AMER. ZOOL., 34:57-69 (1994)
Adaptive Radiation in Insects and Plants:
Time and Opportunity1
BRIAN D. FARRELL
Environmental, Population and Organismic Biology, University of Colorado, Boulder, Colorado 80309
AND
CHARLES MITTER
Department of Entomology, University of Maryland, College Park, Maryland 20742
SYNOPSIS. Insects and their hostplants represent the major part of terrestrial diversity, yet we are just beginning to understand why there are
so very many species. By far the most influential model of insect/plant
diversification has been Ehrlich and Raven's (1964) hypothesis of insect/
plant coevolution. While the coevolution model was based on macroevolutionary patterns in plant defenses and hostplant affiliations, most of
the subsequent work has been on its possible ecological and genetic mechanisms, with relatively little systematic scrutiny of the evolutionary patterns Ehrlich and Raven described. We explore the possible roles insect/
plant interactions may play in the long-term evolution of insect and plant
lineages, and review some of the evidence on whether or not insects and
plants have exerted reciprocal influences on each other's diversification.
Insects and plants have diversified over roughly the same time intervals,
and many insect host-affiliations are evolutionarily conserved, thus
reflecting long-term, phylogenetic history. Rather than accumulating herbivores at a rate proportional to their geographic area of distribution or
biomass, some plant groups pose apparent chemical barriers to potential
herbivore colonists, and seem accessible to relatively few insect lineages,
possibly preadapted by use of chemically similar or related hostplants.
Evolutionary innovations in plant defenses and in insect feeding habits
seem to have spurred their respective adaptive radiations, thus ecological
opportunity may influence long-term evolutionary success. The greater
diversity of insects and plants in the tropics, compared to the temperate
zone, probably reflects the greater age of tropical habitats as well as climatic barriers that limit successful invasion of the temperate zone to just
those primitively tropical groups able to evolve strategies for both overwintering and use of temperate resources. Though evidence is still sparse,
successful invasion of the temperate zone may promote subsequent radiations of both insects and plants.
We conclude that much of the available evidence from systematics is
consistent with Ehrlich and Raven's suggestion that much of insect and
plant diversification has been spurred by a series of ecological opportunities over evolutionary time.
1
From the symposium Science as a Way of Knowing— Biodiversity presented at the Annual Meeting of the
American Society of Zoologists, 27-30 December 1992, at Vancouver, Canada.
57
58
B. D. FARRELL AND C. MITTER
INTRODUCTION
Land plants and their insect enemies
together comprise more than half of all
known terrestrial species and serve as food
for most of the rest. However, we are only
beginning to understand why there are so
many insect and plant species. While such
factors as age or area of geographic distribution, degree of specialization or availability of resources used are often cited in
explanations of why one group of organisms
is more successful (i.e., has many more species) than another, these can be traced to
two fundamental concepts: time and opportunity. In this essay we explore the ways in
which ecological opportunity over evolutionary time has helped shape the current
patterns of insect and plant diversity.
A well-known theory of how insects and
plants might have diversified together over
evolutionary time was proposed by Ehrlich
and Raven (1964). Their model of insect/
plant "coevolution" has profoundly stimulated research on insect/plant interactions.
Ehrlich and Raven suggested that insects
and plants are engaged in an endless evolutionary "arms race," which consists of 1)
the origin of a new chemical defense in some
plant groups, which by reducing herbivore
attack (i.e., permitting escape) allows those
plants to increase in abundance and eventually in diversity (i.e., to radiate); and 2)
subsequent evolution of insect counteradaptations to plant defenses, permitting
insect radiation in the "adaptive zone" represented by the, by now, very diverse plant
group.
Under Ehrlich and Raven's model, the
current differences in diversity and abundance among various insect and plant groups
represent the different stages each has
attained in the historical sequence of "escape
and radiation" (Thompson, 1989).
Though Ehrlich and Raven brought their
respective expertise in insect and plant systematics to their landmark essay, the basis
for Ehrlich and Raven's idea lay in an earlier
concept in evolutionary biology. Thus, part
of the reason the coevolution model has
become popular among biologists is that it
brings together the separate disciplines of
ecology, genetics and systematics in order
to explain the evolutionary success of the
most diverse organisms on earth. Such a
union of disciplines was first proposed in
the 1940s by a group of eminent scientists
(and has been termed the "modern or evolutionary synthesis") but the empirical connections among these areas have not been
well established or understood. A key element in this synthesis is the idea of "adaptive radiations"—that the evolution of an
adaptation (e.g., a new feeding habit or a
new way to escape predators) may permit
one group of organisms to more rapidly
evolve new species (or go extinct less often)
than another. For example, the origin of
wings may have allowed birds and bats the
opportunity to evolve many new species,
each with a slightly different way of feeding
and reproducing off the ground (Simpson,
1953).
Ehrlich and Raven's argument rested
largely on taxonomic patterns of plant secondary chemistry and insect hostplant use.
They pointed out that many very diverse
plant groups have toxic chemicals that deter
most insects from feeding on them, and so
suggested that the ancestor of each such plant
group evolved a new toxin, escaped its enemies and multiplied. Ehrlich and Raven also
pointed out that such plant groups do often
acquire a few, specially adapted insect enemy
groups which are also rich in species, so they
suggested that the ancestors of these groups
evolved the ability to detoxify the plant
defense and then multiplied on the abundant and mostly uneaten resource such plant
groups represent. As one example, Ehrlich
and Raven cited the toxic cardiac glycosides
which characterise the closely related milkweed and dogbane families (Asclepiadaceae
and Apocynaceae). The Asclepiadaceae and
Apocynaceae are now worldwide in distribution and comprise some 4,000 species.
Though poisonous, these plants have been
successfully colonized by the monarch butterflies, able to detoxify the toxins in their
foodplants, and which presently total some
150 species.
Although Ehrlich and Raven's idea of
coevolution was based on this kind of evolutionary (i.e., systematic or taxonomic)
pattern, most of the subsequent work on
coevolution has come from the disciplines
of ecology and genetics. A complete under-
INSECT/PLANT DIVERSIFICATION
standing of the evolution of herbivorous
insects and plants, including definitive tests
of the coevolution model, will require complementary study of their long-term (i.e.,
phylogenetic) history. We will first review
some of the evidence from the newly invigorated discipline of phylogenetic systematics on the evolution of insect/plant interactions and focus on a few of the more
important issues emerging from these studies, concerning the imprint of evolutionary
history on insect/plant communities.
KEY ISSUES
(1) To what degree is insect host use evolutionarily conservative? If new host-affiliations are easy to evolve, insect radiation
restricted to sets of related plants is unlikely
to occur; moreover, new defenses are likely
to be overcome before they have the chance
to promote plant radiation through reduced
herbivory.
(2) How old are the associations between
particular extant insect and plant lineages,
and to what extent have such lineages
evolved together? Old associations, obviously, have had the longest time for the
insect and plant groups to affect each other's
evolution.
(3) Is there evidence for the "escape and
radiation" steps of Ehrlich and Raven's scenario? That is, do the phylogenies of particular groups of plant species reveal evolutionary sequences of increasingly more
effective defenses (and of counter-defenses
in insects)? Do the plant and insect groups
that have these innovations diversify more
rapidly than those that do not have them?
How EASILY CAN INSECTS EVOLVE USE
OF A NEW HOSTPLANT?
There are differing views on just how conservative insect host-affiliations may typically be. A basic premise of Ehrlich and
Raven's scenario is that related insects most
often eat related plants, an observation that
has been long appreciated by entomologists.
However, the evidence on how often insects
switch hostplants has been little quantified.
This question can be approached by
reconstructing the history of host use in an
insect group using a cladogram (i.e., phylogenetic tree)—a branching diagram
59
SPECIES SHAPES
CHANGE IN THIS ANCESTOR
CHANGE IN THIS ANCESTOR
FIG. 1. Cladogram for a group of 6 hypothetical species. This estimate of relationships among the species
minimizes the number of origins of different patterns
and shapes between species by ascribing such changes
to common ancestors.
depicting the sequence of divergence of species from a common ancestor (Fig. 1). The
phylogeny of a group of species may be
inferred by inspection of the forms of comparable structures between each species. A
special modification shared by some (but
not all) species in a group is taken as evidence of a common ancestor, unique to these
species, in which the modification arose. The
species groupings that emerge after similar
comparisons of all features are those that
are depicted in the resulting cladogram.
For example, among all arthropods, the
six-legged forms are inferred to belong to a
group (the insects) that inherited a reduction
in leg number from an ancestor not shared
with other arthropods (which possess 10 or
more pairs of legs). This grouping also
explains why, among all arthropods, these
six-legged species also share certain other
modifications, such as in mouthpart morphology, and is further supported by recent
data from DNA sequences.
Similarly, one may infer the phylogeny of
a group of herbivorous beetles by examining
the traits that some members of the group
share and others do not. The best estimate
of phylogeny is one which best accounts for
the patterns of shared modifications, across
all traits. For the present context, it may be
assumed that the phylogeny estimates are
60
B. D. FARRELL AND C. MITTER
BKFT1.F. HOSTS
PLANT A
BEETLE PHYLOGENY
HOST SHIFT IN THIS ANCESTOR
FIG. 2. Cladogram for a hypothetical group of herbivorous beetles, in which some species feed on plant
group A and others plant group B.
based on characteristics (e.g., morphology
or molecules) other than host-affiliation.
One can quantify the frequency of change
in herbivore diet by counting up the number
of changes in hostplant affiliation on a
cladogram, and dividing by the maximum
number you could observe (i.e., one fewer
than the total number of species). It is necessary to decide beforehand what constitutes a shift in diet, but the major differences
in plant defensive chemicals are between
plant families and these chemicals are among
the most important qualities encountered
by attacking insects. For example, if the
20-,
S.
a
•s
iS
10 •
E
z3
.0-.16
.17-.32
.33-.48
.49-.64
.6S-.8
Frequency of host-family shift
FIG. 3. Frequency distribution of shifts in host-family
in 25 herbivore groups. The largest category is of insect
clades for which fewer than 20% of speciation events
are associated with host transfer between plant families
(data from Mitter and Farrell, 1991).
cladogram for a genus of 6 beetle species
shows that the group switched hostplants
from plant family A to plant family B (Fig.
2), then an index of the lability of diet may
be calculated (1/5) as equal to 0.2.
There are only about two dozen cladograms for insect herbivores, but a frequency
distribution of the number of these showing
little versus much change in hostplant family supports the idea that related insect species most often use related plants: change
in hostplant family typically accompanies
less than 20 per cent of insect speciation
events (Fig. 3). This probably reflects a
response to similarity in plant chemistry,
but exactly how and why plant chemistry
plays such a central role in insect diet evolution is not completely clear.
WHERE D O THE INSECTS ON A PLANT
COME FROM?
If insects generally find it difficult to evolve
new hostplant associations, then the number of insect species on any particular plant
species might be limited to just those insect
groups that possess special pre-adaptations
for life on the new plant. For example, an
insect that feeds on a plant with very hairy
leaves might be more able to colonize
another plant with hairy leaves than would
some insect feeding on a smooth-leaved
plant. No detailed studies of this kind of
evolutionary "filter" has yet been performed, but there are some strong taxonomic patterns in the kinds of plants that
related insects feed on that suggest their
existence. For example, May Berenbaum has
shown that insects that attack the taxonomic subgroup within the carrot family that
bears a particularly toxic group of chemicals
(called angular furanocoumarins), have
apparently evolved only in insect groups
previously adapted to the more widespread,
probably more primitive linear furanocoumarins (Berenbaum, 1983). There is a similar pattern among the relatively few insects
that manage to attack the milkweeds and
their relatives, plants whose excellent
defenses include an intricate canal system
that upon injury emits sticky latex containing toxic secondary compounds (Mitter and
Farrell, in preparation).
Most of the herbivores of milkweeds have
INSECT/PLANT DIVERSIFICATION
Other angiosperms
Latex/resin
clades
Asteridae
Vita
Magn
Ruta
Anac
Sapo
Dipt
Viol
Euph
Urti
Faba
Aste
Dips
Lami
Scro
Sola
61
1111 II
1111 II
1111 II
ilUiililJIi
111 Illlll
VWWll
0
10
20
Number of milkweed herbivore groups
FIG. 4. Frequency distribution of affiliations with other plant orders among 50 independent taxa containing
herbivores of Asclepiadaceae/Apocynaceae. Most records are from the subclass Asteridae or from other latexcanal-bearing groups. Each plant order is presented on vertical axis (with first four letters of ordinal name,
following Cronquist, 1981).
evolved the ability not only to withstand
the potent milkweed poisons, but also to
store these chemicals in their tissues to protect them against predators, and advertise
this toxicity with very bright colors. Given
the typically very effective defenses of these
plants and the great specialization of the few
insects that do feed on them, it is reasonable
to ask just where milkweed insects came
from. Do insects feeding on any plant group
have equal chances of evolving the ability
to feed on milkweeds? Or are only the insects
feeding on a select group of plants so preadapted? To answer this question we can
inspect the diet of the near relatives of milkweed-feeding species, as these should include
the habits that gave rise to milkweed-feeding.
While there are 83 orders of flowering
plants, and insects associated with each,
nearly all of the nearest relatives of milkweed herbivores feed on just twelve (Fig. 4).
These are either closely related to milkweeds or share the same defense: latex and
resin canals. In fact the most frequent habit
is feeding on the one latex-bearing group
that is also closely related to milkweeds: the
morning glory family, Convolvulaceae. Thus
it seems that milkweeds are accessible to
only the few. We may be able to one day
ask whether successful colonization of this
toxic hostplant group has spurred adaptive
radiations in milkweed insects, as predicted
by Ehrlich and Raven's scenario.
How OLD ARE ASSOCIATED INSECTS
AND PLANTS?
Insect/plant associations are often quite
conservative, and so it seems likely that they
may persist over extensive periods of geological time. Long-continued associations,
in which the interacting insect and plant
lineages diversify together, should provide
the greatest opportunity for coevolution, in
the sense of Ehrlich and Raven. On the other
hand, if particular associations have evolved
much more recently (e.g., if the insects are
much younger than the plants), it is unlikely
that any extensive coevolution has occurred.
There is some evidence that at the scale
of geological epochs, the fossil ages of major
insect herbivore groups correspond to those
of their predominant host groups, suggesting a long continued association (Zwolfer,
1978). For example, the Mesozoic fossils of
cerambycid, chrysomelid, curculionid and
scolytid beetles represent primitive groups
whose present day members are mostly
associated with cycads and conifers, whereas
the more advanced groups in these families
mostly attack correspondingly younger,
flowering plant groups such as Asteraceae
(asters and relatives) and Lamiaceae (mints)
(Fig. 5: also see Linsley 1961, 1963; Wood,
1982; Anderson, 1993). The older beetle
groups thus appear to have retained host
preferences established before flowering
plants had appeared. There is also increas-
62
B. D. FARRELL AND C. MITTER
50 -,
40-
t
30-
o
Z
20-
Genera with mid-Tertiary
host-taxa
Genera with Mesozoic
host-taxa
10-
25
35
45
65
Age of first appearance of insect genera
(millions of years)
FIG. 5. Paleontological ages of some extant beetle/hostplant affiliations, compiled from Heer (1865), Handlirsch
(1908), Statz (1938), Linsley (1961, 1963), Larsson (1978), Wood (1982) and our own studies of Dominican
amber (Farrell and Mitter, in preparation). Phytophagous beetle genera presently affiliated with older plant
groups appear significantly earlier in the fossil record than beetles presently affiliated with younger groups (Chisquared = 36.7; P < 0.001; df = 4).
ing evidence that present-day species and
genera of phytophagous insects are very old.
Among beetles, for example, there are many
excellent fossils in 30 to 50 million year old
ambers and shales which are nearly indistinguishable from species which can be seen
today, in forests and fields. A truly striking
observation is that in any given temperate
forest, the more primitive timber beetles,
bark beetles and weevils are still attacking
their original conifer hosts, while their
younger relatives are largely restricted to the
younger herbaceous understory—a persistence of habits that reflects what plants were
available when these insect groupsfirstarose.
There are many other examples from other
insect groups of particular hostplant associations that have persisted for many millions of years (e.g., Hickey and Hodges,
1975; Opler, 1973; Moran, 1989; Humphries et al, 1986; Farrell et ai, 1992; Farrell and Mitter, 1993).
HAVE INSECTS AND PLANTS EVOLVED
TOGETHER?
Given that many insect groups may be
approximately as old as the plant groups
they feed on, these insect and plant lineages
may have diversified during the time they
have been associated, with the accompanying potential for coevolution. One expectation under such "parallel diversification"
is that the phylogenetic order of divergence
among insect species should correspond to
that among their hostplants (Farrell and
Mitter, 1990). There have been relatively
few attempts to document such correspondence of phylogenies, but a summary of the
evidence so far indicates that strongly corresponding phylogenies are rare; only two
relatively clear cases are known (Farrell and
Mitter, 1990; Farrell, 1991; Mitter and Farrell, 1991). A good fraction of the remaining
assemblages show at least some degree of
phylogeny agreement. This may represent
partial evolution in parallel with the hosts,
with periodic "transfer" of insect species to
more distantly related hosts. However, it is
also possible that the insects "colonized"
the plants long after these diversified, in a
sequence following similarities in plant
chemistry that are often correlated with plant
relatedness. It has become clear that estimates of the age of individual insect and
plant species are crucial to deciding which
present-day associations represent parallel
63
INSECT/PLANT DIVERSIFICATION
Tetraopini
Phaea grp. 1
i Phaea grp. 2
Convolvulaceae »
Apocynaceae A .
Marsdenia
•T. ineditus
\
A. subulata » \
P T. elegans
, T . discoideus (MX)
Apocynales
Matelea^N
'T. comes
A. curassavica »
»T. discoideus (US) A . subverticillata ^ \
pT. umbonanis
f T. melanurus
A. glaucescens*
A. tuberosa ^^
T. 5-maculatus
A. amplexicaulis
i T. annulatus
A. sullivanti
T. pUosus
A. arenaria . \
>
^Vjr
cardenolides
•T. varicornis
A. latifolia A \
^ ^ I more complex, toxic
A. syriaca ^nTV
SC / cardenolides
A. notha ^ 5
"*T. femoratus
A. speciosa —•"
> T. mandibularis
•T. tetroptbalmus
»T. sublaevis
^T. basalis
LV
A. e r o s a ^ ./
most toxic cardenolides
concentrated in latex
A. eriocarpa
FIG. 6. Phylogeny estimate of Tetraopes beetles based on morphology and allozymes, compared to literaturebased relationships of hostplants (Farrell, 1991). Host Asclepias shows an apparent progression toward increased
complexity and toxicity of cardenolides, perhaps representing escape and radiation. Distributions of beetle and
hostplant clades suggest Oligocene origins.
diversification. Such datings can potentially
come from fossils, geographic distributions,
or, increasingly, from the degree of nucleotide sequence divergence, which often
accumulates in a roughly clock-like fashion.
The two insect groups which do show
extensive phylogeny congruence with their
hosts, both beetles, show similar life histories intimately tied to the host, which may
be especially conducive to coevolution. Thus
within the 25 species of the North American
longhoraed beetle genus Tetraopes, both the
adults and larvae feed on the same species
in the familar milkweed genus Asclepias;
this contrasts with groups such as butterflies, in which the adults take only nectar
and pollen from flowers, and are not tied to
the larval host. Tetraopes adults feed on the
flowers and leaves, while the larvae bore in
the roots. Tetraopes beetles are all brightly
marked with orange and black and use the
hostplant toxins for their own defense
against predators such as birds. The phylogeny of these beetles closely matches that
of their hostplants (Farrell, 1991; Fig. 6),
suggesting that they may have diversified in
parallel. Distributions and genetic divergence data also suggest that these insect and
plant groups are similar in age, about 20
million years. Therefore it seems possible
that Tetraopes and Asclepias have undergone coevolution in Ehrlich and Raven's
sense. Thus, our current estimate of milkweed phylogeny suggests that the milkweed's defensive chemicals have steadily
increased in complexity, toxicity and concentration over evolutionary time. At present, the youngest, most toxic plants are fed
on (almost solely) by the youngest, most
advanced beetles, while the older, more
primitive milkweeds are attacked by the
more primitive beetles and many other, dif-
64
B. D. FARRELL AND C. MITTER
plant defense type
FIG. 7. Hypothetical example of a plant group that
primitively possesses a certain chemical defense type
(1), and has more recently evolved a new defense (2).
Groups A and B are sister groups.
ferent groups of milkweed insects. For complete test of the coevolution hypothesis, we
need more evidence on exactly how old each
associated beetle and plant species is, as well
as experiments on the effects of the different
milkweed toxins on different insects,
including these beetles.
A N ARMS RACE BETWEEN INSECTS
AND PLANTS?
While it seems that at least some insect/
plant affiliations are so conservative as to
diversify in parallel, such examples are
probably rare, though many sets of related
insects are faithful to a single hostplant group
(e.g, a plant genus or family). However, we
have not yet addressed the most important
idea in Ehrlich and Raven's coevolution
model: that improved plant defenses and
insect counter-adaptations have led to
increased diversification of the lineages in
which they arose. Ehrlich and Raven suggested several possible examples of particular plant defenses that may have spurred
diverisification and this idea has been picked
up by several recent workers, but there have
not been any really detailed studies of this
element of the coevolution hypothesis. We
will review a case involving the defensive
latex canals found in milkweeds and many
other plants, but first need to consider just
how such a study might be performed.
A major problem in studying the possible
effect a new adaptation might eventally have
on diversification is that many traits have
evolved only once. For cases like this it is
hard to ever be sure whether an increase in
diversity is due to the adaptation or to some
other factor that happened at the same time.
For example, there are many more species
of birds than there are crocodilians (their
near relatives), and it might be because birds
evolved feathered wings that allowed them
to use resources and occupy habitats
unavailable to others. However plausible
this may seem, we will never know for sure
because birds have many other characteristics unique to them and any of these may
have permitted them to multiply.
One solution to this problem of confounded influences on diversity is to identify multiple groups which have independently evolved the new trait (e.g., a new
plant defense), and ask whether these are
consistently more diverse than their nearest
relatives. Two groups that are most closely
related to each other (i.e., that share a unique
common ancestor) are said to be "sister
groups" of each other (Fig. 7). Since two
sister groups each diverged from the same
ancestor, they are equal in age. Differences
in diversity between sister groups therefore
indicate that they have diversified at different rates. This fact is critical because, all
else being equal, a group may have more
species simply because it is older. Therefore
it is necessary to compare groups that are
equal in age if we wish to decide whether
some other factor affects diversity.
Many plant defenses have evolved more
than once, and so offer the possibility of
testing their effects on diversity. Latex and
resin canals may be a typical example (Farrell et al, 1991). Latex and resin are plant
defenses whose effectiveness is dramatically
increased when they occur in specialized
anatomical structures termed secretory
canals (Dussourd and Eisner, 1987). Secretory canals, like a many-branched system
of tributaries, contain a much larger volume
of sticky liquid, under turgor pressure, than
is present at any one site. Whereas an herbivore biting into a leaf of a plant without
INSECT/PLANT DIVERSIFICATION
these canals encounters whatever defenses
are in the area, an insect that bites into a
leaf (e.g., of a fig tree, poinsettia or milkweed) or burrows into bark (e.g., of a pine)
containing these secretory canals is immediately confronted with a large volume of
glue-like latex or resin containing toxic
chemicals—much more than they would get
if the plant did not have the canal system
(Dussourd and Denno, 1991). Under Ehrlich and Raven's model, plants that evolve
a very effective new defense, such as latex
or resin canals, gain an opportunity to
diversify free of herbivores, at least temporarily. Insects that later evolve the ability
to feed on the new plant group gain the
opportunity to use a resource that presumably no other insects can.
Latex and resin canals have originated in
some 40 lineages of vascular plants; for 16
of these the phylogenetic relationships are
sufficiently understood to perform sistergroup diversity comparisons. For 13 of these
16 sister-group comparisons, the canalbearing group is more diverse than its sister group,
often by several orders of magnitude (Farrell et al, 1991). There are no other characters, such as particular chemicals or geographic distributions, that co-vary with
secretory canals, across even a minority of
these groups. It thus seems most likely that
their diversity does indeed reflect a property
unique to canal-bearing plants, perhaps a
combination of physical deterrence with
increased effectiveness of whatever particular plant chemical defenses the plants have.
An unsolved question raised by this result
is why a trait, such as latex canals, which
enhances the individual fitness of its bearers, should lead to an increase in the number
of species. Some recent paleontological
studies suggest that population sizes (which
may be enhanced by increased adaptation)
may be important in determining which
species go extinct and which species proliferate over geological time (Lidgard and
Jackson, 1989; Jablonski, 1987). Studies
comparing the population sizes of extant
organisms may also provide some insights.
For example, latex- and resin-canal bearing
trees have been reported to be unusually
abundant in several neotropical forests, a
possible consequence of relative freedom
65
from herbivores and pathogens (Boom,
1986; Prance et al, 1976; Farrell et al, in
preparation).
Another study using this sister-group
diversity approach supports Ehrlich and
Raven's idea that insect diversification has
been greatly accelerated by association with
higher plants (Miner et al, 1988). Plantfeeding has evolved in at least fifty insect
lineages whose collective species diversity
accounts for over one-half of all insects. With
few exceptions, each plant-feeding lineage
is much more diverse than its predaceous
or detritivorous sister group. Whether herbivore diversity is generated by successive
bouts of "escape and radiation" or is simply
a function of the greater resources plants
present to herbivores (as opposed to those
available to insects with other habits) is
unknown: there are still no phylogenetic
studies of the many possible examples of
insect radiation following colonization of
newly-diversified plant groups. We can,
however, rule out one explanation, that rapid
speciation is characteristic of "parasitic"
organisms in a broad sense. In another study
of the many insect clades parasitizing animals, rather than plants, there is no evidence of consistently greater diversity, compared to sister groups with other feeding
habits (Wiegmann et al, 1993). Thus it
seems that there is something about feeding
on plants per se that has spurred insect radiations.
WHY ARE THERE SO MANY INSECTS IN
THE TROPICS?
While Ehrlich and Raven's model seems
useful for understanding insect/plant evolution, consideration of the influence of geographic distribution on diversity is also likely
to be important for a complete understanding of their diversity (Darlington, 1957;
Vermeij, 1987). Plants and insects can
escape their predators or competitors either
by evolving an adaptation, or by invading
a new area where the insects and plants lack
countermeasures to the ones they already
have. For example, although some crop
plants like Theobroma (source of chocolate)
and sugar cane accumulate insect enemies
rapidly when introduced outside their native
range, others like Eucalyptus and cactus
66
B. D. FARRELL AND C. MITTER
remain relatively herbivore free for periods
ranging from decades to millions of years
(Strong et al, 1984; Zwolfer, 1988).
This geographical analogy of the escape
and radiation model may help to explain
the striking differences in diversity between
the tropics and temperate zone. The fossil
record shows that the temperate zone as we
know it is young, and began with a global
cooling and drying trend beginning in the
early Tertiary, some 40 million years ago
(Wolfe, 1978). Because plant families are
nearly all older than this, most temperate
plant groups have evolved from ancestors
that lived in tropical environments. Harsh
climate seems to have limited invasion of
or survival in temperate regions to just those
plant groups able to evolve appropriate
adaptations. For example, most of our temperate herb groups, like the milkweeds, vervains, borages and violets are recently
evolved, unusual members of plant families
which are mostly composed of tropical trees.
Apparently, some primitively tropical tree
groups have evolved the herbaceous habit,
allowing overwintering underground {i.e.,
escape) during the most severe season presented by the comparatively new temperate
zone (Wing and Tiffney, 1987). These herbaceous clades have now radiated and form
a major element of the temperate landscape.
In turn, this recently evolved temperate
flora may have fewer insect enemies (compared to the tropics) because primitively
tropical insect herbivores must develop
analogous adaptations, such as diapause or
migration, for overwintering. These traits
probably arise only in pre-adapted lineages—temperate overwintering diapause,
for example, has evolved only in insect
groups whose tropical representatives show
some form of seasonal quiescence (Tauber
et al., 1986). Herbivores, whose host use
seems so often evolutionarily conservative,
face the additional obstacle of finding suitable hosts in the species-poor temperate
flora. They might therefore be expected to
show even more pronounced differences in
diversity between the tropics and temperate
zone than insects that are not host-limited.
Support for this idea comes from a study
of beetles from the canopies of several different forest types at Tambopata, in Ama-
zonian Peru (Farrell and Erwin, 1988). Each
of 90 different species of rove-beetle, the
largest group of predators, tends to occur in
the canopy of several different kinds of forest (e.g., along the river edge, in the floodplain forest and in the distant uplands). The
number of species and individuals there are
in any given tree is predictable simply by
the physical volume of foliage. In contrast,
most species of leaf-beetles, the dominant
plant-feeding group, are restricted to a single
forest type, and often just a single kind of
tree (Farrell et al, in preparation). It is
impossible to predict how many leaf-beetle
species there are in any given tree through
such simple physical characteristics, though
the leaf-beetles and other herbivores are
usually less abundant in trees with latex or
resin canals than they are in trees without
these defenses. Thus, the local distributions
of predators and herbivores apparently
reflects their different degrees of resource
specialization. We might therefore expect to
see similar differences in comparisons of the
number of species of these groups in the
tropics and temperate zone.
As expected, the number of leaf-beetles
(750 species) at Tambopata is greater than
the number found in a much larger temperate area, the state of Indiana (286 species), while the number of rove-beetles is
almost the same (ca. 400 species) in both
places. The idea that the difference in leafbeetle (but not rove-beetle) diversity reflects
their much more specialized feeding habits
is also supported by biogeography and the
fossil record. The distributions of the genera
of leaf-beetles in these samples are much
more narrow (they are mostly restricted to
South America or the New World) than are
those of the rove-beetles (much more cosmopolitan). This is what you would expect
if leaf-beetles have recently diversified and
remain faithful to their hostplant groups.
The earliest fossils of both leaf- and rovebeetles appeared in the Jurassic, but the
major diversification of leaf beetles, in contrast to rove-beetles, apparently occurred
much later, coincident with the diversification of their mostly tropical host groups,
which have only infrequently entered temperate floras (Farrell and Mitter, 1993).
Among the leaf-beetles and other tropical
67
INSECT/PLANT DIVERSIFICATION
herbivore groups that do reach the temperate zone, radiation may be promoted by
special adaptation to the temperate flora,
e.g., by shift onto dominant temperate plant
groups. Insufficient knowledge of insect
relationships currently prevents test of this
hypothesis, but there are many suggestive
examples. For instance, the temperate fauna
of noctuid moths is dominated by a huge,
evolutionarily advanced "cutworm" clade,
typically ground-dwelling and which feed
on many different herbaceous plants,
whereas relatively primitive noctuids are
primarily arboreal feeders, mostly host specific, and most diverse in tropical forests.
In recent decades, historical explanations
for the greater diversity in the tropics of
many different groups of organisms have
been overshadowed by "equilibrial" theories based on inherent differences between
temperate and tropical environments {e.g.,
Janzen, 1967;Pianka, 1978; Stevens, 1989).
The issue has been clouded by the way
diversity differences have been measured.
A typical approach to the problem is to pick
a group of organisms, say kingfishers or
crayfish, and count up the number of species
at each of two or more points that differ in
latitude, say Kansas and Costa Rica. That
is, it is assumed that the present differences
in diversity have reached a stable level and
will not decrease with time. The problem
with such tallies is the lack of control for
the greatly differing ages of temperate and
tropical climatic conditions, as we've seen.
For the example from leaf-beetles discussed
earlier, the greater tropical diversity is not
evidence of faster diversification in the tropics; we can not exclude the hypothesis that
leaf-beetles have simply had more time to
diversify in the tropics (where their hosts
are largely found).
One solution to the problem of comparing groups of differing ages is to restrict
diversity comparison to sister groups, of
equal age by definition (Fig 8). Only a few
temperate/tropical sister-group comparisons can as yet be identified for herbivorous
insects, but in these there is no suggestion
of a trend toward faster diversification in
the tropics (Farrell and Mitter, 1993).This
result is at least consistent with the view of
temperate/tropical diversity gradients as
Temperate
species
Tropical
species
Millions of years ago
FIG. 8. Hypothetical example of a primitively tropical clade with recently evolved temperate representatives. Tropical element has more species only because
it is older; rate of diversification is higher in temperate
zone.
reflecting the tropical origins of most groups
of organisms.
SUMMARY
There is increasing evidence that insects
are often conservative with respect to the
evolution of new host-affiliations—hence the
structure and diversity of insect/plant communities seem strongly influenced by a long
history. There is substantial evidence that
much of the evolution of currently affiliated
insect and plant lineages has occurred over
similar geological time intervals. Cases of
strictly parallel diversification can be found
but are most certainly the exception rather
than the rule. There is some evidence that
"escalations" in plant defense have resulted
in increased diversity. There is also evidence that plant-feeding has spurred insect
diversification, though it is unknown
whether this involves insect counter-adaptation to plant defenses, per se. Thus, the
available evidence on the evolution of
68
B. D. FARRELL AND C. MITTER
insect/plant communities, while still sparse,
is largely consistent with the conclusions
reached by Ehrlich and Raven (1964).
This view of evolution as driven by ecology is not new; Ehrlich and Raven were
foreshadowed by the early workers who
forged the modern synthesis. However, with
the advent of rigorous techniques for phylogeny estimation and the onslaught of evidence on relationships from molecular biology, we have begun to explore just how the
extraordinary richness of insect/plant communities, so evident in the tropics, is the
product of their intricate interactions.
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