The Ecological Genetics of Homoploid
Hybrid Speciation
B. L. GROSS AND L. H. RIESEBERG
From the Department of Biology, 1001 E. 3rd Street, Jordan Hall 142, Indiana University, Bloomington, IN 47405
Address correspondence to Briana L. Gross at the address above, or e-mail: brgross@indiana.edu
Abstract
Our understanding of homoploid hybrid speciation has advanced substantially since this mechanism of species formation was
codified 50 years ago. Early theory and research focused almost exclusively on the importance of chromosomal
rearrangements, but it later became evident that natural selection, specifically ecological selection, might play a major role as
well. In light of this recent shift, we present an evaluation of ecology’s role in homoploid hybrid speciation, with an emphasis
on the genetics underlying ecological components of the speciation process. We briefly review new theoretical developments
related to the ecology of homoploid hybrid speciation; propose a set of explicit, testable questions that must be answered to
verify the role of ecological selection in homoploid hybrid speciation; discuss published work with reference to these
questions; and also report new data supporting the importance of ecological selection in the origin of the homoploid hybrid
sunflower species Helianthus deserticola. Overall, theory and empirical evidence gathered to date suggest that ecological
selection is a major factor promoting homoploid hybrid speciation, with the strongest evidence coming from genetic studies.
Ecological Speciation: A Historical
Perspective
It is often lamented that ecology has been overlooked
in studies of speciation (Lewontin 1997; Morell 1999;
Schemske 2000). This is a curious claim given that Darwin’s
focus was primarily on ecological divergence and that both
Dobzhansky (1937) and Mayr (1942) argued that adaptation
to different environments led to speciation. Early botanical
students of speciation put an even greater stress on ecology.
For example, Stebbins (1950, p. 199) wrote, ‘‘By far the most
common type of isolation in both the plant and the animal
kingdom is that resulting from the existence of related types
in different geographical regions which differ in the prevailing
climatic and edaphic conditions.’’ Likewise, Clausen’s
(1951) monograph describes how ecological races are transformed
into species and defines species in terms of their
physiologic-genetic properties.
Although it may be that Dobzhansky and Mayr simply
played lip service to ecology (Coyne and Orr 2004), this
argument doesn’t hold for their botanical counterparts.
Stanford University’s influential team of Clausen, Keck, and
Hiesey pioneered the field of ecological genetics (e.g.,
Clausen et al. 1947), Verne Grant’s (1949) empirical work
focused on pollinator-mediated isolation, and Edgar Anderson
(1948) emphasized the role of habitat disturbance in the
breakdown of reproductive barriers and establishment of
hybrids. Even Stebbins, whose empirical work was primarily
cytological, published several papers on ecological aspects of
speciation (e.g., Stebbins 1942, 1952).
It is easier to make the case that ecology was neglected in
the latter half of the twentieth century, even in plants.
Population geneticists and systematists were mesmerized by
new molecular genetic tools that allowed genetic variability
to be measured and the history of populations and species
to be reconstructed, whereas ecologists either were not
interested in speciation or were preoccupied with measuring
selection in natural populations. More generally, the field of
speciation was sidetracked by theoretical arguments favoring
nonecological causes of speciation, such as population
bottlenecks and genetic drift. As a consequence, investigations
of the ecology of speciation stagnated along with other
process-oriented studies of speciation.
Fortunately, the situation has changed dramatically over
the past decade. A new cadre of ecologists has become
interested in speciation, influential models of ecological
speciation have been developed (e.g., Doebeli and Dieckmann
2003), and explicit tests have been put forward to
distinguish ecological speciation from other speciational
mechanisms (Schluter 2001). However, these tests were
developed to assess the role of ecological selection in primary
speciation. A comparable experimental framework for
testing the importance of ecological selection in homoploid
hybrid speciation has not yet been established, although
several requirements have been suggested ad hoc in recent
papers (Gross et al. 2004; Lexer et al. 2003b; Rieseberg et al.
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Journal of Heredity 2005:96(3):241–252 ª 2004 The American Genetic Association
doi:10.1093/jhered/esi026
Advance Access publication December 23, 2004
2003). (See Table 1 and Figure 1 for characteristics of reticulate
speciation.)
The objectives of the present article are to (1) briefly
review new theoretical developments related to the ecology
of homoploid hybrid speciation; (2) propose a set of explicit,
testable questions designed to verify the role of ecological
selection in the process; (3) discuss published work on the
ecology of homoploid hybrid speciation with reference to
these tests; and (4) report new data supporting the importance
of ecological selection in the origin of the homoploid
hybrid sunflower species Helianthus deserticola.
Homoploid Hybrid Speciation: Theory
During homoploid hybrid speciation, a stable, fertile, and
reproductively isolated hybrid derivative arises without a
change in chromosomal number. Reproductive isolation is
thought to occur through rapid chromosomal reorganization,
ecological divergence, and/or spatial isolation (Rieseberg
1997). Early verbal models of the process emphasized the
evolution of chromosomal sterility barriers, which were
thought to arise through the sorting of chromosomal rearrangements
that differentiated the parental species (Grant
1958; Stebbins 1957). This chromosomal model, referred to
as ‘‘recombinational speciation’’ by Grant (1981), has received
the most attention in subsequent study. However, Grant also
noted that a hybrid lineage could arise through ‘‘the segregation
of a new type isolated by external barriers’’ (1981, p. 243).
Templeton (1981) suggested that both forms of isolation
were likely to be important, with chromosomal isolation preventing
extinction through genetic assimilation and ecological
divergence precluding extirpation through competition.
Table 1. Characteristics of reticulate modes of speciation (cf. Figure 1).
Chromosomal
changes
Initial form of
reproductive
isolation
Genetic mechanism(s)
underpinning initial
isolation
Proximate cause(s)
of isolation
Allopolyploidy Genome duplication Intrinsic postzygotic Ploidy differences; mutation Genetic drift
Homoploid hybrid speciationa
1. Recombinational
model
Rearrangements;
recombination of
parental rearrangements
Intrinsic postzygotic New chromosomal
combinations via
hybridization
Genetic drift;
fertility selection
2. External isolation
model
None Ecological prezygotic;
extrinsic postzygotic
New genetic combinations
via hybridization
Divergent natural
selection (includes
ecological selection)
a
Note that many cases of homoploid hybrid speciation incorporate aspects of both the recombinational and external isolation models.
Figure 1. Example of a phylogenetic tree showing reticulation due to homoploid hybrid speciation. Phylogenetic tree for Helianthus
section, Helianthus based on combined chloroplast DNA and nuclear ribosomal DNA data (Rieseberg 1991). The number of mutations
are given above and bootstrap percentages below each branch. Dashed lines indicate parentage of homoploid hybrid species.
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The first mathematical treatment of homoploid hybrid
speciation was a computer simulation of the recombinational
model (McCarthy et al. 1995). Because speciation failed to
occur at an appreciable rate by the sorting of chromosomal
rearrangements alone, McCarthy et al. simulated ecological
selection by arbitrarily assigning a fitness advantage to some
hybrid genotypes. When the fitness advantage was large,
hybrid speciation occurred at an appreciable rate. However,
the McCarthy et al. model describes a special case of hybrid
speciation in which the new hybrid lineage replaces its
parental species rather than coexisting with them. Also,
although it is theoretically possible that a hybrid genotype
might be fitter than its parents in parental habitats (Barton
2001), superior hybrid fitness in a new habitat is considerably
more plausible (Arnold 1997; Rieseberg 1997).
The role of ecological selection was explored explicitly by
Buerkle et al. (2000) in a model featuring habitats for both of
the parental species and a third unoccupied, ecologically
divergent habitat available for colonization. This spatial
model demonstrated that the frequency of hybrid speciation
increased with increasing strength of ecological selection. As
in the McCarthy et al. (1995) model, the sorting of chromosomal
rearrangements alone was unlikely to lead to
speciation. Although strong ecological selection was sufficient
for hybrid speciation, the evolutionary independence of
the new hybrid lineage was increased by chromosomal
isolation as predicted by Templeton (1981). Ecological
selection thus emerged as an important factor for the origin
of homoploid hybrid species, at least theoretically.
This model was subsequently modified by removing the
unoccupied habitat, leaving only the two parental habitats
available (Buerkle et al. 2003). Under these conditions, homoploid
hybrid speciation was rare. When it did occur, the new
hybrid populations were generally small, and unstable, and
appeared to represent a transitory state prior to the genetic
assimilation of one species by the other. Clearly, these results
indicate that the availability and colonization of a novel habitat
are crucial to the origin of homoploid hybrid species.
Finally, there has recently been a more thorough
consideration of the origin of traits that allow hybrids adapt
to new environments and thereby diverge from their parental
species ecologically (Barton 2001; Ellstrand and Schierenbeck
2000; Schwarzbach et al. 2001). Hybrids may have
intermediate trait values, combine traits from both parents,
and/or exhibit extreme trait values. All three possibilities
might allow for high fitness of hybrids in a new environment.
For example, an intermediate hybrid might have higher
fitness in an environment that is intermediate compared to
parental habitats (Anderson 1948), whereas a novel combination
of parental traits might be advantageous in a habitat
that has aspects of both parental environments. However,
some homoploid hybrid species are also found in extreme
habitats, a transition that likely requires the acquisition of
novel, perhaps extreme traits (Gross et al. 2004; Lexer et al.
2003a,b; Rieseberg et al. 1999, 2003; Schwarzbach et al.
2001). Hybridization provides a means by which this could
occur because extreme or transgressive trait values are common
in both natural hybrid populations and controlled crosses
(Rieseberg et al. 1999) and appear to mostly result from the
complementary action of alleles from both parents—that is,
the ‘‘stacking’’ of alleles with the same directional effect on
a given trait (deVincente and Tanksley 1993).
Tests of Ecological Speciation
Schluter (2001) has suggested several tests to distinguish
primary ecological speciation from other speciation mechanisms,
such as ordinary genetic drift, drift resulting from
population bottlenecks, divergence accruing from parallel
selection, and speciation by polyploidy. These tests include
(1) a correlation between the strength of divergent selection
and rate of evolution of reproductive barriers, (2) evidence of
ecological selection against hybrids, (3) evidence of divergent
natural selection on phenotypic traits or specific genes, and
(4) parallel speciation.
The situation for homoploid hybrid speciation is more
complex, however, because we need to show not only that
ecological divergence in the new hybrid lineage contributes to
isolation but also that the divergence arose early in the hybrid
speciation process. If most ecological changes accrue after
hybrid speciation, niche divergence could be incidental to
speciation. Also, it is important to understand the origins of
the ecological divergence in homoploid hybrid species. That
is, we need to demonstrate that hybridization is both sufficient
and necessary for generating the specific trait combinations
and trait values that are the basis for ecological divergence and
reproductive isolation. This would also imply that ecological
divergence arose early in the speciation process.
Given these considerations, we suggest the that a careful
evaluation of the following questions would verify the role of
ecological divergence in homoploid hybrid speciation. Some
of these are self-evident and can largely be inferred from
descriptive analyses of ecogeographic distributions, whereas
others will require explicit experimentation.
1. Are the homoploid hybrid species ecologically divergent
from their parents?
2. Does ecological divergence contribute to reproductive
isolation?
3. Can the new combinations of traits and genes responsible
for ecological divergence be generated via hybridization
(as opposed to the gradual accumulation of
mutations)?
4. Are traits and genes responsible for ecological divergence
under divergent natural selection in the habitat of the
hybrid species?
5. Is selection strong enough to allow divergence in the face
of gene flow (given that homoploid hybrid speciation
must be initiated in sympatry or parapatry with its
parental species)?
6. Is there evidence of parallel hybrid speciation?
Are the Homoploid Hybrid Species Ecologically
Divergent from their Parents?
Although homoploid hybrid speciation is frequently proposed
as an explanation for morphological intermediacy,
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Gross and Reiseberg  Ecological Genetics of Hybrid Speciation
there are still only a handful of instances in which these
hypotheses have been rigorously confirmed using molecular
markers (reviewed by Coyne and Orr 2004; Rieseberg 1997).
The majority of these studies involve plants, but several
examples have recently been reported from invertebrates and
fish. In all cases, there is some measure of ecological
divergence between the hybrid and its progenitors, although
the thoroughness with which this has been documented
varies. In most instances, the only information derives from
brief descriptions of the habitat that hybrid neospecies
occupies (see later discussion), although in few cases
common garden and transplant experiments have been
performed. Ecological divergence in a majority of known
homoploid hybrid species would be unlikely if speciation was
driven by intrinsic factors, such as chromosomal rearrangements.
Overall, the consistent pattern of ecological divergence
described conforms well to expectations if
ecological divergence is important in promoting homoploid
hybrid speciation (Table 2).
The first homoploid hybrid species to be confirmed with
molecular markers was Stephanomeria diegensis, a derivative of
S. exigua and S. virgata (Gallez and Gottlieb 1982). The hybrid
species is found mainly in disturbed or pioneer habitats in
southern California, a range that is restricted in both area and
elevation when compared to those of its progenitors, which
have extensive ranges in southwestern North America.
S. exigua is generally found in sandy soils occupied by sagebrush
or creosote bush, whereas S. virgata is common in
chaparral openings and dry sandy hills.
Iris nelsonii also has a long history in the hybrid literature
(e.g., Randolph 1966), and its diploid hybrid ancestry was
confirmed in 1993 (Arnold). There are three parental species
all found in Louisiana: I. fulva inhabits the shady, shallow
water of bayou margins; I. hexagona is found in sunny, deeper
swamp water; and I. brevicaulis occurs in much drier pastures
and forests. In this system, the hybrid species occupies
a divergent habitat that combines features from habitats of
the parental species, and is found in the shady, deep water of
cypress swamps.
Several hybrid species have been identified in the
widespread Peaonia complex of Europe and Asia (Ferguson
and Sang 2001; Sang et al. 1995, 1997; Sang and Zhang 1999).
However, information on the ecology of the hybrid and parental
Peaonia species is not generally reported. Biogeographic
distributions are known for many of the species, and the
hybrid derivatives are often allopatric with respect to their
progenitors. Interestingly, European populations of the progenitors
appear to have been displaced by the hybrid species,
perhaps due to the superior ability of the hybrids to adapt to
Pleistocene climactic changes in Europe (Sang et al. 1995).
The hybrid species Argyranthemum sundingii (Brochmann
et al. 2000) exhibits a more classic kind of ecological
divergence, occurring at an intermediate elevation and
moisture gradient relative to the parents (Tenerife, Canary
Islands). Greenhouse experiments have identified several
phenotypic differences that are associated with habitat
differentiation in the hybrid neospecies and shown that
these differences are heritable.
Table 2. Confirmed and potential homoploid hybrid species, description of organism type, mode of ecological divergence from
parental species, documentation of multiple origins, and references.
Taxon Description
Ecological
divergence
Multiple
origins Reference
Alcyonium hibernicumb
marine invertebrate habitat unknown McFadden and Hutchinson 2004
Argyranthemum sundingiia
annual herb habitat yes Brochmann et al. 2000
Arisaema ehimenseb
perennial herb habitat and temporal unknown Maki and Murata 2001
Armeria villosa carratracensisb
perennial herb habitat unknown Feliner et al. 2002
Ceanothus speciesb
perennial shrub habitat unknown Hardig et al. 2002
Daphnia mendotaea
freshwater invertebrate habitat unknown Taylor et al. 1996
Encelia virginensisb
perennial shrub habitat unknown Allan et al. 1997
Gila seminudea
freshwater fish habitat unknown DeMarais et al. 1992
Helianthus anomalusa
annual herb habitat yes Rieseberg 1991
Helianthus deserticolaa
annual herb habitat yes Rieseberg 1991
Helianthus paradoxusa
annual herb habitat and temporal no Rieseberg 1991,
Rieseberg et al. 1991
Hyobanche glabratab
parasitic herb habitat and pollinator unknown Wolfe and Randle 2001
Iris nelsoniia
annual herb habitat unknown Arnold 1993
Peaonia species groupa
perennial herb habitat unknown Ferguson and Sang 2001; Sang et al.
1995, 1997; Sang and Zhang 1999
Penstemon clevelandiia
annual herb pollinator unknown Wolfe et al. 1998
Pinus desataa
perennial tree habitat yes Wang et al. 2001
Schistosoma sinensiumb
parasitic invertebrate habitat unknown Hirai et al. 2000
Senecio eboracensisc
annual herb temporal and pollinator no Lowe and Abbott 2004
Stephanomeria diegensisa
annual herb habitat unknown Gallez and Gottlieb 1982
a
Known cases of homoploid hybrid speciation confirmed with molecular markers.
b
Potential but unconfirmed cases of homoploid hybrid speciation.
c
Confirmed hybrid speciation event, only one parent with the same ploidy level as hybrid species.
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The origin of Penstemon clevelandii from P. centranthifolius
and P. spectabilis is of interest because reproductive isolation
of the hybrid neospecies may have been achieved by
selection for a divergent pollination syndrome (Straw 1956;
Wolfe et al. 1998). The hybrid species is bee- and
hummingbird-pollinated, with magenta colored, semi-inflated
flowers and occurs in canyons and road cuts in granitic soils
of southern California and northern Baja. Penstemon spectabilis
is wasp-pollinated with lavender, fully inflated flowers and is
a pioneer species of disturbed habitats in southern California
and northern Baja, whereas P. centranthifolius is hummingbirdpollinated
with red, tubular flowers and is typically found in
sandy washes and roadsides over the same general range as
P. spectabilis.
Senecio eboracensis (2n ¼ 40) is unique relative to many
other hybrid species; it has the same ploidy as the parental
species S. vulgaris (2n ¼ 40) but double the ploidy of the
second parental species S. squalidus (2n ¼ 20) (Abbott and
Lowe 2004). Thus it is neither a homoploid nor a polyploid
hybrid species according to the strict definitions of these
terms. Nonetheless, it is important to consider this example
due to the fact that reproductive isolation between the
S. eboracensis and S. vulgaris must be based on mechanisms
other than ploidy changes. The hybrid species shows only
slight ecological divergence relative to S. vulgaris and the two
taxa occur sympatrically in the British Isles, sometimes only
meters away from each other. However, the species differ
slightly in seed germination, seedling over wintering,
flowering time, and floral morphology (Lowe and Abbott
2004).
There are two genera in which diploid hybrid species
clearly inhabit environments that are extreme relative to the
parental species: Pinus and Helianthus. Pinus densata, which
is derived from hybridization between P. yunnanensis and
P. tabulaeformis, inhabits a high mountain environment where
the parental species are apparently unable to grow (Wang
et al. 2001). The hybrid species occurs between 2700 and
4200 m above sea level on the Tibetan Plateau, whereas the
parental species occur from sea level to 3100 m.
The genus Helianthus (the North American sunflower)
contains three hybrid species that occur in three widely
divergent habitats (Heiser 1947; Heiser et al. 1969; Rogers
et al. 1982), despite sharing the same two parents (Figure 1)
(Rieseberg 1991). Both parental species are widely distributed
across the United States; H. annuus is found in mesic,
clay-based soils and H. petiolaris occurs in dryer, sandier soils.
The hybrid species, in contrast, have restricted ranges in the
southwestern United States; H. anomalus is found on active
sand dunes, H. deserticola occupies xeric habitats in the Great
Basin Desert, and H. paradoxus inhabits desert salt marshes.
Greenhouse comparisons have identified a suite of traits that
differentiate each taxon from its parental species and that
seem likely to confer a fitness advantage to the homoploid
hybrid species in its native habitat (Rosenthal et al. 2002;
Schwarzbach et al. 2001). For example, H. deserticola has early
flowering and small leaves compared to the parental species;
both traits are typical of desert annuals. Transplant experiments
indicate that the parental species fail to survive in
H. paradoxus habitat (Lexer et al. 2003b) may be as fit as
the hybrid taxon in the H. anomalus habitat (Ludwig et al.
in press), and exhibit equivalent or greater fitness than the
hybrid species in H. deserticola habitat (Gross et al. 2004).
However, the parental species showed reduced or no
emergence in the H. anomalus habitat during two following
experiments, suggesting that their exclusion may be due to
failure in germination and early growth. Patterns of seedling
emergence and survival from similar experiments in the
H. deserticola habitat remain unclear and will require further
investigation (Ludwig and Donovan personal communica-
tion).
The best example of hybrid speciation in animals
comes from the fish genus Gila, native to the southwestern
United States (DeMarais et al. 1992). The parental species,
G. robusta robusta and G. elegans, are found sympatrically
in the large Colorado River, whereas the hybrid species,
G. seminude, is found only in the Virgin River, a moderately
sized tributary of the Colorado. Interestingly, the parental
species are never found in the Virgin River, although there
are no known physical barriers that would impede their
migration.
Homoploid hybrid speciation also has been proposed for
the water flea Daphnia mendotae, which occurs in slightly
warmer water and shows less vertical migration than one if
its sympatric progenitors, D. dentifera (Dudycha 2003; Taylor
et al. 1996). Hybrid speciation may also have occurred in the
soft coral genus Alcyonium, where the hybrid species is almost
completely allopatric with its progenitors (McFadden and
Hutchinson 2004).
Finally, there are multiple proposed cases of homoploid
hybrid speciation that have proven difficult to verify even
with molecular markers, including species in the genera
Armeria (Feliner et al. 2002), Arisaema (Maki and Murata
2001), Ceanothus (Hardig et al. 2002), Encelia (Allan et al.
1997), Hyobanche (Wolfe and Randle 2001), and Schistosoma
(Hirai et al. 2000). These taxa may provide additional support
for ecological divergence if their hybrid ancestry can be
confirmed.
Does Ecological Divergence Contribute to Reproductive
Isolation?
Ecological selection may contribute to reproductive isolation
via habitat, floral/pollinator, and temporal divergence. All
three types of divergence are potentially important in
promoting homoploid hybrid speciation, but most research
to date has focused on habitat divergence, which can lead to
spatial isolation (a prezygotic barrier) and reduced fitness of
hybrids in parental habitats (a postzygotic barrier). As noted
by Coyne and Orr (2004), however, habitat divergence does
not necessarily cause reproductive isolation. For example,
plants might partition water usage in different ways but still
flower simultaneously and hybridize readily. Do the ecological
differences documented for various homoploid
hybrid species actually contribute to reproductive isolation?
Not surprisingly, this question remains to be investigated in
many systems, but some answers are emerging.
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Gross and Reiseberg  Ecological Genetics of Hybrid Speciation
Cases where hybrid species and their progenitors
are partially or completely allopatric due to habitat divergence
come the closest to satisfying the requirement of
reproductive isolation. This group includes Peaonia, Pinus,
and Gila on a macrospatial scale and Stephanomeria, Iris, and
Argyranthemum on a microspatial scale. Helianthus is on the
border between these extremes; the parental species overlap
the hybrid taxa on a broad scale but generally occur several
kilometers from each other at a given site. This spatial
isolation appears to be an effective barrier to hybridization.
For example, no hybridization has been detected between
the ancient hybrid sunflower species and their progenitors,
despite extensive fieldwork (Gross et al. 2003; Heiser et al.
1969; Rogers et al. 1982; Schwarzbach and Rieseberg 2002;
Welch and Rieseberg 2002). No attempts have been made to
assess whether synthetic hybrids between a homoploid
hybrid species and its progenitors would have reduced
fitness in hybrid or parental habitats. However, the transplant
experiments conducted for sunflowers (described
earlier) provide a possible explanation for why the parental
species fail to colonize the habitats of their hybrid
derivatives.
Both temporal and pollinator divergence are thought
to contribute to reproductive isolation between S. eboracensis
and S. vulgaris. However, a thorough investigation of reproductive
isolation in this system suggests that these ecological
factors are probably less important in preventing
hybridization than the fact that both species are predominantly
self-fertilizing (Abbott and Lowe 2004; Lowe
and Abbott 2004).
Penstemon offers a possible example of hybrid speciation
dependant on solely ecological isolating barriers (floral/
pollinator isolation and possibly microspatial habitat isolation).
The two parental species are pollinated by different
animals, and the hybrid species is thought to exploit a third
(Straw 1956). Although anecdotally compelling, precise
studies quantifying the degree of pollinator discrimination
have not been conducted for the hybrid species, and
hybridization between the derivative and parental species
has been suggested (Chari and Wilson 2001; Wilson and
Valenzuela 2002). Temporal divergence seems to be important
in sunflower speciation, where Helianthus paradoxus
flowers substantially later than both parental species (Heiser
et al. 1969). However, the effectiveness of this temporal
barrier to hybridization has not been quantified.
Can the New Combinations of Traits and Genes
Responsible for Niche Divergence Be Generated via
Hybridization?
One feature of homoploid hybrid speciation that renders it
unique relative to most other modes of speciation is the
potential for experimental manipulation. Synthetic hybrids
between parental taxa can effectively serve as approximations
of the ancestral genotype of the hybrid species, in
contrast to the situation for most modern species, where the
progenitor is unknown or extinct. It is straightforward,
therefore, to test whether the traits or trait combinations
required for ecological divergence could have been generated
by hybridization. The alternative possibility is that the
ecological divergence was mostly achieved after speciation
through the gradual accumulation of new mutations. As far
as we are aware, these experiments have only been carried in
two systems: Argyranthemum and Helianthus.
Brochman et al. (2000) created synthetic F2 hybrids
between Argyranthemum broussonetii and A. frutescens, the
putative parents of the homoploid hybrid species A. sundingii,
and grew them in the greenhouse along with the pure species.
The hybrid species was intermediate between the two
parental species for all nine measured traits, though usually
closer to A. frutescens than A. broussonetii. The synthetic
hybrids overlapped the phenotypic range of the homoploid
hybrid species for eight of nine traits, showing that the traits
could be produced easily via hybridization. The authors
suggested that A. sundingii was likely generated via a backcross
toward A. frutescens, so a BC1 or BC2 population
would presumably have yielded an even greater overlap in
phenotype.
In sunflowers, hybrid species exhibit many traits that are
extreme relative to parental species, rather than being
exclusively intermediate (Rosenthal et al. 2002; Schwarzbach
et al. 2001). Multiple experiments have been conducted in
the greenhouse and in the natural habitats of the three hybrid
species to evaluate the potential for recreating these extreme
traits in synthetic hybrids (second generation backcrosses
toward both parents; hereafter BC2Ann and BC2Pet).
Analyses of 40 traits in greenhouse-grown plants revealed
that the ancient hybrid species’ trait values could be fully
recovered in synthetic hybrids for all extreme traits in
H. anomalus and H. deserticola and all but three extreme traits
in H. paradoxus (Rieseberg et al. 2003; Rosenthal personal
communication).
For the field experiments, which are more relevant
ecologically, individuals of H. annuus, H. petiolaris, and one of
the hybrid species were planted in that hybrid species’ native
habitat along with the synthetic hybrids. However, the results
were similar. Helianthus anomalus, a desert sand dune endemic,
was positively transgressive for leaf succulence and negatively
transgressive for leaf nitrogen in its natural habitat
(Ludwig et al. in press). Synthetic hybrids overlapped
H. anomalus for both traits, although for leaf succulence the
overlap was slight. Helianthus deserticola, found in the xeric
environment of the Great Basin Desert, was negatively
transgressive for leaf area, stem diameter, and flowering date.
As in the greenhouse studies, extreme values for all three
traits were recovered in synthetic hybrids (Gross et al. 2004).
Helianthus paradoxus inhabits highly saline desert marshes and
field-grown plants were transgressive for five traits: sulfur,
calcium, and boron content; leaf shape; and leaf succulence
(Lexer et al. 2003b). However, unlike the greenhouse
experiments, synthetic hybrids overlapped the H. paradoxus
phenotype for all five traits despite the fact that only BC2Pet
hybrids were tested. These experiments show that extreme or
transgressive phenotypes for ecologically relevant traits can
be re-created via hybridization.
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The sunflower work was extended to determine the
genetic mechanism underlying the generation of extreme
trait values in the synthetic hybrids and to ask if the same
mechanism was responsible for production of similar traits
during the origin of the ancient hybrid species more than
60,000 years ago (Gross et al. 2003; Schwarzbach and
Rieseberg 2002; Welch and Rieseberg 2002). Mapping of
quantitative trait loci (QTLs) in the greenhouse-grown
synthetic hybrids described earlier (Lexer et al. in press;
Rieseberg et al. 2003), as well as those raised in the
H. paradoxus habitat (Lexer et al. 2003a) revealed that extreme
or transgressive trait values were almost certainly generated
by complementary gene action. This makes sense given that
complementary gene action has proven to be the primary
cause of transgressive segregation in crop hybrids (e.g.,
deVincente and Tanksley 1993). Furthermore, it was shown
that closely linked or pleiotropic QTLs generally had effects
in same direction with respect to the phenotypes of the
hybrid species. Given these favorable genetic correlations, it
should be feasible to generate the complex, multitrait
phenotypes of the ancient hybrid species after only a few
generations of recombination.
Despite evidence of feasibility, the possibility remains
that phenotypic/ecological divergence was mostly achieved
after speciation through the gradual accumulation of new
mutations and that the detected hybridization was coincidental
to the process. This objection is laid to rest,
however, by comparisons of the QTL mapping data with
detailed genetic maps of the diploid hybrid species
(Rieseberg et al. 2003). If the phenotypes of the diploid
hybrid species arose through complementary gene action as
hypothesized, then we should be able to predict the genomic
composition of the hybrid species from the QTL mapping
data. Parentage of 71.8% of markers in H. paradoxus,
75.6% of markers in H. anomalus, and 79.3% of markers
in H. deserticola was predicted correctly ( p  .0001 for all
comparisons), indicating that hybridization and complementary
gene action did contribute to the phenotypic and
ecological divergence of ancient sunflower hybrids.
Are Traits and Genes Responsible for Ecological
Divergence under Divergent Natural Selection in the
Habitat of the Hybrid Species?
Synthetic hybrids are useful not only for evaluating trait
expression but also for re-creating the selective pressures
acting on hybrid neospecies at their origin. If ecological
selection was important in speciation and shaped the
phenotype and genotype of the hybrid species, then selection
acting on synthetic hybrids in the field should favor the trait
values found in present-day populations of the ancient
hybrid species. Such investigations have only been carried
out in Helianthus to date; we report the results here.
Parallel phenotypic selection experiments (Lande and
Arnold 1983) have been carried out in the habitat of all three
hybrid sunflower species to estimate the strength and
direction ecological selection acting on early generation
hybrids in the field. Selection differentials and gradients were
calculated for synthetic BC2 hybrids (described earlier), with
a focus on traits that are transgressive in the hybrid species
today. Overall, these field experiments have shown that
many of the extreme traits found in the ancient hybrid
species could have arisen via divergent ecological selection
acting on transgressive hybrids growing in novel habitats.
These traits include high leaf succulence in H. anomalus
(Ludwig et al. in press), small leaves and early flowering in
H. deserticola (Gross et al. 2004), and high leaf succulence,
high calcium content, and low uptake of toxic elements in
H. paradoxus (Lexer et al. 2003b).
However, these studies failed to detect significant
selection on several traits, and in several instances selection
was not in the predicted direction. It may be that these
contradictory results are an artifact of the restricted spatial
and temporal scale of the selection experiments. Given that
selection fluctuates over both time and space (Grant and
Grant 2002), it is not surprising that selective pressures
measured over a single growing season are not fully consistent
with predictions based on current phenotypes of the
hybrid taxa. Despite these shortcomings, the experiments
successfully demonstrate that divergent ecological selection
may allow transgressive sunflower hybrids to colonize new
habitats and thereby achieve some degree of habitat isolation
from their progenitors.
Is Selection Strong Enough to Allow Divergence in the
Face of Gene Flow?
Because hybrids are necessarily produced in proximity with
one or both of their parental species, homoploid hybrid
speciation represents a kind of speciation with gene flow,
which requires that the strength of selection on individual
loci, s, exceed the migration rate, m. The fact that introgression
is a far more frequent outcome of hybridization
than speciation implies either that this condition is rarely met
or that open niches are rarely available for colonization by
hybrids (Arnold 1997; Buerkle et al. 2000; Rieseberg and
Wendel 1993). In those cases where hybrid speciation has
occurred, it is necessary to determine whether ecological
selection alone would have been strong enough to drive
divergence or whether migration rates had to be reduced by
some other form of isolation (e.g., chromosomal or spatial
isolation) before ecological divergence could occur.
The parameter m can be estimated fairly easily from
population-level surveys of molecular markers, such as microsatellites.
Approximating s is more challenging, because
loci controlling a trait of interest must identified and relative
fitness must be estimated for individuals that segregate for
parental species’ alleles at that locus. This combination of
fieldwork and genetic mapping is rare, so the relationship
between migration and selection has only been calculated for
hybrid taxa in the genus Helianthus.
The phenotypic selection study in H. paradoxus was
extended to the genetic level via QTL analyses of the
population of synthetic hybrids grown in salt marsh habitat.
Selection coefficients on individual salt tolerance QTLs in
the H. paradoxus habitat were large (þ0.126, ÿ0.084, and
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Gross and Reiseberg  Ecological Genetics of Hybrid Speciation
ÿ0.094) (Lexer et al. 2003a). Current estimates of the
parameter Nem for annual sunflowers are consistently less
than or equal to 1. Thus, a slight excess of 12 individuals
would be sufficient to allow selection on the founding
population of the H. paradoxus lineage to overcome the
homogenizing effects of gene flow. The analysis also
revealed that QTLs contributing to increased fitness in the
salt marsh were derived from both parental species, as
predicted by the complementary gene action model if
hybridization facilitated adaptation to this new environment.
The phenotypic selection study on the desert floor was
likewise expanded to the genetic level, focusing on the
BC2Pet cross due to its similarity to the H. deserticola
phenotype (Gross unpublished data). The study in the
H. deserticola habitat took advantage of the large number of
QTLs controlling morphological, physiological, and life
history traits that had been documented for the BC2Pet cross
in a previous greenhouse study (Rieseberg et al. 2003), rather
than constructing a new QTL map. Each chromosomal
interval containing a QTL for a trait of interest in the
greenhouse was considered as a candidate QTL region in the
field population, and the BC2Pet field population was
genotyped for the microsatellite markers flanking these
intervals. Microsatellites bounding the candidate intervals for
each trait were compiled into map order based on Lexer et al.
(2003a), and QTL presence was tested using interval
mapping in Map Manager QTX (Manly et al. 2001). Tests
were performed at 1 cm steps, and threshold values for
declaring the potential presence of a QTL were determined
by 1,000 permutations of the data for each trait. Three QTLs
were found; two that were significant at p , .05 and one with
marginal significance (p ¼ .065). The approximate location of
a QTL was established as the chromosomal region where the
likelihood ratio score (LRS) exceeded the significance level.
Selection coefficients on individual QTLs contributing
to adaptive traits (leaf width and stem diameter) in the
H. deserticola environment ranged from ÿ0.027 to ÿ0.050
(Table 3). Although these values are somewhat lower than
those reported for the H. paradoxus habitat, they still are
considerably larger than those likely required for divergence
in parapatry. Our crude estimates indicate that divergence
could occur so long as the ancestral population exceeded
’ 37 individuals, which seems plausible given that
most sunflower populations number in the hundreds or
thousands.
Is There Evidence of Parallel Hybrid Speciation?
Schluter (2000) argues that recurrent speciation is unlikely in
the absence of parallel selective pressures resulting from
adaptation to similar features in the environment. Parallel
speciation is therefore viewed as ‘‘compelling evidence that
divergent natural selection has ultimately brought about the
evolution of reproductive isolation’’ (Schluter 2000, p. 378).
However, there are possible exceptions to this general rule.
Polyploid species, for example, frequently have multiple
origins in the absence of parallel selection. Likewise,
homoploid hybrid species may converge toward a similar
genomic composition due to fertility selection rather than
parallel natural selection (Rieseberg 2000; Rieseberg et al.
1996). However, in homoploid hybrid speciation, fertility
selection does not typically confer parallel ecological changes
(Rieseberg personal observations). Thus the recurrent
formation of ecologically isolated homoploid hybrid species
does indeed provide evidence that speciation was driven in
part by divergent natural selection.
Have the homoploid hybrid species described earlier
arisen multiple times? This is a difficult question to answer
because patterns of molecular variation that appear most
consistent with multiple hybrid speciation events almost
always have alternative explanations (Gross et al. 2003). For
example, the common observation that populations of the
homoploid hybrid species show geographic partitioning of
molecular markers can be explained by multiple hybrid
speciation events or a single speciation event, followed by the
sorting of ancestral variation or local introgression between
the hybrid species and one of the parental species. Therefore,
the evidence supporting claims of multiple origins must be
considered carefully.
Argyranthemum sundingii was the first homoploid hybrid
species for which multiple origins were proposed (Brochmann
et al. 2000). Recurrent speciation was inferred from the
presence of different chloroplast DNA types (one from each
parent), in the two known populations of the species. The
authors suggested that each population had been generated
in situ in separate valleys from local parental populations,
Table 3. Putative QTL linkage groups, interval markers, positions, percent phenotypic variance explained (PVE), additive effects,
proxy microsatellite marker, and selection coefficient (s) for two traits under selection in a second generation backcross (BC2)
population of Helianthus annuus 3 H. petiolaris toward H. petiolaris grown in the habitat of H. deserticola.
Trait
Linkage
group Interval markers
Position
(cM)
PVE
(%) Additive effect LRS Markera
s
Stem diameter 7 ORS702b-ORS163 87–118 3 ÿ1.04 8.7b
ORS163 ÿ0.027
Leaf width 10 ORS591-ORS256 0–11 4 þ3.57 12.7c
ORS256 ÿ0.050
10 ORS3-ORS691 26–28 4 þ3.17 8.9c
ORS3 ÿ0.031
a
Marker used as a proxy for QTL to calculate value of s.
b
LRS value marginally statistically significant, p ¼ .065 based on 1,000 permutations of the data.
c
LRS values exceed the level for statistical significance based on 1,000 permutations of the data.
248
Journal of Heredity 2005:96(3)
although it is impossible to disprove that this pattern resulted
from a single origin followed by dispersal. More recently, the
researchers documented some karyotypic divergence in
different populations of the hybrid species, providing further
support for multiple origins (Borgen et al. 2003).
Possible multiple origins of the diploid hybrid species
P. densata have been investigated carefully, taking advantage
of the fact that chloroplast DNA is paternally inherited and
mitochondrial DNA is maternally inherited in Pinus (Song
et al. 2003; Wang et al. 2001). Patterns of variation in
allozymes, chloroplast DNA, and mitochondrial DNA show
that different populations of P. desata have very diverse genetic
compositions, with varying degrees of genomic contributions
from each parental species. Strikingly, each parental
species has served as a maternal parent in some P. densata
populations and a paternal parent in others (i.e., the
hybrid species shows reciprocal parentage). These differences
suggest that populations of the hybrid species have
experienced unique evolutionary histories and most likely
have independent origins.
The repeatability of diploid hybrid speciation in H.
anomalus and H. deserticola was evaluated using evidence from
patterns of variation in chloroplast DNA, nuclear microsatellite
loci, and population cross-viability/chromosomal
structure. A single origin would likely result in a single
chloroplast DNA type, monophyly for the hybrid species
based on microsatellites, and high interfertility among all
populations. Multiple origins, on the other hand, could
potentially result in multiple chloroplast DNA types, paraphyly
for the hybrid species, and perhaps sharp divisions
in interfertility among populations.
H. anomalus was monophyletic based on microsatellite
loci, but the patterns of chloroplast DNA variation and
crossability were consistent with three independent origins
of the homoploid hybrid species (Schwarzbach and Rieseberg
2002). This combination of data is especially compelling
because differences in chloroplast DNA type were correlated
with population interfertility, a pattern that would be unlikely
if variation in either trait were due to introgression with the
parental species. Sorting of ancestral variation also seemed
an unlikely explanation for the pattern, in that it would
require that the ancestral population include chloroplast
DNA from geographically distant populations of the parental
populations. H. deserticola was paraphyletic with the
parental species H. petiolaris based on microsatellites, and also
contained chloroplast DNA types characteristic of both
parental species (Gross et al. 2003). Although these patterns
are suggestive of multiple origins, they were not as well
supported by population interfertility as in the H. anomalus
example.
There are now four diploid hybrid species that are
thought to be the result of parallel speciation. Even if the
evidence in some of these cases is due to causes other than
multiple origins, it is remarkable that this outcome is
supported so much more frequently than single origins,
which have only been confirmed once (Welch and Rieseberg
2002). Given the limited number of homoploid hybrid
species in the literature, the large proportion that appear to
be multiply derived strongly implies that ecology is a frequent
and significant contributor to this mode of speciation.
Conclusions
Our understanding of the ecological genetics of homoploid
hybrid speciation has increased remarkably over the past five
years. The rapid progress in this area reflects not only the
availability of appropriate molecular tools but also the
changes in prevailing views about the evolutionary forces
driving hybrid speciation in response to new scientific
developments. The majority of early research on homoploid
hybrid speciation focused almost exclusively on the development
of chromosomal isolation. Chromosomal divergence,
generated via recombination of divergent parental
chromosomes or de novo in hybrids, was thought to provide
initial isolation between the hybrid neospecies and its
progenitors, thereby facilitating further divergence. Because
the process was thought to be governed primarily by drift
(Grant 1958; Stebbins 1957), hybrids with the same parental
species were expected to differ in genome content. Subsequent
research, however, indicated that deterministic
forces such as selection for fertility and viability could shape
the genomes of some hybrids, apparently overcoming the
effects of drift (Rieseberg et al. 1996).
As more examples of homoploid hybrid speciation were
identified with molecular data, the potential importance of
nonchromosomal isolating barriers became evident, especially
ecological barriers (e.g., Arnold 1993; Arnold et al.
1990; Rieseberg 1991; Rieseberg 1997). These observations
were incorporated into theory, which showed that homoploid
hybrid species were most likely to arise under
conditions of strong ecological selection and that ecological
divergence was critical for persistence of the new species
(Buerkle et al. 2000; McCarthy et al. 1995).
As shown in this review, empirical evidence gathered to
test the role of ecological selection is consistent with theory.
Essentially all of the taxa fulfill at least one of the six criteria
and two species (both Helianthus) fulfill all six:
1. Many, if not all, homoploid hybrid species are ecologically
divergent as compared to parental species, and in
some cases have colonized extreme habitats.
2. Reproductive isolation is a likely outcome of the types of
ecological divergence found in nature, although much
more work is required to confirm this for all groups.
3. Traits found in hybrid species, presumably those
facilitating the colonization of new habitats, often can
be re-created via hybridization according to both
greenhouse and field experiments.
4. Natural selection favoring the trait values of contemporary
hybrid species’ populations has been demonstrated
in synthetic hybrids transplanted into the habitat of the
former.
5. Selection on individual QTLs contributing to habitat
isolation can be strong enough to bring about divergence
even in the presence of gene flow with parental
populations.
249
Gross and Reiseberg  Ecological Genetics of Hybrid Speciation
6. Molecular evidence suggests parallel homoploid hybrid
speciation is the rule rather than the exception.
Finally, comparative mapping studies in Helianthus have
shown that the current genomic composition of the
homoploid hybrid species corresponds very closely to what
is predicted based on the phenotypes of those species and the
QTLs mapped in the parental species. Thus, habitat mediated
selection acting on transgressive hybrids allowed adaptation
to the extreme habitats where the ancient hybrid species are
now found. Although this comparative mapping approach
may not be feasible in all systems, it provides the strongest
evidence that natural selection acting on variation created by
hybridization created the phenotypes we now see in nature.
It is important to note that although the experimental
work to date has been a useful first step toward understanding
the ecological genetics of homoploid hybrid
speciation, research is complicated by the fact that reproductive
isolation in many groups may be based on both
ecological (habitat divergence) and nonecological (chromosomal
differences) factors. For example, Kirkpatrick and
Barton (1997) argue that habitat colonization is inhibited by
gene flow from the center of a species’ range rather than
limited genetic variance. If they are correct, then it might be
that ecological divergence in hybrid lineages is made possible
by chromosomal isolation rather than new hybrid gene
combinations. Information from systems where reproductive
isolation is purely ecological would be especially useful in
this regard. Of course, the results of such work would be
interesting not only in reference to homoploid hybrid
speciation but also because of implications for the closely
related phenomena of sympatric and ecological speciation
(Schluter 2001; Via 2001).
Acknowledgments
Aaron O. Richardson, Benjamin K. Blackman, and Sarah R. Schaack all
provided valuable time and input for manuscript preparation. The authors
thank Jennifer L. Durphy, Amanda L. Posto, Sophie Karrenberg, and Nolan
C. Kane for their assistance with data collection and analysis in the H.
deserticola project. Funding for this project was provided by the National
Science Foundation Integrative Graduate Education and Research Traineeship
and Predoctoral Fellowship to B.L.G. and National Institutes of Health
grant ROI-G59065 to L.H.R. This paper is based on a presentation given at
the symposium entitled ‘‘Genomes and Evolution 2004,’’ cosponsored by
the American Genetic Association and the International Society of
Molecular Biology and Evolution, at The Pennsylvania State University,
and Evolution 2004, State College, PA, June 17–20, 2004.
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Corresponding Editor: Shozo Yokoyama
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