Anthropogenic disturbance promotes hybridization between
Banksia species by altering their biology
B. B. LAMONT,* T. HE,* N. J. ENRIGHT,* S. L. KRAUSSৠ& B. P. MILLER* *Department of Environmental Biology, Curtin University of Technology, Perth, Australia
School of Anthropology, Geography and Environmental Studies, University of Melbourne, Parkville, Australia
àBotanic Gardens and Parks Authority, Kings Parks and Botanic Garden, West Perth, Australia
§School of Plant Biology, University of Western Australia, Nedlands, Australia
Keywords:
Abstract
anthropogenic disturbance;
Banksia;
flowering phenology;
hybridization.
Putative hybrids between Banksia hookeriana and B. prionotes were identified
among 12 of 106 populations of B. hookeriana located at or near anthropogenically disturbed sites, mainly roadways, but none in 156 undisturbed
populations. Morphometrics and AFLP markers confirmed that a hybrid
swarm existed in a selected disturbed habitat, whereas no intermediates were
present where the two species co-occurred in undisturbed vegetation.
Individuals of both species in disturbed habitats at 12 sites were more
vigorous, with greater size and more flower heads than their counterparts in
undisturbed vegetation. These more fecund plants also showed a shift in
season and duration of flowering. By promoting earlier flowering of
B. hookeriana plants and prolonging flowering of B. prionotes, anthropogenic
disturbance broke the phenological barrier between these two species. We
conclude that anthropogenic disturbance promotes hybridization through
increasing opportunities for gene flow by reducing interpopulation separation,
increasing gamete production and, especially, promoting coflowering.
Introduction
Hybridization between plant species can provide the raw
material for adaptive evolution in rapidly changing environments (Arnold, 1997; Rieseberg & Carney, 1998).
Hybrids are often associated with disturbed habitats
(Anderson, 1948; Arnold, 1997). Disturbances can foster
co-colonization by normally allopatric species, creating
opportunities for hybridization and suitable habitats for
the survival of hybrids. Human disturbance of natural
habitats has increasingly promoted hybrid establishment
between previously isolated species (Loneragan, 1975;
Neuffer et al., 1999; Bleeker & Hurka, 2001). Should there
be hybrid genotypes with superior competitive abilities or
wider environmental tolerances, they may gradually
replace one or more parent species, depending on the
Correspondence: Prof. Byron Lamont, Department of Environmental
Biology, Curtin University of Technology, PO Box U1987, Perth,
WA 6845, Australia.
Tel.: +61 89266 7368; fax: +61 89266 2495;
e-mail: [email protected]
abundance of parents and opportunities for hybridization
(Levin et al., 1996; Bleeker & Hurka, 2001).
Mechanisms that reduce or prevent gene exchange
between otherwise compatible species include selective
pollinator behaviour (Hopper & Burbidge, 1978), spatial
barriers (Grant, 1963) and asynchronous flowering
(McIntosh, 2002). Although co-occurrence is not essential for hybridization (pollen may be wind-dispersed,
many pollinators are strong fliers), coflowering is
essential. We demonstrate here that a previously
unrecognized side-effect of anthropogenic disturbance is
that it can induce coflowering between species normally
displaying asynchronous flowering in undisturbed sites.
Together with increased gamete production in disturbed
sites, this increases the chance of gene exchange between
closely related species even when they do not co-occur.
Banksias are dominant components of the extensive
sandplain flora of Australia (Taylor & Hopper, 1988; Low &
Lamont, 1990). Their reproductive parts are a major
food resource for indigenous animals, and their
spectacular blooms are a focus for the ecotourism and
J. EVOL. BIOL. 16 (2003) 551–557 ª 2003 BLACKWELL PUBLISHING LTD
551
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B. B. LAMONT ET AL.
floriculture (wildflower-picking) industries. Banksia
hookeriana Meissn. is a shrub, up to 4 m tall, that is
restricted to the upper slopes and crests of deep sand dunes
in a 75 · 25 km area, 300 km north of Perth, Western
Australia (Lamont et al., 1989). These are among the
poorest soils known, with low levels of all nutrients and
low water holding capacity (Lamont, 1995). Banksia
prionotes Lindl. is a tree up to 10 m tall, in the lower parts
of dune systems, on calcareous uplands or along drainage
lines, with a distribution area of 815 · 125 km (extending
600 km north and 360 km south-east from Perth).
Although their distribution ranges overlap, B. hookeriana
and B. prionotes usually occupy different parts of the
landscape, although they are sometimes interspersed.
Both species are pollinated by the same nectar-feeding
birds (Meliphagidae), including the white-cheeked honeyeater (Phylidonyris nigra) and brown honeyeater (Lichmera indistincta) (Taylor & Hopper, 1988; personal
observations). Even where populations are separated by
several hundred metres, they are well within the daily
feeding ranges of these birds (Collins & Rebelo, 1987).
On morphological and phylogenetic grounds,
B. prionotes and B. hookeriana are considered sister species
(George, 1981; Thiele & Ladiges, 1996). Flowering times
are mainly January to May for B. prionotes, and June to
October for B. hookeriana (Taylor & Hopper, 1988; Sedgley
et al., 1994). Artificial crossing between B. hookeriana and
B. prionotes has shown that the two species can hybridize
readily, with similar levels of seed set as for natural
pollination of the two species (Sedgley et al., 1996).
George (1984) noted that presumed hybrids among
banksias are rare in Western Australia: ‘only recently
have they been reported … possibly between B. prionotes
and B. hookeriana’. From the above discussion, asynchronous flowering appears to be the most likely cause for the
rarity of these hybrids.
In a recent survey of the distribution of B. hookeriana,
we identified several populations with apparent hybrids
between these two species at disturbed sites (roadways,
tracks, abandoned mine pits, railway lines, firebreaks). It
was noted earlier that individuals of banksias along
roadways are much more fecund than in undisturbed
vegetation (Lamont et al., 1994a,b). We now noted that
the flowering seasons were also extended, potentially
removing asynchronous flowering as the major barrier to
hybridization. We therefore tested the hypothesis that
anthropogenic soil disturbance promotes hybridization
between these two species by altering their biology;
specifically, that gene exchange is fostered by inducing
coflowering and promoting gamete production.
Materials and methods
Study sites
Our study was carried out in the Eneabba Plain, 240–
320 km north of Perth, Western Australia. The climate
in this area is extra-dry Mediterranean (Beard, 1976),
characterized by winter rains and summer drought.
Mean annual rainfall for Eneabba (2952¢S, 11515¢ E)
is 506 mm with a mean minimum monthly (July)
temperature of 9.2 C, and a mean maximum monthly
(January) temperature of 38.8 C. The vegetation is
scrub-heath dominated by banksias on the sand dunes,
with low heath lacking banksias in the intervening
swales. The weak to moderately acid sands are extremely
nutrient-impoverished (Lamont, 1995). The vegetation is
fire-prone and both species are killed by fire (Groeneveld
et al., 2002).
Field surveys were conducted from March to June
2002. We surveyed populations of B. hookeriana at 262
locations and recorded whether they were disturbed or
undisturbed and the occurrence of putative B. hookerianaprionotes hybrids based on morphological attributes (see
below). The survey sought to identify as many hybrid
(morphologically intermediate) plant localities as possible
within the full geographical range of B. hookeriana.
Intensive studies of selected populations were undertaken in nature reserve 39 744 (beekeepers), 15 km north
of Eneabba. The entire area was burnt in a wildfire
5.5 years before. Suitable stands of B. prionotes for the
transect study were difficult to locate (they tended to run
along disturbed sites rather than across them and rarely
flowered at this age) and so sites up to 15 km north of the
reserve were used.
Morphological and phenological analyses
We selected for intensive assessment: (a) the largest
apparent hybrid swarm located and the nearest two
populations of the parent species, and (b) an undisturbed
site where the two species were interspersed, and the
nearest populations to these species. Fifteen typical plants
were assessed in the hybrid swarm, eight paired plants of
each species in the interspersed population, and six
plants from each of the remaining four populations. The
following were measured: plant height, crown width,
maximum number of branches from a node, level of
flowering (1 ¼ early bud to 5 ¼ finished flowering), and
whether florets were persistent on old flower heads
(a feature of B. hookeriana but absent in B. prionotes).
Samples of 20 leaves from the previous growing season
were returned to the laboratory and the mean length and
mid-length width of five intact leaves were taken. Leaves
were then dried in a fan-forced oven at 65 C for 1 week
and bulk weighed. Data for the six quantitative attributes
were placed in five groups (hybrid swarm, two combined
nearest populations of B. hookeriana and B. prionotes, and
interspersed populations of B. hookeriana and B. prionotes)
and were subjected to canonical variates analysis using
SYN-TAX 5.0, Mac version (Podani, 1995). In April and
June, numbers of plants with open flower heads were
noted on 75 B. hookeriana and 240 B. prionotes plants in
the interspersed populations.
J. EVOL. BIOL. 16 (2003) 551–557 ª 2003 BLACKWELL PUBLISHING LTD
Hybridization in Banksias
Genetic analysis
Eighteen individuals of presumed ‘pure’ B. hookeriana, 16
individuals of ‘pure’ B. prionotes and 15 individuals of
their putative hybrids all measured above for their
morphological characteristics were DNA-fingerprinted
using amplified fragment length polymorphism (AFLP)
markers (Vos et al., 1995). Another two putative F1
hybrids, not included in the morphological analysis, from
another two populations were also analysed. Terminal
(actively growing) leaves from each individual were
harvested and placed in air-tight plastic bags with silica
gel in the field, and then kept at room temperature until
analysed.
The DNA was extracted from dried-leaf tissue following
a modified protocol (Doyle, 1991) involving RNAase (final
concentration 20 lL mL)1). The quality and quantity of
the extracted DNA was assessed by agarose gel electrophoresis and spectrophotometry (GeneQuant, Pharmacia,
Cambridge, UK), respectively. DNA samples were diluted
with 0.1 · TE to obtain concentrations of between 150
and 200 ng lL)1. AFLP markers were resolved using
the AFLP TM Plant Mapping Kit protocol from Perkin
Elmer Corporation (Carlsbad, CA, USA) and ABI 377
Auto-sequencer (ABI 377XL; Applied Biosystems, Foster
2 City, CA, USA). The procedure followed Krauss & Peakall
(1998). Arithmetic hybrid index scores using polymorphic
AFLP markers were calculated as described in Fritz et al.
(1994) and Hardig et al. (2000), which extended the
method of maximum likelihood proposed by Rieseberg
et al. (1998). The hybrid index was calculated using a
computer program written by Hardig et al. (2000). All
scores were standardized to range between zero (pure
B. prionotes) and unity (pure B. hookeriana).
Transect study
Flowering stage and plant size were assessed in relation
to distance from the edge of disturbance. Populations
were chosen to represent a range of soil-disturbance
types, with plants both in the disturbed site and spreading 40 m back into undisturbed vegetation. In April
2002, when B. prionotes was in full flower and
B. hookeriana was in bud, individuals along three
B. hookeriana transects (rehabilitated road gravel pit,
two highway sites) and three B. prionotes transects
(unsealed road, two highway sites) were assessed for
distance from disturbance, height, crown width, and
553
numbers of open flower heads and late buds (and thus
total flower heads). All stands had regenerated 5.5 years
ago, except two stands of B. prionotes where plants were
up to 30 years old. In June 2002, when B. hookeriana was
in substantial flower and B. prionotes almost finished, the
same flowering attributes were recorded for another
three B. hookeriana (railway line, two highway sites) and
three B. prionotes (unsealed road, two highway sites) transects. At least 60 individuals were assessed at each site.
Index of flowering was calculated as [2 (no. open
flower heads) + no. late buds] to weight flowering stage
and also minimize the occurrence of zeros (for statistical
reasons) for plants yet to flower. Biovolume of individual
plants was calculated from (4p ⁄ 3 · 6 · 6 · 6) (height +
2 · width)3 that assumes plant shape is ellipsoid (Lamont
et al., 1994a). Results per species per time of assessment
were combined for consecutive 5-m intervals along the
transects. They were also analysed using canonical
variates analysis after linearizing and placing into disturbed and undisturbed groups. Based on the expected
spread of their root systems, we considered plants to
be influenced by disturbance if they were up to 6 m
(B. hookeriana) and 14 m (B. prionotes) away (Lamont &
Bergl, 1991).
Results
Occurrence of putative hybrids
Of 262 sites with B. hookeriana populations, 156 were in
undisturbed vegetation and 106 were in disturbed sites.
Putative hybrids were present at 12 of the disturbed sites,
whereas no putative hybrids were observed in the
undisturbed vegetation (v21 ¼ 17.38, P < 0.001). Four
B. hookeriana and B. prionotes populations overlapped in
undisturbed vegetation and two (both with hybrids) in
disturbed vegetation. The remaining 10 populations had
either B. hookeriana (two) or B. prionotes (eight) present.
Morphological and phenological analyses
At plant age of 5.5 years (all arose from seedlings), there
was no overlap between B. hookeriana and B. prionotes for
seven of eight attributes measured (Table 1, Fig. 1).
Banksia hookeriana was characterized by its shorter
stature, more branches per node, smaller leaves, later
seasonal flowering and retention of old florets, compared
with B. prionotes. The putative hybrids were intermediate
Table 1 Morphology (mean ± SE) of the two Banksia species (n ¼ 20) and their putative hybrid swarm (n ¼ 15) at Beekeepers Reserve.
Eneabba in May 2002.
B. hookeriana
Putative hybrids
B. prionotes
Height (cm)
No. of branches
Leaf length (mm)
Leaf width (mm)
Leaf weight
Level of flowering
Retention of dead florets
113.1 ± 5.3
145.3 ± 11.6
177.1 ± 8.1
23.6 ± 2.7
14.0 ± 1.9
9.9 ± 0.8
166.4 ± 4.1
205.2 ± 12.8
224.9 ± 6.3
7.7 ± 0.2
11.4 ± 1.1
17.7 ± 0.6
0.18 ± 0.00
0.37 ± 0.05
0.57 ± 0.03
1.41 ± 0.15
2.91 ± 0.18
3.67 ± 0.24
–
+⁄–
+
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B. B. LAMONT ET AL.
7
BP
1
10
BH
D
B
HY
A
C
5
E
4
6
3
Frequency
Variate 2 (18.1% variance)
2
5
Variate 1 (52.4% variance)
Fig. 1 Canonical variates analysis of B. hookeriana (BH) and
B. prionotes (BP) and their putative hybrids. Group A (squares): two
populations of BH; B (diamonds): population of BH interspersed with
group D; C (circles): putative hybrid swarm; D (triangles): population
of BP; E (inverted triangles): two populations of BP. Vector 1: plant
height; 2: crown width; 3: level of flowering (in April); 4: leaf length;
5: leaf width; 6: leaf weight; 7: number of branches (square root).
Individuals represented by filled symbols retained their old florets,
whereas those with open symbols did not.
overall for all attributes, although some individuals were
indistinguishable from some individuals of either parent
species (Table 1, Fig. 1).
The interspersed populations of B. hookeriana and B.
prionotes lacked overlap of all attributes except crown
width (Fig. 1). Some individuals were larger than those
in the other two conspecific populations assessed, but
they were embedded among them on the basis of the
other six attributes. In April, no B. hookeriana individuals
at this site flowered, whereas all B. prionotes were, or had
finished, flowering. By June, < 5% of B. prionotes were in
flower, whereas all B. hookeriana were flowering.
Genetic analysis
Using three pairs of primers, 290 polymorphic AFLP
markers were obtained to calculate the hybrid index. The
index ranges from 0 to 1, with B. prionotes having a mean
of 0.161 (all < 0.2) and B. hookeriana a mean of 0.864
(all > 0.8) (Fig. 2). The putative hybrids had a mean of
0.516 (all 0.3–0.7). No marker was consistently expressed
in the hybrids, with 10 plants having an index close to
0.5; seven plants deviated further and could be higherorder crosses or introgressives. BP-29 is noteworthy
because it was identified as a pure B. prionotes in the
field but its index of 0.49 indicated that it was a hybrid.
Transect study
For both species, individuals in or near the disturbed sites
were larger (greater crown volume), produced more
flowers, and had more flower heads open or about to
open (higher index of flowering) (Fig. 3). All variables
0
0.5
0.15
0.25
0.35
0.45
0.55
0.65
0.75
0.85
0.95
Hybrid index class
Fig. 2 Histogram of standardized hybrid index for putative hybrids
(HY, 17 plants) and individuals from the nearest three populations
of B. prionotes (BP, 17 plants) and B. hookeriana (BH, 19 plants), based
on 290 AFLP markers.
were highly correlated with each other (r ¼ ±0.675–
0.915 on 178 and 239 d.f.). In April, B. prionotes had 2.6
times the level of flowering (flowers open or soon to
open) in and up to 15 m from the disturbance as
individuals further from the disturbance (Fig. 4). The
only significant flowering by B. hookeriana at this early
stage in its seasonal cycle was in the disturbed sites. By
June, the only B. prionotes still showing some flowering
were in or up to 5 m from the disturbance. Flowering by
B. hookeriana was strongly related to distance from
disturbance at this time, with 3.4 times the level of
flowering up to 10 m from the disturbance as beyond.
Assuming constant distances between species, there were
10 times more opportunities (B. hookeriana · B. prionotes
both flowering) per plant for interspecific crossing in
disturbed than undisturbed sites in April and 54 times in
June.
Discussion
For natural interspecific hybridization to occur, the
parent species must be in physical proximity (dependent
on pollinator range), they must flower at the same time,
utilize the same pollinators at least occasionally, and
have some degree of pollen compatibility (Whelan &
Burbidge, 1980; Maguire & Sedgley, 1998). Although
they are routinely pollinated by the same bird species,
and readily cross when hand-pollinated, we have shown
that hybrids are not present even among interspersed
J. EVOL. BIOL. 16 (2003) 551–557 ª 2003 BLACKWELL PUBLISHING LTD
Hybridization in Banksias
BH
4
555
(a)
Disturbed site
Up to 6 m from the edge of disturbance
More than 6 m from disturbance
25
BH
Variate 2 (11.6%)
20
3
BP
1
15
2
10
Variate 1 (54.3% of variance)
BP
0
(b)
20
15
Variate 2 (25%)
1
Old stand, > 14 m from disturbance
Young stand, > 6 m from disturbance
Old stand, in or < 14 m from disturbance
Young stand, in or < 6 m from disturbance
Index of flowering
5
2
4
10
3
5
Variate 1 (55.4% of variance)
0
≤0
Fig. 3 Canonical variates analysis of three transects combined for
each species. Vector 1: location of plant along transect; 2: loge
biovolume; 3: loge total flowers; 4: loge index of flowering.
plants of B. hookeriana and B. prionotes in undisturbed
areas. However, the parent species rarely coflower. Thus,
we conclude that the divergence of flowering times is the
critical barrier to hybridization between the two species.
However, anthropogenic disturbance does two things
relevant to promoting hybridization: the plants produce
more flowers (earlier work supported here) and their
flowering season is extended (shown here for the first
time). By promoting earlier seasonal flowering of
B. hookeriana plants and prolonging flowering of
B. prionotes, disturbed sites break the phenological barrier
between them. The net result is that production of
gametes increases and the likelihood of gene exchange is
enhanced.
Soil disturbance also creates colonization opportunities
and, as seeds are wind-dispersed (Lamont et al., 1993),
decreases interpopulation distances (we often noted both
species spread along roadways and firebreaks). Although
the distance between adjacent populations of the two
species in the absence of anthropogenic soil disturbance
may exceed 500 m, the closest populations to account for
the hybrids were still on average 112 m from each other
2.5
7.5
12.5
17.5
22.5
27.5
32.5
37.5
> 40
Distance from disturbance (m)
Fig. 4 Index of flowering (number of open flower heads or late bud)
per plant of B. hookeriana (BH) and B. prionotes (BP) in relation to
distance from edge of disturbance (0) (mean ± SE). (a) April
assessment. (b) June assessment. Three transects each with 60–100
plants combined for each species and month of assessment. Each
flower head possessed 1500–2000 florets.
(range of 5–250 m). This gives a clue to the distances that
bird pollinators may fly without losing their current
pollen load completely.
Both changes in reproductive properties can be attributed to the fact that plants in disturbed sites are larger
(Fig. 3) (Canham & Marks, 1985; Laska, 2001). Larger
plants produce more flowers (Weiner & Thomas, 1986;
Herrera, 1993; Lamont et al., 1994a,b) and plants with
more flowers have a longer flowering season (Lamont &
Watkins, 1985; Ollerton & Lack, 1998). Why the plants
should be larger in disturbed sites has been attributed to
(a) greater access to resources through reduced competition and (b) greater levels of resources. Lamont et al.
(1994a) showed that soil conductivity and levels of four
nutrients, as well as water availability, were higher in
sands supporting B. hookeriana beside roadways than in
undisturbed vegetation.
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Greater flowering in disturbed sites not only increases
the chances of crossing simply through higher gamete
production, but it is also likely to attract more pollinators
(Willson & Price, 1977). In particular, B. prionotes, as one
of the few trees in the area, is likely to dominate roadside
vegetation, maximizing its floral display relative to other
species. For a rare Banksia species, B. tricuspis, 80 km
south of our study area, van Leeuwen (1997) showed
that large plants in dense stands were preferentially
visited by honeyeaters.
Sedgley et al. (1996) were only able to induce
B. prionotes · hookeriana hybrids when B. prionotes was
the pollen donor. However, we found hybrids among
otherwise pure B. prionotes stands in nine cases, with the
nearest B. hookeriana stand 30–250 m away. Only four
hybrid populations were located among B. hookeriana
stands. The most likely explanation is that B. hookeriana
usually acts as the pollen donor. If that is so, then early
flowering by B. hookeriana, rather than late flowering by
B. prionotes, is more critical for hybridization. This
requires further investigation.
The AFLP analysis showed that our assignment of
individuals to either hybrid or ‘pure’ species status on
morphological grounds was correct in 52 of 53 cases. Our
return to the location of the B. prionotes exception (an old
gravel pit) revealed a B. hookeriana-dominant and an
intermediate hybrid present <10 m away, showing that it
was, in fact, a B. prionotes-dominant hybrid (Fig. 2). This
gives us confidence that our field identification of the
12 putative hybrid populations was correct, and supports
our conclusion that hybridization is essentially a disturbance response.
General lack of introgression in morphology and
phenology, and the fact that even the hybrid swarm
had an intermediate hybrid index, support the impression that the high incidence of hybrids we observed here
is a recent phenomenon. Only three populations could be
considered hybrid swarms (i.e. beyond the F1 generation), although the oldest populations were 30 years
old. The major highway, beside which much of our work
was conducted, was built in the 1960s. The firebreaks,
rail and gas lines, many minor roads and mine pits are
post-1970. This highlights the recent occurrence of
anthropogenic disturbance in promoting hybridization
between these species.
The F1 hybrid is fully fertile (Sedgley et al., 1996;
personal observations). At present, distribution of the
two species in the dune landscape is under strong
edaphic control (Lamont et al., 1989). Combined with
increasing opportunities for hybridization, it raises the
possibility of gradual loss of genetic integrity of the parent
species and selection favouring those individuals with
wider habitat tolerance than either parent. This would
require some form of hybrid advantage. At 5 years, the
hybrids are of intermediate stature, so have no size
advantage over B. prionotes but they might over
B. hookeriana. Personal observations indicate that the F1
and later hybrids are more fecund than B. prionotes but
less than B. hookeriana. As hybrid seeds may be blown at
least 80 m from their parents (unpublished), it is possible
that they could reach soils of intermediate properties
with that occupied by the parents that might enable
them to flourish. The net effects of these differences
in fitness, and possible changes in environmental tolerances, await investigation.
With escalating anthropogenic disturbances, including
climate change, occurring throughout the world, we can
expect increasing cases of hybridization to be reported.
No doubt some of the causes will be attributable to
associated changes in the biology of the parents, as we
have demonstrated here. Where the parent species are of
restricted distribution, as is the case with B. hookeriana,
then increasing opportunities for hybridization, introgression and selection might threaten the conservation of
genetic resources. This will occur should any combination prove to have greater competitiveness or environmental tolerances than either parent species (Levin et al.,
1996). The creation of disturbed sites should now be seen
as having biological, as well as habitat consequences on
existing species.
Acknowledgments
We thank the Australian Research Council (Discovery)
for financing this project, the Department of Conservation and Land Management for permission to work in its
reserves, Robyn Taylor, Allan and Lorraine Tinker,
Laurton McGurk, and Meifang Zhao for technical and
logistic assistance, and Scott Armbruster and another
reviewer for their helpful comments on the manuscript.
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Received 9 August 2002; revised 4 March 2003; accepted 14 March 2003
J. EVOL. BIOL. 16 (2003) 551–557 ª 2003 BLACKWELL PUBLISHING LTD