Download Are hybrid species more fit than ancestral parent species in the

doi:10.1111/j.1420-9101.2010.01950.x
Are hybrid species more fit than ancestral parent species in the
current hybrid species habitats?
L. A. DONOVAN*, D. R. ROSENTHAL* 1 , M. SANCHEZ-VELENOSI* 2 , L. H. RIESEBERG &
F. LUDWIG* 3
*Department of Plant Biology, University of Georgia, Athens, Georgia, USA
Department of Botany, University of British Columbia, Vancouver, BC, Canada
Keywords:
Abstract
desert;
fitness;
speciation;
sunflower;
survival.
Hybrid speciation is thought to be facilitated by escape of early generation
hybrids into new habitats, subsequent environmental selection and adaptation. Here, we ask whether two homoploid hybrid plant species (Helianthus
anomalus, H. deserticola) diverged sufficiently from their ancestral parent
species (H. annuus, H. petiolaris) during hybrid speciation so that they are
more fit than the parent species in hybrid species habitats. Hybrid and parental
species were reciprocally transplanted into hybrid and parental habitats.
Helianthus anomalus was more fit than parental species in the H. anomalus
actively moving desert dune habitat. The abilities to tolerate burial and
excavation and to obtain nutrients appear to be important for success in the
H. anomalus habitat. In contrast, H. deserticola failed to outperform the parental
species in the H. deserticola stabilized desert dune habitat, and several possible
explanations are discussed. The home site advantage of H. anomalus is
consistent with environmental selection having been a mechanism for
adaptive divergence and hybrid speciation and supports the use of H. anomalus
as a valuable system for further assessment of environmental selection and
adaptive traits.
Introduction
Hybridization is receiving renewed attention as an
important process in speciation (Arnold, 1997; Rieseberg,
1997; Barton, 2001; Baack & Rieseberg, 2007). For
homoploid hybridization in plants, where chromosome
number remains the same, models and empirical evidence suggest that both fertility selection (i.e. endogenous, genetic or genomic selection) and ecological
Correspondence: L. A. Donovan, Department of Plant Biology, 2502 Plant
Sciences Building, University of Georgia, Athens 30602, Georgia, USA.
Tel.: +1 706 542 2969; fax: +1 706 542 1805;
e-mail: [email protected]
1
Present address: USDA ⁄ ARS – UIUC Institute for Genomic Biology,
Urbana, IL 61801, USA.
2
Present address: Canadian Institute for Health Information,
4110 Yonge Street, Suite 300, Toronto, ON M2P 2B7, Canada.
3
Present address: Earth System Science and Climate Change group,
Wageningen University and Research Centre, 6700 AA Wageningen,
the Netherlands.
selection (i.e. environmental or environment-dependent
selection) play large roles in the speciation process
(Rieseberg et al., 2003; Lexer & Fay, 2005; Karrenberg
et al., 2007). Initial hybridization events can reveal
cryptic variation via transgressive segregation, creating
new phenotypes that can allow them to escape to
habitats where the hybrid traits are more successful than
parental traits (Rieseberg et al., 1999, 2003). Reproductive isolation of hybrids from parentals is then likely
because of several mechanisms (incompatibility of
genomes, assortative mating, spatial isolation) and
facilitates the potential for further environmental selection in the hybrid habitat (Buerkle et al., 2000; Mavarez
et al., 2006; Buerkle & Rieseberg, 2007; Hendry et al.,
2007; Lowry et al., 2008a,b). This leads to the expectation
that in the hybrid habitats, the hybrid species should
have higher fitness than parental species, with the caveat
that habitats may have changed since speciation
occurred. We test this expectation for two homoploid
hybrid Helianthus species.
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Helianthus anomalus (sand sunflower) and H. deserticola
(desert sunflower) are diploid species resulting from the
hybridization of the same two ancestral parental species,
Helianthus annuus (common sunflower) and Helianthus
petiolaris (prairie sunflower) (Rieseberg, 1991; Rieseberg
et al., 1996). Both hybrid species appear to have originated within the last 200,000 years and potentially have
multiple origins (Schwarzbach & Rieseberg, 2002; Gross
et al., 2003, 2007), although much earlier dates of origin
are currently being evaluated (L. H. Rieseberg, unpublished data). The parental species H. annuus and
H. petiolaris are widespread and occur throughout the
central and western United States in disturbed habitats.
Helianthus annuus occurs on mesic clay-based soils,
whereas H. petiolaris occurs on relatively drier and sandier soils. The hybrid species are restricted to the semi-arid
Great Basin and Colorado Plateau regions of the western
United States and are endemic to desert dune habitats
that appear to be more extreme than the parental
habitats (Comstock & Ehleringer, 1992; Schwarzbach
et al., 2001; Gross et al., 2003). Thus, despite overlap in
geographic range, the hybrid species habitats are generally spatially isolated from the parent species, with little
seed dispersal among the habitats. The hybrid species are
also morphologically distinct from the parental species,
with a mixture of parent-like and transgressive traits
(Schwarzbach et al., 2001; Rosenthal et al., 2002, 2005a;
Rieseberg et al., 2003; Karrenberg et al., 2007).
Helianthus anomalus is restricted to actively moving
desert sand dunes in Utah and northern Arizona,
occupying unstable substrates that have low plant cover
and low soil nitrogen (N), but tend to store more water
than adjacent stabilized areas with finer soil texture
(Pavlik, 1980; Hamerlynck et al., 2004; Rosenthal et al.,
2005b; Grigg et al., 2008). Previous studies contrasting
H. anomalus morphology to that of parental species have
noted likely adaptations to the active desert dune habitats
such as large seeds with reserves for substantial root
production, succulent leaves that may enhance water
status or resist abrasion and lower relative growth rate
that conserves nitrogen (Schwarzbach et al., 2001;
Brouillette et al., 2006). Phenotypic selection analyses
of leaf ecophysiological traits indicate that the ability to
maintain a high leaf N is an important adaptation in this
habitat (Donovan et al., 2009). Helianthus anomalus does
have higher N use efficiency than its parental species,
facilitated by longer leaf lifetime and contributing to
greater tolerance of low nutrient stress (Aerts & Chapin,
2000; L. C. Brouillette & L. A. Donovan, unpublished
data).
Helianthus deserticola occurs on stabilized sandy soils on
the desert floor in Nevada, Utah and Arizona. The
stabilized dune habitat is characterized by more plant
cover and higher soil N than that of H. anomalus, but
lower plant water availability as the growing season
progresses because of soil texture and competition from
other plants (Rosenthal et al., 2005b; Donovan et al.,
2007). Previous studies contrasting H. deserticola to parental species have noted likely adaptations to the stabilized
desert dune habitats such as smaller leaves that reduce
leaf temperatures and transpirational water loss, and
earlier flowering that increases the likelihood of reproduction as water availability declines through the season
(Rieseberg et al., 2003; Gross et al., 2004). Phenotypic
selection analyses reinforce the importance of flowering
time in this habitat and additionally suggest that phosphorus and boron nutrition maybe more important than
N (Gross et al., 2004; Donovan et al., 2009).
The objective of this study was to test whether two
hybrid species (H. anomalus and H. deserticola) are more
fit than the parental species (H. annuus and H. petiolaris)
in the hybrid species habitats. Previous studies in 2002
provided partial data for addressing this question. In
those studies, H. anomalus seedling transplants had greater survival and biomass than those of parental species in
the H. anomalus habitat (Ludwig et al., 2004), but
H. deserticola seedling transplants failed to outperform
the parental species in the H. deserticola habitat (Gross
et al., 2004). However, seedling growth and survival is
only one component of plant fitness and may not always
reflect lifetime fitness (Campbell & Waser, 2007). In this
study, we used a combination of seed plot experiments
and seedling transplant experiments to look at germination success, seedling growth and survival, and reproductive output to provide a more complete assessment of
fitness. The performance of the hybrid and parental
species in the parental habitats is also assessed. We
additionally measured plant leaf ecophysiological traits
related to the carbon gain and water use to determine
how they differed across species and habitats, possibly
reflecting adaptive traits.
Materials and methods
The study sites were located in Utah, in the western
United States. For each study species (H. anomalus,
H. deserticola, H. annuus and H. petiolaris), an experimental study area was selected at a location where that
species naturally occurred. These experimental areas are
designated as the ANO, DES, ANN and PET habitats,
respectively. The ANO habitat was located near Jericho
Picnic area at Little Sahara Recreation Area (LSRA)
managed the Bureau of Land Management. This is an
active sand dune habitat with a very low species cover
(Rosenthal et al., 2005b). The DES habitat was also
located at LSRA approximately 5 km from the ANO
habitat on a site with stabilized sandy soils dominated by
bunch grasses, the annual invasive grass Bromus tectorum
and a few Artemisia tridentata shrubs (Rosenthal et al.,
2005b). The ANN habitat was located in Tintic Valley,
approximately 40 km from LSRA, on highway 6 just west
of Eureka, UT, in a habitat dominated by A. tridentata and
Chrysothamnus nauseosus (Donovan & Ehleringer, 1994).
The PET habitat was located in southern Utah 2 km east
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of Zion NP along highway 9 and dominated by grasses
and annual herbs. All four experimental areas have a
prior history of grazing by cattle or sheep. The experimental areas were fenced to deter cattle, and the plots
were weeded to remove native vegetation prior to and
during the experiments.
Seeds of the four species were collected during 2002 in
Utah and Northern Arizona. For H. anomalus, H. deserticola and H. annuus, the seeds came from LSRA. For
H. petiolaris, the seeds came from central Utah along
interstate 15 near the exit to highway 20. Seeds were
stored in a cold room until use.
Seed plot experiments
Achenes (one seeded fruits, hereafter called seeds) of all
four species were planted into all four species habitats.
Within each habitat, we established 10 seed plots, each
set up as a pentagon 1 m to a side and divided into five
triangular subplots. The four species were randomly
assigned to four of the subplots, 60 seeds per subplot, for
a total number of 600 seeds per species and 2400 seeds
per habitat. The remaining fifth subplot was left
unplanted as a control to assess volunteer seedlings.
Before planting, seeds were cold stratified (4 C on moist
filter paper) for four weeks to approximate the effect of
overwintering in the natural environment and to promote germination. Seeds were planted into the seed
plots, 5 cm below the soil surface, 21–25 April 2003.
After planting, seed plots were checked weekly, and
emergent seedlings marked individually with toothpicks
so the total number of seedlings germinating and dying
could be followed throughout the season. At the end of the
growing season, 3–9 September, subplots were assessed for
the number of reproductive units (buds, flowers and seed
heads) and then harvested for aboveground biomass.
Plants were sorted into vegetative biomass (stem and
leaves) and reproductive biomass (buds, flower and seed
heads), dried at 60 C and weighed.
Differences in per cent germination, biomass and numbers of reproductive units were tested with a mixed model
analysis of variance (A N O V A , SAS, 2001) with species and
habitat as fixed factors, plot as a random factor nested with
habitat and degrees of freedom determined with
Satterthwaite method. Differences between species and
habitats were tested with a post hoc LSmeans procedure.
Germination data were arcsine transformed and biomass
data were log transformed before statistical analyses to
better meet A N O V A assumptions.
Seedling transplant experiment
Seed germination was initiated 3–7 April 2003 at the
University of Georgia, following the protocols of
Schwarzbach et al. (2001) and Gross et al. (2004). After
germination and initial seedling growth, seedlings were
transported from Georgia to Utah by truck 8–10 May and
807
then maintained outside in Utah to acclimatize to local
temperature, humidity and UV conditions. Seedlings
were transplanted into the seedling plots on 15–18 May
and watered approximately every other day until 10 days
after planting. Plants that died prior to 22 May, because
of transplant shock, frost damage or burial, were
excluded from the data analyses. Seedlings of all four
species were transplanted into all four habitats, except
that H. anomalus was not transplanted into the DES
habitat because not enough individuals were available.
For the ANN, PET and DES habitats, seedlings were
transplanted into 6 blocks for a total of 60 H. anomalus, 60
H. deserticola, 60 H. annuus and 60 H. deserticola seedlings
in each habitat (except no H. anomalus seedlings in DES
garden). For the ANO habitat, seedlings were transplanted into 8 blocks, but one block was destructively
harvested mid-season and excluded from this study,
leaving 7 blocks and total of 182 H. anomalus, 70
H. deserticola, 126 H. annuus and 126 H. deserticola seedlings in the ANO habitat. We used more individuals in
the ANO habitat because this study was combined with a
phenotypic selection experiment with artificial hybrids.
The results of the selection analysis for H. anomalus are
presented in Donovan et al. (2009).
After study initiation on 22 May, plants were checked
for survival and presence of the first flower every week
until final harvest. Plants were considered dead when all
leaves were wilted or plants were completely buried in
the sand. Aboveground biomass was collected for plants
that died. Mature seed heads were collected every three
weeks to prevent them from falling on the ground and to
be able to determine total number of seed heads
produced per plant. Because many seeds matured and
dispersed between collections, it was not possible to
determine number of seeds for all seed heads and plants.
However, maturing seed heads were collected at a more
frequent interval (2–3 days) as they matured, 12–19
August in the ANO, ANN and DES habitats and assessed
for number of seeds per seed head, seed biomass and seed
head biomass. In the PET habitat, it was not possible to
collect seed heads this frequently because of the distance
from the other habitats.
Leaf traits were assessed 28 June–3 July for each live
plant with more than four leaves and at least one fully
expanded leaf for sampling: leaf size (individual leaf
area), succulence, N concentration and water-use efficiency (WUE, ratio of photosynthetic carbon gain per
unit transpirational water loss). The youngest fully
expanded leaf was collected from each plant between 6
and 8 am (when maximally hydrated), placed in Ziploc
bags to maintain turgor and subsequently measured for
leaf wet biomass and leaf area (CID, Inc., Pullman, WA,
USA). Leaves were then dried at 60C and weighed. Leaf
succulence was calculated as: (wet weight – dry
weight) ⁄ leaf area (Jennings, 1976). The leaves were
then individually ground and analysed for N concentration (per dry leaf biomass) (Carbo Erba NA 1500
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elemental analyzer, Milan, Italy) and leaf carbon isotopic
composition (d13C, Finnegan mass spectrometer, Breman
Germany). Leaf d13C provides a time-integrated measure
of leaf intercellular CO2 concentration (ci). Integrated ci
is, in turn, a relative measure of integrated instantaneous
WUE, provided leaf temperatures are similar (Farquhar
et al., 1989; Ehleringer, 1993). Greater (less negative) leaf
d13C reflects greater WUE.
At the end of the growing season, 3–9 September, all
surviving plants were assessed for the number of reproductive units (buds, flowers and seed heads) and then
harvested for aboveground biomass. Plants were sorted
into vegetative biomass (stem and leaves) and reproductive biomass (buds, flower and seed heads), dried at
60 C and weighed.
Differences in biomass, reproductive organs produced
per plant and leaf traits were tested with a mixed model
A N O V A with species and habitat as fixed factors, block as a
random factor within habitat and degrees of freedom
determined with Satterthwaite method. Differences
between species and habitats were tested with a post hoc
LSmeans procedure. Biomass data were log transformed before statistical analyses to better meet A N O V A
assumptions.
Lifetime fitness
Lifetime fitness for each species and habitat was then
calculated as the product of three stages: (i) per cent
germination from seed plots adjusted to account for
species differences in maximum germination across
habitats (i.e. multiplied by a factor of 1.48, 4.86 and
2.94 for H. anomalus, H. deserticola and H. petiolaris,
respectively), (ii) per cent survival of transplanted
seedling to first flower (from seedling plots) and
(iii) average reproductive output (seed number) for
plants that flowered (from seedling plots). Based on a
subsampling of seed heads as they matured over short
interval in August, the number of seeds per seed head
was assessed for each species in the ANO, ANN and DES
habitats. To estimate the number of seeds per seed heads
for each species in the PET garden, we first used the data
from the ANN garden because that were the most similar
to the PET garden for many traits, but we also calculated
an average for each species from all other gardens. We
present the former, but the fitness calculated by the
methods is correlated (r2 = 0.97, P < 0.001, n = 11, i.e.
all available species*plot combinations), and resulted in
the same species rankings for fitness in the PET habitat.
From the number of seeds per seed head and the number
of reproductive units, we estimated the total number of
seeds for each flowering plant.
Soil nutrient analysis
Soils were sampled 25–27 August for soil nutrient
analysis. Five soil cores were taken per habitat, with
soils sampled at 0, 25, 50 and 75 cm depths. Soils from all
depths were dried at 60 C, ground with a ball mill. Soil P
was estimated from acid persulfate extracts (Nelson,
1987) using Alpkem continuous-flow colorimetry. Soil
organic matter was determined by loss on ignition
(Schulte & Hopkins, 1996). Soils from 0 and 25 cm were
additionally assessed for pH and electrical conductivity
(EC, a common measure of soil salinity) (Robertson et al.,
1999). Samples were also submitted for analysis of N, but
the samples were all below the detection limit for %N
and there was insufficient soil remaining to reanalyse
with a more sensitive method. Differences in soil characteristics were tested with an A N O V A with habitat as a
fixed factor and soil depth as a continuous factor
followed by an LSmeans test for differences between
habitats.
Results
Seed plot experiment
For all four species and habitats, the germinating
seedlings generally emerged within a week of planting,
peaked in number alive during the first few weeks and
then declined to relatively stable numbers through
the remainder of the growing season (Fig. 1), except
for July and August mortality in the DES habitat. The
per cent germination (based on marked seedlings as
they emerged) differed by species and habitat, and
there were significant species by habitat interactions
(Table 1). Looking first at species differences in
maximum germination across habitats, H. annuus had
the highest germination rates (40.3 ± 3.9% in
ANN habitat), followed by H. anomalus (27.3 ± 4.3%
in ANN habitat), H. petiolaris (13.7 ± 1.9% in PET
habitat) and H. deserticola (8.3 ± 1.5% in ANN habitat).
Seedling germination, survival, biomass and reproduction on a subplot basis all differed by species and
habitat, with significant species by habitat interactions
(Table 1).
In the ANO habitat, a few seedlings of each species
emerged, but germination and survival were highest for
H. anomalus (Fig. 1, Table 1). Only H. anomalus seedlings
survived to reproduction in the seed plots in the ANO
habitat. For H. anomalus, germination, biomass and
number of reproductive units per subplot were lower in
the ANO habitat when compared to the parental habitats
(ANN and PET). However, in the parental habitats, the
parental species had greater biomass and more reproductive units than H. anomalus.
In the DES habitat, germination and survival were
generally higher than in the ANO habitat (Fig. 1,
Table 1). However, H. deserticola did not do better than
the parental species in the DES habitat for germination,
survival, biomass or reproductive units per subplot.
Helianthus deserticola had similar performance in its own
habitat (DES) when compared to the ANN habitat,
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DES habitat
ANO habitat
250
809
H. annuus
H. anomalus
H. deserticola
H. petiolaris
200
150
100
Number of plants alive
50
0
ANN habitat
250
PET habitat
200
150
Fig. 1 Number of live plants in seed plots.
Seeds of two hybrid species (Helianthus
anomalus, H. deserticola) and their ancestral
parent species (H. annuus, H. petiolaris) were
planted into each of the four species habitats
(ANO, DES, ANN, PET, respectively).
100
50
0
01-May
01-Jun
01-Jul
01-Aug
01-May
01-Sep
01-Jun
01-Jul
01-Aug
01-Sep
Date
Table 1 Seed plot performance of two hybrid species (Helianthus anomalus, H. deserticola) and their ancestral parent species (H. annuus,
H. petiolaris) planted into each of the four species habitats (ANO, DES, ANN, PET, respectively): germination, survival for germinated seedlings,
biomass and number of reproductive unit per plots.
Habitat
Species
Germination (%)
ANN
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
40.3
27.3
8.3
12.8
3.2
11.6
1.8
1.3
36.0
15.2
6.0
11.4
29.7
13.3
5.8
13.7
d.f.
3,34
3,102
9,102
ANO
DES
PET
Habitat
Species
Habitat* species
annuus
anomalus
deserticola
petiolaris
annuus
anomalus
deserticola
petiolaris
annuus
anomalus
deserticola
petiolaris
annuus
anomalus
deserticola
petiolaris
(3.9)a
(4.3)b
(1.5)cde
(1.8)cd
(2.0)fgh
(4.6)cde
(0.7)gh
(0.6)h
(2.6)ab
(3.0)c
(1.7)def
(2.3)cde
(4.1)ab
(2.3)c
(1.7)efg
(1.9)c
F
32***
38***
5***
Survival (%)
40.9
63.4
24.1
40.5
0.3
64.3
0.0
0.6
69.5
36.1
12.9
52.7
66.3
53.7
57.4
73.5
d.f.
3,35.3
3,92.8
9,90.8
Total Biomass (g)
(6.2)bc
(6.1)ab
(10.0)def
(10.2)bcd
(0.0)f
(13.9)ab
(0.0)f
(0.0)f
(7.3)a
(12.4)cde
(8.3)ef
(8.9)abc
(9.0)a
(6.8)abc
(10.4)abc
(6.4)a
F
15***
9***
5***
110.7
33.1
2.8
28.2
0.0
5.3
0.0
0.0
28.9
3.7
0.4
10.2
261.8
17.4
10.7
83.3
d.f.
3,34
3,102
9,102
(33.5)b
(10.4)c
(1.4)e
(9.7)cd
(0.0)f
(2.7)e
(0.0)f
(0.0)f
(3.6)c
(1.4)e
(0.2)ef
(2.2)d
(44.8)a
(3.8)cd
(3.4)d
(14.6)b
F
55***
58***
11***
Reproductive
Biomass (g)
28.8
5.0
0.9
8.2
0.0
2.2
0.0
0.0
9.8
0.9
0.1
2.1
86.4
5.5
4.5
29.5
d.f.
3,29
3,87
9,87
(9.4)bc
(1.5)e
(0.5)hg
(2.9)e
(0.0)i
(1.3)fgh
(0.0)i
(0.0)i
(1.3)cd
(0.4)ghi
(0.1)hi
(0.5)efg
(16.1)a
(0.9)ed
(1.5)ef
(6.5)b
F
30***
53***
10***
Number reproductive units
80.3
45.7
11.4
70.9
0.0
15.0
0.0
0.0
39.5
8.6
0.6
29.9
121.1
38.0
58.0
171.2
d.f.
3,29
3,87
9,87
(22.4)bc
(12.5)def
(5.8)gh
(23.8)cd
(0.0)h
(9.5)fgh
(0.0)h
(0.0)h
(4.8)defg
(4.2)gh
(0.6)h
(7.9)efgh
(29.8)b
(8.1)cdefgh
(19.7)cde
(33.1)a
F
16***
18***
5***
For F statistics, *P < 0.5, **P < 0.01, ***P < 0.001.
Data are means (SE) of 10 plots per garden. In each plot, 60 seeds of each species were planted. For each trait, means with the same letter are
not significantly different as tested with LSmeans procedure after mixed model A N O V A .
but generally did better in the PET habitat. In the
parental habitats, the parental species generally had
greater biomass and more reproductive units than
H. deserticola.
In both the ANN and PET habitats, H. annuus had
higher germination and biomass than H. petiolaris per
subplot (Fig. 1, Table 1). In the PET habitat, H. petiolaris
produced more reproductive units.
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Transplant seedling survival, biomass and
reproduction
Seedlings of all four species were transplanted into all
four habitats except that H. anomalus seedlings were not
transplanted into in the DES habitat. Seedling survival
across seedling transplant plots was not statistically
compared by species and habitat, because there was only
one seedling transplant plot per habitat. However,
seedling survival at final harvest, by species and habitat
(Fig. 2), roughly paralleled survival observed in the
seedling plots: H. anomalus seedling survival was highest
in its own habitat, but this was not true for H. deserticola
(Table 2). The declining survival of plants through the
growing season reflected both preflowering mortality and
naturally occurring senescence after flowering, particularly for H. deserticola and H. petiolaris. Therefore, survival
of transplanted seedlings to flowering was separated out
as a specific component to be included in our estimates of
lifetime fitness (Table 2). Helianthus anomalus seedling
survival to flowering was highest in its own habitat, but
again, this was not the case for H. deserticola.
For transplanted seedlings, flowering generally initiated earliest for H. deserticola and H. petiolaris in the
hybrid species habitats (ANO and DES) and latest for
H. annuus and H. anomalus in the ANN and ANO habitats
(approximately 2–4 week later). Biomass and reproduction on an individual seedling basis roughly paralleled
that of the combined seedlings in seed plots. In the ANO
habitat, H. anomalus had greater biomass and more
reproductive units than the other species (Table 2).
Helianthus anomalus also had greater biomass and more
reproductive units in its own habitat when compared to
parental ANN and PET habitats. In the DES habitat,
H. deserticola did not have greater biomass or more
reproductive units than the other species. Helianthus
deserticola also did not have greater biomass and more
reproductive units in its own habitat when compared to
parental ANN and PET habitats.
In both the ANN and PET habitats, H. annuus plants
had greater biomass than H. petiolaris. Helianthus petiolaris
produced more total reproductive units in the PET
habitat.
For transplanted seedlings, leaf traits early in the
growing season differed by species and habitat, with
significant species by habitat interactions (Table 2). The
species differences evident across all habitats were that
leaf succulence was highest for H. anomalus, leaf size was
largest for H. annuus and leaf size tended to be smallest
for H. deserticola. Comparing habitats, leaf N was generally highest for plants in the ANN habitat, followed by
the DES and then the ANO and PET habitats. Leaf WUE
was lowest for plants in the ANO habitat. Comparing
species, H. anomalus had a lower leaf N concentration
than the parental species in the parental habitats, but in
its home habitat, it maintained a leaf N concentration
similar to or greater than the parental species.
Lifetime fitness
Lifetime fitness was estimated by integrating data from
the seed plots and the seedling plots (Fig. 3). Lifetime
fitness for each species and habitat was calculated as the
product of three stages: (i) per cent germination (from
seed plots, Fig. 1, Table 1) adjusted to account for species
differences in maximum germination across habitats,
DES habitat
ANO habitat
100
80
60
40
Survival (%)
20
0
ANN habitat
PEThabitat
100
80
60
40
20
0
H. annuus
H. anomalus
H. deserticola
H. petiolaris
01-Jun
01-Jul
01-Aug
01-Sep
Date
01-Jun
01-Jul
01-Aug
01-Sep
Fig. 2 Survival of transplanted seedlings.
Seedlings of two hybrid species (Helianthus
anomalus, H. deserticola) and their ancestral
parent species (H. annuus, H. petiolaris) were
planted into each of the four species habitats
(ANO, DES, ANN, PET, respectively).
ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 805–816
JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 805–816
JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
92
53
89
96
71
88
75
80
95
––
98
100
93
71
68
95
15 Jun
7 Jun
6 Jul
28 Jun
22 Jun
14 Jun
15 Jul
9 Jul
30 Jun
29 Jun
15 Jul
9 Jul
9 Jun
9 Jun
4 Jul
Date of
first
flower
For F statistics, *P < 0.5; **P < 0.01; ***P < 0.001.
Habitat
Species
Habitat* Species
PET
DES
ANO
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
H.
ANN
annuus
anomalus
deserticola
petiolaris
annuus
anomalus
deserticola
petiolaris
annuus
anomalus
deserticola
petiolaris
annuus
anomalus
deserticola
petiolaris
Species
Habitat
Survival
first
flower
(%)
Reproductive
biomass
(g)
14.8 (1.1)a
2.1 (0.4)d
1.8 (0.3)d
6.4 (1.2)b
0.8 (0.1)ef
3.3 (0.3)c
0.4 (0.1)fg
0.3 (0.1)g
3.7 (0.3)b
––
0.5 (0.1)fg
1.9 (0.2)d
12.9 (1.0)a
1.5 (0.3)de
0.8 (0.3)f
6.0 (0.8)b
df
F
3,32
83***
3,837
147***
8,836
59***
Total
biomass
(g)
39.6 (2.6)a
6.0 (1.2)d
4.6 (0.8)d
15.2 (2.2)b
4.2 (0.4)d
15.8 (1.1)b
1.6 (0.4)ef
1.2 (0.1)f
11.9 (1.0)b
––
1.9 (0.3)e
6.5 (0.6)c
39.2 (3.3)a
4.4 (1.0)d
2.3 (0.6)de
15.4 (1.9)b
df
F
3,39
45***
3,838
154***
8,838
58***
2001 (135)b
140 (10)d
410 (53)d
1635 (173)c
269 (28)d
294 (21)d
96 (22)d
183 (22)d
489 (38)d
49 (5)d
195 (20)d
2303 (157)ab
154 (17)d
238 (77)d
2437 (239)a
df
F
3,22
36***
3,705
115***
8,704
35***
7.2 (0.7)ef
22.7 (2.2)cd
39.1 (2.8)b
10.5 (2.1)ef
14.8 (3.7)de
51.8 (5.3)a
df
F
3,41
49***
3,842
23***
8,841
50***
Seeds per
flowering plant
34.9 (2.4)b
9.0 (1.6)ef
22.3 (3.0)cd
35.2 (3.9)b
3.0 (0.3)f
25.8 (1.9)c
6.7 (1.6)ef
3.5 (0.4)f
9.4 (0.8)ef
Reproductive
units
25.2 (2.4)a
5.9 (1.0)defg
4.1 (0.3)efg
7.8 (0.7)d
12.3 (0.7)c
6.7 (0.3)de
2.7 (0.2)g
3.3 (0.2)fg
23.2 (1.2)ab
–
3.2 (0.2)g
6.0 (0.3)def
20.7 (1.5)b
5.1 (0.5)efg
2.2 (0.2)g
4.6 (0.3)efg
df
F
3,25
10***
3,731
289***
8,730
12***
Leaf size
(cm2)
(0.7)fg
(0.1)a
(0.5)efg
(0.5)gh
(0.5)ef
(0.7)a
(1.9)c
(0.8)de
(0.6)g
37.4 (0.5)de
36.4 (0.5)efg
30.7 (0.6)i
40.1 (1.1)cd
30.9 (0.6)hi
30.0 (0.4)i
df
F
3,36
34***
3,733
106***
8,732
2
34.6
47.0
35.8
33.9
36.8
50.4
41.8
37.2
34.4
Leaf
succulence
(mg cm-2)
(0.1)b
(0.1)cd
(0.1)bc
(0.1)a
(0.1)hi
(0.1)efg
(0.1)de
(0.1)efg
(0.1)d
(0.1)def
(0.1)cd
(0.1)fg
(0.1)i
(0.1)fg
(0.1)gh
df
F
3,23
20***
3,726
10***
8,725
12***
3.0
3.4
2.7
2.1
2.7
2.6
3.8
3.4
3.7
4.0
2.4
2.9
3.1
2.8
3.3
Leaf N
(%)
Table 2. Seedling performance of two hybrid species (Helianthus anomalus, H. deserticola) and their ancestral parent species (H. annuus, H. petiolaris) planted into
each of the four species habitats (ANO, DES, ANN, PET, respectively): date of first flower, total biomass, reproductive biomass, number of reproductive units, leaf size,
leaf succulence, leaf N and leaf d13C. Data are means (S.E.). For each trait, means with the same letter are not significantly different as tested with LSmeans procedure
after mixed model ANOVA.
(0.1)b
(0.1)b
(0.1)b
(0.1)b
(0.1)b
(0.1)c
(0.1)c
(0.1)c
(0.1)a
(0.1)b
(0.1)b
(0.1)b
(0.2)b
(0.3)b
(0.1)b
F
9***
29**
5***
)26.6
)26.9
)26.9
)26.7
)27.1
)27.9
)28.1
)28.0
)25.9
)27.2
)26.6
)26.8
)27.0
)27.2
)27.1
df
3,22
3,724
8,723
Leaf d13C
(&)
Hybrid species and adaption to current habitats
811
L. A. DONOVAN ET AL.
H. annuus
H. anomalus
H. deserticola
H. petiolaris
800
Lifetime fitness
Soil organic matter (g*g–1)
1000
600
400
200
0
ANN
ANO
DES
PET
Habitat
Fig. 3 Lifetime fitness of two hybrid species (Helianthus anomalus,
H. deserticola) and their ancestral parent species (H. annuus,
H. petiolaris) in each of the four species habitats (ANO, DES, ANN,
PET, respectively).
Soil total P (mg*g–1)
812
0.06
0.04
0.02
0.00
0.8
0.6
0.4
c
0.2
0.0
Soils
The habitats differed for soil characteristics. Soil organic
matter content differed by habitat and depth (habitat F3,76
= 605.1, P < 0.001; depth F3,76 = 10.3, P < 0.001; habitat*depth F9,76 = 15.4, P < 0.001). The ANN habitat had the
highest soil organic content, followed by successively lower
amounts in the PET, DES and ANO habitats (Fig. 4). Soil P
also differed by habitat and depth (habitat F3,78 = 97.3,
P < 0.001; depth F3,78 = 23.5, P < 0.001; habitat*depth
F9,78 = 4.0, P = 0.004). The ANN and PET habitats had
higher soil total P than the DES and ANO habitats.
Soil pH differed by habitat and depth (habitat
F3,37 = 160.9, P < 0.001; depth F1,37 = 46.9, P < 0.001;
habitat*depth F3,37 = 10.9, P < 0.001). The ANN, PET and
habitats generally had a lower soil pH than the DES and
ANO habitats. Soil EC also differed by habitat, although
not as dramatically as for other soil characteristics
(habitat F3,37 = 5.4, P < 0.004; depth F1,37 = 2.6,
P = 0.120; habitat*depth F3,37 = 2.3, P = 0.097 The
ANN, PET and DES habitats generally had a higher EC
than the ANO habitat.
Discussion
We tested whether the hybrid species H. anomalus and
H. deserticola were each more fit than their parental
8.4
8.0
7.6
Soil EC (µS*cm–1)
(ii) per cent survival of transplanted seedlings to flowering (from seedling plots, Fig. 2, Table 2) and (iii) average
seed production for plants that flowered (from seedling
plots, Table 2). Helianthus anomalus had the highest
lifetime fitness in its own habitat, as did each of the
parental species. Helianthus deserticola did not have the
highest fitness in its home habitat.
Soil pH
8.8
ANN habitat
ANO habitat
DES habitat
PET habitat
300
200
100
0
25
50
75
Soil depth (cm)
Fig. 4 Soil organic matter, P concentration, EC and pH for soils
collected at different depths in the hybrid species (Helianthus
anomalus, H. deserticola) and ancestral parent species (H. annuus,
H. petiolaris) habitats, designated ANO, DES, ANN, PET, respectively.
species in the hybrid species habitat, which would be
consistent with the hypothesized role of environmental
selection in the hybrid speciation process. Although these
two hybrid species are closely related (from same
ancestral parent cross) and both endemic to desert sand
dune habitats, the two hybrid species yielded very
different results in this study.
Helianthus anomalus was the most fit in its own habitat,
based on seed germination and transplanted seedling
performance. For the seed plots, H. anomalus had much
higher germination and survival than parental species in
the ANO habitat. This indicates strong selection at the
recruitment stage, probably because of the need to
ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 805–816
JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Hybrid species and adaption to current habitats
survive burial and excavation in actively moving sand
dune habitat. In the ANO habitat, we observed spring
storms to add or remove as much as 10 cm of the sandy
soil at some locations, with the amount and location of
change being highly variable and dependent on wind
speed and direction. Helianthus anomalus has much larger
seeds and thus potential reserves to achieve necessary
growth in response to burial or excavation (Chen &
Maun, 1999; Schwarzbach et al., 2001). It would be
interesting to test whether H. anomalus also has greater
ability to tolerate burial, reallocate biomass to shoot
growth when buried, elongate stems when buried, or
suberize roots when exposed (Brown, 1997).
For the seedling transplants, H. anomalus survival to
flowering was higher than parental species in the ANO
habitat, consistent with results from the previous year
(Ludwig et al., 2004). The higher survival of H. anomalus
relative to parental species in the ANO habitat was not
obviously because of any single factor. Rather, parental
species failed to thrive, possibly because of ANO habitat
soil characteristics of lower fertility and EC, higher pH
and extremely sandy soil texture that affect rooting
architecture, soil cation exchange capacity and water
retention (Pavlik, 1980; Hamerlynck et al., 2004;
Rosenthal et al., 2005b; Grigg et al., 2008). Additionally,
sand abrasion of leaves and other unknown factors likely
played a role. The higher survival of H. anomalus seedlings in the ANO habitat did not appear to be because of
differences in plant water status, based on a lack of
species differences in plant predawn water potential
measurements at mid-season (L. A. Donovan, unpublished data). The estimated number of seeds produced per
flowering plant did not differ by species within the ANO
habitat, although the low sample sizes limited statistical
power. Nevertheless, the individual seed germination
and seedling transplant studies, as well as the resulting
estimate of integrated lifetime fitness, all demonstrate a
clear home site advantage for H. anomalus.
The greater success of H. anomalus in its own habitat
came at the expense of its performance in parental
habitats. Helianthus anomalus had higher or similar
germination in the parental habitats compared to its
home habitat, but seedling survival to flowering and
seed production per flowering plant was lower in the
parental habitats. The lower inherent relative growth
rate of H. anomalus may reflect a lower competitive
ability, which might be a factor in its lack of success in
the higher plant cover of the parental habitats (Grime,
1977; Brouillette et al., 2006). However, in our experiments, the lower performance of H. anomalus in the
parental habitats likely was not because of competition
because the plants in the seedling plots were spaced
at least 30 cm apart, excavated roots did not appear to
be intertwined and all volunteer plants were periodically removed. We hypothesize that the rooting and
nutrient-related traits that allow for H. anomalus success
in its unstable sandy dune habitat come at the cost of
813
success in the parental habitat soils that are stable and
higher in clay content.
Helianthus deserticola was not most fit in its own habitat
in this study. For the seed plots, relatively few H. deserticola seeds emerged in any habitat and very few of the
emerged plants survived until reproduction. Seedlings of
H. deserticola transplanted into the DES habitat did better
than the seeds, but the parental species still had a higher
survival and produced more flowers and reproductive
biomass than H. deserticola. These results are consistent
with the seedling transplant data from the previous year
(Gross et al., 2004). Thus, none of the results for
individual fitness components, or integrated lifetime
fitness, indicate that H. deserticola is more fit than the
parental species in this DES habitat.
We can offer several possible interpretations of this
unexpected result. One interpretation is that in general
(across all sites and years), H. deserticola is not more fit
than parental species in DES habitats, suggesting that
environmental selection did not play a large role in
speciation. Although this is a possibility, we think that
this interpretation is not yet warranted given the strong
modelling and genetic evidence of the importance
of environmental selection in hybrid speciation
(Karrenberg et al., 2007) and that this study assessed
only one H. deserticola site and one year. One obvious
way to further address this question would be to repeat
the study with more sites and seed sources for each of the
species and to capture genetic and environmental
variation among populations (Schwarzbach & Rieseberg,
2002; Gross et al., 2007). This would strengthen the
inference of the study as a whole, but was not possible in
the current study because of the extensive investment of
time and resources in the seed and seedling studies at the
four chosen sites. Until more data are available, we offer
several other possibilities for consideration.
One possibility is that the H. deserticola advantage in
DES habitat is only apparent in extreme years that were
not represented this study year with average precipitation. Desert habitats are known for their extreme annual
variability in climate, particularly rainfall (Noy-Meir,
1973; Comstock & Ehleringer, 1992), and the early
flowering of H. deserticola may be particularly advantageous in drought years when soil water is depleted early
in the growing season. However, the seedling transplant
growth and survival data from this study are consistent
with those in 2002 (Gross et al., 2004), which was the
driest year out of the 28 years for which precipitation
data are available for this area (1980–2007). Thus,
although possible, we currently have no support for this
hypothesis.
A second possibility is that H. deserticola does not have
a home site advantage at this site and time because
hybrid speciation and population establishment
occurred when conditions were different. This site is at
the northern edge of the current range, and conditions
have been changing in terms of longer term climate and
ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 805–816
JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
814
L. A. DONOVAN ET AL.
shorter term invasions of exotic species. The climate of
the region where H. deserticola is found (Great Basin and
adjacent Colorado Plateau) has fluctuated since the
species is estimated to have arisen. Paleoclimate data for
the last 50 000 years indicate that precipitation and
temperatures were cooler and wetter during the North
America glacial maxima, followed by a drying and
warming trend over the last 13 000 years (Wharton
et al., 1990). However, records from pollen and woodrat
middens suggest that over this time interval, varied
topography (elevation, aspect) and microhabitat diversity provided local refugia, allowing major vegetation
associations to persist despite climate change (Wharton
et al., 1990; Nowak et al., 1994). Given the complexity
of potential plant and climate interactions, it is not
likely that we will be able to reconstruct the long-term
success of the hybrid species when compared to parental
species at this particular site.
On a shorter timescale, invasive plants have modified
much of the region where H. deserticola is found. For
example, since the late 1900s, the non-native annual
grass Bromus tectorum (cheatgrass) has invaded the Great
Basin and Colorado Plateau regions, facilitated by
domestic livestock grazing, and reduced the number of
native grasses and annual forbs (Knapp, 1996). Although
not found on the unstable dunes where H. anomalus
thrives, B. tectorum is often the dominant herbaceous
plant on the stabilized substrates where H. deserticola is
located. Bromus tectorum tends to out-compete other
annual species by depleting soil moisture early in the
growing season (Knapp, 1996). This might explain the
pattern that we observed while collecting seeds of
H. deserticola: it occurs only in areas where B. tectorum is
either locally absent or in low density. Additionally,
B. tectorum alters soil nutrient and carbon dynamics and
biota (microarthropods, nematodes, arbuscular mycorrhizal fungi), facilitates dispersal of some pathogens and
may change the herbivores in the community (Sperry
et al., 2006; Meyer et al., 2008; Rowe & Brown, 2008). In
the DES habitats study plots, we removed the B. tectorum
before planting and weeded out any volunteers, so any
effects of B. tectorum were not because of direct competition. However, it is possible that an invasive plant like
B. tectorum, or some other recent change at this DES site,
made the environment less favourable for H. deserticola
when compared to parental species. It might be possible
to test this hypothesis if H. deserticola sites can be found
that vary in the extent and duration of B. tectorum
invasion.
Another related possibility is that there is a local site
disadvantage because of local adaptation of pathogens, as
has been found for California dwarf flax and the rust
fungus Melampsore lini (Springer, 2007). Our experiments
confounded habitat site with seed collection site for the
two hybrid species. Again, reciprocal transplants among
multiple species sites and seed sources would be needed
to evaluate this possibility.
Both of the parental species had a home site advantage
based on the lifetime fitness estimate, although this
advantage was not apparent in all of the seed and
seedling stages. This is consistent with the finding that
parental species’ cytoplasms were strongly locally
adapted for hybrids of known parentage transplanted
into each species habitat in New Mexico (Sambatti et al.,
2008).
Why did the hybrid species differ in their results? One
likely reason is that the ANO habitat differed from the
parental habitats more than the DES habitat. In the ANO
habitat, the disturbance of the moving sand and the low
fertility apparently imposes stronger selection than in the
DES habitat. The ranking of soil organic content, a rough
measure of nutrient availability, was ANO < DES <
PET < ANN habitats in this study. This is consistent with
previous reports of lower soil organic content and lower
soil N in ANO than in DES habitats (Rosenthal et al.,
2005b; Donovan et al., 2007) and nutrient limitation of
H. anomalus growth in the ANO habitat (Ludwig et al.,
2006). The only soil N data available for the parental
habitats come from seed collection trips in 1999 and 2000
(n = 5–6 sites per habitat and 2–4 replicates per site, L. A.
Donovan, unpublished data). For those collection sites,
soil N was lower for the ANO when compared to the ANN
and DES sites (0.017 ± 0.004, 0.060 ± 0.011, 0.052 ±
0.01 mg g)1, respectively, P < 0.003). Thus, the two
parental habitats were again more similar to each, and
ANO habitat most extreme. The greater similarity
between the DES and parental habitats may have made
the species rankings in this hybrid habitat more labile in
response to climate change, invasive species and ⁄ or local
habitat adaptation.
The extreme nature of the ANO habitat is also reflected
in the leaf trait data. Generally, plants in the ANO habitat
exhibited among the lowest WUE, as expected based on
greater water availability, and among the lowest leaf N,
as expected based on lowest N availability. The leaf trait
patterns can also be related to phenotypic selection
results within the hybrid species habitats. Although all
species tended to have higher succulence in the ANO
habitat, and H. anomalus consistently had the highest leaf
succulence in each habitat, phenotypic selection analysis
has not demonstrated any adaptive advantage for higher
leaf succulence in the ANO habitat (Donovan et al.,
2009). The relatively high ranking of H. anomalus in the
ANO habitat for leaf N, compared to its lower ranking in
the parental habitats, is consistent with greater leaf N and
associated traits being important for fitness in the ANO
habitat (Donovan et al., 2009).
Overall, one of the hybrid species and both parental
species were more fit in their home habits than the other
habitats. This is consistent with a home site advantage
and thus local adaptation, as has been found in many
reciprocal transplant studies of populations and species
(e.g. Joshi et al., 2001; Campbell & Waser, 2007; Schemske
& Bierzychudek, 2007; Lowry et al., 2008a,b; Hereford,
ª 2010 THE AUTHORS. J. EVOL. BIOL. 23 (2010) 805–816
JOURNAL COMPILATION ª 2010 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Hybrid species and adaption to current habitats
2009; but see Kimball et al., 2008). In this case, the
known evolutionary relationship between the species,
and the models of hybrid speciation mechanisms, allow
us to interpret the clear home site advantage for
H. anomalus as consistent with environmental selection
having been a mechanism for adaptive divergence and
hybrid speciation. This makes H. anomalus a valuable
system for further assessment of environmental selection
and adaptive traits. For H. deserticola, the jury is still out.
Acknowledgments
We appreciate the help with the experiments from
Jennifer Lance, Jill Johnston, Briana Gross, Nolan Kane
and Christian Lexer. We also thank Ferris Clegg, the
Bureau of Land Management, and Little Sahara Recreation Area for use of the field site and Utah State
University for use of Tintic field station. This project was
funded by National Science Foundation grants 0131078
and 0614739 to LAD and National Institute of Health
grant GM59065 to LHR.
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Received 12 June 2009; revised 26 November 2009; accepted
12 January 2010
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