RESEARCH ARTICLE Open Access
How common is ecological speciation in plant-
feeding insects? A ?Higher? Nematinae
perspective
Tommi Nyman1*, Veli Vikberg2, David R Smith3, Jean-Luc Boev?4
Abstract
Background: Ecological speciation is a process in which a transiently resource-polymorphic species divides into
two specialized sister lineages as a result of divergent selection pressures caused by the use of multiple niches or
environments. Ecology-based speciation has been studied intensively in plant-feeding insects, in which both
sympatric and allopatric shifts onto novel host plants could speed up diversification. However, while numerous
examples of species pairs likely to have originated by resource shifts have been found, the overall importance of
ecological speciation in relation to other, non-ecological speciation modes remains unknown. Here, we apply
phylogenetic information on sawflies belonging to the ?Higher? Nematinae (Hymenoptera: Tenthredinidae) to infer
the frequency of niche shifts in relation to speciation events.
Results: Phylogenetic trees reconstructed on the basis of DNA sequence data show that the diversification of
higher nematines has involved frequent shifts in larval feeding habits and in the use of plant taxa. However, the
inferred number of resource shifts is considerably lower than the number of past speciation events, indicating that
the majority of divergences have occurred by non-ecological allopatric speciation; based on a time-corrected
analysis of sister species, we estimate that a maximum of c. 20% of lineage splits have been triggered by a change
in resource use. In addition, we find that postspeciational changes in geographic distributions have led to broad
sympatry in many species having identical host-plant ranges.
Conclusion: Our analysis indicates that the importance of niche shifts for the diversification of herbivorous insects
is at present implicitly and explicitly overestimated. In the case of the Higher Nematinae, employing a time
correction for sister-species comparisons lowered the proportion of apparent ecology-based speciation events from
c. 50-60% to around 20%, but such corrections are still lacking in other herbivore groups. The observed convergent
but asynchronous shifting among dominant northern plant taxa in many higher-nematine clades, in combination
with the broad overlaps in the geographic distributions of numerous nematine species occupying near-identical
niches, indicates that host-plant shifts and herbivore community assembly are largely unconstrained by direct or
indirect competition among species. More phylogeny-based studies on connections between niche diversification
and speciation are needed across many insect taxa, especially in groups that exhibit few host shifts in relation to
speciation.
Background
Ecological speciation is a process in which a shift in
resource or habitat use within an ancestral species trig-
gers the formation of two new sister species, each
adapted to exploit different niches [1,2]. The speciation
process is thought to involve an initial period of
resource polymorphism, during which the parent lineage
utilizes multiple environments or niches [3,4]; subse-
quently, tradeoffs in the efficiency by which individuals
can use different resources lead to disruptive selection
and, eventually, to lineage splitting [5,6]. Ecological spe-
ciation has recently been focus of intensive research,
and it is becoming increasingly clear that niche-based
selection may underlie or at least speed up the
* Correspondence: Tommi.Nyman@uef.fi
1Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101
Joensuu, Finland
Full list of author information is available at the end of the article
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
? 2010 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.
diversification of, for example, many bird [7,8], lizard
[9], fish [10], and invertebrate [11,12] groups.
Many of the best examples of species pairs that may
have formed as a result of ecological speciation come
from plant-feeding insects [2,13,14]. Insect herbivores
are typically highly specialized in their host-plant prefer-
ences, and exhibit elaborate physiological [15], beha-
vioural [16], and morphological [17] adaptations for
utilizing their respective host plants. However, although
only a small fraction of available plants constitute a sui-
table food source for most insect species, contrasts of
herbivore versus plant phylogenies have in many cases
revealed drastic discrepancies between the phylogenetic
trees [18-20]. In essence, this means that host-plant
associations are evolvable and change occasionally dur-
ing the evolutionary history of insect lineages [21-23].
Occasional colonizations of novel hosts can theoretically
cause ecological speciation, which could provide an
explanation for the enormous species diversity of plant-
feeding insects on the Earth [24-26].
A considerable proportion of evolutionary insect-plant
research has been devoted to the possibility that ecologi-
cal speciation in plant-feeding insects occurs in sympa-
try, so that both sister lineages are formed within a
continuous geographical area [4,13,27]. However, a
more likely scenario is that ecological speciation is
initiated in allopatric or partially allopatric (para- or
peripatric) settings; in these cases, increasing specializa-
tion onto different hosts in different parts of the geogra-
phical range of an insect species is thought to reduce
the probability of hybridization if the populations later
come into contact again [2,28]. Hence, the main differ-
ence to ?ordinary? allopatric speciation is that the cause
for reproductive isolation lies in the disparate ecology of
the incipient species, rather than in gradual accumula-
tion of genetic incompatibilities between geographically
isolated populations [29,30].
While numerous putative cases of ecology-based spe-
ciation in plant-feeding insects are known, we still lack
an understanding of the actual frequency or importance
of ecological shifts in the formation of new species
[22,27,31]. Investigations of ecologically divergent spe-
cies pairs can provide insights into traits or circum-
stances that enhance the likelihood of niche-based
divergence, but studying the frequency of ecological spe-
ciation requires use of a broader, phylogeny-based
approach [22,30,32,33]. The usefulness of phylogenies
stems from the fact that different speciational processes
should produce very different distributions of niches on
the phylogenetic trees of insect herbivores: if speciation
is mainly allopatric and non-ecological, particular host
taxa should be closely clustered on the tips of the insect
phylogeny (Fig. 1a). Conversely, if speciation is mainly
ecology-based, closely related insects should tend to
a
b
Insect sp. 1
Insect sp. 2
Insect sp. 3
Insect sp. 4
Insect sp. 5
Insect sp. 6
Insect sp. 7
Insect sp. 8
Insect sp. 9
Insect sp. 1
Insect sp. 2
Insect sp. 3
Insect sp. 4
Insect sp. 5
Insect sp. 6
Insect sp. 7
Insect sp. 8
Insect sp. 9
Host sp. A
Host sp. B
Host sp. C
Figure 1 Phylogenetic distributions of host-plant taxa arising
from different speciation modes in insects. (a) Distribution of
host-plant taxa on the phylogeny of a hypothetical insect group in
which speciation is mainly allopatric, and in which host shifts occur
relatively infrequently in relation to speciation events. (b)
Distribution of host taxa when speciation is mainly associated with
host shifts. Note that only two host shifts are needed to explain
current host-plant associations in a, whereas a minimum of six
changes are needed to produce the pattern in b, although the
number of speciation events is eight in both cases.
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 2 of 13
have different hosts, meaning that plants would occur in
an intermixed fashion along the tips of the insect phylo-
geny (Fig. 1b). In the first case, the number of inferred
host-plant shifts should be distinctly lower than the
number of speciation events that are required to pro-
duce the extant herbivore species, whereas, in the latter
case, the number of inferred host shifts should be close
to the number of lineage splits.
Here, we apply a molecular phylogenetic analysis of
sawflies belonging to the so-called ?Higher? Nematinae
(Hymenoptera: Tenthredinidae) to estimate the relative
importance of ecological versus non-ecological specia-
tion in plant-feeding insects. This group of over 700
species comprises most of the taxonomic and ecological
diversity found within the tenthredinid subfamily Nema-
tinae, which prompted Ross [34] to speculate: ?The
higher group of genera must have evolved some highly
beneficial biological characteristics, because they are at
present the most abundant boreal sawfly group in num-
ber of species and probably also in population.? Indeed,
higher nematines are ubiquitous in most habitats across
the Northern Hemisphere, and their larvae feed on a
wide variety of northern plant taxa [35-37]. Their larval
feeding habits are equally diverse: in addition to ?normal?
external folivores, the group includes berry miners,
flower and catkin feeders, leaf folders, and various gall-
inducing species (Fig. 2) [38]. Combined with the high
species number, such broad diversity in species-specific
resource use presents many possibilities for studying the
tempo and mode of speciation.
Methods
Taxon sampling, amplification, and sequencing
Our study builds on a previous phylogenetic analysis of
the whole subfamily Nematinae [39] by adding 78 new
species and sequences of a third gene (Cytochrome b)
to the published dataset. The current taxon sample
includes 127 exemplars of 125 Higher Nematinae spe-
cies, meaning that nearly all higher-nematine species
groups and main ecological niches (host-plant taxa and
larval habits) are represented [35,36]. Multiple represen-
tatives were included for all large genera and species
groups (Additional file 1). Trees were rooted by includ-
ing three non-nematine tenthredinids and ten species
belonging to the nematine tribes Hoplocampini, Stauro-
nematini, Pseudodineurini, Caulocampini, Susanini,
Dineurini, and Cladiini as outgroups in the analyses.
These small ?Lower? Nematinae groups form a paraphy-
letic grade with respect to the ingroup [39].
Sequence data were collected from two mitochondrial
genes (Cytochrome oxidase I [CoI]: 810 bp; Cytochrome
b [Cytb]: 718 bp) and from two exons (501 bp + 276 bp =
777 bp) of the F2 copy of the nuclear Elongation
factor-1a (EF-1a) gene following previously-described
protocols [39,40]. The concatenated data matrix con-
sists of 2305 bp of sequence data for 140 species.
Sequences are missing for three, nine, and six species
for CoI, Cytb, and EF-1a, respectively, but every
included species has full-length sequences from at least
two genes. New sequences have been submitted to
GenBank under accession numbers HM237366-
HM237589, and the Nexus-formatted data matrix,
together with resultant phylogenetic trees, is available
as Additional file 2.
Phylogenetic analyses
Modeltest 3.5 [41] was implemented in conjunction with
PAUP* 4.0b10 [42] to identify the least complex substi-
tution model for use in Bayesian phylogenetic analyses
in MrBayes 3.1.2 [43]. Hierarchical likelihood ratio tests
indicated a GTR+I+?4 model as optimal for each of the
three genes. A separate, unlinked substitution model
was allowed for each gene in a three-partition analysis.
A single run employing default priors was run for eight
million generations with eight incrementally heated (t =
0.1) chains; tree sampling was done from the current
cold chain every 100th generation, and the first 10,001
trees recovered prior to reaching stationarity were dis-
carded as a burnin. The consensus tree showing all
compatible groupings (Fig. 3) was calculated on the
basis of the remaining 70,000 trees. A corresponding
maximum-likelihood (ML) analysis was performed using
RAxML 7.0.4 [44]. This analysis employed a separate
GTR+I+?4 model for each gene, but branch lengths
were estimated jointly for the whole data (Additional file
2). Clade support was estimated on the basis of 500
bootstrap replicates of the data matrix (Fig. 3).
BEAST 1.4.8 [45] was used to estimate the relative
ages of various nematine groups based on a Bayesian
relaxed molecular clock method. The topologically
unconstrained analysis allowed a separate GTR+I+ ?4
model of substitution for each gene and employed an
uncorrelated relaxed lognormal clock model for rate
variation among branches, a Yule prior on speciation,
and default priors for other parameters except for the
mean of branch rates (ucld.mean), which was fixed to 1.
Three independent runs with automatic tuning of opera-
tors were run for 80 million generations, and parameters
and trees were sampled every 1,000 generations (the
XML file is available as Additional file 3). After inspec-
tion of adequate convergence of runs and effective sam-
ple sizes of the parameters in Tracer 1.4.1 [46], the tree
files were combined in LogCombiner 1.4.8 (part of the
BEAST package). The first 40,000 trees from each file
were discarded as a burnin, and the tree file was subse-
quently thinned by resampling trees every 3,000
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 3 of 13
ad
f
b
c
e
g
Figure 2 Examples of the diversity of resource use within the Higher Nematinae. (a) Female of Pristiphora mollis ovipositing on a leaf of
Vaccinium myrtillus. (b) Larva of Amauronematus amplus feeding on Betula pubescens. (c) Colony of Pristiphora erichsonii larvae on Larix sp. (d)
Larva of Phyllocolpa leucosticta inside opened leaf fold on Salix caprea. (e) Larva of Pristiphora angulata feeding on flowers of Spiraea
chamaedryfolia. (f) Larva of Pontania pustulator inside opened leaf gall on Salix phylicifolia. (g) Melastola sp. larva inside opened berry of
Vaccinium parvifolium. The locations of these exemplar species on the phylogeny of Higher Nematinae are indicated by letters in Fig. 3.
(Photographs by T. Nyman).
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 4 of 13
Figure 3 Phylogeny of the Higher Nematinae and the diversification of host-plant use within the group. The tree was reconstructed
according to a Bayesian phylogenetic analysis allowing a separate GTR+I+?4 model of substitution for each gene. Numbers above branches
show Bayesian posterior probabilities (%) followed by bootstrap proportions (%) from the corresponding ML analysis (hyphens in the place of
bootstrap values denote clades that were not present in the ML tree). Branches are colored according to a maximum-parsimony reconstruction
of host-family use, larval feeding habits are indicated by font colors and by symbols after species names (see legend). Species illustrated in Fig. 2
are indicated to the right of the tree.
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 5 of 13
generations; the maximum clade credibility (MCC) tree
showing mean branch lengths (Fig. 4) is based on the
40,001 post-stationarity trees that remained after
thinning.
Character analyses
To reconstruct ancestral host-plant families and feeding
habits, these traits were treated as unordered multistate
characters and maximum-parsimony optimized on the
phylogenetic trees using Mesquite 2.6 [47]. Oligo- and
polyphagous taxa were coded with all used host families.
To estimate the number of ecological shifts that have
occurred during the radiation of the Higher Nemati-
nae, we first identified all distinct ecological niches
(feeding habit ? host plant(s)) found in the ingroup
species included in the phylogenetic analysis, and
coded each niche with a separate state within a single
character (outgroup states were coded as unknown).
Because the aim was to calculate numbers of changes,
the typical number of steps between two different
states was 1. However, we also created ?generalist ?
states for species that utilize multiple plant taxa and
then used the step-matrix option in Mesquite to define
the cost to these states, from the plant taxa that are
included within the generalist host range, as being
zero. By doing so, we essentially assumed that a clear
overlap in the host ranges of different species implies
that they have not speciated ecologically (theoretical
models of resource-based speciation typically assume
distinct, non-overlapping niches as the cause of diver-
gent selection [2,30]). Phylogenetic uncertainty in the
estimate was taken into account by recording the num-
bers of steps in the niche character across the 70,000
post-burnin trees that were sampled by MrBayes
during the phylogenetic analysis [48].
As a separate estimate of the proportion of lineage
splits accompanied by a shift in resource use, we inden-
tified all terminal sister-species pairs across the MCC
tree (Fig. 4), and then separated these 35 pairs into
those in which both species have identical or overlap-
ping niches, and into those in which the species have
different niches. Thereafter, we performed a logistic
regression in SPSS for Windows 17.0 (SPSS, Inc., 233 S.
Wacker Drive, Chicago, IL 60606-6307, USA) to test
whether the probability that sister species have a differ-
ent niche depends on the time elapsed since their most
recent common ancestor (= relative node height in the
MCC tree).
Proportions of higher nematine species feeding on dif-
ferent plant genera (Fig. 5) were extracted from
Lacourt?s [36] list of host-plant affiliations of sawflies of
the Western Palearctic region. Only species with known
hosts were included, and proportions were calculated
separately for the tribe Pristiphorini and for the
Nematini+Mesoneurini clade (see Figs. 3, 4 and 5).
Oligo- and polyphagous species were counted as an
additional species for each plant genus on which they
feed (for example, the oligophagous Craesus latipes (Vil-
laret) was treated as one species on Alnus and another
on Betula).
Results
Phylogenetic trees
The Bayesian and ML analyses of the sequence data
produced relatively well-supported trees showing that
the Higher Nematinae constitutes a monophyletic clade
within the subfamily Nematinae (Figs. 3 and 4; the ML
tree is included in Additional file 2). The three topolo-
gies are largely congruent, with discrepancies mainly
evident in tree regions that are weakly supported. Major
divisions within the ingroup correspond closely with the
traditional tribes Nematini, Pristiphorini, and Mesoneur-
ini (Figs. 3 and 4). Conflict with traditional classifica-
tions is mostly evident in that the largest nematine
genera (Nematus, Pristiphora, and Amauronematus)
come out as para- and polyphyletic (see [39]). Posterior
probabilities and bootstrap proportions of many group-
ings within Nematini are low, but because these uncer-
tainties concern mainly relationships among strongly
supported middle-level clades, they have only minor
importance for the conclusions below.
The trees document a pattern of frequent faunal
exchange across the Holarctic region, because European,
North American, and Asian exemplar species (see Addi-
tional file 1) are intermixed throughout the trees. Nearc-
tic species are found scattered among European ones in
all major higher-nematine genera (Nematus, Amaurone-
matus, and Pristiphora), but also in smaller groups such
as Eitelius, Pontopristia, and Pikonema (Figs. 3 and 4).
Our analysis also confirms Smith?s [49] hypothesis of a
close relationship between the North American Nema-
tus erythrogaster -group and the Holarctic genus Crae-
sus, as well as his earlier [50] suggestion of a connection
between the exclusively Nearctic genus Neopareophora
and European Nepionema.
Evolutionary dynamics of resource use
Diversification of the Higher Nematinae has been a
dynamic process in which host-plant associations and
larval lifestyles change continually, although feeding-
habit changes are distinctly rarer than shifts in
host-plant use (Figs. 3 and 4). Various forms of internal
feeding, such as gall induction, leaf folding, catkin feed-
ing, and berry mining, have evolved repeatedly from
ancestors whose larvae were external feeders on leaves
or on needles (Fig. 4). Higher-nematine larvae are cur-
rently found on plants belonging to over 16 families, but
most species are concentrated on plants in Salicaceae,
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 6 of 13
Figure 4 Relaxed molecular-clock phylogeny of the Higher Nematinae, and the evolution of different larval habits within the group.
The maximum clade credibility tree resulted from a topologically unconstrained Bayesian phylogenetic analysis employing a relaxed lognormal
clock and a separate GTR+I+?4 model of substitution for each gene. Numbers above branches show posterior probabilities (%), and blue shaded
bars the 95% highest posterior density intervals for relative node ages for nodes with probabilities over 50%. Branch colors denote larval feeding
habits according to unordered maximum-parsimony optimization, symbols to the right of species names show host-plant genera and families of
the exemplar species (see legend). Full host ranges of polyphagous species are given in Additional file 1.
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 7 of 13
Betulaceae, Rosaceae, Ericaceae, and Pinaceae (Fig. 5),
partly because colonization and recolonization events
have occurred repeatedly among these plant taxa (Fig.
3). Interestingly, the distribution of species across uti-
lized plant families differs between the clade formed by
Pristiphorini and its sister clade formed by Nematini
+Mesoneurini (Fig. 5; c2= 155.93, df = 15, P < 0.0001),
the clearest discrepancy being the high proportion of
Salix-feeding species within the most species-rich tribe
Nematini.
Speciation and niche shifts
The existence of the 125 sampled ingroup species
demands 124 past speciation events, but explaining the
current distribution of species-level niches on the Baye-
sian consensus tree (Fig. 3) and on the ML tree requires
only 68 shifts in feeding habits and/or host taxa. This
estimate is robust against phylogenetic uncertainty,
because when niches are similarly maximum-parsimony
optimized on the 70,000 Bayesian post-burnin trees, 67-
69 shifts (mean = 68.13) are needed. Even if shifts to
generalist host-use states are treated as a true niche
shift (= 1 step from other states), the Bayesian consen-
sus tree is only 75 steps long (ML tree = 74 steps), and
all trees in the Bayesian tree sample require between 73
and 75 changes (mean = 74.73 steps).
When only sister-taxon pairs on the MCC tree are
considered, species in 19 out of 35 pairs (54.3%) have
non-overlapping host ranges and/or a distinct difference
in their larval feeding modes. However, the logistic
regression (Fig. 6) shows that the probability of sister
species having different niches is strongly affected by
the time since their most recent common ancestor: Pdif-
ference = 1/(1+e
-(-1.29+15.12*split age)), the constant (P =
0.045) and the effect of split age (P = 0.013) being statis-
tically significant.
Discussion
Research on ecological speciation has traditionally
focussed on sister-species pairs or on small groups of
closely related lineages that differ in their resource use,
and which could therefore have originated by niche
shifts. While such studies have convincingly shown that
ecology-based diversification is possible in highly dispa-
rate taxa and under many plausible scenarios (e.g.,
[8,51,52]), the overall frequency of ecological speciation
remains unknown. Recently, broader phylogenetic
approaches have provided insights into the relative
importance of alternative speciation modes [53-55]. For
example, comparative analyses employing age-range cor-
rections have shown that closely related species tend to
have less overlap in their geographical ranges than do
distantly related species, which indicates that speciation
rarely occurs in sympatric settings [53,56-58]. However,
the finding that speciation is largely allopatric does not
exclude the possibility that the build-up of reproductive
isolation between incipient species has an ecological
basis: as mentioned above, ecological divergence can,
and in fact is more likely to, occur in complete or par-
tial allopatry [27,28,30]. Therefore, phylogenetic studies
on the frequency of niche shifts in relation to the num-
ber of past speciation events are more likely to produce
a correct view of the prevalence of ecological speciation
[22,31,33,56].
The traditional paradigm in plant-herbivore research
is that host shifts are a major factor promoting species
divergence [23,59,60]. However, there are two good rea-
sons for suspecting that the importance of niche shifts
for speciation is overestimated: First, there has been a
huge?most likely disproportionate?interest in the intri-
guing possibility that host-associated speciation in insect
herbivores could occur in sympatry, i.e., without geogra-
phical isolation [4,13,27,58]. Second, it seems probable?
and perfectly logical?that insect groups that are chosen
for phylogenetic studies on host-plant shifts are selected
preferentially from taxa in which species are known a
priori to be relatively specialized and to exhibit clear
interspecific variation in host-plant use (e.g., [19,40,61]).
In the case of the Higher Nematinae, our phylogenetic
analysis reveals a pattern of frequent niche shifts both in
terms of larval lifestyles and host-plant use (Figs. 3 and
4). Despite this, optimizing larval niches on the Bayesian
tree sample shows that at most about 60% of lineage
splits could have been caused by ecological factors. This
value should be considered as an upper limit, because
our ecologically overdispersed taxon-sampling scheme
will raise the relative number of niche shifts, and the
sampling design should also override the tendency of
maximum parsimony to underestimate the frequency of
changes in fast-evolving traits [62]. When only sister
species are considered, the percentage of pairs having
divergent niches is 54. This raw value is intriguingly
close to Winkler & Mitter?s [22] recent ?fifty-fifty? esti-
mate of the proportions of ecological vs. nonecological
speciation, which was based on a broad literature survey
of sister species of herbivorous insects. However, our
logistic regression (Fig. 6) shows that immediately after
speciation only an estimated 21.6% of higher-nematine
sister-species pairs would have non-overlapping niches.
The discrepancy between the methods is most likely
explained by postspeciational host shifts, which can
inflate the apparent frequency of ecological speciation in
uncorrected sister-species comparisons. Although denser
taxon sampling will be needed for a more exact estimate
of the prevalence of ecology-based diversification within
the Higher Nematinae, the marked drop in the inferred
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 8 of 13
proportion in the age-adjusted analysis suggests that
phylogenetic time corrections would be useful also in
surveys of other insect herbivore taxa.
It is possible, however, that the frequency of ecological
speciation varies among clades [22,31]. In particular, it
appears that the extreme diversity (400-500 species
[63,64]) of gall-inducing nematines in the subtribe Euur-
ina (Figs. 3 and 4) has been spurred by host-shifting
among Salix species. Like other gall-inducing insects
[65], Euurina gallers are very host-specific compared to
willow-associated nematines having external-feeding lar-
vae, which tend to utilize multiple host species [36,66],
and which therefore probably may have radiated mainly
allopatrically. Higher-nematine subgenera and species-
groups feeding externally on other plant taxa are like-
wise often dominated by species having identical or
broadly overlapping host-plant ranges [36,38,66], and
niche shifting seems to be particularly infrequent in
relation to speciation in groups associated with Picea,
Larix, Vaccinium, and plants within Betulaceae (Fig. 3).
It remains to be studied whether such non-ecological
radiations can be used to estimate the proportion of
non-ecological speciation in related groups in which
species differ in their host use, because some proportion
of host switches also in these groups undoubtedly have
occurred well before or after speciation events (cf. [33]).
While earlier hypotheses on insect diversification
emphasized coevolution of plant defenses and herbivore
counterdefenses as a major driver of insect diversifica-
tion [59,67,68], recent studies applying dated phyloge-
nies have uncovered a possible role of long-term
Figure 5 Distributions of Higher Nematinae species on different plant genera. Proportions are shown separately for the tribe Pristiphorini
and for its sister clade composed of the tribes Mesoneurini and Nematini (see Figs. 3 and 4). Host data and estimates of species numbers are
from Lacourt?s [36] checklist of Western Palearctic sawflies, plant families are denoted by separate font colors (see legend). Numbers in
parentheses after tribe names are in the order: total number of species/number of Western Palearctic species/number of Western Palearctic
species with known hosts.
Figure 6 The probability that higher-nematine sister species
have different niches in relation to time since their divergence.
Data on pairwise niche differences (1 = different hosts and/or larval
feeding habits; 0 = identical or overlapping niches) and split ages
(= relative time since common ancestor) was taken from the 35
terminal sister-taxon pairs in the Bayesian MCC tree (Fig. 4), and the
probability curve was estimated using logistic regression.
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 9 of 13
climatic conditions in determining rates of speciation
and extinction in various herbivore groups [69-71].
Throughout the Earth?s history, climatic changes have
lead to major shifts in plant communities and global
vegetation patterns, with direct negative or positive con-
sequences for associated herbivores [72]. In particular,
systems experiencing repeated cycles of range contrac-
tions, expansions, and faunal mixing can constitute ?spe-
ciation machines? that lead to escalating diversification
across multiple trophic levels [73-75]. A Cenozoic high-
latitude speciation machine could explain why higher
nematines seem to have an inordinate fondness for wil-
lows: nearly a third of Western Palearctic species in the
tribe Pristiphorini feed on Salix species, and in the
Nematini the percentage is as high as 68 (Fig. 5; this
general pattern holds also in North America [35,37]).
The largest willow-associated radiations have occurred
within the aforementioned gall-inducing subtribe Euur-
ina, and in the predominantly willow-feeding Amaurone-
matus+Pontopristia clade, which includes at least 112
species [36,76]. These temporally overlapping radiations
began c. 30 million years ago (Mya), assuming that the
most recent common ancestor of the Higher Nematinae
lived about 70 Mya (Fig. 4; see [39]). Interestingly, this
would place the onset of these radiations at the time of
strong cooling of the global climate, which began in the
early Oligocene c. 35 Mya, and which was followed by
alternating periods of cold ice ages and warmer intergla-
cials [77]. Such climatic oscillations, with resultant long-
distance migrations of whole ecosystems, could have
promoted the diversification of willows that are concen-
trated in relatively cool habitats and that currently com-
prise over 400 species [78,79]. The conditions that
generated diversity in Salix would simultaneously have
acted also on the insect groups that depend on them
and, like in higher nematines, willows currently support
a considerable proportion of species also in, for exam-
ple, northern butterflies and moths [80], phytophagous
beetles [80,81], and leafhoppers [31].
The role of competition in directing the historical
assembly and present structure of herbivore communities
has been debated for decades [82-84]. If competition was
a force directing host switching, shifts would tend to
occur towards un- or underused plant taxa, meaning
that, over time, herbivore host-plant associations would
become overdispersed with regard to plant phylogeny. By
contrast, higher-nematine host use is strongly underdis-
persed, shifts having occurred repeatedly and in many
directions among a handful of dominant northern plant
families, while a large proportion of the Holarctic flora
apparently has been effectively ignored for tens of mil-
lions of years. This shifting pattern conforms to the
?resource island model? [23,85,86] of herbivore diversifi-
cation, in which phylogenetically biased colonizations
and back-colonizations among plant taxa, in combination
with abundance-dependent extinction, lead to accumula-
tion of herbivore species on common plants that have
many relatives [80,87,88]. Competition could still operate
more subtly, if recruitment follows a ?macroevolutionary
ideal free distribution? (cf. [89]), so that the number of
herbivore species that can be supported depends on the
commonness (or overall biomass) of a given plant [90].
However, the convergent, asynchronous, and undoubt-
edly ongoing colonizations of many plant taxa by various
higher-nematine groups (Figs. 3 and 4) indicates that
ecological pre-emption of host taxa does not occur, and
that northern insect-plant communities are still unsatu-
rated and could therefore soak up even more herbivore
species in the future. The broad overlaps in the geogra-
phical distributions [35,36] of many closely related, eco-
logically near-identical higher-nematine species?that
necessarily must have diverged in allopatry and then
brought to sympatry by postspeciational range shifts?
provides further support for the view that interspecific
competition, either via direct resource competition or via
indirect competition caused by shared natural enemies, is
of minor importance in structuring herbivore commu-
nities [73,82,84,91].
Conclusions
Our phylogeny-based analysis of the Higher Nematinae
strongly indicates that the importance of niche shifts for
speciation in plant-feeding insects is at present explicitly
and implicitly overestimated. In particular, applying a
time correction for sister-group comparisons lowered
the proportion of apparent ecology-based speciation
events from roughly 50% to around 20%. The vast
majority of lineage splits in higher nematines therefore
seem to have occurred non-ecologically in allopatry, and
this may well be true also for most other plant-feeding
insects. Reconciling this result with the finding of Janz
et al. [92] that species richness in nymphalid butterfly
clades correlates positively with collective host ranges
requires further work; we propose that the correlation
follows from reduced extinction probabilities in ecologi-
cally versatile groups, rather than from increased ecolo-
gical speciation within them.
Evolutionary dynamics observed within the Higher
Nematinae favour a largely non-interactive, non-equili-
brium view of community assembly in northern plant-
herbivore networks: geographical shifts across the whole
Northern Hemisphere have been commonplace in many
higher-nematine groups, and the frequent co-occurrence
of related species utilizing seemingly identical niches
indicates that distributional changes occur largely unim-
peded by direct or indirect competitive interactions.
More detailed surveys of local communities are, how-
ever, necessary in order to exclude the possibility that
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 10 of 13
competitive repulsion occurs on smaller geographical
scales, which could lead to a mosaic pattern of patch
occupancy by ecologically equivalent relatives [93].
The Higher Nematinae comprises well over 70% of the
species in the subfamily Nematinae, but the main part of
higher-nematine diversity lies within the tribe Nematini,
in which a strikingly high proportion of species use wil-
lows as hosts. This suggests that the success of higher
nematines was caused, not by the evolution of superior
biological characteristics as suggested by Ross [34], but
by a fortuitous association with willows at a time of a
cyclically cooling global climate. Reliably dated molecu-
lar-phylogenetic analyses of Salix and Salix-associated
herbivores are desperately needed to test our hypothesis
that the diversification of willow-based food webs was
accelerated during the latter half of the Cenozoic Era.
The genus Salix has thus far proven to be an extremely
challenging target for such studies [94,95], but even
comparative analyses across herbivore taxa would surely
provide interesting insights into the evolutionary history
of Holarctic plant-herbivore communities.
Additional material
Additional file 1: Collection data for exemplar specimens, and
taxonomic and ecological background information. Excel file
containing collection data for the specimens used in the study, as well
as species numbers, geographical distributions, larval lifestyles, and
collective host ranges of genera, subgenera, and species groups within
the Higher Nematinae.
Additional file 2: Sequence data used in phylogeny reconstruction
and resultant phylogenetic trees. NEXUS file containing the data
matrix and trees obtained from the Bayesian phylogenetic analyses in
MrBayes and BEAST, and the maximum-likelihood tree from the analysis
using RAxML.
Additional file 3: Data file and run parameters for BEAST. XML file
used for the phylogenetic analysis in BEAST.
Acknowledgements
We especially wish to thank colleagues who provided samples of higher-
nematine species, many of which would otherwise have been impossible to
obtain: Lauri Kapari, Heikki Roininen, Alexey Zinovjev, Ewald Altenhofer, Mikk
Heidemaa, Marko Prous, Akira Yamagami, Matti Viitasaari, Herbert R.
Jacobson, Valerie Caron, Urs Schaffner, Jens Rydell, Jeffrey Joy, and B.
DeJonge. We also thank two anonymous referees for their constructive
criticisms, which helped to improve the manuscript. The Centre of Scientific
Computing in Helsinki and the Cyberinfrastructure for Phylogenetic Research
(CIPRES) project in San Diego allocated computing resources for
phylogenetic analyses on their servers. This research was initiated with
support from the SYNTHESYS Project http://www.synthesys.info which is
financed by the European Community Research Infrastructure Action under
the FP6 ?Structuring the European Research Area Programme? (project BE-
TAF-1462), and the main part of the funding was provided by the Academy
of Finland (project 124695 for TN).
Author details
1Department of Biology, University of Eastern Finland, P.O. Box 111, FI-80101
Joensuu, Finland. 2Liinalammintie 11 as. 6, FI-14200 Turenki, Finland.
3Systematic Entomology Laboratory, PSI, Agricultural Research Service, US
Department of Agriculture, c/o National Museum of Natural History,
Smithsonian Institution, P.O. Box 37012, MRC 168, Washington, DC 20013-
7012, USA. 4Department of Entomology, Royal Belgian Institute of Natural
Sciences, Rue Vautier 29, B-1000 Brussels, Belgium.
Authors? contributions
The study was conceived and designed by TN and JLB. TN performed
laboratory and data analyses, prepared figures, and wrote the manuscript.
JLB planned taxon sampling and study setup, and assisted in writing. VV and
DRS provided taxonomic and ecological background information and
identified specimens used in the analyses. All authors read and approved
the manuscript.
Received: 14 February 2010 Accepted: 1 September 2010
Published: 1 September 2010
References
1. Schluter D: The Ecology of Adaptive Radiation Oxford, Oxford University
Press 2000.
2. Rundle HD, Nosil P: Ecological speciation. Ecol Lett 2005, 8:336-352.
3. Smith TB, Sk?lason S: Evolutionary significance of resource
polymorphisms in fishes, amphibians, and birds. Annu Rev Ecol Syst 1996,
27:111-133.
4. Dr?s M, Mallet J: Host races in plant-feeding insects and their importance
in sympatric speciation. Phil Trans R Soc Lond B 2002, 357:471-492.
5. R?s?nen K, Hendry AP: Disentangling interactions between adaptive
divergence and gene flow when ecology drives diversification. Ecol Lett
2008, 11:624-636.
6. Nosil P, Harmon LJ, Seehausen O: Ecological explanations for (incomplete)
speciation. Trends Ecol Evol 2009, 24:145-156.
7. Ryan PG, Bloomer P, Moloney CL, Grant TJ, Delport W: Ecological
speciation in South Atlantic island finches. Science 2007, 315:1420-1423.
8. Irestedt M, Fjelds? J, Dal?n L, Ericson PGP: Convergent evolution, habitat
shifts and variable diversification rates in the ovenbird-woodcreeper
family (Furnariidae). BMC Evol Biol 2009, 9:268.
9. Thorpe RS, Surget-Groba Y, Johansson H: The relative importance of
ecology and geographic isolation for speciation in anoles. Phil Trans R
Soc B 2008, 363:3071-3081.
10. Schluter D, Conte GL: Genetics and ecological speciation. Proc Natl Acad
Sci USA 2009, 106:9955-9962.
11. Parent CE, Crespi BJ: Sequential colonization and diversification of
Gal?pagos endemic land snail genus Bulimulus (Gastropoda:
Stylommatophora). Evolution 2006, 60:2311-2328.
12. Nyman T, Bokma F, Kopelke J-P: Reciprocal diversification in a complex
plant-herbivore-parasitoid food web. BMC Biol 2007, 5:49.
13. Via S: Sympatric speciation in animals: the ugly duckling grows up.
Trends Ecol Evol 2001, 16:381-390.
14. Peccoud J, Ollivier A, Plantegenest M, Simon J-C: A continuum of genetic
divergence from sympatric host races to species in the pea aphid
complex. Proc Natl Acad Sci USA 2009, 106:7495-7500.
15. Despr?s L, David J-P, Gallet C: The evolutionary ecology of insect
resistance to plant chemicals. Trends Ecol Evol 2007, 22:298-307.
16. Karban R, Agrawal AA: Herbivore offense. Annu Rev Ecol Syst 2002,
33:641-664.
17. Toju H: Natural selection drives the fine-scale divergence of a
coevolutionary arms race involving a long-mouthed weevil and its
obligate host plant. BMC Evol Biol 2009, 9:273.
18. Percy DM, Page RDM, Cronk QCB: Plant-insect interactions: double-dating
associated insect and plant lineages reveals asynchronous radiations.
Syst Biol 2004, 53:120-127.
19. Lopez-Vaamonde C, Wikstr?m N, Labandeira C, Godfray HCJ, Goodman SJ,
Cook JM: Fossil-calibrated molecular phylogenies reveal that leaf-mining
moths radiated several million years after their host plants. J Evol Biol
2006, 19:1314-1326.
20. Hunt T, Bergsten J, Levkanicova Z, Papadopoulou A, St. John O, Wild R,
Hammond PM, Ahrens D, Balke M, Caterino MS, G?mez-Zurita H, Ribera I,
Barraclough TG, Bocakova M, Bocak L, Vogler AP: A comprehensive
phylogeny of beetles reveals the evolutionary origins of a
superradiation. Science 2007, 318:1913-1916.
21. Janz N, Nylin S: The oscillation hypothesis of host plant-range and
speciation. In Specialization, Speciation, and Radiation: the Evolutionary
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 11 of 13
Biology of Herbivorous Insects. Edited by: Tilmon KJ. Berkeley, University of
California Press; 2008:203-215.
22. Winkler IS, Mitter C: The phylogenetic dimension of insect-plant
interactions: a review of recent evidence. In Specialization, Speciation, and
Radiation: the Evolutionary Biology of Herbivorous Insects. Edited by: Tilmon
KJ. Berkeley, University of California Press; 2008:240-263.
23. Nyman T: To speciate, or not to speciate? Resource heterogeneity, the
subjectivity of similarity, and the macroevolutionary consequences of
niche-width shifts in plant-feeding insects. Biol Rev 2010, 85:393-411.
24. Mitter C, Farrell B, Wiegmann B: The phylogenetic study of adaptive
zones: has phytophagy promoted insect diversification? Am Nat 1988,
132:107-128.
25. Dyer LA, Singer MS, Lill JT, Stireman JO, Gentry GL, Marquis RJ, Ricklefs RE,
Greeney HF, Wagner DL, Morais HC, Diniz IR, Kursar TA, Coley PD: Host
specificity of Lepidoptera in tropical and temperate forests. Nature 2007,
448:696-700.
26. Futuyma DJ, Agrawal AA: Macroevolution and the biological diversity of
plants and herbivores. Proc Natl Acad. Sci USA 2009, 106:18054-18061.
27. Futuyma DJ: Sympatric speciation: norm or exception? In Specialization,
Speciation, and Radiation: the Evolutionary Biology of Herbivorous Insects.
Edited by: Tilmon KJ. Berkeley, University of California Press; 2008:136-148.
28. Funk DJ: Isolating a role for natural selection in speciation: host
adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles.
Evolution 1998, 52:1744-1759.
29. Funk DJ, Nosil P, Etges WJ: Ecological divergence exhibits consistently
positive associations with reproductive isolation across disparate taxa.
Proc Natl Acad Sci USA 2006, 103:3209-3213.
30. Rundell RJ, Price TD: Adaptive radiation, nonadaptive radiation, ecological
speciation and nonecological speciation. Trends Ecol Evol 2009,
24:394-399.
31. Ross HH: An uncertainty principle in ecological evolution. Univ Arkansas
Mus Occ Pap 1972, 4:133-157.
32. Barraclough TG, Hogan JE, Vogler AP: Testing whether ecological factors
promote cladogenesis in a group of tiger beetles (Coleoptera:
Cicindelidae). Proc R Soc Lond B 1999, 266:1061-1067.
33. Peterson AT, Sober?n J, S?nchez-Cordero V: Conservatism of ecological
niches in evolutionary time. Science 1999, 285:1265-1267.
34. Ross HH: A generic classification of the Nearctic sawflies. Ill Biol Monogr
1937, 34:1-173.
35. Smith DR: Suborder Symphyta. In Catalog of Hymenoptera in America North
of Mexico. Edited by: Krombein KV, Hurd PD Jr, Smith DR, Burks BD.
Washington, Smithsonian Institution Press; 1979:3-137.
36. Lacourt J: R?pertoire des Tenthredinidae ouest-pal?arctiques. M?m SEF
1999, 3:1-432.
37. Kouki J: Latitudinal gradients in species richness in northern areas: some
exceptional patterns. Ecol Bull 1999, 47:30-37.
38. Nyman T, Farrell BD, Zinovjev AG, Vikberg V: Larval habits, host-plant
associations, and speciation in nematine sawflies (Hymenoptera:
Tenthredinidae). Evolution 2006, 60:1622-1637.
39. Nyman T, Zinovjev AG, Vikberg V, Farrell BD: Molecular phylogeny of the
sawfly subfamily Nematinae (Hymenoptera: Tenthredinidae). Syst
Entomol 2006, 31:569-583.
40. 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.
41. Posada D, Crandall KA: Modeltest: testing the model of DNA substitution.
Bioinformatics 1998, 14:817-818.
42. Swofford DL: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other
Methods), version 40b10 Sunderland, Sinauer 2002.
43. Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference
under mixed models. Bioinformatics 2003, 19:1572-1574.
44. Stamatakis A, Hoover P, Rougemont J: A rapid bootstrap algorithm for the
RAxML web-servers. Syst Biol 2008, 75:758-771.
45. Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by
sampling trees. BMC Evol Biol 2007, 7:214.
46. Rambaut A, Drummond AJ: Tracer, version 1.4.1. 2007 [http://beast.bio.ed.
ac.uk/Tracer].
47. Maddison WP, Maddison DR: Mesquite: a modular system for
evolutionary analysis, version 2.6. 2009 [http://mesquiteproject.org].
48. Huelsenbeck JP, Rannala B, Masly JP: Accommodating phylogenetic
uncertainty in phylogenetic studies. Science 2000, 288:2349-2350.
49. Smith DR: The abbotii and erythrogaster groups of Nematus Panzer
(Hymenoptera: Tenthredinidae) in North America. Proc Entomol Soc Wash
2008, 110:647-667.
50. Smith DR: Nepionema, a nematine sawfly genus new to North America,
and an unusual new species of Nematus (Hymenoptera: Tenthredinidae).
Proc Entomol Soc Wash 1994, 96:133-138.
51. Savolainen V, Anstett M-C, Lexer C, Hutton I, Clarkson JJ, Norup MV,
Powell MP, Springate D, Salamin N, Baker WJ: Sympatric speciation in
palms on an oceanic island. Nature 2006, 441:210-213.
52. Kempf F, Boulinier T, De Mee?s T, Arnathau C, McCoy KD: Recent evolution
of host-associated divergence in the seabird tick Ixodes uriae. Mol Ecol
2009, 18:4450-4462.
53. Barraclough TG, Vogler AP: Detecting the geographical pattern of
speciation from species-level phylogenies. Am Nat 2000, 155:419-434.
54. Barraclough TG, Nee S: Phylogenetics and speciation. Trends Ecol Evol
2001, 16:391-399.
55. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB,
Riesenberg LH: The frequency of polyploid speciation in vascular plants.
Proc Natl Acad Sci USA 2009, 106:13875-13879.
56. Kozak KH, Wiens JJ: Does niche conservatism promote speciation? A case
study in North American salamanders. Evolution 2006, 60:2604-2621.
57. Perret M, Chautems A, Spichiger R, Barraclough TG, Savolainen V: The
geographical pattern of speciation and floral diversification in the
Neotropics: the tribe Sinningieae (Gesneriaceae) as a case study.
Evolution 2007, 61:1641-1660.
58. Linnen CR, Farrell BD: A test of the sympatric host race formation
hypothesis in Neodiprion (Hymenoptera: Diprionidae). Proc R Soc Lond B
2010.
59. Ehrlich PR, Raven PH: Butterflies and plants: a study in coevolution.
Evolution 1964, 18:586-608.
60. Diehl SR, Bush GL: An evolutionary and applied perspective of insect
biotypes. Annu Rev Entomol 1984, 29:471-504.
61. Ronquist F, Liljeblad J: Evolution of the gall wasp-host plant association.
Evolution 2001, 55:2503-2522.
62. Schluter D, Price T, Mooers A?, Ludwig D: Likelihood of ancestor states in
adaptive radiation. Evolution 1997, 51:1699-1711.
63. Kopelke J-P: Gall-forming Nematinae, their willow hosts (Salix spp.) and
biological strategies (Insecta, Hymenoptera, Symphyta, Tenthredinidae,
Nematinae: Euura, Phyllocolpa, Pontania). Senckenb Biol 2003, 82:163-189.
64. 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 Inc; 2005:467-494.
65. Price PW: Adaptive radiation of gall-inducing insects. Basic Appl Ecol 2005,
6:413-421.
66. Taeger A, Altenhofer E, Blank SM, Jansen E, Kraus M, Pschorn-Walcher H,
Ritzau C: Kommentare zur Biologie, Verbreitung und Gef?hrdung der
Pflanzenwespen Deutschlands (Hymenoptera, Symphyta). In
Pflanzenwespen Deutschlands (Hymenoptera: Symphyta). Edited by: Taeger A,
Blank SM. Keltern, Goecke 1998:49-135.
67. Farrell BD, Mitter C, Futuyma DJ: Diversification at the insect-plant
interface. Insights from phylogenetics. BioScience 1992, 42:34-42.
68. Becerra JX, Noge K, Venable DL: Macroevolutionary chemical escalation in
an ancient plant-herbivore arms race. Proc Natl Acad Sci USA 2009,
106:18062-18066.
69. McKenna DD, Farrell BD: Tropical forests are both evolutionary cradles
and museums of leaf beetle diversity. Proc Natl Acad Sci USA 2006,
103:10947-10951.
70. McLeish MJ, Chapman TW, Schwarz MP: Host-driven diversification of gall-
inducing Acacia thrips and the aridification of Australia. BMC Biol 2007,
5:3.
71. Winkler IS, Mitter C, Scheffer SJ: Repeated climate-linked host shifts have
promoted diversification in a temperate clade of leaf-mining flies. Proc
Natl Acad Sci USA 2009, 106:18103-18108.
72. Wilf P, Labandeira CC, Johnson KR, Coley PD, Cutter AD: Insect herbivory,
plant defense, and early Cenozoic climate change. Proc Natl Acad Sci USA
2001, 98:6221-6226.
73. Ross HH: The origin of species diversity in ecological communities. Taxon
1972, 21:253-259.
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 12 of 13
74. Esselstyn JA, Timm RM, Brown RM: Do geological or climatic processes
drive speciation in dynamic archipelagos? The tempo and mode of
diversification in Southeast Asian shrews. Evolution 2009, 63:2595-2610.
75. Proche? ?, Forest F, Veldtman R, Chown SL, Cowling RM, Johnson SD,
Richardson DM, Savolainen V: Dissecting the plant-insect diversity
relationship in the Cape. Mol Phylogenet Evol 2009, 51:94-99.
76. Taeger A, Blank SM: ECatSym - Electronic World Catalog of Symphyta (Insecta,
Hymenoptera). Program version 3.9, data version 34 M?ncheberg, Digital
Entomological Information 2008.
77. Zachos JC, Dickens GR, Zeebe RE: An early Cenozoic perspective on
greenhouse warming and carbon-cycle dynamics. Nature 2008,
451:279-283.
78. Argus GW: Infrageneric classification of Salix (Salicaceae) in the New
World. Syst Bot Monogr 1997, 52:1-121.
79. Skvortsov AK: Willows of Russia and adjacent countries. Taxonomical and
geographical revision. Univ Joensuu Fac Math Nat Sci Rep Ser 1999,
39:1-307.
80. Kennedy CEJ, Southwood TRE: The number of species of insects
associated with British trees: a re-analysis. J Anim Ecol 1984, 53:455-478.
81. Mardulyn P, Milinkovitch MC, Pasteels JM: Phylogenetic analyses of DNA
and allozyme data suggest that Gonioctena leaf beetles (Coleoptera;
Chrysomelidae) experienced convergent evolution in their history of
host-plant family shifts. Syst Biol 1997, 46:722-747.
82. Lawton JH, Strong DR Jr: Community patterns and competition in
folivorous insects. Am Nat 1981, 118:317-338.
83. Denno RF, McClure MS, Ott JR: Interspecific interactions in phytophagous
insects: competition reexamined and resurrected. Annu Rev Entomol
1995, 40:297-331.
84. Kaplan I, Denno RF: Interspecific interactions in phytophagous insects
revisited: a quantitative assessment of competition theory. Ecol Lett 2007,
10:977-994.
85. Janzen DH: Host plants as islands in evolutionary and contemporary
time. Am Nat 1968, 102:592-595.
86. McKenna DD, Sequeira AS, Marvaldi AE, Farrell BD: Temporal lags and
overlap in the diversification of weevils and flowering plants. Proc Natl
Acad Sci USA 2009, 106:7083-7088.
87. Kelly CK, Southwood TRE: Species richness and resource availability: a
phylogenetic analysis of insects associated with trees. Proc Natl Acad Sci
USA 1999, 96:8013-8016.
88. Lewinsohn TM, Novotny V, Basset Y: Insects on plants: diversity of
herbivore assemblages revisited. Annu Rev Ecol Evol Syst 2005, 36:597-620.
89. Fretwell SD, Lucas HL Jr: On territorial behavior and other factors
influencing habitat distribution in birds. I. Theoretical development. Acta
Biotheor 1970, 19:16-36.
90. Rabosky DL: Ecological limits and diversification rate: alternative
paradigms to explain the variation in species richness among clades
and regions. Ecol Lett 2009, 12:735-743.
91. Tack AJM, Ovaskainen O, Harrison PJ, Roslin T: Competition as a
structuring force in leaf miner communities. Oikos 2009, 118:809-818.
92. Janz N, Nylin S, Wahlberg N: Diversity begets diversity: host expansions
and the diversification of plant-feeding insects. BMC Evol Biol 2006, 6:4.
93. Emerson BC, Gillespie RG: Phylogenetic analysis of community assembly
and structure over space and time. Trends Ecol Evol 2008, 23:619-630.
94. Azuma T, Kajita T, Yokoyama J, Ohashi H: Phylogenetic relationships of
Salix (Salicaceae) based on rbcL sequence data. Am J Bot 2000, 87:67-75.
95. Chen J-H, Sun H, Wen J, Yang Y-P: Molecular phylogeny of Salix L.
(Salicaceae) inferred from three chloroplast datasets and its systematic
implications. Taxon 2010, 59:29-37.
doi:10.1186/1471-2148-10-266
Cite this article as: Nyman et al.: How common is ecological speciation
in plant-feeding insects? A ?Higher? Nematinae perspective. BMC
Evolutionary Biology 2010 10:266.
Submit your next manuscript to BioMed Central
and take full advantage of: 
? Convenient online submission
? Thorough peer review
? No space constraints or color figure charges
? Immediate publication on acceptance
? Inclusion in PubMed, CAS, Scopus and Google Scholar
? Research which is freely available for redistribution
Submit your manuscript at 
www.biomedcentral.com/submit
Nyman et al. BMC Evolutionary Biology 2010, 10:266
http://www.biomedcentral.com/1471-2148/10/266
Page 13 of 13