1741 7007 5 49

BMC Biology
BioMed Central
Open Access
Research article
Reciprocal diversification in a complex plant-herbivore-parasitoid

food web
Tommi Nyman*1, Folmer Bokma2 and Jens-Peter Kopelke3
Address: 1Faculty of Biosciences, University of Joensuu, FI-80101 Joensuu, Finland, 2Department of Ecology and Environmental Science, Ume
University, SE-90187 Ume, Sweden and 3Forschungsinstitut Senckenberg, D-60325 Frankfurt am Main, Germany
Email: Tommi Nyman* - Tommi.Nyman@joensuu.fi; Folmer Bokma - Folmer.Bokma@emg.umu.se; JensPeter Kopelke - Jens.Kopelke@senckenberg.de
* Corresponding author
Published: 1 November 2007

BMC Biology 2007, 5:49
doi:10.1186/1741-7007-5-49
Received: 24 September 2007

Accepted: 1 November 2007
This article is available from: http://www.biomedcentral.com/1741-7007/5/49

2007 Nyman et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background: Plants, plant-feeding insects, and insect parasitoids form some of the most complex
and species-rich food webs. According to the classic escape-and-radiate (EAR) hypothesis, these
hyperdiverse communities result from coevolutionary arms races consisting of successive cycles of
enemy escape, radiation, and colonization by new enemy lineages. It has also been suggested that
"enemy-free space" provided by novel host plants could promote host shifts by herbivores, and that
parasitoids could similarly drive diversification of gall form in insects that induce galls on plants.
Because these central coevolutionary hypotheses have never been tested in a phylogenetic
framework, we combined phylogenetic information on willow-galling sawflies with data on their
host plants, gall types, and enemy communities.
Results: We found that evolutionary shifts in host plant use and habitat have led to dramatic
prunings of parasitoid communities, and that changes in gall phenotype can provide "enemy-free
morphospace" for millions of years even in the absence of host plant shifts. Some parasites have
nevertheless managed to colonize recently-evolved gall types, and this has apparently led to
adaptive speciation in several enemy groups. However, having fewer enemies does not in itself
increase speciation probabilities in individual sawfly lineages, partly because the high diversity of the
enemy community facilitates compensatory attack by remaining parasite taxa.
Conclusion: Taken together, our results indicate that niche-dependent parasitism is a major force
promoting ecological divergence in herbivorous insects, and that prey divergence can cause
speciation in parasite lineages. However, the results also show that the EAR hypothesis is too
simplistic for species-rich food webs: instead, diversification seems to be spurred by a continuous
stepwise process, in which ecological and phenotypic shifts in prey lineages are followed by a lagged
evolutionary response by some of the associated enemies.
Background
One of the main challenges of biological research is to
understand the evolutionary assembly and maintenance
of complex, multitrophic food webs [1,2]. The classic
escape-and-radiate (EAR) hypothesis [3] envisions the

current remarkable diversity of plants and herbivorous
insects [4,5] as a result of a cyclic coevolutionary process:
a plant lineage that acquires a new defensive trait (e.g., a
Page 1 of 9
(page number not for citation purposes)
toxic chemical) becomes free to proliferate and rapidly

divides into multiple descendant lineages [3,6]. Over
time, the defenses of the new clade are overcome by some
insect species, which now enter a vacant adaptive zone
and diversify to exploit the species of the hitherto herbivore-free plant group [3,7]. A new cycle of diversification
starts whenever a novel defense evolves in one of the plant
lineages.
Although the EAR hypothesis was originally formulated in
terms of plants and herbivores, it has recently been suggested that a concurrent EAR process operates between
plant-feeding insects and their associated parasitoids
[1,8]. Parasitic insects typically inflict heavy mortality on
herbivore populations [9,10], and the specialized host use
of both insect herbivores and parasitoids leads to the
intriguing possibility that these hyperdiverse interaction
networks are created "from within", that is, by diversifying
effects that are transmitted or even amplified through
many trophic levels. "Bottom-up" speciation cascades
could result if diversification of plants spurs speciation of
herbivores [5,7,11] that, in turn, leads to increased
resource diversity for associated parasitoids [2,12,13].
"Top-down" diversifying forces could be equally important if parasitoids use plants as cues for finding their host
insects; in such cases, an evolutionary shift to a novel host
plant could provide "enemy-free space" for the herbivores
[9,14,15]. Release from enemies could accelerate diversification in the herbivore lineage that, in turn, would create
more possibilities for parasitoid speciation.
Diversifying selection exerted by natural enemies might
similarly underlie the unusual diversity of many gallinducing insect groups. The ability to induce galls on
plants has evolved convergently in dozens of distantly
related insect taxa and, as a result of spectacular adaptive
radiations, many of these groups contain hundreds of species that differ markedly with respect to their host plant
use and gall morphology [16,17]. Phylogeny-based comparative studies have demonstrated that galls represent
"extended phenotypes" of the gallers, meaning that gall
form and location is determined mainly by the galling
insects and not by their host plants [17,18]. Because galler
parasitoids have to penetrate a protective wall of modified
plant tissue in order to gain access to their victims, Stone
and Schnrogge [17] recently concluded that morphology-dependent parasitism remains the most plausible
adaptive explanation for the diversification of gall form,
but they also noted that the needed phylogenetic tests are
lacking.
Despite its intuitive appeal, the EAR hypothesis has never
been tested in a phylogenetic framework [8]. Therefore,
we investigated how phylogenetic patterns of parasitism
and diversification in gall-inducing sawflies belonging to
http://www.biomedcentral.com/1741-7007/5/49
the nematine subtribe Euurina (Hymenoptera: Tenthredinidae) conform to the predictions of the hypothesis. Euurina sawflies induce leaf folds or rolls, or various closed
galls on willows (Salix spp.) and, at over 400 species, the
subtribe includes over 10 times more species than its sister
group with larvae that feed externally on leaves [19,20].
Their main sources of mortality are larvae of parasitoids
(that feed on galler larvae) and parasitic inquilines (that
consume gall tissues but kill the sawfly larvae in the process) [19,21]. In all, the associated enemy complex comprises nearly 100 species that belong to 17 families in four
insect orders [19,22]. Sawfly gallers are particularly suited
for studying the evolutionary assembly of complex food
webs, because while each galler species is typically a specialist on a single willow species, all of the seven main
types of closed galls can be found on multiple willow
hosts [19,21]; this cross-replication of willows and galls
makes it possible to tease apart the respective effects of
host plants and gall phenotypes on the composition of
the enemy community attacking each galler species.
Results and discussion

As a first step, we reconstructed the phylogenetic tree of
willow gallers on the basis of DNA sequence data from
two mitochondrial genes (see Methods). The strongly supported phylogeny (Figure 1) confirms earlier results that
species inducing closed galls evolved from external-feeding sawfly lineages via leaf folders [18,20], and demonstrates that the galler community on any given willow
species is a collection of sawflies inducing different galls
that have colonized the host, or one of its ancestors, at different time intervals.
Contrasting the galler phylogeny with quantitative data
on the mortalities inflicted by inquiline and parasitoid
species shows that evolutionary changes in many different
ecological traits can lead to full or partial release from natural enemies (Figure 2). Permutation tests demonstrate a
strong correlation between galler phylogeny and specieslevel enemy communities (Figure 3A, p < 0.0001), which
mainly follows from the fact that the largest differences in
enemy communities occur among gall types, which are
likewise strongly conserved with respect to the galler tree.
Constraining permutations of species-level enemy communities to occur only within gall types also leads to
longer data lengths (Figure 3B, p = 0.0022), but the
increase tends to be less pronounced than in unconstrained randomizations. Within gall-type groups, enemy
communities in many cases differ markedly among willow species, but a statistically significant host plant effect
extends also across gall-type boundaries (Figure 3C;
paired samples t test, t = -1.72, 95% c.i. - to -0.104, onetailed p = 0.043). These results are robust enough to be
found also in randomization tests based on qualitative
Page 2 of 9
Petiole gall
ML reconstruction
of gall location:
Leaf
Equivocal
Leaf roll/fold
100
Galler species / Salix host
Euura venusta / S. aurita

99
45 Euura hastatae / S. hastata
Bud gall
100
Euura lappo / S. lapponum
81 Euura lanatae / S. lanata
100
Euura boreoalpina / S. glauca
Shoot gall
100 Euura mucronata / S. aurita
96
Euura myrsinifoliae / S. myrsinifolia
100
100
Euura gemmafoetidae / S. foetida
Euura gemmahelveticae / S. helvetica
100 Euura eleagnos / S. eleagnos
100
Euura lapponica / S. lapponum
Euura atra / S. alba
Shoot /
37 Pontania nivalis / S. glauca
bud /
100 Pontania varia / S. myrsinifolia
petiole
95
Pontania norvegica / S. borealis
35
Pontania gallarum / S. caprea
100
Pontania reticulatae / S. reticulata
100
24
100
Pontania glabrifrons / S. lanata
Pontania samolad / S. lapponum
21
Pontania hastatae / S. hastata
100
Pontania myrsiniticola / S. myrsinites
Pontania retusae / S. retusa
Leaf midrib pea gall
100
100 Pontania arcticornis / S. phylicifolia
83 Pontania pedunculi / S. cinerea
99 100 Pontania acutifoliae / S. daphnoides
Pontania collactanea / S. repens
Leaf midrib bean gall 100
36
Pontania kriechbaumeri / S. eleagnos
Pontania viminalis / S. purpurea
100
100
Pontania vesicator / S. purpurea
66 Pontania foetidae / S. foetida
100
Pontania maculosa / S. helvetica
Pontania herbaceae / S. herbacea
99
Pontania lapponica / S. lapponum
100 Pontania dolichura / S. phylicifolia
Leaf blade sausage gall
100
Pontania lapponicola / S. lapponum
Pontania glaucae / S. glauca
100
58
Pontania nigricantis / S. myrsinifolia
Pontania virilis / S. purpurea
100
63
Pontania bridgmanii / S. aurita
100
Pontania obscura / S. foetida
Leaf blade bean gall
100
Pontania bridgmanii 2 / S. appendiculata
95
Pontania proxima / S. fragilis
Pontania triandrae / S. triandra
Phyllocolpa carinifrons / S. pentandra
100
100
Phyllocolpa alienata / S. aurita
Phyllocolpa anomaloptera / S. caprea
Phyllocolpa tuberculata / S. starkeana
Nematus melanaspis / S. pentandra
External leaf feeder (outgroup)
0.01 changes/site
Evolutionary
use
Figure
in willow-galling
1 diversification
sawfliesof gall morphology and host plant
Evolutionary diversification of gall morphology and host
plant use in willow-galling sawflies. The tree is according to a
Bayesian phylogenetic analysis of 1 528 bp of DNA sequence data
from two mitochondrial genes (see Methods), numbers above
branches show posterior probabilities of clades. Host plants are
indicated after the sawfly species names. Ancestral gall types were
reconstructed using Accelerated transformations parsimony optimization (the ancestral state of the Euura clade is equivocal, but it
was probably shoot galling [18]). The pie diagram at the node
between Euura and their sister group shows the relative likelihood
of different gall locations as reconstructed by maximum likelihood.
(presence/absence) data on enemy communities (Figure

4AC).
Sawflies inducing identical galls on different host species
are in many cases attacked by very different parasite
assemblages (Figure 2), which indicates that directional
selection coefficients imposed by natural enemies can be
extremely strong during host plant shifts. For example,
host-provided enemy-free space evidently can be found
especially on several distantly related willow species that
grow in sub-arctic and arctic-alpine habitats (e.g., S. lapponum, S. reticulata, and S. myrsinites) where, for example, the predominantly southern inquilines Curculio crux
(Coleoptera: Curculionidae) and Hydriomena ruberata
(Lepidoptera: Geometridae) occur only rarely (Figure 2).
Conversely, leaf gallers on northern willows generally suffer from increased attack by the parasitic wasps Shawiana
lapponica and Lathrostizus flexicauda (Hymenoptera:
Ichneumonidae). Contrasting selection pressures caused

by spatial and temporal variation in enemy communities
[22-24] could explain why some prevalent and seriously
lethal parasite species have been both lost and gained during the diversification of leaf-galling sawfly lineages (Figure 2).
However, the most dramatic shift in enemy communities
coincides with the evolutionary transition from the ancestral condition of leaf galling to gall induction on shoots,
buds, and petioles (Figures 1 and 2). This seemingly
minor change in gall phenotype, which occurred at least
six million years ago [25], led to a near-complete elimination of parasitic inquilines and to a coincident pruning of
the parasitoid community (Figures 2 and 5A; Table 1),
demonstrating that gall-inducing insects can find immediate and long-lasting "enemy-free morphospace" even in
the absence of host plant shifts. The community plot
shows that the novel gall types were subsequently tracked
and colonized by parasitic lineages that apparently were
derived mainly from the ancestral pool of enemies. In
accordance with the EAR hypothesis, at least five probable
cases of adaptive splitting along gall-type boundaries can
be identified in the parasitic wasp genera Lathrostizus (Ichneumonidae), Pteromalus (Pteromalidae), and Eurytoma
(Eurytomidae) (Figure 2), probably because successful
attack on different galls requires specialized adaptations
in the parasitoids' search behaviors and ovipositor structures [10,22,24].
The central prediction of the EAR hypothesis is that
escapes from enemies trigger rapid radiations in prey lineages [3,6,8], but our phylogenetic results (Figures 1 and
2) directly contradict this proposition. Current estimates
[19,21] of species numbers in the conspicuously parasitepoor Euura clade (ca. 100 spp.) are lower than those of
their enemy-rich sister group composed of leaf midrib
bean and pea gallers (ca. 150 spp.), and both of these
clades contain more species than the monophyletic group
comprising the enemy-rich leaf blade bean and sausage
gallers (ca. 80 spp.). Additional comparative studies
involving other insect taxa are needed to confirm this conflicting pattern, but it has been argued that the prediction
of elevated speciation rates in enemy-free lineages has a
weak theoretical basis [8], and our data suggest two explanations for the absence of notable speciation bursts. First,
in complex food webs, release from some enemies can be
quickly compensated by an increase in the severity of
attack by the remaining ones, which is evidenced by a lack
of association between numbers of parasite species and
rates of parasite-inflicted mortality in comparisons across
galler species (Pearson's r = 0.165, p = 0.291; Figure 5B,
Table 2). Less obvious zero-sum games of survival are also
possible, so that while overall rates of parasitism are
slightly lower in Euura species than in leaf gallers, the ben-
Page 3 of 9
Maximum mortality
Posterior
* = probalility
100%
Petiole gall
Genus (gall type)

Euura
Euura
99
Bud gall
81
*
Shoot gall
96
*
*
Euura
Pontania
95
Equivocal
Leaf midrib
pea gall
83
99
*
k
Pontania
66
To leaf
folders
99
Leaf midrib bean gall

*
*
63
*
Pontania
58
*
95
Pontania
Salix host
aurita,caprea,cinerea
hastata
lapponum
lanata
glauca
aurita
myrsinifolia
foetida
helvetica
eleagnos
lapponum
alba,fragilis
glauca,glaucosericea
myrsinifolia
borealis
caprea
reticulata
lanata
lapponum
hastata
myrsinites
retusa
phylicifolia
cinerea
daphnoides
repens,rosmarinifolia
eleagnos
purpurea
purpurea
foetida
helvetica
herbacea
lapponum
phylicifolia
lapponum
glauca
myrsinifolia
purpurea
aurita,caprea,cinerea
foetida
appendiculata
alba,fragilis
triandra
Inquiline / parasitoid species
C
u
Aprcu
i lio
Eu on cr
r m u
Eu yto inimx /
sa
p m
H hra a a um li c
yd n c
ivo
Br rio ta i cu
ru
s
ac m to lat
Br on en xo a
ac b a ne
Br on re rub ur
v
a
e a
Br con dis ius rat
c
c
a
u a
Br con epi oide lus
tr u
a
Br con fulv iptu s
a
u s
Br con livid s
a
u
Br con pic s
tic
a
Ap con pul orn
c i
a
Ap nte rom her s
a l a
Li nte es ni
ss l ?
Co og es mo
l a s rr
Co ast ste p. isi
l e r
Co ast s fl sub
e av c
C last s ? ita om
o e in rs p
Shlast s la cer is leta
aw es ev tus
Sh i a s is
a w n a p.
Ic i a l
h
a
A p neu na l p po
t t is n
Th esi es l s o ica
e s a ga
Ca ros nig ppo ste
m co roc nic r
Ca po p in u
p u c s
La mpo lex s he ta
t p
m
La hro lex sca ip
p te
t s
La hro tizu sp. osu ron
s
s
t
s
La hro tizu fle
x
s
s
t
La hro tizu for icau
t s s ti d
La hro tizu lug cau a
t s s e d
O hro tizu ste ns a
le s s r
O sic tizu sp noc
le a s .1 e
ru
Li sic mp sp
s
ss a e .2
M on mp sp.
e o e 1
Sa sol ta ? sp.
o ei a 2
Sa tis us lpin
o s s i
Sa tis p.1 p. s to
r
o s
Sc tis p.2
a s
E r m b p .4
id u
Ad oli s v
el us es
Ad og py ic
e n g a
Di log ath ma rius
a n u e
Pr par ath s c us
o s u u
Eu ble is s s s bic
r s tr p e
Eu yto cla am .2 ps
r m v in
To yto a n ico eip
r m o rn e
Eu ym a s bb is s
l e us al i ei
Pt nc s ci
e h p. s
P t r om etr
e a o
Pt rom lus n to
e a
r
Pt rom lus cap ym
e a
r o
Pt rom lus dol eae ides
ic
e a
M rom lus euu hur
ac a p r a us
Eu ro lus on e
t
p n
Eu elmeur sp. ani
ae
a
d
D er u us v e
ic s u si
Pn lad al rozo cul
i o b n a
Pn gal cer itar us ris
i i o u si
C gal ne s w s
hr i o m e
En yso pe ati stw
oo
t c c
Pe edo ha tico
di
d n ri r
C ob he s e nis
irr iu y l o
An osp s s eri nga
ta
a i a
Ap pro lus uliu
r s v s
Te ost toc itta
t o e tu
Te ras cet tus s
t ti u
Te ras chu s ?aacu
t ti s l m
Te ras chu sp v ea ina
t t i s .1 t u t u
Ap ras chu sp
s s
hi tich s s .2
di u p
i d s .3
ae s
in p.5
de
t.
0.01-1%
1.01-10%
10.01-50%
50.01-90%
90.01-100%
Galls Loc.(Rear.)
1349
10(17)
17(32)
2572
19(27)
1193
9(11)
771
13(17)
2009
11(14)
1416
9(14)
2923
8(13)
1872
11(21)
2965
11(17)
2279
12(17)
1076
5(7)
415
25(43)
4203
27(43)
6274
5(5)
909
13(18)
1527
6(11)
1172
11(15)
2129
14(19)
2116
19(33)
3460
7(9)
1627
5(9)
901
14(20)
3794
8(16)
1029
18(23)
2206
8(8)
1490
11(12)
1607
31(42)
3103
16(22)
3110
9(18)
1645
9(13)
1209
8(12)
2850
17(21)
2752
10(10)
482
18(21)
646
6(11)
1122
8(15)
2283
6(9)
1052
16(24)
1298
10(18)
1170
12(13)
844
20(32)
6976
489
4(5)
PARASITOIDS
C
o
C leop
Hy oleo ter
m pt a:
en er C
op a: ur c
te C u
Le
p D ra urc lion
H ido ipte : Eu uli ida
ym pt r r on e
Hy en era a: T yto ida
m op : G ep mi e
Hy en te e h da
m o r o ri e
H en pte a: B me tida
ym o r
t e
H en pte a: Brac rida
ym o r
on e
Hy en pte a: Brac ida
o e
m o r
H en pte a: Brac nida
ym o r r on e
Hy en pte a: B ac ida
o e
m o r
ym o r
o e
ym o r
o e
Hy en pte a: Brac nida
o e
m o r
o e
m o r
o e
m o r
ym o r
on e
H en pte a: Braco ida
ym o r
n e
H en pte a: Brac ida
on e
ym o r
H en pte a: Braco ida
ym o r r n e
a
Hy Hy en pte : B aco ida
m me opt ra: rac nid e
Hy en n e B o a
m o o ra r n e
Hy en pte pte : B aco ida
m o r ra r n e
Hy en pte a: I : B aco ida
m o r c r n e
H en pte a: I hne aco ida
ym o r c u n e
H en pte a: I hne mo ida
ym o r c u n e
Hy en pte a: I hne mo ida
m o r c u n e
ym o r c u n e
m o r c u n e
ym o r c u n e
m o r c u n e
m o r c u n e
ym o r c u n e
m o r c u n e
m o r c u n e
m o r c u n e
m o r c u n e
ym o r c u n e
m o r c u n e
m op ra ch um nid e
Hy en te : I ne o a
m o r c u n e
ym o r c u n e
ym o r c u n e
e pt a: hn m id
Hy nop era Ich eumoni ae
d
m t : n
Hy en era Ich eumoni ae
m o p : Ic n e o d a
u n e
e
H n te hn m id
H ym opt ra: eu on ae
ym e e E m id
H en no r a: ur y on ae
ym o p E t id
H en pte tera ury omi ae
ym o r : t d
H en pte a: P To omi ae
ym o r
ry d
Hy en pte a: Ptero mi ae
m d
m o r
Hy en pte a: Ptero ali ae
m op ra te ma da
Hy eno ter : Pt rom li d e
m p te a : e r o a l a e
Hy en r Pt m i da
m op a: P ero ali e
H en te te m da
ym o ra r a e
Hy en pte : E om li da
m o ra u a e
H en pte : E pel li da
ym o r u m e
Hy en pte a: E pe ida
lm e
m o r
H en pte a: Eulop ida
ym o r
h e
Hy en pte a: Eulop ida
m o r
h e
m o r
h e
m o r
h e
m o r
h e
m o r
h e
ym o r
h e
ym o r u h e
a
p
l
Hy en te : E op ida
m o r
h e
m o ra u h e
H en pte : E lop ida
ym o ra u h e
en pte : E lop ida
op ra: ulo hid e
te E p h a e
ra ulo id
:A p a
ph hid e
id ae
iid
ae
INQUILINES
Inquiline / parasitoid taxon (Order: Family)
phylogeny,
Figure
Maximum
2 rates
gall morphology,
of mortality inflicted
and hostby
plants
72 inquiline
of the gallers
and parasitoid species on 43 willow-galling sawfly species in relation to the
Maximum rates of mortality inflicted by 72 inquiline and parasitoid species on 43 willow-galling sawfly species in relation
to the phylogeny, gall morphology, and host plants of the gallers. Sawfly names have been omitted, but their order is the same
as in Figure 1. Each column in the plot represents one inquiline or parasitoid species, maximum rates of parasitism observed in extensive
population rearings of each galler species [21,22] are indicated by the colour of the cells (see legend). See Additional file 1 for exact rates
of parasitism. Enemy species and genera mentioned in the text are highlighted by a coloured font, and the taxon to which each parasite
species belongs is indicated below the matrix (note that the wasp genus Eurytoma includes two parasitoids and an inquiline). Numbers of
dissected galls, collection localities, and population rearings are given in the last two columns. Numbers above branches on the tree show
Bayesian posterior probabilities (only values 50% shown, asterisks denote clades with a 100% posterior probability).
efit seems to be offset by an increased susceptibility to

defence reactions on behalf of the host plants [19,22].
Second, if prey species are (like most plant feeding insects
[4,5]) themselves resource specialists, a moderate enemy
pressure might promote the prey's colonization of novel
niches (e.g., plants [9,14,15]) and thus facilitate ecological speciation in prey lineages. This could especially be the
case if geographical variation in enemy assemblages drives
different populations of widespread prey species into
using different resources.
Conclusion
Coevolutionary studies on parasitoids and their prey commonly focus on physiological defenses and counterdefenses [26], but our results clearly show that ecological
traits constitute a central part of the defensive arsenal of
herbivorous insects. Prior to a niche shift, an evolving
prey lineage must exhibit a polymorphism in resource
use, which can be followed by quick fixation of one of the

alternative states whenever different resources are associated with different enemy attack patterns. Furthermore,
our finding that several parasitoid lineages have
responded to gall-type divergence by adaptive speciation
provides strong support for suggestions [1,2,8] that coevolutionary arms races have played an important role in
the generation of the unusual diversity of herbivorous
insects and parasitoids. Nevertheless, our data also indicate that in its classic form the EAR hypothesis is too simplistic to explain reciprocal diversification effects in
complex food webs, in which escapes from enemies will
tend to be too brief to lead to the predicted speciation
bursts. Instead, the observed patterns of parasitism and
diversification are consistent with a scenario of stepwise
antagonistic coevolution: colonization of new ecological
niches by prey lineages is being continuously driven by
temporary relief from parasitism, after which an evolu-
Page 4 of 9

1XPEHURISHUPXWDWLRQV

2EV

'DWDOHQJWK

2EV

'DWDOHQJWK
&

2EV

'DWDOHQJWK

1XPEHURIUHSODFHPHQWV

1XPEHURIUHSODFHPHQWV
'DWDOHQJWK

&


2EV

'LIIHUHQFHLQGDWDOHQJWKFKDQJH

'LIIHUHQFHLQGDWDOHQJWKFKDQJH
Distributions
tions
Figure
phylogeny
of 3gallerof
enemy
data lengths
communities
resulting
in relation
from random
to thepermutagaller
Distributions
tions
Figure
phylogeny
of 4galler of
enemy
data lengths
communities
resulting
in relation
from random
to thepermutagaller
Distributions of data lengths resulting from random permutations of galler enemy communities in relation to the
galler phylogeny. In (A) and (B), the arrow indicates the length
of the observed quantitative parasitism data, as calculated on the
basis of the galler topology in Figure 2. (A) Distribution of data
lengths when enemy communities (rows) are permuted 10000
times across the whole galler phylogeny. (B) Distribution of data
lengths when enemy communities are similarly permuted within
gall-type groups. (C) Distribution of the difference in the absolute
change in data length when the enemy complex of a galler species
is replaced by those of two species from another gall type, of
which only one also has a different host willow. Negative values of
the difference indicate that the change in data length is smaller
when the replacing species occurs on the same host plant (see
Methods).
Distributions of data lengths resulting from random permutations of galler enemy communities in relation to the
galler phylogeny. The histograms show the distributions of data
lengths when qualitative (i.e., presence/absence) data on enemy
species are used instead of the quantitative rates of mortality used
in Figure 3. In (A) and (B), the arrow indicates the length of the
observed qualitative parasitism data, as calculated on the basis of
the galler topology in Figure 2. (A) Distribution of data lengths
when enemy communities (rows) are permuted 10000 times
across the whole galler phylogeny (p < 0.0001). (B) Distribution of
data lengths when enemy complexes are similarly permuted within
gall-type groups (p = 0.0158). (C) Distribution of the difference in
the absolute change in data length when the enemy complex of a
galler species is replaced by those of two species from another gall
type, of which only one also has a different host willow (see Methods). Negative values of the difference indicate that the change in
data length is smaller when the replacing species occurs on the
same host plant (paired samples t test, t = -4.93, 95% c.i. - to 0.174, one-tailed p < 0.001).
tionary response by some of the associated enemies

returns mortalities to normal levels. In its complexity, the
willow-galler-parasite food web is representative of many
antagonistic networks in which specialized interactions
link species across multiple trophic levels. A close integration of ecological and evolutionary research is clearly
needed if the origins of such networks are to be fully
understood.
Methods
Parasitism data and taxon sampling
Enemy rearing methods and collection localities of galler
population samples have been described previously
[21,22]. In brief, populations were sampled extensively
throughout Europe between 1981 and 1998, and galls
were opened to score the presence of galler or parasitoid/
Page 5 of 9
Table 1: Effects of gall type and sample size (= number of galls collected) on the number of parasitoid species observed attacking each
galler species
Source
Type III sum of squares
df
Mean square
p Value
Corrected model
Intercept
Number of galls
Gall type
Error
Total
Corrected total
592.188*
64.579
166.368
382.832
333.431
5046.000
925.619
6
1
1
5
35
42
41
98.698
64.579
166.368
76.566
9.527
10.360
6.779
17.464
8.037
<0.001
0.013
<0.001
<0.001
df, degrees of freedom

Gall type was included as a fixed factor and sample size as a covariate in the ANCOVA model. Sample sizes were ln-transformed prior to the
analysis, because logarithmic regressions produced more biologically realistic results and a better fit to the observed data (Figure 5A) than did linear
regressions with untransformed sample sizes.
*R2 = 0.640 (adjusted R2 = 0.578).
25
Gall type:
Petiole gall
Bud gall
Shoot gall
Number of parasite species
20
15
r2 = 0.012
r2 = 0.998
r2 = 0.614
r2 = 0.331
r2 = 0.303
r2 = 0.415
10
0
0
1000
2000 3000 4000 5000 6000

Number of galls collected
7000
Average parasite-inflicted mortality
1.0
Gall type:
Petiole gall
Bud gall
Shoot gall
0.8
0.6
r2 = 0.025
r2 = 0.151
r2 = 0.004
r2 = 0.254
r2 = 0.001
r2 = 0.046
0.4
0.2
0.0
0
10
15
20
25
Factors explaining
inflicted
Figure
5mortalitiesnumbers
in individual
of enemy
galler species
species and parasiteFactors explaining numbers of enemy species and parasite-inflicted mortalities in individual galler species. Each
point in the plots represents one galler species. (A) Numbers of
associated enemy species in relation to gall types and sample sizes.
Lines show logarithmic regression curves for each gall type. (B)
Average parasite-inflicted mortalities of individual galler species
[22] in relation to their gall types and numbers of associated parasite species. Lines are not shown for petiole gallers that are represented by a single species (triangle). ANCOVA results for (A) and
(B) are given in Tables 1 and 2, respectively.
inquiline larvae. Enemy larvae were classified to preliminary morphospecies, and the identity of each morphospecies was determined by connecting them to adults
emerging after hibernation. The severity of parasitism by
each enemy species in each galler species was defined as
the maximum observed level of mortality inflicted in the
population samples (see Additional file 1 for exact rates of
parasitism), which is a valid indicator of the potential
importance of natural enemies [10]. To control for sampling effects, our phylogenetic analysis includes the 43
galler species (Table 3) that have parasitism data from at
least four locations and a total sample size of over 400
galls. In accordance with previous results [18,25], we used
the free-feeding nematine Nematus melanaspis and four
leaf-folding or -rolling Phyllocolpa species as outgroups in
the phylogenetic analyses.
Phylogeny reconstruction
DNA sequence data was generated for 1528 base pairs of
two mitochondrial genes (cytochrome oxidase I: 810 bp;
cytochrome b: 718 bp) using protocols described previously [18,25]. All sequences have been deposited in GenBank under accession numbers DQ302205, DQ302212,
and EU083911EU084004. Modeltest 3.5 [27] was used
in conjunction with PAUP* 4.0b10 [28] to select the
GTR+I+4 substitution model subsequently implemented
in a Bayesian phylogenetic analysis in MrBayes 3.1.1 [29].
Two parallel runs employing default priors and consisting
of four incrementally heated chains (t = 0.2) were run for
six million generations while sampling trees from the current cold chain every 100 generations, and 110002 postburn-in trees were used to calculate a Bayesian consensus
tree. Because the tree is strongly supported and maximum-parsimony and maximum-likelihood analyses of
the sequence data led to near-identical results, only the
Bayesian tree was used in the permutation tests described
below.
Page 6 of 9
Table 2: Effects of gall type and number of associated parasite species on average mortalities in individual galler species
Source
Type III sum of squares
df
Mean square
p Value
Corrected model
Intercept
Gall type
Error
Total
Corrected total
0.378*
2.431
0.001
0.362
0.576
20.437
0.954
6
1
1
5
35
42
41
0.063
2.431
0.001
0.072
0.016
3.834
147.756
0.040
4.401
0.005
<0.001
0.843
0.003
Gall type was included as a fixed factor and number of parasite species as a covariate in the ANCOVA model (see Figure 5B). Mortalities were
arcsine square root transformed prior to the analysis.
*R2 = 0.397 (adjusted R2 = 0.293).
Character evolution analyses and statistical tests

Ancestral gall types were inferred by accelerated transformations parsimony optimization [30], and ancestral gall
locations (leaf, shoot, bud, or petiole) by maximum likelihood (ML) reconstruction in Mesquite 1.11 [31]. In the
ML analysis, we employed an Mk1 model (= equal forward and reverse rates) after pruning the external-feeding
outgroup from the galler tree. Because maximum rates of
parasitism by different enemy species are not independent
in galler population samples, we treated species-level
enemy communities (= rows in the table in Additional file
1) as the observation for each galler species, and then
devised three alternative permutations of enemy communities over galler species to test correlations between the
parasitism matrix and the galler phylogeny. If parasite
communities tend to be similar among closely related galler species, the length of the enemy data, as calculated on
the basis of the galler topology, will be shorter than
expected from random assignment. Data length [32] was
calculated first from the observed data, and subsequently
from 10000 random permutations of enemy communities over galler species. The probability that by chance data
is as short as observed is calculated by comparing the
observed data length with the distribution of permuted
data lengths. Possible phylogenetic correlations within
gall types were tested by restricting the permutations to
occur only among sawfly species that induce similar galls.
To test whether an effect of the willow host species

extends across gall-type boundaries, we used a paired
replacement procedure: the enemy community of a randomly chosen galler species was replaced with the enemy
communities of two randomly selected species. Those two
species had the same gall type (different from that of the
species being replaced) but only one of those two had a
different host plant. The other species thus had the same
host plant as the species being replaced. The absolute
change in data length was calculated for each of the two
replacements, and subsequently the difference in datalength change was calculated between the two replacements. If the replacement with a species that shares the
host plant with the species being replaced results in a

smaller absolute change in data length, the difference in
absolute data length change becomes negative (and conversely, positive if the species not sharing the host plant
yields a smaller data-length change). The distribution of
differences in absolute tree-length change resulting from
10000 such paired replacements was evaluated against the
null hypothesis (= mean change in absolute data length
equal) using a paired samples t test. For the purposes of
the species effect tests, willows belonging to two species
complexes consisting of sister taxa with extensive hybridization (S. alba and S. fragilis; and S. caprea, S. aurita, and
S. cinerea) were synonymized under two "superspecies".
All permutation and replacement tests were performed in
Matlab (The MathWorks, Inc., 3 Apple Hill Drive, Natick,
MA 01760-2098, USA), see Additional file 2 for the scripts
used for the tests. ANCOVA tests used for testing factors
influencing numbers of associated parasitoid species and
rates of parasite-inflicted mortality were performed using
SPSS for Windows 14.0 (SPSS, Inc., 233 S. Wacker Drive,
Chicago, IL 60606-6307, USA).
Authors' contributions
TN was responsible for research planning, sequencing,
phylogeny reconstruction, and writing. Statistical tests
were devised by TN and FB and programmed by FB. Galler
population sampling and enemy rearings were performed
by JPK. All authors participated in the writing process. All
the authors have read and approved the final manuscript.
Additional material
Additional file 1
Excel file showing maximum rates of mortality inflicted by each inquiline
and parasitoid species on each galler species.
Click here for file
[http://www.biomedcentral.com/content/supplementary/17417007-5-49-S1.xls]
Page 7 of 9
Table 3: Taxa and samples used in the study, their gall types, willow hosts, and collection data
Genus (gall type)
Species
Salix host
Sample code
Specimen
Location and date
Collector
Pontania (Leaf blade sausage gall)
dolichura
glaucae
lapponicola
nigricantis
virilis
phylicifolia
glauca
lapponum
myrsinifolia
purpurea
04151/Q1
97194/Q2
05149/Z1
04236/Q3
05018/Y2
Larva
Larva
Larva
Larva
Larva
Korvua, Finland, 9.vii.2004

Kilpisjrvi, Finland, 4.viii.1997
Nuorgam, Finland, 3.vii.2005
Hintertux, Austria, 8.viii.2004
Kiesnitz, Oder, Germany, 18.v.2005
T. Nyman
T. Nyman
T. Nyman
T. Nyman
A. Liston
Pontania (Leaf blade bean gall)
bridgmanii
proxima
triandrae
obscura
"bridgmanii 2"
aurita, caprea, cinerea

alba, fragilis
triandra
foetida
appendiculata
97076/Q4
04388/Q5
97455/Q6
04264/X6
04125/X1
Larva
Larva
Larva
Larva
Larva
Mekrijrvi, Finland, 22.vii.1997

Oulu, Finland, 8.x.2004
Keminmaa, Finland, 29.vii.1997
Vent-Slden, Austria, 20.vi.2004
T. Nyman, A. Zinovjev
T. Nyman
T. Nyman
T. Nyman
T. Nyman
Pontania (Leaf midrib bean gall)
foetidae
herbaceae
lapponica
maculosa
retusae
vesicator
foetida
herbacea
lapponum
helvetica
retusa
purpurea
04263/Q9
98230/QX
98308/R1
04308/R2
04243/R3
04200/R5
Larva
Larva
Larva
Larva
Larva
Larva

Abisko, Sweden, 12.viii.1998
Abisko, Sweden, 16.viii.1998
Vent, Austria, 12.viii.2004
Obergurgl, Austria, 5.viii.2004
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
Pontania (Leaf midrib pea gall)
acutifoliae daphnoides
arcticornis
collactanea
gallarum
glabrifrons
hastatae
kriechbaumeri
myrsiniticola
nivalis
norvegica
pedunculi
reticulatae
samolad
varia
viminalis
daphnoides
phylicifolia
repens, rosmarinifolia
caprea
lanata
hastata
eleagnos
myrsinites
glauca, glaucosericea
borealis
cinerea
reticulata
lapponum
myrsinifolia
purpurea
97490/R6
98328/R7
04124/R8
98132/R9
98335/RX
01153/S1
04333/S2
98364/S3
98346/S4
98374/S5
98393/S6
04240/S7
98373/S8
98198/Z2
04226/SX
Larva
Larva
Larva
Larva
Larva
Larva
Larva
Larva
Larva
Larva
Larva
Larva
Larva
Larva
Larva
Latvia, 22.viii.1997
Blvand, Denmark, 16.vi.2004
Joensuu, Finland, 21.vii.1998
Pertisau, Austria, 13.viii.2004
Janakkala, Finland, 13.viii.1998
Slden, Austria, 7.viii.2004
H. Roininen, A. Zinovjev
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
A. Zinovjev
T. Nyman
T. Nyman
T. Nyman
T. Nyman
Euura (Bud gall)
hastatae
lanatae
lappo
mucronata
gemmafoetidae
boreoalpina
gemmahelveticae
myrsinifoliae
hastata
lanata
lapponum
aurita
foetida
glauca
helvetica
myrsinifolia
97497/T1
98024/T2
98362/T3
04385/T4
04360/T5
98363/T6
04363/T7
98371/T8
Larva
, ex larva
Larva
Larva
Larva
Larva
Larva
Larva

Oulu, Finland, 8.ix.2004
Vent, Austria, 4.viii.2004
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
T. Nyman
Euura (Shoot gall)
atra
eleagnos
lapponica
alba, fragilis
eleagnos
lapponum
97005/T9
04357/TX
98329/V1
, ex pupa
Larva
Larva
Joensuu, Finland, 30.v.1997

Pertisau, Austria, 13.viii.2004
T. Nyman
T. Nyman
T. Nyman
Euura (Petiole gall)
venusta
aurita, caprea,
cinerea
00038/V3
Larva
Joensuu, Finland, 20.viii.2000
T. Nyman
Phyllocolpa (Leaf fold/roll)
carinifrons1
anomaloptera2
alienata3
sp. (near tuberculata)
pentandra
caprea
aurita, cinerea
starkeana
98120/C2
97097/X9
04055/X5
97063/E9
Larva
Larva
Larva
Larva
Keslahti, Finland, 16.vii.1998

Nymindegab, Denmark, 17.vi.2004
St. Petersburg, Russia, 15.vi.1997
H. Roininen
T. Nyman
T. Nyman
A. Zinovjev
Nematus (External feeder)
melanaspis
pentandra
01092/D6
, ex larva
Parikkala, Finland, 24.vi.2001
T. Nyman
Outgroups
In the case of oligophagous species, the host of the sampled individual is underlined
1Species name according to recent revision [33], previously named P. excavata.
2Species name according to recent revision [34], previously named P. leucapsis.
3Species name according to recent revision [35], previously named P. coriacea.
Page 8 of 9
20.
Additional file 2
PDF file giving scripts used to perform permutation and replacement tests
in Matlab
Click here for file
[http://www.biomedcentral.com/content/supplementary/17417007-5-49-S2.pdf]
21.
22.
23.
24.
Acknowledgements
We thank H Roininen and A Zinovjev for providing samples of missing galler species, and H Roininen, O-P Tikkanen and the two anonymous reviewers for comments that helped to improve the manuscript. Funding for this
study was provided mainly by the Academy of Finland (project number
118931).
25.
References
28.
1.
29.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
Singer MS, Stireman JO III: The tri-trophic niche concept and

adaptive radiation of phytophagous insects. Ecol Lett 2005,
8:1247-1255.
Kitching RL: Crafting the pieces of the diversity jigsaw puzzle.
Science 2006, 313:1055-1057.
Ehrlich PR, Raven PH: Butterflies and plants: a study in coevolution. Evolution 1964, 18:586-608.
Strong DR, Lawton JH, Southwood TRE: Insects on Plants: Community
Patterns and Mechanisms Oxford: Blackwell Science; 1984.
Novotny V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, Weiblen
GD: Why are there so many species of herbivorous insects in
tropical rainforests? Science 2006, 313:111-118.
Farrell BD, Dussourd DE, Mitter C: Escalation of plant defense:
do latex and resin canals spur plant diversification? Am Nat
1991, 138:881-900.
Farrell BD: "Inordinate fondness" explained: why are there so
many beetles? Science 1998, 281:555-559.
Vamosi SM: On the role of enemies in divergence and diversification of prey: a review and synthesis. Can J Zool 2005,
83:894-910.
Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis
AE: Interactions among three trophic levels: influence of
plants on interactions between insect herbivores and natural
enemies. Annu Rev Ecol Syst 1980, 11:41-65.
Hawkins BA: Pattern and Process in Host-Parasitoid Interactions Cambridge: Cambridge University Press; 1994.
Janz N, Nylin S, Wahlberg N: Diversity begets diversity: host
expansions and the diversification of plant-feeding insects.
BMC Evol Biol 2006, 6:4.
Abrahamson WG, Blair CP, Eubanks MD, Morehead SA: Sequential
radiation of unrelated organisms: the gall fly Eurosta solidaginis and the tumbling flower beetle Mordellistena convicta. J
Evol Biol 2003, 16:781-789.
Stireman JO III, Nason JD, Heard SB, Seehawer JM: Cascading hostassociated genetic differentiation in parasitoids of phytophagous insects. Proc R Soc Lond B 2006, 273:523-530.
Lill JT, Marquis RJ, Ricklefs RE: Host plants influence parasitism
of forest caterpillars. Nature 2002, 417:170-173.
Murphy SM: Enemy-free space maintains swallowtail butterfly
host shift. Proc Natl Acad Sci USA 2004, 101:18048-18052.
Price PW, Fernandes GW, Waring GL: Adaptive nature of insect
galls. Environ Entomol 1987, 16:15-24.
Stone GN, Schnrogge K: The adaptive significance of insect
gall morphology. TREE 2003, 18:512-522.
Nyman T, Widmer A, Roininen H: Evolution of gall morphology
and host-plant relationships in willow-feeding sawflies
(Hymenoptera: Tenthredinidae). Evolution 2000, 54:526-533.
Roininen H, Nyman T, Zinovjev AG: Biology, ecology, and evolution of gall-inducing sawflies (Hymenoptera: Tenthredinidae
and Xyelidae). In Biology, Ecology, and Evolution of Gall-inducing
Arthropods Edited by: Raman A, Schaefer CW, Withers TM. Enfield:
Science Publishers; 2005:467-494.
26.
27.
30.
31.
32.
33.
34.
35.
Nyman T, Farrell BD, Zinovjev AG, Vikberg V: Larval habits, hostplant associations, and speciation in nematine sawflies
(Hymenoptera: Tenthredinidae). Evolution 2006, 60:1622-1637.
Kopelke J-P: Gallenerzeugende Blattwespen Europas Taxonomische Grundlagen, Biologie und kologie (Tenthredinidae: Nematinae: Euura, Phyllocolpa, Pontania). Cour Forsch-inst
Senckenb 1999, 212:1-183.
Kopelke J-P: Natural enemies of gall-forming sawflies on willows (Salix spp.). Entomol Gener 2003, 26:277-312.
Thompson JN: Specific hypotheses on the geographic mosaic
of coevolution. Am Nat 1999:1-14.
Craig TP, Itami JK, Horner JD: Geographic variation in the evolution and coevolution of a tritrophic interaction. Evolution
2007, 61:1137-1152.
Nyman T, Zinovjev AG, Vikberg V, Farrell BD: Molecular phylogeny of the sawfly subfamily Nematinae (Hymenoptera: Tenthredinidae). Syst Entomol 2006, 31:569-583.
Pennacchio F, Strand MR: Evolution of developmental strategies
in parasitic Hymenoptera. Annu Rev Entomol 2006, 51:233-258.
Posada D, Crandall KA: Modeltest: testing the model of DNA
substitution. Bioinformatics 1998, 14:817-818.
Swofford DL: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other
Methods), version 40b10 Sunderland: Sinauer; 2002.
Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic
inference under mixed models.
Bioinformatics 2003,
19:1572-1574.
Swofford DL, Maddison WP: Reconstructing ancestral character
states under Wagner parsimony. Math Biosci 1987, 87:199-229.
Maddison WP, Maddison DR: Mesquite: a modular system for
evolutionary analysis, version 1.11. 2006 [http://mesquite
project.org].
Pauplin Y: Direct calculation of a tree length using a distance
matrix. J Mol Evol 2000, 51:41-47.
Kopelke J-P: The species of the Phyllocolpa leucosticta-group in
Europe (Hymenoptera: Tenthredinidae: Nematinae). Senckenb Biol 87:75-109.
Kopelke J-P: The species of the Phyllocolpa crassispina-,
scotaspis-, and piliserra-group in Europe (Hymenoptera: Tenthredinidae: Nematinae). Senckenb Biol in press.
Kopelke J-P: The species of the Phyllocolpa leucapsis-group in
Europe (Hymenoptera: Tenthredinidae: Nematinae). Senckenb Biol in press.
Publish with Bio Med Central and every

scientist can read your work free of charge
"BioMed Central will be the most significant development for
disseminating the results of biomedical researc h in our lifetime."
Sir Paul Nurse, Cancer Research UK
Your research papers will be:

available free of charge to the entire biomedical community
peer reviewed and published immediately upon acceptance
cited in PubMed and archived on PubMed Central
yours you keep the copyright
BioMedcentral
Submit your manuscript here:

http://www.biomedcentral.com/info/publishing_adv.asp
Page 9 of 9

1741 7007 5 49

Încărcat de

Informații document

Titlu original

Drepturi de autor

Formate disponibile

Partajați acest document

Partajați sau inserați document

Opțiuni de partajare

Vi se pare util acest document?

Este necorespunzător acest conținut?

Drepturi de autor:

Formate disponibile

1741 7007 5 49

Încărcat de

Drepturi de autor:

Formate disponibile

BMC Biology

Reciprocal diversification in a complex plant-herbivore-parasitoid

Published: 1 November 2007

Received: 24 September 2007

This article is available from: http://www.biomedcentral.com/1741-7007/5/49

escape-and-radiate (EAR) hypothesis [3] envisions the

BMC Biology 2007, 5:49

toxic chemical) becomes free to proliferate and rapidly

Results and discussion

BMC Biology 2007, 5:49

Galler species / Salix host

Euura venusta / S. aurita

(presence/absence) data on enemy communities (Figure

Ichneumonidae). Contrasting selection pressures caused

BMC Biology 2007, 5:49

Genus (gall type)

Leaf midrib bean gall

Inquiline / parasitoid species

Inquiline / parasitoid taxon (Order: Family)

efit seems to be offset by an increased susceptibility to

use, which can be followed by quick fixation of one of the

BMC Biology 2007, 5:49

tionary response by some of the associated enemies

BMC Biology 2007, 5:49

Type III sum of squares

df, degrees of freedom

Number of parasite species

2000 3000 4000 5000 6000

Average parasite-inflicted mortality

BMC Biology 2007, 5:49

Type III sum of squares

Character evolution analyses and statistical tests

To test whether an effect of the willow host species

host plant with the species being replaced results in a

BMC Biology 2007, 5:49

Location and date

Pontania (Leaf blade sausage gall)

Korvua, Finland, 9.vii.2004

Pontania (Leaf blade bean gall)

aurita, caprea, cinerea

Mekrijrvi, Finland, 22.vii.1997

Pontania (Leaf midrib bean gall)

Hintertux, Austria, 9.viii.2004

Pontania (Leaf midrib pea gall)

Euura (Bud gall)

Kilpisjrvi, Finland, 13.viii.1997

Euura (Shoot gall)

Joensuu, Finland, 30.v.1997

Euura (Petiole gall)

Joensuu, Finland, 20.viii.2000

Phyllocolpa (Leaf fold/roll)

Keslahti, Finland, 16.vii.1998

Nematus (External feeder)

Parikkala, Finland, 24.vi.2001

BMC Biology 2007, 5:49

Singer MS, Stireman JO III: The tri-trophic niche concept and

Publish with Bio Med Central and every

Your research papers will be:

Submit your manuscript here:

S-ar putea să vă placă și