The phylogenetic dimension of insect/plant interactions: A review of recent evidence

Full text

240
The dramatic expansion of research on insect-plant interac-
tions prompted by Ehrlich and Raven’s (1964) essay on
coevolution focused at first mainly on the proximate mech-
anisms of those interactions, especially the role of plant sec-
ondary chemistry, and their ecological consequences. Sub-
sequently, in parallel with the resurgence of phylogenetics
beginning in the 1970s and 1980s, there arose increasing
interest in the long-term evolutionary process envisioned
by Ehrlich and Raven (e.g., Benson et al. 1975; Zwölfer
1978; Berenbaum 1983; Mitter and Brooks 1983; Miller
1987). Since the early 1990s, spurred in part by the increas-
ing accessibility of molecular systematics, there has been a
happy profusion of phylogenetic studies of interacting
insect and plant lineages. The results so far have reinforced
skepticism about the ubiquity of the particular macroevolu-
tionary scenario envisioned by Ehrlich and Raven, now
commonly termed “escape and radiation” coevolution
(Thompson 1988). However, this model continues to
inspire and organize research on the evolution of insect-
plant assemblages because it embodies several themes of
neo-Darwinism, each of interest in its own right, which
have been taken up anew in the modern reembrace of evo-
lutionary history. In this chapter we attempt to catalog
some of the postulates about phylogenetic history derivable
from Ehrlich and Raven’s essay and evaluate their utility for
explaining the structure of contemporary insect-plant inter-
actions.
The escape and radiation model (reviewed in Berenbaum
1983) tacitly assumes, first, that the traits governing species’
interactions, such as insect host-plant preference, are phylo-
genetically conserved due to constraints such as limited
availability of genetic variation. Such constraints create time
lags between successive insect and plant counteradaptations,
allowing the lineage bearing the most recent innovation to
increase its rate of diversification. Second, a related general
implication is that, because of genetic or other constraints
on evolutionary response to new biotic surroundings, the
structure of present-day insect-plant interactions (e.g., who
eats whom) will be governed more by long-term evolution-
ary history than by recent local adaptation. This postulate
parallels a broader recent shift in thinking about community
assembly, from a focus on equilibrium processes to a greater
appreciation of the role of historical contingency (Webb et
al. 2002; Cattin et al. 2004; DiMichele et al. 2004). Third, the
radiation component of escape and radiation perfectly
encapsulates the “new synthesis” view, lately enjoying a
revival (Schluter 2000), that diversification is driven prima-
rily by ecological interactions. Insect-plant interactions have
figured prominently in the modern reexamination of all
three of these broad postulates.
This chapter surveys the recent evidence on the phy-
logeny of insect-plant interactions, focusing chiefly on
among-species differences in larval host-plant use by herbiv-
orous insect lineages (largely neglecting pollinators, which
are treated by Adler in this volume), and organized around
the themes sketched above. We draw mostly on literature of
the past dozen years, that is, subsequent to early attempts at
a similar survey (e.g., Mitter and Farrell 1991; Farrell and
Mitter 1993). Given the great diversity of phytophage life
histories and feeding modes, full characterization of host-use
evolution will require, in addition to hypothesis tests in par-
ticular groups, the estimation of relative frequencies of alter-
native evolutionary patterns across a broad sampling of line-
ages. Our emphasis here is on the latter approach. A
complete catalog is no longer feasible, but we have made a
concerted and continuing effort to compile as many phylo-
genetic studies of phytophagous insect groups as possible.
These are entered into a database that at this writing con-
tained over 1000 entries, many of which were obtained from
the Zoological Record database. Our analyses and conclu-
sions are based chiefly on approximately 200 of these reports
that contain both a phylogenetic tree and information on
EIGHTEEN
The Phylogenetic Dimension of Insect-Plant Interactions:
A Review of Recent Evidence
ISAAC S. WINKLER AND CHARLES MITTER

host-plant use. Many of the phylogenies are based on DNA
sequences, while for others the chief evidence is morphol-
ogy. This database, intended as a community resource to
promote further synthesis, is available at www.chemlife
.umd.edu/entm/mitterlab, as are the data compilations and
other supplementary materials mentioned in the text. Our
nomenclature follows APGII (2003) for angiosperm families
and higher groups, and Smith et al. (2006) for ferns.
Conservatism of Host-Plant Use
Full understanding of the influence of evolutionary history
on insect-plant associations will require a broad accounting
of the degree to which the different dimensions of the feed-
ing niches of phytophagous insects are phylogenetically
conserved. Much evidence on some aspects of this question
has accumulated in the past decade.
Conservation of Host-Taxon Associations
The strongest generalization that can be made about the
evolution of host-plant use is that related insect species most
often use related hosts. This long-standing conclusion is
now supported by numerous studies in which the history of
host-taxon use has been reconstructed, most often under the
parsimony criterion, on an insect phylogeny inferred from
other characters. An early compilation (Mitter and Farrell
1991) of the few phylogenetic studies then available (25)
suggested that on average, less than 20% of speciation events
were accompanied by a shift to a different plant family;
strictly speaking, the compilation was of the fraction of
branches subtended by the same node on the phylogeny
that have diverged in host-family use, as inferred under the
parsimony criterion. We have now repeated that calculation
using essentially all applicable phylogenies we could find,
totaling 93 (27 Coleoptera, 28 Hemiptera, 19 Lepidoptera, 12
Diptera, 5 Hymenoptera, and 1 each of Thysanoptera and
Acari [honorary insects for the purposes of this chapter]).
Some of the uncertainty in host-shift estimates comes from
incomplete sampling of species. In the earlier compilation,
host-shift frequency was calculated as the total number of
host-family shifts inferred under the parsimony criterion,
divided by one less than the number of sampled species with
known hosts. This should be an unbiased estimate of the
actual frequency of host shifts, if the included species are a
random subset of the clade sampled. However, sampling in
phylogenetic studies is often deliberately overdispersed
across subclades (e.g., genera within a tribe), which should
tend to inflate the average evolutionary distance among
sampled species and hence the apparent frequency of host
shifts. To evaluate the importance of this effect, we also cal-
culated a corrected frequency estimate, dividing the number
of shifts detected on the phylogeny by the total number of
species with known hosts, including ones not included in
the phylogenetic study. We will refer to these two estimates,
in the order here described, as maximum versus minimum.
In further contrast to the earlier tabulation, this one
excluded the relatively few polyphagous species (defined
here as those using more than two plant families); several
phylogenies including a high proportion of polyphagous
species were excluded, as well. A detailed tabulation of the
phylogenies is given in the Online Supplementary Table S2,
while the results are summarized in (Fig. 18.1).
The histogram of Fig. 18.1 shows a result very similar to
that of the earlier tabulation, underscoring the prevalence
of host conservatism. The distributions of host-family shift
frequencies, strongly right-skewed, have medians of 0.08
(maximum frequency) and 0.03 (minimum frequency). Sta-
tistical tests of the hypothesis of nonrandom phylogenetic
conservatism in host-genus or host-family use have now
become routine within studies of the kind tabulated here.
These most often use the so-called PTP test (permutation
tail probability [Faith and Cranston 1991]), in which the
null distribution is generated by random redistribution of
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 241
0
5
01
51
02
52
03
53
04
e
n
o
n(
)devresbo
+
1
9
.
0
09.0-
1
8
.
0
0
8
.
0
-
17.0
07
.
0
-1
6
.
0
0
6
.
0
-
15.0
0
5
.
0-
1
4
.
0
0
4
.
0
-
13.00
3
.
0-12.002.
0
-
11.001
.
0
-
10
0
.
0
host shift frequency
number of studies
.qerf .nim
.qerf .xam
FIGURE 18.1. Frequency of host
shifts per speciation event for 93 phy-
tophagous insect phylogenies, calcu-
lated by dividing number of host-fam-
ily shifts observed on phylogeny by
number of included in-group species
(solid bars, maximum host-shift fre-
quency), and by total number of
described species in the ingroup clade
(hatched bars, minimum host-shift
frequency). For references and taxa
included, see Online Supplementary
Table S2

the observed host-family associations across the insect phy-
logeny. Significant “phylogenetic signal” has been detected
in nearly every instance (e.g., Table 18.2). In addition, sev-
eral authors have used randomization tests on frequencies
of shift among different host families or groups thereof to
show that these preferentially involve related high-rank
host taxa (Janz and Nylin 1998; Ronquist and Liljeblad
2001); conservatism at the level of major angiosperm clades
(APGII 2003) is probably common as well.
It is widely accepted that conserved host-taxon associa-
tions primarily reflect conserved recognition of and other
adaptations to plant secondary chemistry, but this assump-
tion has been difficult to test because of the generally close
correlation of chemistry with plant taxonomy. Several cases
of mismatch between host-chemical and taxonomic similar-
ity have now been examined phylogenetically and shown
closer correspondence of insect phylogeny to chemistry
than plant relatedness (Becerra 1997; Wahlberg 2001; Ker-
goat et al. 2005). Recent studies include reexamination of
classic examples (Dethier 1941; Feeny 1991) of repeated
shifts by lepidopterans between unrelated host families
bearing similar secondary compounds (e.g., Lauraceae,
Rutaceae, and/or Apiaceae [Berenbaum and Passoa 1999;
Zakharov et al. 2004; Berenbaum, this volume]). This sub-
ject is by no means exhausted, as many more such syn-
dromes surely await documentation. It should be noted,
however, that herbivore groups feeding on plants without
distinctive chemical defenses or on undefended plant parts
can also show similarly specialized, conserved host associa-
tions (e.g., leafhoppers [Nickel 2003]).
Variation in Rates of Major Host Shift
Although conservatism is pervasive, phylogenetic studies
continue to document great variation among phytophage
lineages in the frequency of “major” host shifts (e.g., to dif-
ferent plant families). Establishing patterns to this variation
will be a key step toward understanding the constraints on
diet evolution. Many predictors for differential host-shift
rates have been advanced (reviewed in Mitter and Farrell
1991), some invoking properties of plant taxa and/or com-
munities, others invoking traits of the phytophages.
Attempts to test these, however, remain few, and the subject
seems ripe for further synthesis. In one of the few explicit
analyses, Janz and Nylin (1998) present evidence that
among butterflies, shifts among major angiosperm clades are
less frequent in herb feeders than tree feeders. Nyman et al.
(2006) found that internally feeding nematine sawfly clades
have colonized significantly fewer plant families than their
externally feeding sister groups. Radiations on oceanic
islands have been suggested to undergo exaggerated diver-
gence in niches, including host-plant use, compared to con-
tinental relatives (e.g., Schluter 1988). In the only test for
phytophages, the eight genera of delphacid planthoppers
endemic to various Pacific islands were found to have a sig-
nificantly higher mean rate of host-family shift (two times
higher), and frequency of polyphagy, than the 52 continen-
tal genera (Wilson et al. 1994); systematic work in progress
will permit reanalysis with better control for phylogeny. Pos-
sible explanations for elevated host-shift rates on islands
include limited availability of preferred hosts of colonizers,
lesser chemical distinctiveness among host species due to
relaxed herbivore pressure, and absence of continental com-
petitors and/or insect natural enemies (reviewed in Wilson
et al. 1994). Further comparisons to insular radiations may
help to identify causes of the prevailing host specificity and
conservatism of mainland phytophages.
Compilations of host-shift rates as in Online Supplemen-
tary Table S2 should permit further tests of hypotheses
about differential host conservatism. Following Fagan et al.
(2002), we used phylogenies from the literature to concate-
nate all the groups in the table into a single metaphylogeny
(presented in Online Supplementary Fig. S3). One can then
map onto the phylogeny the inferred host-shift frequencies
plus the distribution of traits postulated to affect them (e.g.,
internal versus external feeding). The metatree can then be
divided into a maximal number of independent regions
(contrasts), each consisting of a set of contiguous branches
and containing an inferred evolutionary change in the
putative predictor trait. For each contrast, a single response
measure is calculated (e.g., the difference in mean host-shift
frequency between groups having the opposing states of the
predictor variable). Paired comparisons are then used to test
for a consistent effect of the predictor variable on host-shift
frequency. In a first analysis, strong support was found for
elevated mean frequency of host-family shifts inferred from
just the oligophagous species (i.e., polyphages not scored)
in lineages that include one or more polyphagous species, as
opposed to lineages lacking polyphages (12/12 contrasts dif-
fering in the same direction; P  0.0001, sign test). This
finding supports the conjecture (e.g., Janz and Nylin, this
volume) that rapid shift among host taxa and polyphagy of
individual species are related phenomena.
It has often been suggested (e.g., Farrell and Mitter 1990)
that dependence on host-derived toxins for larval and/or
adult phytophage defense should reduce the likelihood of
major host shifts. This postulate has had no formal compar-
ative test. However, recent phylogenetic evidence suggests
that use of such defenses itself is in general not so conserva-
tive, or so intimately tied to larval diet, as might be sup-
posed (Dobler et al. 1996; Dobler 2001), probably because
herbivores often have multiple defenses. Thus, in the
chrysomelid beetle subtribe Chrysomelina (Termonia et al.
2001; Kuhn et al. 2004) the ancestral larval defense is
entirely autogenous, but there have been two independent
origins, within Salicaceae-feeding lineages, of dependence
on host-derived salicin. Within one of these groups there
has been subsequent addition of a second type of defense,
based on a combination of autogenous and host-derived
pathways, followed by multiple host shifts to another fam-
ily (Betulaceae) from which salicin is not available. Avail-
ability of more than one defense-metabolism pathway may
242 CO- AND MACROEVOLUTIONARY RADIATION

likewise have facilitated repeated host-family shifts in other
groups, such as the tropical chrysomeline genus Platyphora
(Termonia et al. 2002). Moths of the typically aposematic
family Arctiidae are one of several groups that have con-
verged on defensive use of plant-derived pyrrholizidine
alkaloids (PAs), while producing endogenous other toxins as
well. A recent phylogeny for arctiids implies a single origin
of larval feeding on PA-containing plants and sequestration of
PAs that are retained into the adult stage (Weller et al. 1999).
In a species-rich subclade of the ancestrally PA-plant-feed-
ing lineage, there have been repeated shifts to non-PA larval
hosts, implying lack of constraint by chemical dependence.
Adult defense, however, shows strong apparent phyloge-
netic inertia, as adults in this subclade have evolved to
actively collect and use PAs. A similar “constraint” explana-
tion was proposed for the propensity of adults in one
African and one New World galerucine chrysomelid sub-
tribe to feed on, and use in courtship and defense, toxic
cucurbitacins from Cucurbitaceae, which are at present fed
on by larvae in just a single genus in each subtribe. Recent
phylogenetic evidence (Gillespie et al. 2003, 2004), how-
ever, strongly supports independent New World and Old
World origins for both larval and adult use of cucurbits, and
points, albeit less strongly, to adult use arising first.
Other Conserved Aspects of Host Use
Most discussion of the impact of host-plant use on insect
diversification has focused on host-taxon differences, but
other conserved dimensions of the feeding niche have also
been recognized (e.g., Powell 1980; Powell et al. 1998),
including host growth form and habitat, plant part
exploited, mode of insect feeding, and phenology of ovipo-
sition and feeding. Most herbivorous insects are specialized
to particular host tissues, such as leaves, flowers, fruits,
seeds, stems, or roots, in addition to particular host taxa. On
any one plant part, moreover, insects are typically special-
ized for one of a great variety of feeding modes. For exam-
ple, a partial list of feeding behaviors exhibited by insects
that eat leaves includes galling, mining, leaf rolling or tying,
and external folivory. The relative rates of evolution of the
various niche dimensions are fundamental to assessing their
roles in phytophage diversification.
Several authors have begun to quantify these rates and
their variation. Cook et al. (2002) used a maximum likeli-
hood approach to show that a genus of cynipid gall wasps
shifts among host-plant organs more often than among sec-
tions of their host genus, oaks. Farrell and Sequeira (2004)
used similar methods to demonstrate, conversely, that in
chrysomeloid beetles, shift among major host clades out-
paces shift among host tissues. Other reports reinforce this
latter trend at the host species level (Condon and Steck 1997;
Favret and Voegtlin 2004). However, studies of gallers are
mostly consistent in finding rapid shift among host tissues
(e.g., Yang and Mitter 1994; Plantard et al. 1997; Nyman et al.
2000; Dorchin et al. 2004); shifts in gall location, shape, and
timing, often on the same host species, may be important
facilitators of galler speciation. Host growth form (i.e., trees
versus herbs) often shows very strong phylogenetic conser-
vatism relative to host clade (Ronquist and Liljeblad 2001;
Bucheli et al. 2002; Lopez-Vaamonde et al. 2003), but not
always (Janz and Nylin 1998; Schick et al. 2003). Timing of
oviposition or development with respect to host phenology
is another dimension of host use that may frequently con-
tribute to speciation, either on the same host or on a novel
host (e.g., Wood 1993; Pratt 1994; Whitcomb et al. 1994;
Harry et al. 1998; Filchak et. al. 2000; Weiblen and Bush
2002; Sachet et al. 2006).
A special form of oft-conserved host use, occurring in
some groups of aphids and gall wasps (Cynipidae), is obli-
gate alternation between different host taxa in successive
generations. Host alternation may have originated multiple
times in aphids (Moran 1988, 1992; von Dohlen and Moran
2000; von Dohlen et al. 2006), though this inference rests
mostly on differences in the mode of host alternation and
other life-history features, as the phylogenetic evidence can-
not adequately distinguish between gains and losses of host
alternation per se. Regardless, this kind of complex host
association has clearly evolved only a few times, while the
loss of one or the other host has occurred repeatedly within
ancestrally host-alternating lineages (Moran 1992; see also
Cook et al. 2002). The degree to which host alternation (as
opposed to simply shifting to a different host) reflects con-
straint versus adaptation has been debated (Moran 1988,
1990, 1992; Mackenzie and Dixon 1990).
Parallelism, Reversal, and Genetic
Constraints on Host Shift
Although conservatism of host-use traits can suggest the
influence of phylogenetic “constraint” or “inertia” (Blomberg
and Garland 2002), this interpretation is not automatic, as
stabilizing selection is a plausible alternative (Hansen and
Orzack 2005). The constraint interpretation would receive
powerful support if one could demonstrate limitations on
within-population genetic variation, for traits determining
host use, that corresponded to the actual history of shifts
undergone by the larger clade to which the test populations
belonged. In a series of studies deserving wide emulation,
Futuyma and colleagues (reviewed in Futuyma et al. 1995; see
also Gassman et al. 2006) reconstructed the history of host
use in oligophagous Ophraella leaf beetles, then screened four
species for genetic variation in larval and adult ability to feed
and survive on the hosts (various genera of Asteraceae, in sev-
eral tribes) fed on by their congeners. In only 23 of 55 tests
(species by host) was there any detectable genetic variation
for ability to use the alternative host. Such variation as did
appear was mainly for use of hosts of closely related beetle
species; these plants were themselves closely related to the
normal host. Thus, lack of available variation for use of alter-
native hosts is probably much of the explanation for the con-
served association of this genus with Asteraceae. Other lines
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 243

of evidence, less direct, point to an analogous conclusion for
other clades and traits. Many authors have noted (e.g., Janz
and Nylin 1998; Hsiao and Windsor 1999; Janz et al. 2001;
Swigon´ová and Kjer 2004; Zakharov et al. 2004) that host-
family use is often highly homoplasious (i.e., showing multi-
ple independent origins of the same habit), sometimes with
repeated colonizations of a single plant family inferred to be
an ancestral host. Janz et al. (2001) tested the long-standing
hypothesis that such a propensity reflects retained ability to
use former hosts, finding that Nymphalini butterfly larvae of
most species were willing to feed on the ancestral host
(Urtica), regardless of what host they normally fed on. Some
specific kinds of phylogenetic pattern also strongly suggest
genetic constraint. Thus, in several unrelated groups of
galling insects, it has been found that features such as gall
structure or gall position on the plant follow an ordered mul-
tistep progression on the phylogeny, for example from sim-
ple to successively more complex (Nyman et al. 2000; Ron-
quist and Liljeblad 2001). If the evolution of such traits were
not limited by genetic variation, it is hard to see why it
should nonetheless follow the presumptive path of “genetic
least resistance” (Schluter 2000). The nature and extent of
genetic constraints, critical to a full understanding of host-
use evolution, is an underexplored subject on which modern
genetic/genomic approaches hold promise for rapid progress
(e.g., Berenbaum and Feeny, this volume).
Conservatism, Host Shifts, and Speciation
Given the pervasive conservatism of higher-host-taxon use,
one might wonder whether diet conservatism on a finer
scale has been underestimated, and shifts to different host
species consequently assigned too large a role in phy-
tophagous insect speciation. One requisite for answering
this question is a broad estimate of the proportion of speci-
ation events that are accompanied by a change in host
species. To our knowledge, no such survey has been pub-
lished. We provide an estimate based on 145 presumptive
sister species pairs found within 45 phylogenies of phy-
tophagous insect genera or species groups in our database
for which information about hosts and geographic distribu-
tion was available. Taxa other than confirmed species (e.g.,
host races or unconfirmed sibling species) were excluded.
Each species pair was scored as sharing a host-plant species
or not; pairs were also scored as having hosts from the same
genus, family, or higher angiosperm clade (defined in APGII
2003). To contrast the frequency of host differences to that
of differences in distribution, each sister pair was also scored
as having distributions overlapping by 10% or more (subjec-
tively estimated) versus 10%. No characterization of the
accuracy of these phylogenies was attempted. A possible
source of bias is that island radiations, which show a some-
what greater frequency of allopatry between sister species
than continental forms and (surprisingly) a somewhat lower
mean proportion of host differences, comprise over 25% of
our data set. Therefore, we also present results with and
without island lineages. Our tabulation and its sources are
given in Online Supplementary Table S4, and the results are
summarized in (Table 18.1).
Overall, about 48% of the divergence events we tabulated
are associated with an apparent change in host species. This
is our best estimate of the fraction of speciation events that
could have been driven by host shifts (though of course we
have no way of knowing whether the host differences actu-
ally accompanied speciation, rather than arising prior to or
after speciation). Our results are consistent with a major role
for host shifts in phytophage speciation, but not a ubiqui-
tous one; we estimate that about half of all speciation
events are unaccompanied by a host shift. Of course, many
of the latter could have involved change in tissue fed upon
or other aspects of host use.
Greater circumspection is required in interpreting our
compilation of differences in distribution, which potentially
bear on the controversial question of sympatric speciation
244 CO- AND MACROEVOLUTIONARY RADIATION
TABLE
18.1
Summary of Host and Distribution Overlap versus Nonoverlap for 145 Sister-Species Pairs from 45 Phytophagous
Insect Phylogenies
Total Host Host Host Host Total Total
Species Species Species Species Species Hosts Distributions
Pairs Overlap Overlap Disjunct Disjunct Disjunct Disjunct
Distributions Distributions Distributions Distributions
Overlap Disjunct Overlap Disjunct
All pairs 145 27 48 26 44 48% 63%
Continental pairs only 101 22 27 22 30 52% 56%
Island pairs only 44 5 21 4 14 41% 80%
NOTE: Host species overlap, members of pair sharing at least one host species; host species disjunct, sharing no host species; distributions overlap,
with 10% areal overlap in geographic distribution; distributions disjunct, with 10% overlap in geographic distribution. Details including sources in
Online Supplementary Table S4.

(Lynch 1989). The utility of phylogenetic evidence on this
issue has been doubted, even dismissed, because species’
distributions can shift rapidly (Barraclough and Vogler
2000; Losos and Glor 2003; Fitzpatrick and Turelli 2006).
Thus, the proportion of sister species that are sympatric
might reflect dispersal ability rather than frequency of sym-
patric speciation (Chesser and Zink 1994; Losos and Glor
2003). Indeed, allopatric speciation has recently been sug-
gested to play a prominent role even in the Rhagoletis
pomonella group, the poster child for sympatric speciation
(Barraclough and Vogler 2000). Nonetheless, we follow
Berlocher (1998) in holding the comparative approach wor-
thy of further exploration. Berlocher suggested that there
should be a higher frequency of sympatry between sister
species in host shifting than in non-host-shifting taxa, if
host differences are commonly important in allowing
species to originate, or at least remain distinct, in sympatry.
In our compilation, however, extant sister species using dif-
ferent host species were sympatric only slightly (and not
significantly) more often than those not differing in host,
37% (N  70) versus 36% (N  75). This result seems to cast
doubt on the ubiquity of divergence by sympatric host shift,
but that interpretation may be too conservative. For exam-
ple, among-group variation in dispersal ability, which we
did not correct for, might obscure the “signal” for host-asso-
ciated sympatric divergence in our tabulation. Moreover,
the probability of sympatric divergence may depend
strongly on how different the hosts are. Thus, sister species
that differ in host genus used show a markedly higher fre-
quency of sympatry (50%) than pairs whose hosts are con-
generic if they differ at all (33%), though this difference was
not statistically significant (P  0.189, 
2
test). This observa-
tion is at least consistent both with a role for “major” host
differences in promoting sympatric divergence, and with
the postulate that shifts to distantly related hosts are more
likely in sympatry, which allows for prolonged prior adapta-
tion (Percy 2003). We should note, finally, that the study of
phytophagous insect speciation and host-shift mechanisms
is being revolutionized by, among other advances, the
advent of fine-scale, intraspecific molecular phylogenetics
including phylogeography sensu Avise (2000). These appli-
cations of phylogenies are treated elsewhere in this volume.
Phylogenesis of Host Range
Special attention has focused on the evolution of diet
breadth, namely, the diversity of host plants fed on by a sin-
gle herbivore species. Restriction to a small subset of the
available plants is a dominant feature of phytophagous
insect ecology. In addition to demanding an explanation in
its own right (Bernays and Chapman 1994), it has made
herbivorous insects a leading exemplar for investigating
the ecological and evolutionary consequences of specializa-
tion (Schluter 2000; Funk et al. 2002). Phylogenies can
potentially serve three roles in the study of host range.
First, they delimit independent contrasts for identifying
traits or geographic and other circumstances whose occur-
rence is correlated with evolutionary changes in host range,
facilitating both comparative and experimental studies of the
adaptive significance and consequences of those changes.
Second, the rate and direction of changes in host range
inferred on a phylogeny can point to genetic/phylogenetic
constraints or lack thereof on host-range evolution. Third,
phylogenies can in principle detect differential effects of
broad versus narrow host range on diversification rates.
Analyses of the second and third kinds could potentially sup-
port nonadaptive, macroevolutionary explanations for the
predominance of host specificity, such as more frequent spe-
ciation in specialists than in generalists, in contrast to
hypotheses invoking a prevailing individual advantage
(Futuyma and Moreno 1988).
The study of host-range evolution is still something of a
conceptual and methodological tangle. A fundamental
question is how to define host range. Although broad,
somewhat arbitrary categories of relative specialization may
often suffice to reveal evolutionary patterns (e.g., Janz et al.
2001), objective, quantitative measures may yield greater
statistical power and allow more meaningful comparisons
across studies (Symons and Beccaloni 1999). However it is
defined, host range is surely a composite feature likely to
reflect different combinations of (typically unknown) adult
and immature traits in different groups. It is probably sub-
ject to a heterogeneous mix of influences that vary in rela-
tive strength with the scale of comparison. Small-scale
changes in host range might reflect behavioral plasticity or
local adaptation in response to differences in host abun-
dance or quality, or host-associated assemblages of competi-
tors, predators, or parasitoids (e.g., Singer et al. 2004;
Bernays and Singer 2005). Such changes could also repre-
sent short-lived intermediate steps in the evolution of new
specialist species (e.g., Hsiao and Pasteels 1999; Janz et al.
2001, 2006). In contrast, changes evident mainly on longer
time scales, and spanning a greater range of diet breadths,
could reflect less frequent but more pervasive evolutionary
shifts involving multiple component adaptations. At any
scale of examination, broader host range could result from
different causes in different lineages.
Given the heterogeneity of potential causes, evolutionary
patterns of host range are likely to differ widely among
groups. Phylogenetic evidence has begun to accumulate,
but we are far from having an adequate characterization of
that variation, let alone an explanation. The most useful
studies will be those in which (1) unambiguous distinctions
are evident in host range, reflecting intrinsic differences
among species (not higher taxa as in Berenbaum and Passoa
[1999], contra Nosil [2002] and Nosil and Mooers [2005]),
and (2) taxon sampling is dense enough to permit detection
of evolutionary trends if these exist. Only a handful of the
studies in our database appear to meet these criteria. We
summarize the nine that we judged to come closest in
(Table 18.2). No criticism is implied of any work not
included in this somewhat subjective selection, particularly
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 245

TABLE 18.2
Synopsis of Nine Recent Studies Bearing on Phylogenetic Patterns of Host Range
No. Specialists Criterion for Forms of
vs. no. Specialist Directionality Significant Host-Taxon Significant Host-Range
Insect Taxon Taxon Sample Generalists vs. Generalist Reported Conservation? Conservation? Source
Coleoptera:
Chrysomelidae:
Oreina
Coleoptera:
Curculionidae:
Scolytinae:
Dendroctonus
Coleoptera:
Bruchidae: Stator
Lepidoptera:
Nymphalidae:
Melitaeini
12/24 spp., spanning
all ecological
variation in genus
18/19 spp. (position
of remaining
species taken from
literature)
21/22 spp. with
known hosts
10/10 gen., 65/250
spp.; sparse
sampling in one
large Neotropical
clade
6 vs. 6
6 vs. 13
4 vs. 16
51 vs.14
1 vs.  1 host
tribe
Using 
1
⁄2 vs. 
1
⁄2
of available host
species
1 vs.  1 host
tribe
1 vs. 1 host
family
None
Specialists
limited to
tips of
phylogeny
Generalists
derived
Host-family
gains 
losses
Host family and tribe
conserved, P  0.01
PTP
Host genus conserved,
P  0.01, PTP
(authors)
Use of 1 of 4 host
genera conserved,
P  0.03, PTP
(authors)
Host-family use
conserved, P 
0.003 (author)
No: P  0.47, PTP
No: P  1.00, PTP
(authors)
No: P  1.00,
multiple tests
(authors)
No for gen. vs. spec.
(P  0.34 PTP; yes
(P  0.02) for
number of host
families (1–6)
Dobler et al.
1996
Kelley and
Farrell 1998
Morse and
Farrell 2005
Wahlberg 2001

Lepidoptera:
Nymphalidae:
Nymphalini
Lepidoptera:
Nymphalidae:
Polygonia
Lepidoptera:
Saturniidae:
Hemileuca
Diptera:
Tephritidae:
Tomoplagia
Phasmida:
Timematidae:
Timema
27/70 spp.; most
taxa in some
nearctic lineages
14/16 spp.
22 populations in 17
spp./28 spp. total;
excluded taxa may
be synonyms
19/59 spp.; sampling
limited to part of
Brazil
14 spp. (17 taxa)/21
spp. (remainder
described
subsequently)
17 vs. 10
7 vs. 5
15 vs. 7
11 vs. 8, or
14 vs. 5, or
15 vs. 4
11 vs. 6
1 vs. 1 host
order
1 vs. 1 host
order
Using primarily 1
vs. 1 host
family
1 vs. 1 host
genus, or subtribe,
or tribe
1 (95% of records)
vs. 1 host genus
Specialist
ancestor;
host gains 
losses
Specialist
ancestor;
host gains 
losses
None
Depends on
criterion
Generalist
ancestor
Host-family use
conserved, P  0.01,
PTP (authors)
Host-order use
conserved,
P  0.001, PTP
Host-family use
conserved, P  0.02,
PTP
No: P  0.18 (PTP)
for host subtribe use
Host genus
conserved, P  0.04
(authors)
Marginal: P  0.06,
PTP
No for gen. vs. spec.
and number of host
orders (1–5;
P  0.30, PTP)
No: P 
1.00, PTP
(authors)
No: P  0.50, PTP,
all criteria
No: P  0.59, PTP
Janz et al.
2001
Weingartner
et al. 2006
Rubinoff and
Sperling 2002
Yotoko et al.
2005
Crespi and
Sandoval
2000
NOTE: See “Table References” for source information. Gen., generalist; PTP, permutation tail probability test; spec., specialist; spp., species.

since the tracing of diet breadth has only rarely been an
explicit goal.
The strongest generalization evident so far is that host
range is quite evolutionarily labile, much more so than use
of particular host taxa. As a gauge of that lability, we tabu-
lated the results of PTP tests (Faith and Cranston 1991) on
degree of host specificity treated as a binary character with
changes in the two directions equally weighted (one versus
more than one host family, or other criteria specified by the
authors or otherwise appropriate to the study group; about
half these analyses were performed by the authors). In seven
of nine cases, this test cannot reject a random distribution
of host range on the phylogeny, whereas in each case but
one, use of individual host taxa is significantly conserved.
As several authors have noted, host range is clearly not sub-
ject to strong forms of phylogenetic constraint or “inertia”
(Blomberg and Garland 2002), such as absolute irreversibil-
ity (Nosil and Mooers 2005; Yotoko et al. 2005). In fact, the
paucity of obvious phylogenetic signal may complicate fur-
ther characterization of host-range evolution by limiting
the utility of some standard strategies of phylogenetic char-
acter analysis. Thus, when a two-state likelihood model is
applied to estimate the relative rates of transition to and
from specialization, the rates can most often be closely pre-
dicted from just the proportions of specialists and general-
ists among the terminal taxa (Nosil 2002; Nosil and Mooers
2005). This outcome, intuitively expected if the states are
distributed randomly on the tree, might be taken to suggest
that phylogenies have little to contribute to the understand-
ing of host-range evolution. And indeed, it is possible that
much of the variation in host range analyzed so far is in fact
phylogenetically “random” in the sense of reflecting idio-
syncratic local fluctuation, for example in the availability
of, and/or selective advantage of using, particular hosts.
This may be especially true when all the species within the
study group are specialists in the broad sense of feeding on
plants in, for instance, the same family.
As several authors have noted, however, it is plausible that
larger-scale phylogenetic regularities remain to be discovered
through the elaboration of more detailed, process-oriented
models of host-range evolution (Stireman 2005). Multiple
approaches can be distinguished. Thus, host range might be
thought of as a trait phylogenetically ephemeral in itself, but
with probabilities of change predictable from the states of
other, more conserved features, inviting use of the “compar-
ative method.” For example, distribution of the use of two
versus more than two tribes of legumes appears by itself to
be random on a phylogeny of the seed beetle genus Stator.
Closer inspection, however, shows that independent origins
of broader host range are significantly concentrated in line-
ages that oviposit on predispersal seeds, rather than on intact
seed pods or dispersed seeds (Morse and Farrell 2005).
An alternative approach focuses on the genetic and eco-
logical mechanisms by which host range changes. Thus,
Crespi and Sandoval (2000; see also Nosil et al. 2003) con-
clude that host specialization in Timema walking sticks
comes about when host-associated color polymorphism in
polyphagous ancestors is converted into species differences
under disruptive selection by predators. Phylogenetic evi-
dence by itself is consistent with but does not strongly
establish ancestral polyphagy. However, that interpretation is
supported by abundant experimental and other evidence.
Similar logic is reflected in the elaboration of a novel hypoth-
esis about butterfly host range (e.g., Janz et al. 2001; Wein-
gartner et al. 2006; Janz and Nylin, this volume). A phylogeny
for the nymphalid tribe Nymphalini suggests ancestral restric-
tion to Urticales followed by repeated host-range expansions
as well as contractions, with multiple ostensibly independent
colonizations of a set of disparate plant families. Complemen-
tary experiments show that larvae of many species are able to
feed on hosts not presently used by that species, but charac-
teristic of their inferred ancestors and/or extant relatives.
Retained latent feeding abilities may help to explain rapid
expansions (and hence observed lability) of host range.
Polyphagy may also facilitate radical host shifts (and/or fur-
ther broadening of host range), given that less specialized
species seem to generally make more oviposition mistakes
(Janz et al. 2001), and has been suggested to thereby promote
diversification (Janz et al. 2006; Weingartner et al. 2006; Janz
and Nylin, this volume). This postulate stands in direct con-
trast to the prediction that specialization promotes faster spe-
ciation, for which evidence is currently lacking (see below).
Several of the foregoing hypotheses may apply to a broad
phylogenetic pattern of host range in the noctuid moth sub-
family Heliothinae (Mitter et al. 1993; Cho 1997; Fang et al.
1997; S. Cho, A. Mitchell, C. Mitter, J. Reiger, M. Matthews,
submitted). A paraphyletic basal assemblage, species-rich
and almost entirely oligophagous or monophagous (80% on
Asteraceae), contrasts sharply with an advanced “Heliothis
clade” containing a much higher proportion of polyphages.
Host range is correlated with phylogeny, albeit weakly, but
the most dramatic difference is in its much higher rate of
change in the Heliothis clade. That lineage appears to have a
set of conserved life-history features (higher fecundity, body
size, and other traits) that are relatively permissive of
changes in host range, while the low fecundity, small size,
low vagility, and other traits of the more basal species may
strongly disfavor host-range expansion. Phylogenetically
controlled analyses of the life-history correlates of diet
breadth are still too few, but the number is growing (e.g.,
Beccaloni and Symons 2000) and further synthesis seems
imminent (Jervis et al. 2005).
With so many promising recent leads at hand, we can
look forward to rapid progress in understanding of the phy-
logenetic patterns of host-range evolution.
Signatures of Long-Term History in
Extant Insect-Plant Interactions
Strong conservatism of host taxon or other aspects of host-
plant use raises the possibility that the current distribution of
insects across plant species reflects some form of long-term
248 CO- AND MACROEVOLUTIONARY RADIATION

synchrony in the diversification of those associates. One
extreme form of synchronous evolution would be strict par-
allel phylogenesis or cospeciation, in which descendant line-
ages of the insect ancestor maintain continuous and exclu-
sive association with the descendants of the ancestral plant
species; the expected signature is a characteristic form of cor-
respondence between the phylogenetic relationships, and
the absolute ages, of the extant associates. Extensive method-
ological and empirical work on this general issue over the
past 15 years, in many groups of organisms, has established
that strict or nearly strict parallel phylogenesis is almost
entirely limited to parasites and other symbionts that are
directly transmitted between host parent and offspring indi-
viduals (e.g., Page 2003). However, variants of this scenario
more likely for free-living phytophages have also been envi-
sioned, involving intermittent and/or less specific association
of insect species with particular host-plant taxa, and produc-
ing corresponding forms of incomplete phylogeny matching.
Under escape and radiation coevolution, for example, the
closest match is expected not between phylogenies per se,
but between phylogenetic sequences of escalating plant
defenses and insect counteradaptations (Mitter and Brooks
1983). The marks of other forms of shared evolutionary his-
tory might lie primarily elsewhere. For example, it has been
proposed that differences in the predominant host associa-
tions of major phytophagous insect clades reflect differences
in which plant groups dominated the global flora in the dif-
ferent eras in which those phytophages arose (Zwölfer 1978).
The critical evidence on such postulates will often be
absolute datings. For the full range of questions considered in
this section, a combined approach from phylogenetics and
paleontology is proving especially powerful (reviewed in
Labandeira 2002; see also Grimaldi and Engel 2005). There is
currently a surge of interest in molecular dating studies,
driven in part by the increasing sophistication of methods for
combining evidence from fossils and molecular divergence
(reviewed in Magallón 2004; Welch and Bromham 2005),
though the reliability of such datings is still poorly under-
stood.
In this section we attempt to sketch out and evaluate the
evidence for several forms of historical imprint on insect-
plant associations. Such inquiry matters for two reasons.
First, traces of shared long-term history imply that there has
been at least the opportunity for prolonged reciprocal evo-
lutionary influence—coevolution in a broad sense—and
may even provide evidence on the nature and extent of that
coevolution. Second, from the ecological point of view,
unique marks of history imply that the assembly of extant
insect-plant communities cannot be fully explained by just
the current properties of local or regional species pools or
even the evolutionary propensities of these; one may need
also to invoke the contingent historical sequence in which
particular insect and plant lineages appeared on earth (Far-
rell and Mitter 1993).
Early in the current era of phylogenetic studies, there was
much interest in the possibility of parallel phylogenesis
between insect and host-plant clades. There is now enough
evidence to state with confidence that correspondence of
phytophagous insect and host phylogeny is rare on the tax-
onomic scale at which it has most often been examined,
namely within and among related insect genera. Even
groups involved in obligate pollination mutualisms show
much less correspondence with host phylogeny than previ-
ously assumed (Pellmyr 2003; Kawakita et al. 2004;
Machado et al. 2005). An early compilation (Mitter and Far-
rell 1991) examined 14 studies, in only one of which was
there unambiguous support for parallel phylogenesis. Here
we tabulate a subset of 18 of the many relevant studies
appearing since then, limited to papers in which the
authors themselves drew conclusions about parallel clado-
genesis (Table 18.3). In the great majority of these, there is
little evidence, from either cladogram concordance or dat-
ings, for parallel diversification. Our sample undoubtedly
underestimates the true prevalence of such negative evi-
dence, as we did not include the many papers in which par-
allel cladogenesis is implicitly ruled out at the start. One
exception to the rule is particularly instructive: a group of
psyllids showed significant phylogeny concordance with its
legume hosts, but molecular clock and fossil datings indi-
cate that host diversification was likely complete before the
group was colonized by these phytophages (Percy et al.
2004). Presumably, host shifts in these herbivores have been
governed by plant traits correlated with plant phylogeny; it
is less clear why colonization should start at the base of the
host phylogeny. In light of this finding, it seems especially
important that newly discovered instances of possible
cladogram match, for example, as reported for a group of
gracillariid moths that obligately pollinate their hosts
(Kawakita et al. 2004), be investigated for equivalence of
ages.
The few plausible cases for both cladogram match and
equivalence of ages include two genera of herb-feeding bee-
tles (leaf beetles on skullcap mints [Farrell and Mitter 1990];
longhorn beetles on milkweeds [Farrell and Mitter 1998;
Farrell 2001]). The vast assemblage of figs and their mutualist
wasp pollinators, the subject of many recent phylogenetic
studies (Silvieus et al., this volume), shows clear elements of
parallel diversification, although it now appears that host
specificity and parallel speciation are much less strict than
was formerly thought (Machado et al. 2005).
Datings based on fossils, molecular clocks, and biogeogra-
phy also continue to identify other patterns suggesting
long-continued, not necessarily coevolutionary interactions
(e.g., von Dohlen et al. 2002). One of the most elaborate
apparent historical interaction signatures involves Blephar-
ida alticine leaf beetles and related genera. Beetle phylogeny
shows only tenuous concordance with that of the chief
hosts, Bursera and relatives (Burseraceae/Anacardiaceae), but
much stronger match to a phenogram of leaf extract gas
chromatography profiles (compounds not specified)
(Becerra 1997). Shared geographic disjunction between the
New World and African tropics implies comparable overall
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 249

TABLE 18.3
Synopsis of 18 Recent Studies Testing for Parallel Insect-Plant Phylogenesis at Lower Taxonomic Levels
Insect Order and Overall Phylogeny Equivalent Ages
Family Insect Clade Host Clade(s) Correspondence Plausible? Plausible? Sources
Coleoptera: Tetraopes Asclepias (Apocynaceae) Yes, significant Yes Farrell 2001, Farrell
Cerambycidae cladogram similarity and Mitter 1998
Coleoptera: Ophraella Asteraceae No, cladograms do No, beetles younger Funk et al. 1995
Chrysomelidae not match than hosts
Coleoptera: Blepharida Burseraceae Maybe, depends on Yes Bercerra 1997, 2003
Chrysomelidae analysis
Coleoptera: Anthonomus Hampea (Malvaceae) No, cladograms do Not tested Jones 2001
Curculionidae grandis grp. not match
Hymenoptera: Euurina Salix (Salicaceae) No, cladograms do Not tested Nyman et al. 2000,
Tenthredinidae (Nematinae) not match Roininen et al. 2005
Hymenoptera: Major lineages Asteraceae, Lamiaceae, Fagaceae, No, cladograms not Maybe (based on fossils, Ronquist and
Cynipidae of cynipids Rosaceae, Papaveraceae significantly similar biogeography) Liljeblad 2001
Hymenoptera: Agaoninae Ficus (Moraceae) Yes,
a
but correspondence Yes Machado et al. 2005
Agaonidae not universal
Hymenoptera: Apocryptophagus Ficus (Moraceae) No, cladograms not Not tested Weiblen and
Agaonidae (nonpollinators) significantly similar Bush 2002
Diptera: Urophora Cardueae (Asteraceae) No, cladograms not No, flies younger Brändle et al. 2005
Tephritidae significantly similar than hosts
Lepidoptera: Epicephala Glochidion (Phyllanthaceae) Maybe, depends on type Not tested Kawakita et al. 2004
Gracillariidae of analysis
Lepidoptera: Phyllonorycter 30 families of angiosperms No, cladograms not No (individual moth/host Lopez-Vaamonde et al.
Gracillariidae significantly similar radiations tested) 2003, 2006

Lepidoptera: Lithinini Ferns, multiple families No, multiple shifts to No, moths younger Weintraub et al. 1995
Geometridae distantly related hosts than hosts
Hemiptera: Uroleucon Asteraceae No, multiple shifts to No, aphids much younger Moran et al. 1999
Aphididae distantly related hosts than hosts
Hemiptera: Arytaininae Fabaceae: Genisteae of Yes, significant cladogram No, psyllids much Percy et al. 2004
Psyllidae Macaronesia similarity younger than hosts
Hemiptera: Calophya, Schinus (Anacardiaceae) Maybe, depends on Not tested Burckhardt and
Psyllidae Tainarys group and analysis Basset 2000
Hemiptera: Tribes of Various monocots Little evidence for Maybe (ages uncertain) Wilson et al. 1994
Delphacidae delphacids cladogram match
Hemiptera: Nesosydne Hawaiian silverswords Maybe, depends on analysis Yes Roderick 1997
Delphacidae (Asteraceae: Heliantheae, (sampling incomplete)
3 genera)
Acari: Cecidophyopsis Ribes (Grossulariaceae) No, cladograms No, mites younger than hosts Fenton et al. 2000
Eriophyidae do not match
NOTE: See “Table References” for source information.
a
Machado et al. (2005) found fig and pollinator wasp phylogeny congruence to be nonsignificant and point out the paucity of evidence for cladogram matching of figs and their pollinating wasps at lower lev-
els, as well. However, it is evident that substantial overall codivergence has occurred (Rønsted et al. 2005), and widespread (but not universal) congruence at lower levels still seems plausible (see also Weiblen and
Bush 2002; Silvieus et al., this volume, and references therein).

ages (112 million years; but see Davis et al. 2002) for the
interacting clades, and molecular clocks point to similar,
younger ages for two associated beetle and plant subsets
marked by corresponding innovations in resin canal
defense and counterdefense (Becerra 2003). This case, an
exemplar of the broad syndrome of parallel origins of
resin/latex canal defenses and counteradaptations thereto
(Farrell et al. 1991), is perhaps the most detailed to date for
long-term insect-plant “arms race” sequences as envisioned
by Ehrlich and Raven (1964; but see Berenbaum 2001),
though evidence for the accelerated diversification expected
with each innovation is lacking.
We digress here to note that such putative escalations of
plant defense are underinvestigated and possibly rare. Aside
from resin/latex canals, the two most strongly stated
hypotheses involve evolutionary trends toward chemical
complexity in coumarins and other secondary compounds
in Apiaceae (reviewed in Berenbaum 2001) and in cardeno-
lides of milkweeds (Asclepias; reviewed in Farrell and Mitter
1998). Although the modern revolution in plant phylogeny
has underscored the conservatism of some major secondary
chemistry types (e.g., Rodman et al. 1998), phylogenetic
studies directed explicitly at the evolution of plant defense
are still few (but see Armbruster 1997; Wink 2003; Rudgers
et al. 2004). Agrawal and Fishbein (2006) mapped an array
of putative defense traits that included total cardenolides
(though not the hypothesized arms race aspects thereof)
onto a molecular phylogeny for 24 Asclepias species. Rather
than reflecting plant phylogeny, these traits appear to
define three distinct, convergently evolved defense syn-
dromes, each possibly optimal in the right circumstances.
This implicit optimality/equilibrium view of plant defense
is very different from the historically contingent view inher-
ent in the arms race hypothesis. Under the latter, we expect
some lineages to have acquired novel defenses that confer,
at least temporarily, a ubiquitous fitness advantage over rel-
atives lacking those innovations. The relative applicability
of these two views of defense evolution across the diversity
of plants and their defensive traits has yet to be determined.
Reinforcing the view that ancient host associations may
have left widespread, if not numerically dominant, traces
on contemporary assemblages is the increasing evidence for
broad-scale correspondence between the ages of currently
associated insect and plant groups, over time spans encom-
passing major evolutionary changes in the global flora. The
case for this long-standing postulate (see Zwölfer 1978)
is best developed for the beetle clade Phytophaga
(Chrysomeloidea  Curculionoidea, 135,000 species),
whose hosts span the chief lineages of seed plants (Farrell
1998; Marvaldi et al. 2002; Farrell and Sequeira 2004).
Recent phylogeny estimates show most of the basal phy-
tophagous lineages in both superfamilies to feed exclusively
on conifers or cycads, the most basal seed plants. The five
gymnosperm-associated clades, totaling about 220 species,
have apparently Gondwanan-relict distributions, and sev-
eral are known as Jurassic fossils from the same deposits as
are members of their present-day host groups. Within both
superfamilies, moreover, there are early splits between
monocot and (eu)dicot feeders, possibly established during
the early divergence between these two main lineages of
angiosperms (Farrell 1998). A similar pattern is evident, in
abbreviated form, in the Lepidoptera, first known from the
early Jurassic (Grimaldi and Engel 2005). Larvae of the most
basal lineage (Micropterigidae) inhabit riparian moss and
liverwort beds, apparently feeding on these and/or other
plant materials. Their habits match those of the inferred
common ancestor of Lepidoptera and their sister group Tri-
choptera (Kristensen 1997). Recent morphological and
molecular phylogenies (Kristensen 1984; Wiegmann et al.
2000, 2002) firmly establish that the most basal lineage of
the remaining Lepidoptera, which are otherwise mostly
restricted to advanced angiosperms, consists of two Aus-
tralasian species that feed inside cones of the conifer Arau-
caria. This association, which parallels basal gymnosperm
feeding (specifically within reproductive structures) in Phy-
tophaga (Farrell 1998), is quite plausibly viewed as predat-
ing the availability (or at least the dominance) of
angiosperm hosts. It is, however, the only obvious such
relictual habit in Lepidoptera. While other primitive line-
ages also have apparent Gondwanan-relict distributions,
suggesting mid-Mesozoic ages, they feed on advanced
(mainly eurosid) dicots, and their phylogenetic relation-
ships correspond not at all to those of their chief host-plant
taxa (Powell et al. 1998). Host use appears to evolve consid-
erably faster in Lepidoptera than in Phytophaga, thus traces
of earlier feeding habits are probably more quickly obliter-
ated.
Ancient host associations in other phytophagous lineages
that date to the early Mesozoic and before, less well charac-
terized, await clarification by modern studies. Recent
progress on phylogeny of sawflies (basal hymenopterans)
(e.g., Schulmeister 2003), modern families of which date to
the early Jurassic or even Triassic, should permit elucidation
of the degree to which the multiple conifer feeding lineages,
totaling several hundred species, represent ancestral habits.
We can hope for similar enlightenment about the Aphido-
morpha (aphids and relatives), probably Triassic in age, in
which the phylogenetic positions of the few extant gym-
nosperm-associated lineages are still obscure (Heie 1996;
Normark 2000; von Dohlen and Moran 2000; Ortiz-Rivas et
al. 2004). Moreover, documentation of such deep-level
relictual host associations may prompt reexamination of
some younger groups for which synchronous diversification
with hosts seems at first glance implausible. Thus, analysis
of the more than 1000 species of cynipid gall wasps detected
no significant overall phylogeny match with their host-
plant families, mostly woody rosids and herbaceous asterids
(Ronquist and Liljeblad 2001). However, recently discovered
taxa have raised the possibility that the ancestral gall wasps,
like one basal extant lineage, fed on Papaveraceae, a mem-
ber of the most basal eudicot lineage, Ranunculales (but see
Nylander 2004; Nylander et al. 2004). Fossils date the gall
252 CO- AND MACROEVOLUTIONARY RADIATION

wasps to at least the late Cretaceous, thus it is possible that
this habit has been retained since before the rise to promi-
nence of the host groups commonly used today (Ronquist
and Liljeblad 2001). A similar history is possible for some
genera of leaf-mining agromyzid flies (Spencer 1990).
Aphids, agromyzids, and other groups may participate in
another broad historical pattern that is receiving increased
attention. Insect groups whose chief diversity is associated
with modern (especially poaceous or euasterid) herbaceous
plants in temperate regions might well have diversified in
parallel with the great Tertiary expansion of open habitats
and herbaceous vegetation, driven by global cooling, dry-
ing, and latitudinal climate stratification trends (Behrens-
meyer et al. 1992; Graham 1999). This postulate, in need of
rigorous test, shares some elements with escape-and-radia-
tion coevolution, including the ascription of diversification
to ecological opportunity, and the distribution of insect lin-
eages across plants to long-term historical trends. The
hypothesis predicts that phylogenies of these herbivores
should exhibit trends toward use of successively younger
host groups (and/or perhaps from trees to herbs), and sub-
clade ages should roughly match those of their hosts and/or
biomes (Dietrich 1999; von Dohlen and Moran 2000; von
Dohlen et al. 2006). One among many candidate lineages is
the so-called trifine Noctuidae (Noctuidae sensu stricto;
more than 11,000 species). Trifines have a markedly higher
ratio of temperate-to-tropical species than any other large
family of Macrolepidoptera and, unlike those families, are
mostly herb feeders instead of tree feeders. Recent phyloge-
nies confirm that the trifine groups most closely adapted to
open, boreal habitats, which are often ground-dwelling
“cutworms” as larvae, are among the most derived (Hol-
loway and Nielsen 1998; Mitchell et al. 2006).
Diversification of Phytophagous Insects
The extraordinary species richness of plant-feeding insects
is a salient feature of terrestrial biodiversity (Strong et al.
1984). It is therefore not surprising that insect-plant interac-
tions have been a prominent model in the modern revival
of interest in diversification (Wood 1993; Schluter 2000;
Coyne and Orr 2004). Full understanding of the diversifica-
tion of phytophagous insects will require both detailed
analysis of speciation (and extinction) mechanisms, and
comparative study of broad diversification patterns. These
enterprises are of course intertwined, and phylogeny is rele-
vant to both. Our review, however, will focus mainly on the
comparative aspect.
A fundamental question to be asked is whether the appar-
ent exceptional diversity of phytophagous insects is actually
the result of consistent clade selection (Williams 1992),
rather than a coincidental impression created by a few
groups whose hyperdiversity could reflect some other cause.
Sister-group comparisons between independently originat-
ing phytophagous insect clades and their nonphytophagous
sister groups, which control for clade age and other traits
possibly influencing diversification rate, show that phy-
tophages have consistently elevated diversities (Mitter et al.
1988). This conclusion is at least consistent with the results
of an analysis screening for significant variation in diversifi-
cation rate across the insect orders (Mayhew 2002). It
should be noted that the finding rests at present on only a
small fraction of the potential evidence, as the phylogenetic
positions of most originations of insect phytophagy are
only now beginning to be resolved. Thus, further test of this
hypothesis is desirable.
Why should phytophagous insects have elevated diver-
sification rates? Several broad hypotheses have been
advanced. One possibility is adaptive radiation (Simpson
1953), redefined loosely by Schluter (2000) as “evolution of
ecological diversity in a rapidly multiplying lineage” (p. 1).
Vascular plants might constitute an “adaptive zone” provid-
ing an extraordinary diversity of underutilized, distinct
resources on which insect specialization is possible. A con-
tributing factor might be that more niches supporting a sus-
tainable population size are available at the primary con-
sumer level than to higher levels or to decomposers, no
matter how those niches are filled. Diversification could be
accelerated still further if plant diversity continually
increases due to coevolution sensu Ehrlich and Raven
(1964). In a contrasting, though complementary, hypothe-
sis (Price 1980), phytophage diversity reflects instead a
broad propensity of the “parasitic lifestyle” for rapid diversi-
fication, due in part to the ease with which populations of
small, specialized consumers can be fragmented by the
patchy distribution of hosts.
Some progress has been made toward sorting out these
alternatives. The finding that insect groups parasitic on ani-
mals are, if anything, less diverse than their nonparasitic sis-
ter groups (Wiegmann et al. 1993) casts strong doubt on the
primacy of the parasitic lifestyle hypothesis. The leading
hypothesis, adaptive radiation, makes two chief predictions.
One of these, the subject of a vigorous area of research (Via
2001; Berlocher and Feder 2002; Rundle and Nosil 2005;
other chapters this volume), is that shifts to new plant
resources should be a major contributor to the origin of new
species. Earlier, we estimated that about 50% of speciation
events in phytophagous insects involve shifts to a different
host-plant species. This is an underestimate of the impor-
tance of plant resource diversity to speciation, because
niche shifts within the same host-plant species (e.g., to dif-
ferent host organs or tissues) and changes in host range
(with retention of at least one previous host) are not
included. Comparative data, then, are at least consistent
with a major role for host-related divergence in phytophage
diversification. It should be noted that ecological differ-
ences between sister species can arise by multiple mecha-
nisms before, during, or after speciation (Futuyma 1989;
Schluter 2000). Even if host-related differences were inci-
dental to speciation, however, a broad form of the adaptive
zone or radiation hypothesis could be said to hold, if those
differences produced higher net diversification rate by
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 253

forestalling extinction due to competition for resources or
enemy-free space. As the foregoing suggests, hypotheses
attributing diversification to ecological differentiation have
rarely been explicit about which of the many possible
mechanisms are involved (reviewed in Allmon 1992).
Ongoing ecological study of the importance of competition
and natural enemies to phytophage fitness and host use
(e.g., Denno et al. 1995; Murphy 2004) should help to dis-
tinguish among plausible candidate mechanisms.
A second prediction of the adaptive radiation hypothesis
is that the diversification rate of a phytophagous lineage
should be correlated with the number of plant resource
niches available to it. The strongest evidence on this ques-
tion so far comes from studies of the beetle clade Phy-
tophaga. In each of 10 contrasts identified so far (Farrell
1998; Farrell et al. 2001), beetle groups feeding on conifers
or other gymnosperms were less diverse than their
angiosperm-feeding sister groups. To these can be added the
contrast in Lepidoptera between the basal conifer-feeding
lineage Agathiphagidae (two species) and its almost entirely
angiosperm-feeding sister group Heterobathmiidae  Glos-
sata (160,000 spp.; Wiegmann et al. 2000). Although
exceptions will undoubtedly be found (e.g., probably lach-
nine aphids [Normark 2000]; xyelid sawflies [Blank 2002]),
elevated diversity of angiosperm feeders seems likely to
remain one of the strongest diversification effects known
(Coyne and Orr 2004) as the numerous additional contrasts
are examined. Ascription of this trend to the much greater
taxonomic and chemical diversity of flowering plants,
rather than some unique historical circumstance or the
global biomass difference between angiosperms and gym-
nosperms, gains credibility from the great variation in ages
and geographic distributions among the contrasted lineage
pairs, and the fact that some represent secondary return to
gymnosperms (Farrell et al. 2001). It will now be of great
interest to determine whether association of enhanced
insect diversification with more diverse host groups holds
on smaller plant-taxonomic scales as well.
Ehrlich and Raven (1964) speculated that diversification
of the angiosperms was promoted by their novel and diverse
secondary chemistry, which improved protection from her-
bivores. Correspondingly greater diversity in angiosperm-
feeding insects than in related relict gymnosperm feeders is
at least consistent with their hypothesis. Broad-scale escape
and radiation coevolution is also lent credence by recent
evidence that adaptations to and interaction with insects
(and other organisms) have marked influence on plant
diversification rates. Plant clades bearing latex or resin
canals, one of the most elaborate plant defense syndromes
known, were shown to be consistently more diverse than
sister groups lacking such canals (Farrell et al. 1991). More
recently, several types of innovations in reproductive struc-
tures, affecting pollinator fidelity or fruit dispersal, have
also been shown to be associated with more rapid plant
diversification (Sargent 2004; Bolmgren and Erikkson 2005;
reviewed in Coyne and Orr 2004). Thus, mounting evidence
supports a central tenet of the new synthesis, implicit in
escape and radiation coevolution, namely that adaptations to
biotic interactions have major influence on diversification.
While substantial progress has been made in establishing
phytophage diversification patterns at the broadest scale,
countless questions remain, particularly at shorter evolu-
tionary time scales. There is almost no unambiguous evi-
dence on whether repeated counteradaptations to plant
defenses have accelerated insect diversification, as predicted
under escape-and-radiation coevolution (but see Farrell et
al. [2001] regarding mutualism with ambrosia fungi in bark
beetles; parallel examples of fungal mutualism in cecidomyiid
gall midges discussed by Bisset and Borkent [1988] and
Gagné [1989] await further phylogenetic study). Numerous
other causes have been postulated for differential diversifi-
cation of phytophages, including, among others, species
richness, secondary chemical diversity, growth form, and
geographic distribution of the host group (e.g., Price 1980;
Strong et al. 1984; Lewinsohn et al. 2005); mode of feeding,
including plant tissue attacked, internal versus external
feeding, and gall-making (and advanced forms thereof)
(Ronquist and Liljeblad 2001); trenching and other forms of
herbivore “offense” (Karban and Agrawal 2002); degree of
food plant specialization; host-shift frequency; and various
traits (often host-use-related) rendering phytophages less
susceptible to natural enemies (Singer and Stireman 2005).
Indeed, just about any trait that might be conserved on
phylogenies becomes a plausible candidate. Ideally, one
would like to determine the relative importance of and
interactions among these factors, and compare them to
other types of influence on diversification. In the Lepi-
doptera, for example, the most pervasive differential influ-
ence on diversification may prove to be the repeated evolu-
tion of ultrasound detectors allowing adults to avoid bat
predation (e.g., Yack and Fullard 2000), rather than any
“bottom-up” factor having to do with host plants.
Progress on testing such hypotheses has been quite lim-
ited so far, probably for several reasons. First, although phy-
logenies are accumulating rapidly, the detailed phylogenetic
resolution needed to detect correlates of diversification rates
is still lacking within most families of phytophagous
insects; in some cases, even species diversities are not yet
well characterized. Second, we are only beginning to under-
stand the phylogenetic distributions of most candidate
traits. Many of these appear to be much more evolutionarily
labile than the relatively conserved features reviewed earlier.
Rapid trait evolution can frustrate estimation of ancestral
states, particularly when life-history information is incom-
plete, making reliable sister-group comparisons hard to
identify. For example, our scan of published studies uncov-
ered essentially no unambiguous contrasts between lineages
with broader versus narrower species host ranges, though
sister clades often differed in average host range. Moreover,
the groups characterized by labile traits, when identifiable,
will often be so recent that dissecting deterministic from
stochastic influences on diversification would require a
254 CO- AND MACROEVOLUTIONARY RADIATION

large number of comparisons. Sister-group comparisons
remain the most robust and straightforward method for
detecting traits correlated with diversification rate (Vamosi
and Vamosi 2005). But, unless traits that vary mostly at
lower taxonomic levels are to be dismissed as unlikely to
influence diversification rates, additional approaches will be
needed (Ree 2005).
Fortunately, there is now a diverse, rapidly growing litera-
ture on diversification rate analysis, a full survey of which is
beyond the scope of this chapter. Any of several approaches
might prove useful for testing the association of relatively
labile traits with diversification rates, depending on the
nature of the data. If the chief difficulty is that inferred trait
origins do not clearly define sister-group comparisons, one
might identify comparisons a priori, then score sister groups
simultaneously for diversity and some appropriate measure
of frequency of the predictor trait. To select potentially
informative comparisons, one might employ one of the var-
ious model-based methods proposed for identifying signifi-
cant shifts in rates of diversification (Sanderson and
Donoghue 1994; Magallón and Sanderson 2001; Moore et
al. 2004); possible drawbacks include the need for well-
resolved phylogenies and high variance of trait frequency
estimates in extremely asymmetrical comparisons. For
quantitative predictor variables (e.g., average host range) a
variant of the independent contrasts method is available
(Isaac et al. 2003). When lack of deeper-level phylogeny res-
olution limits identification of sister groups, one might
make independent comparisons among groups of different
ages, using estimates of absolute or relative diversification
rates (Purvis 1996; Bokma 2003; application in Nyman et al.
2006). For relatively recent radiations, average time between
speciation events may be a more sensitive estimator of
diversification rate than species numbers per se (Ree 2005).
Clock-based temporal analyses of diversification can in
principle also detect changes in diversification rate over
time (e.g., Nee et al. 1992, 1996; Paradis 1997), allowing test
of such refinements of the adaptive zone hypothesis as the
postulated slowing of diversification as niches are filled
(Simpson 1953; Schluter 2000). Recently, this and other
approaches have been used to identify periods of acceler-
ated insect diversification and correlate these with potential
causes such as radiation of particular plant clades, or partic-
ular biogeographic events (e.g., McKenna and Farrell 2006;
Moreau et al. 2006; but see Brady et al. 2006).
While phytophage diversification rate variation at lower
levels is a daunting problem, even the analysis of relatively
conserved traits remains underdeveloped. To underscore
this point, we end with a summary of progress on one
much-discussed issue that bears on the puzzle of phy-
tophagous insect diversity, namely, the macroevolutionary
consequences of internal versus external feeding. Both habits
are widespread, although their frequencies differ markedly
across insect phylogeny. Most hemimetabolous insect herbi-
vores, in orders such as Orthoptera, Phasmida, Hemiptera,
and Thysanoptera, are free-living external feeders, though
some (e.g., thrips) may hide in flowers or other plant struc-
tures; the chief exceptions are gall-formers, which have
evolved repeatedly in the piercing/sucking lineages. In
contrast, larvae of a large fraction of phytophagous
Holometabola, including the basal members of nearly all
the major lineages, actively bore or mine inside living
plants. External phytophagy has arisen infrequently in most
holometabolous orders, or not at all (e.g., higher Diptera),
while return to endophagy has occurred somewhat more
often. Overall, the opposing traits seem sufficiently con-
served, yet also sufficiently labile, to permit replicated sister-
group comparisons.
Opposing predictions have been made about diversifica-
tion under these contrasting feeding modes, drawing on
broader theories about ecological specialization (reviewed in
Wiegmann et al. 1993; Yang and Mitter 1994). Although
analyses controlled for phylogeny are needed (Nyman et al.
2006), internal feeders appear to be more host specific than
external feeders (e.g., Gaston et al. 1992). Greater specializa-
tion, as argued earlier, could promote speciation by increas-
ing the strength of population subdivision and diversifying
selection (e.g., Miller and Crespi 2003). Internal feeding
could also be viewed as an adaptive zone providing escape
from pathogens and some parasites, and desiccation or
other physical stresses (Connor and Taverner 1997). Con-
versely (Powell et al. 1998; Nyman et al. 2006), one could
predict that external feeding, by providing release from con-
straints on body size, voltinism, and leaf excision, might
typically increase individual and (thereby) clade fitness.
Moreover, by lowering the barriers to colonization of alter-
native hosts and habitats, exophagy might open more
opportunities for speciation.
Sister-group contrasts between internal and external feed-
ers are potentially numerous. For example, there is strong
evidence for several to many independent transitions
between internal and external larval feeding within Lepi-
doptera (Powell et al. 1998), Coleoptera-Phytophaga (Mar-
valdi et al. 2002; Farrell and Sequiera 2004), and basal
Hymenoptera (sawflies), and between galling and free-living
habits within Aphidoidea (von Dohlen and Moran 2000),
Coccoidea (Cook and Gullan 2004), Psylloidea (Burckhardt
2005), and Thysanoptera (Morris et al. 1999). Surprisingly,
however, from our literature survey we are able to extract at
most eight unambiguous comparisons (Table 18.4). The
only phylogenetic analysis study directed specifically at this
question is that of Nyman et al. (2006); others are clearly
needed.
Disregarding the one tie, five of the seven sister-group
comparisons we identified show the external-feeding line-
age to be more diverse than its internal-feeding closest rela-
tives. Nyman et al. (2006), in a nonoverlapping set of com-
parisons within the sawfly subfamily Nematinae
(Tenthredinidae), found external feeders to be more diverse
in 10 of 13 sister-group contrasts. Taken together, these
compilations yield a result just significant by a two-tailed
sign test (external feeders more diverse in 15 of 20 pairs,
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 255

P  0.042), corroborating the trend in an earlier, more lim-
ited compilation by Connor and Taverner (1997).
Although progress is evident, continued study of this
question is desirable. The statistical significance of the
observed trend is still marginal; several of the comparisons
in Table 18.4 are based on provisional phylogenies, and in
several the diversity differences are small; it will also be of
much interest to separately test the effects of different cate-
gories of internal feeding (e.g., gallers versus miners), and of
gains versus losses of external feeding. At the least, however,
the current evidence appears to firmly reject the hypothesis
of consistently faster diversification by internal feeders. The
result parallels previous rejection of the hypothesis of
higher diversification in animal-parasitic than free-living
insects due to their exceptionally specialized lifestyles
(Wiegmann et al. 1993). Together, these observations sug-
gest that, even if phytophages are more ecologically special-
ized in some sense that other insects, specialization per se is
an unlikely explanation for their exceptional diversity.
Rather, the evidence increasingly points to the importance
of the sheer diversity of niches available to insects feeding
on plants, particularly flowering plants.
Synopsis and Conclusions
In this chapter we have attempted to compile and synthe-
size the recent literature (mainly since 1993) treating
aspects of the phylogenesis of associated insects and
plants. We have focused on phylogenies at the among-
species level and higher, mostly for insects, and on their
bearing on three general questions posed implicitly by
Ehrlich and Raven’s hypothesis of coevolution. These are
(1) the degree to which the various traits governing use of
host plants are conserved during phylogenesis; (2) the
degree to which contemporary associations show evi-
dence, from phylogenies and other sources, of long-con-
tinued interactions between particular insect and plant
lineages; and (3), the degree to which evolution in traits
affecting their interactions affects the diversification rates
of interacting insect and plant lineages. Our main conclu-
sions are as follows:
1. Ubiquitous conservation of plant higher taxon use
during insect phylogenesis is confirmed and quanti-
fied in a compilation of 93 phylogenies of mostly
256 CO- AND MACROEVOLUTIONARY RADIATION
TABLE
18.4
Sister Group Diversity Comparisons Between Endo- and Exophytophage Lineages
Higher Taxon Internally Feeding Clade Diversity Externally Feeding Clade Diversity Sources
Coleoptera: Bruchinae  Sagriinae 3,300 Chrysomelinae  Criocerinae 10,000 Farrell and
Chrysomelidae  others, minus secondary Sequeira 2004
internal feeders
Hymenoptera Cephidae  Siricidae 280 Pamphilidae  350 Brown 1989,
 Anaxyelidae  Megalodontesidae Heitland 2002,
Xiphydriidae, with Schulmeister
parasitic subclade 2003
Vespina excluded
Hymenoptera Blasticotomidae 9 Remaining Tenthredinoidea 7,000 Nyman et al.
2006, Schul-
meister 2003
Hymenoptera: Xyelinae 71 Macroxyelinae 11 Blank 2002,
Xyelidae Schulmeister
2003
Lepidoptera Cossoidea 1,873 Zygaenoidea 2,115 Powell et al.
1998
Lepidoptera Obtectomera minus 22,0000 Macrolepidoptera 87,000 Powell et al.
Macrolepidoptera 1998
(part or all)
Lepidoptera: Lamprolophus  56 Epicroesa  Philocoristis 6 Hsu and Powell
Heliodinidae 9 genera 2004
Thysanoptera: Kladothrips 22 Rhopalothripoides 22 Crespi et al. 2004,
Phlaeothripidae ( 5 possibly related Morris
genera) et al. 2002
NOTE: Compilation excludes nematine tenthredinid sawflies, studied by Nyman et al. (2006). See “Table References” for source information.

oligophagous insect groups. The median frequency of
shift to a different plant family is estimated to be
about 0.03 to 0.08 per speciation event. Important
initial insights have been gained on the reasons for
this conservatism.
2. There are many hypotheses to explain among-clade
variation in the frequency of among-plant-family
shift, but few quantitative tests. The strongest evi-
dence to date is for more frequent host shifting in tree
feeders than in herb feeders among butterflies, and
among oligophages within lineages that contain one
or more polyphagous species than in lineages that do
not (across 95 insect phylogenies). Recent case studies
suggest that reliance on plant-derived compounds for
insect defense poses less of a barrier to larval host shift
than was formerly thought.
3. In contrast to the prevailing broad-scale host conser-
vatism, shifts to a different host species have accom-
panied about 50% of 145 phytophage speciation
events tabulated, consistent with a substantial but not
universal role for host shifts in phytophage specia-
tion. There is a suggestive but not statistically signifi-
cant tendency for greater host differentiation between
sympatric than allopatric species pairs.
4. The as yet limited evidence on phylogenetic patterns
of host-plant range provides no support for direction-
ality or other strong constraints but suggests an
important distinction between ephemeral, phyloge-
netically random fluctuation, and larger-scale trends
interpretable using experimental approaches com-
bined with phylogenetic “comparative methods.”
5. It is now clear that with very few exceptions, the host-
use variation within and among phytophagous insect
genera, in contrast to that in some vertically transmit-
ted parasites and symbionts, reflects colonization of
already-diversified hosts rather than any form of strict
parallel phylogenesis. At the same time, however, evi-
dence is increasing that associations established in the
distant past, especially the Mesozoic, have left wide-
spread if not numerically dominant marks on con-
temporary insect-plant assemblages; the full range of
such historical “signatures” is only beginning to be
explored.
6. Because phylogenetic studies directed specifically at
plant defense evolution are still few, we do not yet
know whether that evolution is characterized more by
sequential coevolutionary “escalations,” or by stably
coexisting syndromes reflecting optimal adaptations
for differing environments.
7. Replicated sister-group comparisons have estab-
lished elevated diversification rates for phy-
tophagous over nonphytophagous insects and for
angiosperm over nonangiosperm feeders among
phytophages, both at least consistent with diffuse
insect-plant coevolution sensu Ehrlich and Raven
(1964). Recent studies on plant diversification rates
demonstrate a role for interaction with insects and
other animals, likewise consonant with that the-
ory, though most examples do not involve defense.
Evidence on most phytophage diversification
hypotheses (including “offense” innovations),
however, has been slow to accumulate, and diversi-
fication studies at finer taxonomic scales, mostly
lacking, may face methodological obstacles. A
progress report on sister-group comparisons of
internal versus external feeders effectively negates
the hypothesis of faster radiation by endophages,
thought to be more specialized, and strongly sug-
gests the opposite trend.
Given the range of questions mapped out, the tools avail-
able, and the cornucopia of phylogenetic studies now ongo-
ing in nearly all major herbivorous insect groups and their
host plants, we can look forward to spectacular near-future
advances in understanding of the evolution of insect-plant
interactions, with increasing integration between phyloge-
netic and other perspectives.
Author’s Note: For online supplementary tables and figures, go
to www.chemlife.umd.edu/entm/mitterlab. These include the
following:
.
Item S1: Database of insect/plan phylogeny studies.
FileMaker, Access formats.
.
Item S2: Table compiling host-shift frequencies on phy-
logenies. Excel format.
.
Item S3: Figure showing metaphylogeny of taxa
included in table S2 for comparative analysis of host-
shift frequency versus host range. PDF format.
.
Item S4: Table compiling host and distribution differ-
ences for speciation events. Excel format.
Acknowledgments
We are grateful to Anurag Agrawal, Brian Farrell, Kathleen
Pryer, Stephan Blank, and their coauthors for sharing
unpublished material, to the editor and reviewers for help-
ful comments on the manuscript, and to the National Sci-
ence Foundation and U.S. Department of Agriculture for
financial support.
Table References
Becerra, J. X. 1997. Insects on plants: macroevolutionary chemical
trends in host use. Science 276: 253–256.
Becerra, J. X. 2003. Synchronous coadaptation in an ancient case of
herbivory. Proc. Natl. Acad. Sci. USA 100: 12804–12807.
Blank, S. M. 2002. Biosystematics of the extant Xyelidae with partic-
ular emphasis on the Old World taxa (Insecta: Hymenoptera).
Dissertation, Freie Universität Berlin.
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 257

Brändle, M., S. Knoll, S. Eber, J. Stadler, and R. Brandl. 2005. Flies on
thistles: support for synchronous speciation? Biol. J. Linn. Soc.
84: 775–783.
Brown, W. L. 1989. Hymenoptera, pp. 652–680. In S. P. Parker (ed.),
Synopsis and classification of living organisms. McGraw Hill,
New York.
Burckhardt, D., and Y. Basset. 2000. The jumping plant-lice
(Hemiptera, Psylloidea) associated with Schinus (Anacardiaceae):
systematics, biogeography and host plant relationships. J. Nat.
Hist. 34: 57–155.
Crespi, B. J., and C. P. Sandoval. 2000. Phylogenetic evidence for the
evolution of ecological specialization in Timema walking-sticks. J.
Evol. Biol. 13: 249–262.
Crespi, B. J., D. C. Morris, and L. A. Mound. 2004. Evolution of eco-
logical and behavioral diversity: Australian Acacia thrips as model
organisms. CSIRO, Canberra, Australia.
Dobler, S., P. Mardulyn, J.M. Pasteels, and M. Rowell-Rahier. 1996.
Host-plant switches and the evolution of chemical defense and life
history in the leaf beetle genus Oreina. Evolution 50: 2373–2386.
Farrell, B. D. 2001. Evolutionary assembly of the milkweed fauna:
cytochrome oxidase I and the age of Tetraopes beetles. Mol. Phylo-
genet. Evol. 18: 467–478.
Farrell, B. D., and C. Mitter. 1998. The timing of insect/plant diversi-
fication: might Tetraopes (Coleoptera: Cerambycidae) and Ascle-
pias (Asclepiadaceae) have co-evolved? Biol. J. Linn. Soc. 63:
553–577.
Farrell, B. D., and A. S. Sequeira. 2004. Evolutionary rates in the
adaptive radiation of beetles on plants. Evolution 58: 1984–
2001.
Fenton, B., A. N. E. Birch, G. Malloch, P. G. Lanham, and R. M. Bren-
nan. 2000. Gall mite molecular phylogeny and its relationship to
the evolution of plant host specificity. Exp. Appl. Acarol. 24:
831–861.
Funk, D., D. J. Futuyma, G. Orti, and A. Meyer. 1995. A history of
host associations and evolutionary diversification for Ophraella
(Coleoptera: Chrysomelidae): new evidence from mitochondrial
DNA. Evolution 49: 1008–1017.
Heitland, W. 2002. U. Ord. Symphyta. Pflanzenwespen, sawflies.
www.faunistik.net/DETINVERT/HYMENOPTERA/symphyta.html.
Hsu, Y.-F., and J. A. Powell. 2004. Phylogenetic relationships within
Heliodinidae and systematics of moths formerly assigned to
Heliodines Stanton. University of California Publications in Ento-
mology, Vol. 24.
Janz, N., K. Nyblom, and S. Nylin. 2001. Evolutionary dynamics of
host-plant specialization: a case study of the tribe Nymphalini.
Evolution 55: 783–796.
Jones, R. W. 2001. Evolution of the host plant associations of the
Anthonomus grandis species group (Coleoptera: Curculionidae):
phylogenetic tests of various hypotheses. Ann. Entomol. Soc. Am.
94: 51–58.
Kawakita, A., A. Takimura, T. Terachi, T. Sota, and M. Kato. 2004.
Cospeciation analysis of an obligate pollination mutualism: have
Glochidion trees (Euphorbiaceae) and pollinating Epicephala
moths (Gracillariidae) diversified in parallel? Evolution 58:
2201–2214.
Kelley, S. T., and B. D. Farrell. 1998. Is specialization a dead end? The
phylogeny of host use in Dendroctonus bark beetles (Scolytidae).
Evolution 52: 1731–1743.
Lopez-Vaamonde, C., H. C. J. Godfray, and J. M. Cook. 2003. Evolu-
tionary dynamics of host-plant use in a genus of leaf-mining
moths. Evolution 57: 1804–1821.
Lopez-Vaamonde, C., N. Wikström, C. Labandeira, H.C. J. Godfray,
S. J. Goodman, and J. M. Cook. 2006. Fossil-calibrated molecular
phylogenies reveal that leaf-mining moths radiated millions of
years after their host plants. J. Evol. Biol. 19: 1314–1326.
Machado, C. A., N. Robbins, M. T. P. Gilbert, and E. A. Herre. 2005.
Critical review of host specificity and its coevolutionary implica-
tions in the fig/fig-wasp mutualism. Proc. Natl. Acad. Sci. USA
102: 6558–6565.
Moran, N. A., M. E. Kaplan, M. J. Gelsey, T. G. Murphy, and E.A.
Scholes. 1999. Phylogenetics and evolution of the aphid genus
Uroleucon based on mitochondrial and nuclear DNA sequences.
Syst. Entomol. 24: 85–93.
Morris, D. C., M. P. Schwarz, S. J. B. Cooper, and L.A. Mound. 2002.
Phylogenetics of Australian Acacia thrips: the evolution of behav-
iour and ecology. Mol. Phylogenet. Evol. 25: 278–292.
Morse, G. E., and B. D. Farrell. 2005. Ecological and evolutionary
diversification of the seed beetle genus Stator (Coleoptera:
Chrysomelidae: Bruchinae). Evolution 59: 1315–1333.
Nyman, T., A. Widmer, and H. Roininen. 2000. Evolution of gall
morphology and host-plant relationships in willow-feeding
sawflies (Hymenoptera: Tenthredinidae). Evolution 54: 526–533.
Nyman, T., B. D. Farrell, A. G. Zinovjev, and V. Vikberg. 2006. Larval
habits, host-plant associations, and speciation in nematine sawflies
(Hymenoptera: Tenthredinidae). Evolution 60: 1622–1637.
Percy, D. M., R. D. M. Page, and Q. C. B. Cronk. 2004. Plant-insect
interactions: double-dating associated insect and plant lineages
reveals asynchronous radiations. Syst. Biol. 53: 120–127.
Powell, J. A., C. M. Mitter, and B. Farrell. 1998. Evolution of larval
feeding habits in Lepidoptera, pp. 403–422. In N. P. Kristensen
(ed.), Handbook of zoology, Lepidoptera. Vol. 1: Systematics and
evolution. W. de Gruyter, Berlin.
Roderick, G. K. 1997. Herbivorous insects and the Hawaiian silver-
sword alliance: co-evolution or co-speciation? Pacific Sci. 51:
440–449.
Roininen, H., T. Nyman, and A. Zinovjev. 2005. Biology, ecology,
and evolution of gall-inducing sawflies (Hymenoptera: Tenthre-
dinidae and Xyelidae), pp. 467–494. In A. Raman, C. W. Schaefer,
and T. M. Withers (eds.), Biology, ecology, and evolution of gall-
inducing arthropods. Science Publishers, Enfield, NH.
Ronquist, F., and J. Liljeblad. 2001. Evolution of the gall wasp-host
plant association. Evolution 55: 2503–2522.
Rønsted, N., G. D. Weiblen, J. M. Cook, N. Salamin, C. A. Machado,
and V. Savolainen. 2005. 60 million years of co-divergence in the
fig-wasp symbiosis. Proc. R. Soc. Lond. B 272: 2593–2599.
Rubinoff, D., and F.A.H. Sperling. 2002. Evolution of ecological
traits and wing morphology in Hemileuca (Saturniidae) based on a
two-gene phylogeny. Mol. Phylogenet. Evol. 25: 70–86.
Schulmeister, S. 2003. Simultaneous analysis of basal Hymenoptera
(Insecta): introducing robust-choice sensitivity analysis. Biol. J.
Linn Soc. 79: 245–275.
Wahlberg, N. 2001. The phylogenetics and biochemistry of host-
plant specialization in melitaeine butterflies (Lepidoptera:
Nymphalidae). Evolution 55: 522–537.
Weiblen, G. D., and G. L. Bush. 2002. Speciation in fig pollinators
and parasites. Mol. Ecol. 11: 1573–1578.
Weingartner, E., N. Wahlberg, and S. Nylin. 2006. Dynamics of host
plant use and species diversity: a phylogenetic investigation in
Polygonia butterflies (Nymphalidae). J. Evol. Biol. 19: 483–491.
Weintraub, J. D., J. H. Lawton, and M. J. Scoble. 1995. Lithinine
moths on ferns: a phylogenetic study of insect-plant interactions.
Biol. J. Linn. Soc. 55: 239–250.
258 CO- AND MACROEVOLUTIONARY RADIATION

Wilson, S., C. Mitter, R. F. Denno, and M. R. Wilson. 1994. Evolu-
tionary patterns of host plant use by delphacid planthoppers and
their relatives, pp. 7–113. In R. F. Denno and J. Prefect (eds.), The
ecology and management of planthoppers. Chapman and Hall,
New York.
Yotoko, K. S. C., P. I. Prado, C. A. M. Russo, and V. N. Solferini. 2005.
Testing the trend towards specialization in herbivore-host plant
associations using a molecular phylogeny of Tomoplagia (Diptera:
Tephritidae). Mol. Phylogenet. Evol. 35: 701–711.
References Cited
Agrawal, A. A., and M. Fishbein. 2006. Plant defense syndromes.
Ecology 87: S132–S149.
APGII. 2003. An update of the angiosperm phylogeny group classifi-
cation for the orders and families of flowering plants: APG II. Bot.
J. Linn. Soc. 141: 399–436.
Allmon, W. D. 1992. A causal analysis of stages in allopatric specia-
tion, pp. 219–257. In D. Futuyma and J. Antonovics (eds.), Oxford
surveys in evolutionary biology, vol. 8. Oxford University Press,
Oxford.
Armbruster, W. S. 1997. Exaptations link the evolution of plant-her-
bivore and plant-pollinator interactions: a phylogenetic inquiry.
Ecology 78: 1661–1674.
Avise, J.C. 2000. Phylogeography: the history and formation of
species. Harvard University Press, Cambridge, MA.
Barraclough, T. G., and A. P. Vogler. 2000. Detecting the geographical
pattern of speciation from species-level phylogenies. Am. Nat.
155: 419–434.
Beccaloni, G. W., and F. B. Symons. 2000. Variation of butterfly diet
breadth in relation to host-plant predictability: results from two
faunas. Oikos 90: 50–66.
Becerra, J. X. 1997. Insects on plants: macroevolutionary chemical
trends in host use. Science 276: 253–256.
Becerra, J. X. 2003. Synchronous coadaptation in an ancient case of
herbivory. Proc. Natl. Acad. Sci. USA 100: 12804–12807.
Behrensmeyer, A. K., J. D. Damuth, W. A. DiMichele, R. Potts, H. D.
Sues, and S. L. Wing (eds.). 1992. Terrestrial ecosystems through
time: evolutionary paleoecology of terrestrial plants and animals.
University of Chicago Press, Chicago.
Benson, W. W., K. S. Brown, and L. E. Gilbert. 1975. Coevolution of
plants and herbivores: passion flower butterflies. Evolution 29:
659–680.
Berenbaum, M. R. 1983. Coumarins and caterpillars: a case for
coevolution. Evolution 37: 163-179.
Berenbaum, M. R. 2001. Chemical mediation of coevolution: phylo-
genetic evidence for Apiaceae and associates. Ann. Missouri Bot.
Gard. 88: 45–59.
Berenbaum, M. R., and S. Passoa. 1999. Generic phylogeny of North
American Depressariinae (Lepidoptera: Elachistidae) and hypothe-
ses about coevolution. Ann. Entomol. Soc. Am. 92: 971–986.
Berlocher, S. H. 1998. Can sympatric speciation via host or habi-
tat shift be proven from phylogenetic and biogeographic evi-
dence? pp. 99–113. In D. J. Howard and S. H. Berlocher (eds.),
Endless forms: species and speciation. Oxford University Press,
Oxford.
Berlocher, S. H., and J. L. Feder. 2002. Sympatric speciation in phy-
tophagous insects: moving beyond controversy? Annu. Rev. Ento-
mol. 47: 773–815.
Bernays, E. A., and R. F. Chapman. 1994. Host-plant selection by
phytophagous insects. Chapman and Hill, New York.
Bernays, E. A., and M. S. Singer. 2005. Insect defences: taste alter-
ation and endoparasites. Nature 436: 476.
Bisset, J., and A. Borkent. 1988. Ambrosia galls: the significance of
fungal nutrition in the evolution of the Cecidomyiidae (Diptera),
pp. 203–225. In K. A. Pirozynski and D. L. Hawksworth (eds.),
Coevolution of fungi with plants and animals. Academic Press,
London.
Blank, S. M. 2002. Biosystematics of the extant Xyelidae with partic-
ular emphasis on the Old World taxa (Insecta: Hymenoptera).
Dissertation, Freie Universität Berlin.
Blomberg, S. P., and T. Garland. 2002. Tempo and mode in evolu-
tion: phylogenetic inertia, adaptation and comparative methods.
J. Evol. Biol. 15: 899–910.
Bokma, F. 2003. Testing for equal rates of cladogenesis in diverse
taxa. Evolution 57: 2469–2474.
Bolmgren, K., and O. Eriksson. 2005. Fleshy fruits: origins, niche
shifts, and diversification. Oikos 109: 255–272.
Brady, S. G., T. R. Schultz, B. L. Fisher, and P. S. Ward. 2006. Evaluat-
ing alternative hypothesis for the early evolution and diversifica-
tion of ants. Proc. Nat’l. Acad. Sci. U.S.A. 103: 18172–18177.
Bucheli, S., J. F. Landry, and J. Wenzel. 2002. Larval case architecture
and implications of host-plant associations for North American
Coleophora (Lepidoptera; Coleophoridae). Cladistics 18: 71–93.
Burckhardt, D. 2005. Biology, ecology, and evolution of gall-inducing
psyllids (Hemiptera: Psylloidea), pp. 144–157. In A. Raman, C. W.
Schaefer, and T. M. Withers (eds.), Biology, ecology, and evolution
of gall-inducing arthropods. Science Publishers, Enfield, NH.
Cattin, M. F., L.F. Bersier, C. Banasˇek-Richter, R. Baltensperger, and J.
P. Gabriel. 2004. Phylogenetic constraints and adaptation explain
food-web structure. Nature 427: 835–839.
Chesser, P. T., and R. M. Zink. 1994. Modes of speciation in birds: a
test of Lynch’s method. Evolution 48: 490–497.
Cho, S. 1997. Molecular phylogenetics of the Heliothinae (Lepi-
doptera: Noctuidae) based on the nuclear genes for elongation
factor-1 and dopa decarboxylase. Ph.D. dissertation, University
of Maryland, College Park.
Condon, M. A., and G. J. Steck. 1997. Evolution of host use in fruit
flies of the genus Blepharoneura (Diptera: Tephritidae): cryptic
species on sexually dimorphic host plants. Biol. J. Linn. Soc. 60:
443–466.
Connor, E. F., and M. P. Taverner. 1997. The evolution and adaptive
significance of the leaf-mining habit. Oikos 79: 6–25.
Cook, L. G., and P. J. Gullan. 2004. The gall-inducing habit has
evolved multiple times among the eriococcid scale insects (Sternor-
rhyncha: Coccoidea: Eriococcidae). Biol. J. Linn. Soc. 83: 441–452.
Cook, J. M., A. Rokas, M. Pagel, and G. N. Stone. 2002. Evolutionary
shifts between host oak sections and host-plant organs in Andri-
cus gallwasps. Evolution 56: 1821–1830.
Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland,
MA.
Crespi, B. J., and C. P. Sandoval. 2000. Phylogenetic evidence for the
evolution of ecological specialization in Timema walking-sticks. J.
Evol. Biol. 13: 249–262.
Davis, C. C., C. D. Bell, S. Mathews, and M. J. Donoghue. 2002.
Laurasian migration explains Gondwanan disjunctions: evidence
from Malpighiaceae. Proc. Natl. Acad. Sci. USA 99: 6833–6837.
Denno, R. F., M.S. McClure, and J.R. Ott. 1995. Interspecific interac-
tions in phytophagous insects: competition reexamined and res-
urrected. Annu. Rev. Entomol. 40: 297–331.
Dethier, V. 1941. Chemical factors determining the choice of food
plants by Papilio larvae. Am. Nat. 75: 61–73.
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 259

Dietrich, C. H. 1999. The role of grasslands in the diversification of
leafhoppers (Homoptera: Cicadellidae): a phylogenetic perspective,
pp. 44–49. In C. Warwick (ed.), Proceedings of the 15th North
American Prairie Conference. Natural Areas Association, Bend, OR.
DiMichele, W. A., A. K. Behrensmeyer, T. D. Olszewski, C. C. Laban-
deira, J. M. Pandolfi, S. L. Wing, and R. Bobe. 2004. Long-term sta-
sis in ecological assemblages: evidence from the fossil record.
Annu. Rev. Ecol. Syst. 35: 285–322.
Dobler, S. 2001. Evolutionary aspects of defense by recycled plant
compounds in herbivorous insects. Basic Appl. Ecol. 2: 15–26.
Dobler, S., P. Mardulyn, J. M. Pasteels, and M. Rowell-Rahier. 1996.
Host-plant switches and the evolution of chemical defense and life
history in the leaf beetle genus Oreina. Evolution 50: 2373–2386.
Dorchin, N., A. Freidberg, and O. Mokady. 2004. Phylogeny of the
Baldratiina (Diptera: Cecidomyiidae) inferred from morphological,
ecological and molecular data sources, and evolutionary patterns
in plant-galler relationships. Mol. Phylogenet. Evol. 30: 503–515.
Ehrlich, P. R., and P.H. Raven. 1964. Butterflies and plants: a study in
coevolution. Evolution 18: 586–608.
Fagan, W. F., E. Siemann, C. Mitter, R. F. Denno, A. F. Huberty, H.A.
Woods, and J. J. Elser. 2002. Nitrogen in insects: implications for
trophic complexity and species diversification. Am. Nat. 160:
784–802.
Faith, D. P., and P.S. Cranston. 1991. Could a cladogram this short
have arisen by chance alone? On permutation tests for cladistic
structure. Cladistics 7: 1–28.
Fang, Q. Q., S. Cho, J. C. Regier, C. Mitter, M. Matthews, R. W. Poole, T. P.
Friedlander, and S. W. Zhao. 1997. A new nuclear gene for insect phy-
logenetics: dopa decarboxylase is informative of relationships within
Heliothinae (Lepidoptera: Noctuidae). Syst. Biol. 46: 269–283.
Farrell, B. D. 1998. Inordinate fondness explained: why are there so
many beetles? Science 281: 555–559.
Farrell, B. D. 2001. Evolutionary assembly of the milkweed fauna:
cytochrome oxidase I and the age of Tetraopes beetles. Mol. Phylo-
genet. Evol. 18: 467–478.
Farrell, B., and C. Mitter. 1990. Phylogenesis of insect-plant interac-
tions: have Phyllobrotica leaf beetles and Lamiales diversified in
parallel? Evolution 44: 1389–1403
Farrell, B. D., and C. Mitter. 1993. Phylogenetic determinants of
insect/plant community diversity, pp. 253–266. In R. E. Ricklefs
and D. Schluter (eds.), Species diversity: historical and geographi-
cal perspectives. University of Chicago Press, Chicago.
Farrell, B. D., and C. Mitter. 1998. The timing of insect/plant diversifi-
cation: might Tetraopes (Coleoptera : Cerambycidae) and Asclepias
(Asclepiadaceae) have co-evolved? Biol. J. Linn. Soc. 63: 553–577.
Farrell, B. D., and A. S. Sequeira. 2004. Evolutionary rates in the
adaptive radiation of beetles on plants. Evolution 58: 1984–2001.
Farrell, B. D., D. Dussourd, and C. Mitter. 1991. Escalation of plant
defense: Do latex/resin canals spur plant diversification? Am. Nat.
138: 881–900
Farrell B. D., A. S. Sequeira, B. C. O’Meara, B. B. Normark, J. H. Chung,
and B. H. Jordal. 2001. The evolution of agriculture in beetles (Cur-
culionidae: Scolytinae and Platypodinae). Evolution 55: 2011–2027.
Favret, C., and D. J. Voegtlin. 2004. Speciation by host-switching in
pinyon Cinara (Insecta: Hemiptera: Aphididae). Mol. Phylogenet.
Evol. 32: 139–151.
Feeny, P. 1991. Chemical constraints on the evolution of swallowtail
butterflies, pp. 315–339. In P. W. Price, T.M. Lewinsohn, G.W.
Fernandes, and W. W. Benson (eds.), Plant-animal interactions:
evolutionary ecology in tropical and temperate regions. John
Wiley and Sons, New York.
Filchak, K. E., J. B. Roethele, and J. L. Feder. 2000. Natural selection
and sympatric divergence in the apple maggot Rhagoletis
pomonella. Nature 407: 739–742.
Fitzpatrick, B. M., and M. Turelli. 2006. The geography of mam-
malian speciation: mixed signals from phylogenies and range
maps. Evolution 66: 601–615.
Funk, D. J., K. E. Filchack, and J. L. Feder. 2002. Herbivorous insects:
model systems for the comparative study of speciation ecology.
Genetica 116: 251–267.
Futuyma, D. J. 1989. Macroevolutionary consequences of speciation,
pp. 557–578. In D. Otte and J. A. Endler (eds.), Speciation and its
consequences. Sinauer, Sunderland, MA.
Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological
specialization. Annu. Rev. Ecol. Syst. 12: 207–233.
Futuyma, D. J., M. C. Keese, and D. J. Funk. 1995. Genetic con-
straints on macroevolution: the evolution of host affiliation in
the leaf beetle genus Ophraella. Evolution 49: 797–809.
Gagné, R. J. 1989. The plant-feeding gall midges of North America.
Cornell University Press, Ithaca, NY.
Gassman, A. J., A. Levy, T. Tran, and D. J. Futuyma. 2006. Adapta-
tions of an insect to a novel host plant: a phylogenetic approach.
Funct. Ecol. 20: 478–485.
Gaston, K. J., D. Reavey, and G.R. Valladares. 1992. Intimacy and
fidelity: internal and external feeding by the British microlepi-
doptera. Ecol. Entomol. 17: 86–88.
Gillespie, J. J., K. M. Kjer, C. N. Duckett, and D. W. Tallamy. 2003.
Convergent evolution of cucurbitacin feeding in spatially isolated
rootworm taxa (Coleoptera: Chrysomelidae; Galerucinae, Luperini).
Mol. Phylogenet. Evol. 29: 161–175.
Gillespie, J. J., K. M. Kjer, E. G. Riley, and D. W. Tallamy. 2004. The
evolution of cucurbitacin pharmacophagy in rootworms: insight
from Luperini paraphyly, pp. 37–57. In P. Jolivet, J. A. Santiago-
Blay, and M. Schmitt (eds.), New developments in the biology of
Chrysomelidae. SPB Academic Publishing, The Hague, The
Netherlands.
Graham, A. 1999. Late cretaceous and cenozoic history of North
American vegetation north of Mexico. Oxford University Press,
Oxford.
Grimaldi, D., and M. S. Engel. 2005. Evolution of the insects. Cam-
bridge University Press, Cambridge, MA.
Hansen, T. F., and S. H. Orzack. 2005. Assessing current adaptation
and phylogenetic inertia as explanations of trait evolution: the
need for controlled comparisons. Evolution 59: 2063–2072.
Harry, M., M. Solignac, and D. Lachaise. 1998. Molecular evidence
for parallel evolution of adaptive syndromes in fig-breeding Lis-
socephala (Drosophilidae). Mol. Phylogenet. Evol. 9: 542–551.
Heie, O. E. 1996. The evolutionary history of aphids and a hypothe-
sis on the coevolution of aphids and plants. Boll. Zool. Agr.
Bachic. 28: 149–155.
Holloway, J. D., and E. S. Nielsen. 1998. Biogeography of the Lepi-
doptera, pp. 423–461. In N. P. Kristensen (ed.), Handbook of zoology,
Lepidoptera. vol. 1: Systematics and evolution. W. de Gruyter, Berlin.
Hsiao, T. H., and J. M. Pasteels. 1999. Evolution of host-plant affilia-
tion and chemical defense in Chrysolina-Oreina leaf beetles as
revealed by mtDNA phylogenies, pp. 321–342. In M. L. Cox (ed.),
Advances in Chrysomelidae biology. Backhuys, Leiden, The
Netherlands.
Hsiao, T. H., and D. M. Windsor. 1999. Historical and biological rela-
tionships among Hispinae inferred from 12S mtDNA sequence
data, pp. 39–50. In M. L. Cox (ed.), Advances in Chrysomelidae
biology. Backhuys, Leiden, The Netherlands.
260 CO- AND MACROEVOLUTIONARY RADIATION

Isaac, N. J. B., P. M. Agapow, P. H. Harvey, and A. Purvis. 2003. Phyloge-
netically nested comparisons for testing correlates of species richness:
a simulation study of continuous variables. Evolution 57: 18–26.
Janz, N., and S. Nylin. 1998. Butterflies and plants: a phylogenetic
study. Evolution 52: 486–502.
Janz, N., K. Nyblom, and S. Nylin. 2001. Evolutionary dynamics of
host-plant specialization: a case study of the tribe Nymphalini.
Evolution 55: 783–796.
Janz, N., S. Nylin, and N. Wahlberg. 2006. Diversity begets diversity:
host expansions and the diversification of plant-feeding insects.
BMC Evol. Biol. 6: 4.
Jervis, M. A., C. L. Boggs, and P. N. Ferns. 2005. Egg maturation strat-
egy and its associated trade-offs: a synthesis focusing on Lepi-
doptera. Ecol. Entomol. 30: 359–375.
Joy, J. B., and B. J. Crespi. 2007. Adaptive radiation of gall-inducing
insects within a single host-plant species. Evolution 61: 784–795.
Karban, R., and A. A. Agrawal. 2002. Herbivore offense. Annu. Rev.
Ecol. Syst. 33: 641–664.
Kawakita, A, and M. Kato. 2006. Assessment of the diversity and
species specificity of the mutualistic association between Epi-
cephala moths and Glochidion trees. Mol. Ecol. 15: 2567–2581.
Kawakita, A., A. Takimura, T. Terachi, T. Sota, and M. Kato. 2004.
Cospeciation analysis of an obligate pollination mutualism: have
Glochidion trees (Euphorbiaceae) and pollinating Epicephala
moths (Gracillariidae) diversified in parallel? Evolution 58:
2201–2214.
Kergoat, G. J., A. Delobel, G. Fédière, B. Le Rü, and J.-F. Silvain.
2005. Both host-plant phylogeny and chemistry have shaped the
African seed-beetle radiation. Mol. Phylogenet. Evol. 35:
602–611.
Kristensen, N. P. 1984. Studies on the morphology and systematics
of primitive Lepidoptera (Insecta). Steenstrupia 10: 141–191.
Kristensen, N. P. 1997. Early evolution of the Lepidoptera  Tri-
choptera lineage: phylogeny and the ecological scenario. Mem.
Mus. Natl. Hist. Nat. 173: 253–271.
Kuhn, J., E. M. Pettersson, B. K. Feld, A. Burse, A. Termonia, J. M. Pas-
teels, and W. Boland. 2004. Selective transport systems mediate
sequestration of plant glucosides in leaf beetles: a molecular basis
for adaptation and evolution. Proc. Natl. Acad. Sci. USA 101:
13808–13813.
Labandeira, C. C., 2002. The history of associations between plants
and animals, pp. 26–74. In C. Herrera and O. Pellmyr (eds.),
Plant-animal interactions: an evolutionary approach. Blackwell
Science, Oxford.
Lewinsohn, T. M., V. Novotny, and Y. Basset. 2005. Insects on plants:
diversity of herbivore assemblages revisited. Annu. Rev. Ecol.
Evol. Syst. 36: 597–620.
Lopez-Vaamonde, C., H. C. J. Godfray, and J. M. Cook. 2003. Evolu-
tionary dynamics of host-plant use in a genus of leaf-mining
moths. Evolution 57: 1804–1821.
Losos, J.B., and R.E. Glor. 2003. Phylogenetic comparative methods
and the geography of speciation. Trends Ecol. Evol. 18: 220–227.
Lynch, J.D. 1989. The gauge of speciation: on the frequencies of
modes of speciation, pp. 527–553. In D. Otte and J. A. Endler
(eds.), Speciation and its consequences. Sinauer, Sunderland, MA.
Machado, C. A., N. Robbins, M. T. P. Gilbert, and E. A. Herre. 2005.
Critical review of host specificity and its coevolutionary implica-
tions in the fig/fig-wasp mutualism. Proc. Natl. Acad. Sci. USA
102: 6558–6565.
Mackenzie, A., and A. F.G. Dixon. 1990. Host alternation in aphids:
constraint versus optimization. Am. Nat. 136: 132–134.
Magallón, S. 2004. Dating lineages: molecular and paleontological
approaches to the temporal framework of clades. Int. J. Plant. Sci.
165: S7-S21.
Magallón, S., and M. J. Sanderson. 2001. Absolute diversification
rates in angiosperm clades. Evolution 55: 1762–1780.
Marvaldi, A. E., A. S. Sequeira, C. W. O’Brien, and B. D. Farrell. 2002.
Molecular and morphological phylogenetics of weevils
(Coleoptera, Curculionoidea): do niche shifts accompany diversi-
fication? Syst. Biol. 51: 761–785.
Mayhew, P. J. 2002. Shifts in hexapod diversification and what Hal-
dane could have said. Proc. R. Soc. Lond. B 269: 969–974.
McKenna D. D., and B. D. Farrell. 2006. Tropical forests are both evo-
lutionary cradles and museums of leaf beetle diversity. Proc. Natl.
Acad. Sci. USA 103: 10947–10951.
Miller, D. G., and B. Crespi. 2003. The evolution of inquilinism,
host-plant use and mitochondrial substitution rates in Tamalia
gall aphids. J . Evol. Biol. 16: 731–743.
Miller, J. S. 1987. Host-plant relationships in the Papilionidae (Lepi-
doptera): parallel cladogenesis or colonization? Cladistics 3:
105–120.
Mitchell, A., C. Mitter, and J. C. Regier. 2006. Systematics and evolu-
tion of the cutworm moths (Lepidoptera: Noctuidae): evidence
from two protein-coding nuclear genes. Syst. Entomol. 31: 21–46.
Mitter, C., and D. R. Brooks. 1983. Phylogenetic aspects of coevolu-
tion, pp. 65–98. In D. J. Futuyma and M. Slatkin (eds.), Coevolu-
tion. Sinauer, Sunderland, MA.
Mitter, C., and B. Farrell. 1991. Macroevolutionary aspects of insect-
plant relationships, pp. 35–78. In E. A. Bernays (ed.), Insect/plant
interactions, vol. 3. CRC Press, Boca Raton, FL.
Mitter, C., B. Farrell, and B. Wiegmann.1988. The phylogenetic
study of adaptive zones: has phytophagy promoted insect diversi-
fication? Am. Nat. 132: 107–128.
Mitter, C., R. W. Poole, and M. Matthews. 1993. Biosystematics of
the Heliothinae (Lepidoptera: Noctuidae). Annu. Rev. Entomol.
38: 207–225.
Moore, B. R., K. M. A. Chan, and M. J. Donoghue. 2004. Detecting
diversification rate variation in supertrees, pp. 487–533. In O. R. P.
Bininda-Emonds (ed.), Phylogenetic supertrees: combining infor-
mation to reveal the tree of life. Kluwer Academic Publishers, Dor-
drecht, The Netherlands.
Moran, N. A. 1988. The evolution of host plant alternation in aphids:
evidence for specialization as a dead end. Am. Nat. 132: 681–706.
Moran, N. A. 1990. Aphid life cycls: two evolutionary steps. Am. Nat.
136: 135–138.
Moran, N. A. 1992. The evolution of aphid life cycles. Annu. Rev.
Entomol. 37: 321–348.
Moreau, C. S., C. D. Bell, R. Vila, S.B. Archibald, and N. E. Pierce.
2006. Phylogeny of the ants: diversification in the age of
angiosperms. Science 312: 101–104.
Morris, D. C., L. A. Mound, M. P. Schwarz, and B. J. Crespi. 1999.
Morphological phylogenetics of Australian gall-inducing thrips
and their allies: the evolution of host-plant affiliations, domicile
use and social behaviour. Syst. Entomol. 24: 289–299.
Morse, G. E., and B. D. Farrell. 2005. Ecological and evolutionary
diversification of the seed beetle genus Stator (Coleoptera:
Chrysomelidae: Bruchinae). Evolution 59: 1315–1333.
Murphy, S. M. 2004. Enemy-free space maintains swallowtail butter-
fly host shift. Proc. Natl. Acad. Sci. USA 101: 18048–18052.
Nee, S., A. O. Mooers, and P. H. Harvey, 1992. Tempo and mode of
evolution revealed from molecular phylogenies. Proc. Natl. Acad.
Sci. USA 89: 8322–8326.
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 261

Nee, S., T. G. Barraclough, and P. H. Harvey. 1996. Temporal changes
in biodiversity: detecting patterns and identifying causes, pp.
230–252. In K. J. Gaston (ed.), Biodiversity: a biology of numbers
and difference. Blackwell Scientific, Oxford.
Nickel, H. 2003. The leafhoppers and planthoppers of Germany
(Hemiptera, Auchenorrhyncha): patterns and strategies in a
highly diverse group of phytophagous insects. Pensoft Series Fau-
nistica No. 28. Pensoft Publishers, Sofia, Bulgaria.
Normark, B. B. 2000. Molecular systematics and evolution of the
aphid family Lachnidae. Mol. Phylogenet. Evol. 14: 131–140.
Nosil, P. 2002. Transition rates between specialization and general-
ization in phytophagous insects. Evolution 56: 1701–1706.
Nosil, P., and A. O. Mooers. 2005. Testing hypotheses about ecologi-
cal specialization using phylogenetic trees. Evolution 59: 2256–
2263.
Nosil, P., B. J. Crespi, and C. P. Sandoval. 2003. Reproductive isola-
tion driven by the combined effects of ecological adaptation and
reinforcement. Proc. R. Soc. Lond. B 270: 1911–1918.
Nylander, J. A. A. 2004. Bayesian phylogenetics and the evolution of
gall wasps. Ph.D. dissertation, University of Uppsala, Uppsala,
Sweden.
Nylander, J., F. Ronquist, J. P. Huelsenbeck, and J. L. Nieves-Aldrey.
2004. Bayesian phylogenetic analysis of combined data. Syst.
Biol. 53: 47–67.
Nyman, T., A. Widmer, and H. Roinnen. 2000. Evolution of gall
morphology and host-plant relationships in willow-feeding
sawflies (Hymenoptera: Tenthredinidae). Evolution 54: 526–533.
Nyman, T., B. D. Farrell, A. G. Zinovjev, and V. Vikberg. 2006. Larval
habits, host-plant associations, and speciation in nematine sawflies
(Hymenoptera: Tenthredinidae). Evolution 60: 1622–1637.
Ortiz-Rivas, B., A. Moya, and D. Martínez-Torres. 2004. Molecular
systematics of aphids (Homoptera: Aphididae): new insights from
the long-wavelength opsin gene. Mol. Phylogenet. Evol. 30:
24–37.
Page, R. D. M. (ed.). 2003. Tangled trees: phylogeny, cospeciation and
coevolution. University of Chicago Press, Chicago.
Paradis, E. 1997. Assessing temporal variations in diversification
rates from phylogenies: estimation and hypothesis testing. Proc.
R. Soc. Lond. B 264: 1141–1147.
Pellmyr, O. 2003. Yuccas, yucca moths and coevolution: a review.
Ann. Missouri Bot. Gard. 90: 35–55.
Percy, D. M. 2003. Radiation, diversity, and host-plant interactions
among island and continental legume-feeding psyllids. Evolution
57: 2540–2556.
Percy, D. M., R. D. M. Page, Q. C. B. Cronk. 2004. Plant-insect interac-
tions: double-dating associated insect and plant lineages reveals
asynchronous radiations. Syst. Biol. 53: 120–127.
Plantard, O., J. D. Shorthouse, and J. Y. Rasplus. 1997. Molecular
phylogeny of the genus Diplolepis (Hymenoptera: Cynipidae), pp.
247–260. In G. Csoka, W. J. Mattson, G. N. Stone, and P. W. Price
(eds.), Biology of gall inducing arthropods. Gen. Tech. Rep. NC-
199. U.S. Department of Agriculture, Forest Service, North Central
Forest Experiment Station, St. Paul, MN.
Powell, J. A. 1980. Evolution of larval food preferences in microlepi-
doptera. Annu. Rev. Entomol. 25: 133–159.
Powell, J. A., C. Mitter, and B. Farrell. 1998. Evolution of larval feed-
ing habits in Lepidoptera, pp. 403–422. In N. P. Kristensen (ed.),
Handbook of zoology, Lepidoptera. Vol. 1: Systematics and evolu-
tion. W. de Gruyter, Berlin.
Pratt, G. F. 1994. Evolution of Euphilotes (Lepidoptera: Lycaenidae)
by seasonal and host shifts. Biol. J. Linn. Soc. 51: 387–416.
Price, P. W. 1980. Evolutionary biology of parasites. Monographs in
population biology, vol. 15. Princeton University Press, Princeton,
NJ.
Purvis, A. 1996. Using interspecies phylogenies to test macroevolu-
tionary hypotheses, pp. 153–168. In P. H. Harvey, A. J. L. Brown,
J. M. Smith, and S. Nee (eds.), New uses for new phylogenies.
Oxford University Press, Oxford.
Ree, R. H. 2005. Detecting the historical signature of key innovations
using stochastic models of character evolution and cladogenesis.
Evolution 59: 257–265.
Rodman, J. E., P. S. Soltis, D. E. Soltis, K. J. Sytsma, and K. G. Karol.
1998. Parallel evolution of glucosinolate biosynthesis inferred
from congruent nuclear and plastid gene phylogenies. Am. J. Bot.
85: 997–1006.
Ronquist, F., and J. Liljeblad. 2001. Evolution of the gall wasp-host
plant association. Evolution 55: 2503–2522.
Rudgers, J. A., S. Y. Strauss, and J.F. Wendel. 2004. Trade-offs among
anti-herbivore resistance traits: insights from Gossypieae (Mal-
vaceae). Am. J. Bot. 91: 871–880.
Rundle, H. D., and P. Nosil. 2005. Ecological speciation. Ecol. Lett. 8:
336–352.
Sachet, J. M., A. Roques, and L. Després. 2006. Linking patterns and
processes of species diversification in the cone flies Strobilomyia
(Diptera: Anthomyiidae). Mol. Phylogenet. Evol. 41: 606–621.
Sanderson, M. J., and M. J. Donoghue. 1994. Shifts in diversification
rate with the origin of angiosperms. Science 264: 1590–1593.
Sargent, R. D. 2004. Floral symmetry affects speciation rates in
angiosperms. Proc. R. Soc. Lond. B 271: 603–608.
Schick, K., Z. W. Liu, and P. Goldstein. 2003. Phylogeny, historical
biogeography, and macroevolution of host use among Diastro-
phus gall wasps (Hymenoptera: Cynipidae). Proc. Entomol. Soc.
Wash. 105: 715–732.
Schluter, D. 1987. Character displacement and the adaptive diver-
gence of finches on islands and continents. Am. Nat. 131:
799–824.
Schluter, D. 1988. Character displacement and the adaptive diver-
gence of finches on islands and continents. Am. Nat. 131:
799–824.
Schluter, D. 2000. The ecology of adaptive radiation. Oxford Univer-
sity Press, Oxford.
Schulmeister, S. 2003. Simultaneous analysis of basal Hymenoptera
(Insecta): introducing robust-choice sensitivity analysis. Biol. J.
Linn. Soc. 79: 245–275.
Simpson, G. G. 1953. The major features of evolution. Columbia
University Press, New York.
Singer, M. S., and J. O. Stireman. 2005. The tri-trophic niche concept
and adaptive radiation of phytophagous insects. Ecol. Lett. 8:
1247–1255.
Singer, M. S., Y. Carriere, C. Theuring, and T. Hartmann. 2004. Dis-
entangling food quality from resistance against parasitoids: diet
choice by a generalist caterpillar. Am. Nat. 164: 423–429.
Smith, A. R., K. M. Pryer, E. Schuettpelz, P. Korall, H. Schneider, and P.
G. Wolf. 2006. A classification for extant ferns. Taxon 55: 705–731.
Spencer, K. A. 1990. Host specialization in the world Agromyzidae
(Diptera). Kluwer Academic Publishers, Dordrecht, The Netherlands.
Stireman, J. O. 2005. The evolution of generalization? Parasitoid flies
and the perils of inferring host range evolution from phylogenies.
J. Evol. Biol. 18: 325–336.
Strong, D. R., J. H. Lawton, and R. Southwood. 1984. Insects on
plants: community patterns and mechanisms. Harvard University
Press, Cambridge, MA.
262 CO- AND MACROEVOLUTIONARY RADIATION

Swigonˇová, Z., and K. M. Kjer. 2004. Phylogeny and host-plant asso-
ciation in the leaf beetle genus Trirhabda LeConte (Coleoptera:
Chrysomelidae). Mol. Phylogenet. Evol. 32: 358–374.
Symons, F.B., and G.W. Beccaloni. 1999. Phylogenetic indices for
measuring the diet breadths of phytophagous insects. Oecologia
1119: 427–434.
Termonia, A., T. H. Hsiao, J. M. Pasteels, and M. C. Milinkovitch.
2001. Feeding specialization and host-derived chemical defense
in chrysomeline leaf beetles did not lead to an evolutionary dead
end. Proc. Natl. Acad. Sci. USA 98: 3909–3914.
Termonia, A., J. M. Pasteels, D. M. Windsor, and M. C. Milinkovitch.
2002. Dual chemical sequestration: a key mechanism in transitions
among ecological specialization. Proc. R. Soc. Lond. B 269: 1–6.
Thompson, J. N. 1988. Coevolution and alternative hypotheses on
insect plant interactions. Ecology 69: 893–895.
Vamosi, S. M., and J. C. Vamosi. 2005. Endless tests: guidelines for
analyzing non-nested sister-group comparisons. Evol. Ecol. Res. 7:
567–579.
Via, S. 2001. Sympatric speciation in animals: the ugly duckling
grows up. Trends Ecol. Evol. 16: 381–390.
von Dohlen, C. D., and N. A. Moran. 2000. Molecular data support a
rapid radiation of aphids in the Cretaceous and multiple origins
of host alternation. Biol. J. Linn. Soc. 71: 689–717.
von Dohlen, C. D., U. Kurosu, and S. Aoki. 2002. Phylogenetics and
evolution of the eastern Asian–eastern North American disjunct
aphid tribe, Hormaphidini (Hemiptera: Aphididae). Mol. Phylo-
genet. Evol. 23: 257–267.
von Dohlen, C. D., C. A. Rowe, and O. E. Heie. 2006. A test of mor-
phological hypotheses for tribal and subtribal relationships of
Aphidinae (Insecta: Hemiptera: Aphididae) using DNA sequences.
Mol. Phylogenet. Evol. 38: 316–329.
Wahlberg, N. 2001. The phylogenetics and biochemistry of host-
plant specialization in Melitaeine butterflies (Lepidoptera:
Nymphalidae). Evolution 55: 522–537.
Webb, C. O., D. D. Ackerly, M. A. McPeek, and M. J. Donoghue. 2002.
Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33:
475–505.
Weiblen, G. D., and G. L. Bush. 2002. Speciation in fig pollinators
and parasites. Mol. Ecol. 11: 1573–1578.
Weingartner, E., N. Wahlberg, and S. Nylin. 2006. Dynamics of host
plant use and species diversity in Polygonia butterflies (Nymphali-
dae). J. Evol. Biol. 19: 483–491.
Welch, J. J., and L. Bromham. 2005. Molecular dating when rates
vary. Trends Ecol. Evol. 20: 320–327.
Weller, S. J., N. L. Jacobson, and W. E. Connor. 1999. The evolution
of chemical defenses and mating systems in tiger moths (Lepi-
doptera: Arctiidae). Biol. J. Linn. Soc. 68: 557–578.
Whitcomb, R. F., A.L. Hicks, H.D. Blocker, and D. E. Lynn. 1994. Bio-
geography of leafhopper specialists of the shortgrass prairie:
evidence for the roles of phenology and phylogeny in determina-
tion of biological diversity. Am. Entomol. 40: 19–35.
Wiegmann, B.M., C. Mitter, and B. Farrell. 1993. Diversification of
carnivorous parasitic insects: extraordinary radiation or special-
ized dead end? Am. Nat. 142: 737–754.
Wiegmann, B.M., C. Mitter, J. C. Regier, T. P. Friedlander, D. M. Wag-
ner, and E. S. Nielsen. 2000. Nuclear genes resolve Mesozoic-aged
divergences in the insect order Lepidoptera. Mol. Phylogenet.
Evol. 15: 242–259.
Wiegmann, B.M., J.C. Regier, and C. Mitter. 2002. Combined
molecular and morphological evidence on the phylogeny of the
earliest lepidopteran lineages. Zool. Scripta 31: 67–81.
Williams, G.C. 1992. Natural selection: domains, levels, and chal-
lenges. Oxford University Press, New York.
Wilson, S., C. Mitter, R. F. Denno, and M. R. Wilson. 1994. Evolu-
tionary patterns of host plant use by delphacid planthoppers and
their relatives, pp. 7–113. In R. F. Denno and J. Prefect (eds.), The
ecology and management of planthoppers. Chapman and Hall,
New York.
Wink, M. 2003. Evolution of secondary metabolites from an ecolog-
ical and molecular phylogenetic perspective. Phytochemistry 64:
3–19.
Wood, T. K. 1993. Speciation of the Enchenopa binotata complex
(Insecta: Homoptera: Membracidae), pp. 300–317. In D. R. Lees
and D. Edwards (eds.), Evolutionary patterns and processes. Acad-
emic Press, London.
Yack, J. E., and J. H. Fullard. 2000. Ultrasonic hearing in nocturnal
butterflies. Nature 403: 265–266.
Yang, M. M., and C. Mitter. 1994. Biosystematics of hackberry psyl-
lids (Homoptera: Psylloidea): a preliminary report, pp. 172–184.
In P. W. Price, W. Mattson, and Y. Baranchikov (eds.), The ecology
and evolution of gall-forming insects. Gen. Tech. Rep. NC-174.
U.S. Department of Agriculture, Forest Service, North Central For-
est Experiment Station, St. Paul, MN.
Yotoko, K.S. C., P.I. Prado, C.A.M. Russo, and V.N. Solferini. 2005.
Testing the trend towards specialization in herbivore-host plant
associations using a molecular phylogeny of Tomoplagia (Diptera:
Tephritidae). Mol. Phylogenet. Evol. 35: 701–711.
Zakharov, E. V., M. S. Caterino, and F. A. H. Sperling. 2004. Molecular
phylogeny, historical biogeography, and divergence time esti-
mates for swallowtail butterflies of the genus Papilio (Lepidoptera:
Papilionidae). Syst. Biol. 53: 193–215.
Zwölfer, H. 1978. Mechanismen und ergebnisse der co-evolution
von phytophagen und entomophagen insekten und höheren
pflanzen. Sonderbd. Naturwiss. Ver. Hamburg 2: 7–50.
PHYLOGENETIC DIMENSION OF INSECT-PLANT INTERACTIONS 263