order to determine the timing of transcriptional
changes associated with homoploid hybridization (Hegarty &
al, 2009).
Our analysis of wild S. squalidus identified 311 array fea
tures (4.9% of features on the array) which displayed gene ex
pression significantly different to the average of the parental ex
pression values. Of these, 80.7%) showed upregulation relative
to the parental midpoint. We then filtered the data further to
identify genes with expression levels outside the range of either
parent ('transgressive' expression) and found that 65% of genes
displaying non-additive expression also showed transgressive
Fig. 4. Seed germination and survival rates for resynthesized Senecio
squalidus hybrid lines. Percentage seed germination after three weeks
and percentage of germinating seedlings that survived to six weeks
in the first five generations of resynthesized S. squalidus hybrids.
Survival in the F2 generation was reduced due to the occurrence of
albino individuals which could not photosynthesize effectively. (From
Hegarty & al, 2009; reproduced with permission of John Wiley &
Sons Inc.)
expression patterns. Amongst these genes were a number in
volved in defence and stress responses, which are also typically
affected in allopolyploid hybrid systems. More interestingly, we
observed significant upregulation of two genes, encoding glu
tathione S-transferase and ATP-sulfurylase, which are known
to be upregulated as a consequence of sulphur deficiency. As
soils in Britain generally contain much lower levels of sulphur
than the volcanic soil of Mount Etna where S. squalidus arose,
upregulation of these genes may represent the effects of adap
tive divergence since the species' introduction to Britain.
Our survey of gene expression in synthetic S. squalidus
hybrids was also informative. We identified 690 array features
(10.89% of the array) displaying non-additive expression across
the first three generations of synthetic hybrids, typically dis
playing the greatest deviation from the parental midpoint in
the F2 generation. However, all of these non-additive features
displayed a return to additivity in the F4 and F5 generations (Fig.
3), which was correlated with an observed increase in seed ger
mination after reductions in the F2 and F3 generations (Fig. 4).
It might be, therefore, that some of the extreme expression
patterns observed in the F2-F3 generations were eliminated
due to selection against those patterns at the level of seed vi
ability. Indeed, the majority of genes displaying non-additive
and 'transgressive' expression in the F4-F5 generations are
different to those seen in the F2-F3 generations. Mitochondrial
and photosynthetic genes were most heavily affected in the syn
thetic hybrids, including several genes known to be involved
in adaptation to varying UV light conditions. These genes also
displayed significant differences in expression between the
parental taxa, suggesting a role in local adaptation to UV light
conditions at the two parental altitude ranges on Mount Etna. In
the majority of cases, these genes did not show significant vari
ation from the parental midpoint in wild S. squalidus. This sug
gests that early transgressive effects in these genes have been
ameliorated over evolutionary time. Our findings show that ex
treme, transgressive changes to gene expression are generated
rapidly in early hybrid generations and provide hybrids with
genetic novelty which may influence their successful evolution
into new species. However, selective pressures are a necessary
component in determining whether these novel genetic traits
are maintained or eliminated over time. Future experimenta
tion in Senecio will attempt to determine whether hybrids are
indeed better adapted to the environmental conditions present
in the hybrid range, such as soil sulphur content and UV light
exposure and, if so, whether these traits may have been fixed
by selection in the wild British population.
CONCLUSIONS AND FUTURE RESEARCH
Most of our current understanding of homoploid hybrid
speciation is derived from the comprehensive research con
ducted on three homoploid hybrid species of sunflower, Heli
anthus anomalus, H. deserticola and H. paradoxus, each of
which originated following hybridization between H. annuus
and H. petiolaris. This work, conducted by Rieseberg and co
workers, has shown that new fertile homoploid hybrid species
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Abbott & al Homoploid hybrid speciation TAXON 59 (5) October 2010: 1375-1386
that are reproductively isolated from their parents can originate
rapidly. However, a longer period is likely to be required before
the new species exhibits stabilized and distinctive phenotypic
and genomic variation relative to that which it exhibits soon
after its hybrid origin. Theory shows that ecological and spa
tial divergence of the hybrid species from its parents is key to
successful establishment, and that this can occur even in the
absence of post-zygotic isolation caused by chromosomal and/
or genetic sterility barriers. While for many traits a hybrid
species might exhibit intermediate phenotypes to its parents,
often it either combines a distinctive mix of parental-like traits
or exhibits transgressive traits that enable it to occupy a novel
and perhaps more 'extreme' habitat relative to those of its par
ents. Studies of Helianthus homoploid hybrid species have
shown that the generation of transgressive traits has been of
great importance in adapting these species to habitats that are
ecologically and spatially divergent from those of the parents.
Our work on the newly originated homoploid hybrid spe
cies, Senecio squalidus, is valuable in determining how this
species has diverged from its two parent species and their hy
brids that occur on Mount Etna, Sicily. The origin of S. squal
idus differs from that of all other known homoploid hybrid
species in that human actions played a direct role in geographi
cally isolating hybrids by introducing them into Britain from
Sicily. A small population of introduced hybrid material was
then cultivated for many years allowing genetic change to take
place and for a successful invasive hybrid species to evolve, in
the absence of gene flow from the two parent species. Pheno
typically, S. squalidus is similar to one of its parents, S. chry
santhemifolius, for most traits recorded, but for some traits it
is more similar to the other parent, S. aethnensis, while for
some others it exhibits a transgressive phenotype. In fact, our
studies of changes in gene expression in S. squalidus relative
to its parents, suggest that many changes are transgressive and
some of these could have been important in adapting the new
species to conditions in the U.K. Moreover, it is apparent from
our studies of early generation synthetic hybrids that increased
variation in gene expression is correlated with loss of fitness,
but that gene expression is stabilized and fitness restored very
quickly due presumably to the effects of selection.
A notable finding from our studies on S. squalidus is that
this new species is already genetically divergent from the wide
range of hybrid genotypes that are found in the hybrid zone
between S. aethnensis and S. chrysanthemifolius on Mount
Etna (James & Abbott, 2005; Brennan & al, in prep.). This
divergence is due to a combination of reduced genetic diversity
and greater allele frequency differences in S. squalidus com
pared with both parent species and Sicilian hybrid material.
It is expected that future research on homoploid hybrid spe
ciation will uncover additional examples of homoploid hybrid
species in diverse plant, animal and fungal groups in which
interspecific hybridization occurs. The discovery of new exam
ples of homoploid hybrid species will provide new opportuni
ties for investigating the different ways in which they originate,
particularly when these species represent early stages in origi
nation. We anticipate that resolving the mechanisms underlying
the reproductive isolation and adaptive novelties of homoploid
hybrid species will continue to be a major focus of research
with considerable effort aimed at isolating and characterizing
the genes and genomic regions involved in this. In our own
research on the origin and evolution of Senecio squalidus, we
are currently undertaking a comparison of genetic linkage and
QTL maps of S. aethnensis, S. chrysanthemifolius and S. squal
idus to further investigate genomic relationships between the
new hybrid species and its parents, and have also embarked on
a genomic analysis of adaptation in the three species by means
of genomic screens of the entire gene-space (the non-repetitive
gene-rich fraction of the genome) of S. squalidus to identify
genes associated with adaptation and divergence of this species
in Britain. The recent advances in DNA sequencing technolo
gies (454 and Illumina) now permit unprecedented access to
genomic data allowing us to begin to determine the relative
importance of genomic changes to coding versus regulatory
regions of genes in adaptation of the three Senecio species
to contrasting environments. We will further interrogate the
Senecio genome to analyse genetic and epigenetic changes at
candidate loci potentially involved in generating 'transgressive'
expression patterns associated with hybrid speciation and po
tential adaptation of S. squalidus to low sulphur and UV light
conditions that were identified from our recent transcriptomic
studies (Hegarty & al, 2009). In this way, we intend to obtain
over the next few years a detailed understanding of the genetic
and adaptive changes responsible for the origin, establishment
and rapid spread of what is the most recently originated homo
ploid hybrid plant species currently known in the wild.
ACKNOWLEDGEMENTS
We thank Tod Stuessy for inviting us to contribute this paper,
and also two anonymous reviewers for their helpful comments on an
earlier version of the manuscript. Our research on homoploid hybrid
speciation in Senecio has been funded by the Natural Environment
Research Council (NERC) through grants NER/T/S/2001/00995 (to
SJH/RJA), NE/D014166/1 (to RJA), and NE/D005353/1 and NE/
G018448/1 (to SJH).
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