B R I E F C O M M U N I C AT I O N

doi:10.1111/j.1558-5646.2009.00768.x

THE MACROEVOLUTIONARY DYNAMICS

OF ANT DIVERSIFICATION
Marcio R. Pie1,2 and Marcel K. Tschá1
1
Laboratório de Dinâmica Evolutiva e Sistemas Complexos, Departamento de Zoologia, Universidade Federal do Paraná,
C.P. 19020, 81531-990 Curitiba, PR, Brazil
2
E-mail: [email protected]

Received August 30, 2007

Accepted June 8, 2009

The availability of increasingly comprehensive phylogenies has provided unprecedented opportunities to assess macroevolutionary
patterns, yet studies on invertebrate diversification are few. In particular, despite the ecological and evolutionary importance of
ants, little is known about their tempo and mode of diversification. Recent advances in ant phylogenetics can now provide a basis
for rigorous analyses of the diversification of ant lineages. The goals of the present study are threefold. First, we demonstrate that a
hypothesized disproportionate increase in ant diversification during the angiosperm radiation is largely artifactual. Rather, current
evidence points to a fairly constant rate of lineage growth during its history. Moreover, an analysis of diversification patterns
across the ant phylogeny indicates considerable rate heterogeneity among lineages. Indeed, and contrary to the expectation if
lineages had experienced a single rate of lineage increase, we found no correspondence between genus age and diversity. Finally,
we demonstrate a statistically significant phylogenetic signal in ant diversification: closely related genera have diversities that are
more similar to one another than one would expect by chance. This suggests that the capacity for diversification may be itself a
biological trait that evolved during the radiation of the family Formicidae.

KEY WORDS: Adaptive radiation, cladogenesis, Formicidae, speciation.

Phylogenies are often said to display the signatures of the Hölldobler 2005). With more than 12,000 species worldwide, ants
evolutionary processes that generated them (Nee et al. 1992; are nearly three times more diverse than all other eusocial groups
Katzourakis et al. 2001; Mooers and Heard 2002). This real- combined (Grimaldi and Agosti 2000). In addition, although ants
ization has led to the prolific use of phylogenetic information account for less than 2% of the known insect fauna of the world,
in the study of diversification processes (e.g., Nee et al. 1992; they compose at least one-third of its biomass, with a global
Kirkpatrick and Slatkin 1993; Harvey et al. 1996; Mooers and population of approximately 1015 individuals (Wilson 1990). An
Heard 1997; Barraclough et al. 1998; Gittleman and Purvis 1998; estimate of the animal fauna in the Amazon region indicated that
Katzourakis et al. 2001; Morrow et al. 2003; Isaac et al. 2005). In three-fourths of the animal biomass in the terra firme forest is
particular, the advent of more complex null models of diversifica- composed of ants and termites (Beck 1971; Fittkau and Klinge
tion has added the necessary rigor, such that eventual deviations 1973). Such ecological success has resulted in the presence of ants
can then be inspected to understand correlates of species rich- in nearly all terrestrial environments outside Antarctica (Wilson
ness (Kirkpatrick and Slatkin 1993; Slowinsky and Guyer 1993; 1987; Hölldobler and Wilson 1990).
Mooers and Heard 1997; Paradis 1997). However, few studies to The past seven years have witnessed a strong interest in ant
date have involved comprehensive analyses of invertebrate taxa, molecular phylogenetics (Brady 2003; Ward and Brady 2003;
despite their accounting for the bulk of metazoan biodiversity. Astruc et al. 2004; Saux et al. 2004; Brady et al. 2006; Moreau
Ants are a remarkable case of ecological and evolutionary et al. 2006; Ouellete et al. 2006), building upon the classical work
success (Wilson 1976; Hölldobler and Wilson 1990; Wilson and using morphological characters (Brown 1954; Baroni Urbani et al.


C 2009 The Author(s). Journal compilation 
C 2009 The Society for the Study of Evolution.

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1992). These studies have provided important insight into the phy- of that study. Diversification was simulated using a constant di-
logenetic relationships among the main ant lineages and the extent versification, in which each lineage has the same instantaneous
to which different subfamilies are monophyletic, although the re- probability of speciating or going extinct. We used the method
lationships among the most basal lineages are still a matter of proposed by Paradis (2003) to combine taxonomic and phyloge-
dispute (Brady et al. 2006; Moreau et al. 2006). One aspect of ant netic data and estimated the speciation and extinction rates during
diversification that has received recent attention is the suggestion ant diversification, assuming that those rates remained constant,
that the radiation of the family was associated with the origin using the function “bd.ext” in APE (Paradis et al. 2004). Given
of flowering plants and the ensuing increased habitat complex- that the extinction rate was estimated to be zero (see below),
ity provided by soil and ground litter of angiosperm-dominated each single lineage was allowed to evolve at a speciation rate of
forests, particularly in the tropics (e.g., Wilson and Hölldobler 0.01 (without extinction) in each iteration until reaching 12,000
2005; Moreau et al. 2006). In support for this hypothesis, Moreau species (the approximate number of known ant species to date).
et al. (2006) used maximum-likelihood methods developed by The complete phylogeny was then randomly pruned of the fol-
Paradis (1997) to test three alternative ant diversification sce- lowing fractions of its lineages: 0, 50, 75, 90, and 98.8%. The
narios: (1) a constant diversification rate; (2) a variable diversi- last fraction was chosen to represent the approximate proportion
fication rate; and (3) two diversification rates, either before or of all ant lineages included in the phylogeny by Moreau et al.
after 100 million years (Myr). The third scenario provided the (2006) and was repeated 100 times to provide a Monte Carlo ap-
best fit to the data, suggesting a possible tracking of the rise of proach to determine the confidence intervals of the diversification
angiosperm-dominated forests between the Early Paleocene and model. Lineages-through-time (LTT) plots (cumulative counts of
the Late Cretaceous. However, the method of Paradis (1997) was the number of lineages over time) were used to represent the
developed to analyze complete phylogenies. Thus, although the increase in ant diversity over time in each of those conditions.
study by Moreau et al. (2006) uses one of the largest ant phylo- Although it is known that extinction did occur during ant his-
genies to date, it includes less than 2% of all known ant species. tory, a model without extinction was nevertheless chosen in the
The effects of such limited taxon sampling on the inferred pattern present study, both because it provided the best fit according to the
of ant diversification are currently unknown. method of Paradis (2003), and also because it would be the most
The goals of the present study are threefold. First, we assess conducive scenario to generate the pattern detected by Moreau
whether the hypothesized disproportionate increase in ant diversi- et al. (2006), given that adding a constant extinction would result
fication during the Angiosperm radiation is largely an artifact of an in an apparent increase in diversification near the present in the
incomplete taxon sampling. Second, we investigate the extent of reconstructed LTT (Nee et al. 1994). However, even when a con-
variation in diversification rates among different lineages across stant birth–death process was used to generate the phylogenies,
the ant phylogeny. Third, we use maximum-likelihood methods the level of taxon sampling in the studied phylogeny is so low
to assess the level of phylogenetic signal in ant diversification, that even this difference nearly disappeared after the trees were
i.e., whether closely related genera have diversities that are more pruned and the results were qualitatively similar (not shown). All
similar to one another than one would expect by chance. The im- of those simulations were done using the software Phyl-O-Gen
plications of these results for the evolution of ants are discussed. (Rambaut 2002).
Variation in diversification rate within the ant clade was in-
vestigated using three complementary methods. First, we calcu-
Materials and Methods lated the degree of imbalance in each node of the tree using the
The analyses carried out in the present study were based on method of Slowinski and Guyer (1993). The number of species in
the comprehensive phylogeny of ant relationships provided by each genus (all of which were assumed to be monophyletic) was
Moreau et al. (2006), which included 19 of the 20 currently rec- based on the respective number of described species, as indicated
ognized subfamilies. There is a disagreement over the best root- in the ANTBASE database (Agosti and Johnson 2005; accessed
ing of the ant tree (see Brady et al. 2006), but the relationships on May 31, 2007). One of the issues with this type of analysis
within the family seem well-supported. Although the phylogeny is the possibility of false-positive results due to multiple statis-
by Moreau et al. (2006) does not include all ant genera, those tical tests. One proposed solution to this problem is to compare
included encompass nearly 90% of all known ant species. There- the number of nodes showing significant imbalance to the total
fore, an analysis of this reduced dataset should nevertheless be number of tested nodes using the binomial test (Katzourakis et al.
representative of the entire family. 2001). However, simulations have indicated that the probability of
First, we used simulations to test whether the observed con- false-positives using the Slowinsky–Guyer test under a constant
centration of cladogenesis events observed by Moreau et al. (2006) diversification rate is very small (M. R. Pie, unpubl. data), and
is artifactual given the incomplete lineage sampling of ant lineages therefore we simply provided the statistically significant nodes

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without any correction in their associated probabilities. Second,

100
we tested for shifts in diversification rates using a maximum-
likelihood method recently developed by Rabosky et al. (2007).

50
This method splits the tree along an edge, fitting one rate to the
subtending clade and another to the rest of the (paraphyletic) tree.
This “two-rate” model is compared to a single-rate model using

20
a likelihood-ratio test. The test is repeated on all the edges of
the tree to identify when the shift in diversification was most

10
likely. The use of the entire tree in each comparison provides a
crucial difference between the method of Rabosky et al. (2007)

5
and the more commonly used Slowinsky–Guyer test, which only
compares diversification rate differences between sister clades
(see Sanderson and Donogue [1994] for a third, hybrid, method).

2
Given that there are several branches for which the shift in diver-
sification is most likely, we identified all the branches for which

1
the likelihood-ratio test was significant. However, to minimize 0 1
false-positives, we adjusted the critical value as 0.05 divided by RELATIVE TIME
the number of branches in the phylogeny. Finally, we computed
Figure 1. Lineages-though-time (LTT) plots indicating the effect
a linear regression analysis of the relationship between genus age
of incomplete taxon sampling on the reconstructed ant diversi-
and its species richness. If ant evolution experienced a single
fication process. The heavy line in the main plot is the LTT plot
nearly constant underlying diversification rate, there should be a recreated from Moreau et al. (2006), whereas the light lines repre-
statistically significant relationship between the age of different sent each one of 100 samples from a complete birth tree of 14,000
genera and their respective number of species. species pruned by 98.8%, equal to the estimated sampling from
We investigated the evolution of the diversification rates Moreau et al.
themselves by testing whether there was statistically significant
phylogenetic autocorrelation across the phylogeny for the size of species turnover during ant history, given that the maximum-
a genus. This was done by using the model developed by Pagel likelihood estimate of the extinction rate was zero (d/b = 0, SE =
(1999) based on an extension of a constant-variance random-walk 0, b − d = 0.079, SE = 0.0011, where b: speciation rate and
model (sometimes called Brownian motion). Under those condi- d: extinction rate). Therefore, the subsequent simulations were
tions, the degree of similarity in a given trait between two lineages based on a pure-birth (Yule) process.
is proportional to the extent of their shared history, as indicated by The effects of an incomplete taxon sampling on the LTT plots
the phylogeny, such that traits evolve at each instant of “time” dt are shown in Figure 1. Although the underlying “true tree” in the
with a mean character change of zero and an unknown but constant simulation diversified at a constant rate (resulting in a straight
variance σ2 . Pagel introduced another parameter, λ, to estimate line in the semi-log plot), randomly removing varying fractions
the extent to which the phylogeny correctly predicts patterns of of the lineages generated an apparent deceleration of lineage di-
similarity among species. This parameter can range from 1 (as versification, such that the effect was stronger as the proportion
predicted by the Brownian motion model) to 0 (trait similarity of removed lineages increased. In particular, a reconstructed phy-
among species is independent of phylogeny). Hypothesis testing logeny using only 1.2% of the extant lineages generated a curve
using this approach is based on the likelihood-ratio statistic, which very similar to that observed by Moreau et al. (2006).
compares the goodness of fit of a model to the data with that of a There was considerable heterogeneity in diversification rates
simpler model that lacks one or more of the parameters. Analyses among ant lineages, despite differences among methods in terms
using Pagel’s method were implemented using CONTINUOUS of when shifts in diversification took place during ant history
(Pagel 1999). A similar approach in the use of Pagel’s method (Fig. 2). Based on the method of Slowinsky and Guyer (1993),
to study diversification was presented by Phillimore et al. (2006, the largest asymmetries involved the contrast between the “living
2007). fossil” Aneuretus simoni and the remaining dolichoderines (1 and
616 species, respectively) and between Tranopelta and Pheidole
(2 and 969 species, respectively) (Table 1). On the other hand,
Results the method of Rabosky et al. (2007) identified the strongest shifts
The inference of speciation and extinction rates based on the in the lineages leading to Camponotus and Polyrhachis. Interest-
method of Paradis (2003) provided little evidence for extensive ingly, it also detected significant shifts in several species-poor

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Figure 2. Variation in diversification rates among ant lineages. The histogram on the right of the phylogeny shows the number of
currently described species for each genus. Circles indicate nodes inferred to have experienced significant shifts in diversification rate
based on the Slowinsky–Guyer test. Numbers on branches indicate significant shifts in diversification rate according to the method of
Rabosky et al. (2007), indicating increasingly lower likelihood scores, from 1 (highest) to 13 (lowest, but still significant).

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Table 1. Number of species in each of the nodes where a significant shift in diversification rate was detected based on the Slowinsky–
Guyer test.

Genera in the Number of Genera in the larger clade Number of P

smaller clade species in species in
the smaller the larger
clade clade
Xenomyrmex, Proatta, 16 Tetramorium, Calyptomyrmex, Terataner, Melissotarsus, 921 0.017094
Dilobocondyla Rhopalomastix, Crematogaster
Melissotarsus, 9 Crematogaster 448 0.019737
Rhopalomastix
Atopomyrmex 3 Oligomyrmex, Carebara, Pheidologeton 183 0.016216
Tranopelta 2 Pheidole 969 0.002062
Myrmecorhynchus, 53 Cataglyphis, Proformica, Formica, Polyergus, Oecophyla, 2108 0.024537
Melophorus, Prolasius, Euprenolepis, Acropyga, Anoplolepis, Polyrhachis,
Notonchus Camponotus, Opisthopsis, Myrmoteras, Stigmacros
Polyergus 7 Formica 298 0.023026
Myrmoteras 32 Opisthopsis, Camponotus, Polyrhachis 1536 0.020421
Opisthopsis 13 Polyrhachis, Camponotus 1523 0.008469
Aneuretus 1 Bothriomyrmex, Dolichoderus, Froggattella, Iridomyrmex, 616 0.001623
Ochetellus, Philidris, Anonychomyrma, Papyrius,
Linepithema, Dorymyrmex, Forelius, Azteca, Leptomyrmex,
Technomyrmex, Liometopum, Tapinoma
Tatuidris, Paraponera 3 Platythyrea, Centromyrmex, Dinoponera, Leptogenys, 861 0.003476
Myopias, Odontoponera, Odontomachus, Anochetus,
Hypoponera, Diacamma, Cryptopone, Pachycondyla
Centromyrmex 10 Cryptopone, Pachycondyla, Diacamma, Hypoponera, 809 0.012225
Anochetus, Odontomachus, Odontoponera, Myopias,
Leptogenys, Dinoponera
Dinoponera 6 Myopias, Leptogenys 250 0.023529
Odontoponera 1 Anochetus, Odontomachus 161 0.006211

lineages, particularly those leading to Onychomyrmex and Con- should not simply be dismissed as something “wrong” with the
coctio, which suggests that those shifts might in fact have lead to analysis. Interestingly, the heterogeneity in diversification rates
decreases in diversification rate. However, it is important to under- is also mirrored by the lack of association between the age of a
score that the method of Rabosky et al. (2007) was not designed to genus and its species richness (Fig. 3, r = −0.1267; P = 0.1371),
identify multiple shifts in diversification—it involves simply the suggesting that heterogeneity in diversification rates also took
comparison of a single-rate against a two-rate model in several place within genera during ant evolution.
alternative branches. The inferred list of nodes/branches where a Finally, there was a statistically significant phylogenetic sig-
significant shift in diversification rate was detected is probably nal in the genus richness during ant evolution. The fit of a null
not exhaustive, and more refined phylogenetic information, par- model in which diversity was independent of the phylogenetic
ticularly within the most diverse genera, might provide even more relationships among the genera (ln lik = −264.846) was signifi-
instances. It is important to note that several of the nodes/branches cantly poorer than a model in which phylogenetic autocorrelation
identified above are nested within each other. The interpretation was allowed (ln lik = −259.083) according to a likelihood-ratio
of these cases should be done with caution, given that it is often test (P = 0.00068), with the maximum-likelihood estimate of λ
unclear how to discriminate between diverse subclades causing being estimated as 0.267.
apparent significant diversification shifts in its more inclusive
nodes, or whether a more complex series of radiations took place
sequentially. In fact, one should not expect that a shift in diversi- Discussion
fication place should necessarily occur on single nodes/branches. The simulations of the effects of an incomplete taxon sampling
The incremental evolution of key innovations could potentially on the reconstructed LTT plot clearly indicate that the suggested
take place over a longer period of time, so that nested shifts increase in ant diversification associated with the rise of flowering

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orate Wilson’s suggestion with respect to the unusual diversifi-

cation of Crematogaster and Pheidole (Table 1). However, the
Camponotus radiation appears to be more complex, with its on-
set predating its divergence with Polyrhachis. Moreover, several
other cases of radiation within the family have been identified
(Fig. 2, Table 1). The evolutionary causes underlying these events
clearly deserve to be addressed in more detail by future studies.
Although the phylogeny used here does not represent a ran-
dom sample of ant species, but rather an overdispersed one, the
differences between the two at this level of sampling are likely
very minor, at least for simple models of diversification. In both
cases, most of older nodes are reconstructed. This point is clear in
Nee and May’s (1997) study of the effect of Raup’s (1973) “field
of bullets” extinction scenario on tree shape; one needs only to
Figure 3. Relationship between the age and the diversity of ant substitute sampling for extinction.
genera. Divergence times were obtained from the phylogeny pro- There is an apparent incongruence between some of our main
vided by Moreau et al. (2006). results. The LTT simulations and the analysis of the fossil record
seem consistent with a fairly constant diversification rate over
plants proposed by Moreau et al. (2006) is most likely artifactual. time, yet the SG tests and the ML method of Rabosky et al. (2007)
Indeed, when a sample of the above-mentioned phylogenies was showed statistically significant evidence for heterogeneity in di-
subject to the same analysis as Moreau et al. (2006), model A versification rates among clades, thus raising the question: was
(constant diversification) was always erroneously rejected in def- the diversification rate constant or variable during ant evolution?
erence to models B (changing diversification through time based We provide two hypotheses to explain this discrepancy. First, one
on a Weibull distribution) and C (two diversification rates divided should recognize that there are two axes on a tree, allowing for
by a breakpoint) (<χ2A,C > = 99.7; <χ2A,B > = 157.9; N = 20 different patterns when one looks at variation over time or across
simulations). Similar effects of an incomplete taxon sampling on clades, such that the existence of a considerable variation in diver-
LTT plots have been shown previously (e.g., Nee et al. 1994), and sification among clades can be reconstructed as a constant overall
might in fact point to the opposite conclusion, i.e., a relatively rate through time (Mooers and Heard 1997). Moreover, there is an
constant rate of diversification throughout ant evolutionary his- important fact that is frequently overlooked in this kind of anal-
tory. This proposition is consistent with the known fossil record ysis, namely that a statistically significant shift in diversification
in ants. Although ant representation in the oldest Lagerstätte such rate does not necessarily imply that the shift was positive. In fact,
as the Upper Cretaceous amber of the Kheta Formation is minis- even though there are several terms associated with positive shifts
cule (0.001% of all insects), that proportion increased steadily in diversification rates (e.g., adaptive radiation, key innovations),
over time, reaching 40% of all insects in the Ranzano Forma- no corresponding well-established terms for negative shifts are
tion in the Oligocene (see Grimaldi and Agosti 2000 for a recent present in the literature. A negative shift in diversification rate
review). In fact, when the relative proportion of ants in the dif- should have an effect similar to background extinction, given
ferent Lagerstätten reviewed by Grimaldi and Agosti (2000) is that, over time, those lineages would tend to be eliminated from
compared, there is a statistically significant linear increase over the reconstructed phylogeny. Negative shifts seem widespread
time (N = 10, r2 = 0.8, P = 0.0004). This result indicates that during ant evolution and might be associated with limited ecolog-
the bulk of ant diversification took place in the Eocene onward, ical flexibility or geographical range. This area clearly requires
a result that is also consistent with the molecular phylogeny of more extensive methodological and conceptual developments be-
Brady et al. (2006). fore one can recognize the relative importance of positive versus
Forty years ago, Wilson (1976) singled out three ant genera— negative diversification rates.
Pheidole, Crematogaster, and Camponotus—as the most preva- It has been recently suggested that differences in species
lent in the world based on four criteria: species diversity, extent numbers among clades result predominantly from variation in
of geographical range, diversity of adaptation, and local abun- their age rather than from their diversification rates (Mayhew
dance. The reason for their prevalence, however, would not be 2007; McPeek and Brown 2007; but see Magallón and Sanderson
based on any physical or behavioral trait, but rather on their 2001; Mayhew 2002) or from external forces, such as lithospheric
“ability to avoid competitive replacement by other prevailing complexity and the frequency of vicariance events (Cracraft 1982,
groups” (Wilson 1976). The results of the present study corrob- 1985). The patterns inferred in the present study are inconsistent

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with either of the above-mentioned suggestions. First, there is no Cracraft, J. 1982. A non-equilibrium theory for the rate-control of speciation
association between genus age and its species richness (Fig. 3). and extinction and the origin of macroevolutionary patterns. Syst. Zool.
31:348–365.
Moreover, there is strong evidence for a phylogenetic signal in
———. 1985. Biological diversification and its causes. Ann. Mo. Bot. Gard.
diversification patterns, suggesting the existence of heritability of 72:794–822.
diversification potential over evolutionary time, either in terms of Fittkau, E. J., and H. Klinge. 1973. On biomass and trophic structure of the
speciation rate or extinction risk. Such heritability is often implied central Amazonian rain forest ecosystem. Biotropica 5:2–14.
in macroevolutionary studies (e.g., Heard 1996), but little direct Gittleman, J. L., and A. Purvis. 1998. Body size and species richness in
carnivores and primates. Proc. R. Soc. Lond. B 265:113–119.
evidence has been available to date to support it (e.g., Lovette Grimaldi, D., and D. Agosti. 2000. A formicine in New Jersey Cretaceous
et al. 2001; Moyle et al. 2009). amber (Hymenoptera: Formicidae) and early evolution of the ants. Proc.
Why should there be a phylogenetic signal in diversification Natl. Acad. Sci. USA 97:13678–13683.
patterns? Savolainen et al. (2002) indicated two general classes of Harvey, P. H., A. J. Leigh Brown, J. Maynard Smith, and S. Nee. 1996. New
uses for new phylogenies. Oxford Univ. Press, Oxford.
possible explanation. First, there is a tendency for the habitat in
Heard, S. B. 1996. Patterns in phylogenetic tree balance with variable and
which a clade diversifies to be “heritable” over evolutionary time, evolving speciation rates. Evolution 50:2141–2148.
amplifying or reducing the diversification potential of that clade. Hölldobler, B., and E. O. Wilson. 1990. The ants. Harvard Univ. Press,
Second, diversification rates might depend on organismal traits Cambridge.
Isaac, N. J. B., K. E. Jones, J. L. Gittleman, and A. Purvis. 2005. Correlates of
(e.g., body size, mutation rates) that are themselves heritable over
species richness in mammals: body size, life history, and ecology. Am.
evolutionary time. The former hypothesis does not appear to play Nat. 165:600–607.
a role at the phylogenetic level of our study, given that species-rich Katzourakis, A., A. Purvis, S. Azmeh, G. Rotheray, and F. Gilbert. 2001.
and species-poor are largely sympatric throughout the world. The Macroevolution of hoverflies (Diptera: Syrphidae): the effect of using
second hypothesis seems more plausible in the case of ants, yet higher-level taxa in studies of biodiversity, and correlates of species
richness. J. Evol. Biol. 14:219–227.
the biological traits favoring diversification, either by increasing
Kirkpatrick, M., and M. Slatkin. 1993. Searching for evolutionary patterns in
speciation or reducing extinction, are unclear. The phylogenetic the shape of a phylogenetic tree. Evolution 47:1171–1181.
distribution of obvious traits such as foraging strategy, colony Lovette, I. J., E. Bermingham, and R. E. Ricklefs. 2001. Clade-specific mor-
size, and caste polymorphism do not seem to correlate directly phological diversification and adaptive radiation in Hawaiian songbirds.
Proc. R. Soc. Lond. B 269:37–42.
with species richness. A large-scale comparison of the degree of
Magallón, S., and M. J. Sanderson. 2001. Absolute diversification rates in
evolutionary heritability of different organismal traits across ant angiosperm clades. Evolution 55:1762–1780.
evolution is fundamental to clarify this issue. Mayhew, P. J. 2002. Shifts in hexapod diversification and what Haldane could
have said. Proc. R. Soc. Lond. B 269:969–974.
———. 2007. Why are there so many insect species? Perspectives from fossils
ACKNOWLEDGMENTS and phylogenies. Biol. Rev. Camb. Philos. Soc. 82:425–54.
We thank E. A. B. Almeida, M. V. Domingues, R. P. Freckleton, and W. A. McPeek, M. A., and J. M. Brown. 2007. Clade age and not diversification
Boeger for helpful comments on previous versions of this manuscript. rate explains species richness among animal taxa. Am. Nat. 169:E97–
E106.
Mooers, A. O., and S. B. Heard. 1997. Inferring evolutionary process from
phylogenetic tree shape. Quart. Rev. Biol. 72:31–54.
LITERATURE CITED ———. 2002. Using tree shape. Syst. Biol. 51:833–834.
Agosti, D., and N. F. Johnson. Eds. 2005. Antbase. World Wide Web electronic Moreau, C. S., C. D. Bell, R. Vila, S. B. Archibald, and N. P. Pierce. 2006.
publication. antbase.org, version (05/2005). Phylogeny of the ants: diversification in the age of angiosperms. Science
Astruc, C., J. F. Julien, C. Errard, and A. Lenoir. 2004. Phylogeny of ants 312:101–104.
(Formicidae) based on morphology and DNA sequence data. Mol. Phy- Morrow, E. H., T. E. Pitcher, and G. Arnqvist. 2003. No evidence that sex-
logent. Evol. 31:880–893. ual selection is an ‘engine of speciation’ in birds. Ecol. Lett. 6:228–
Baroni Urbani, C., B. Bolton, and P. S. Ward. 1992. The internal phylogeny 234.
of ants. Syst. Entomol. 17:301–329. Moyle, R. G., C. E. Filardi, C. E. Smith, and J. Diamond. 2009. Explosive
Barraclough, T. G., S. Nee, and P. H. Harvey. 1998. Sister-group analysis in Pleistocene diversification and hemispheric expansion of “great specia-
identifying correlates of diversification. Evol. Ecol. 12:751–754. tor”. Proc. Natl. Acad. Sci. USA 106:1863–1868.
Beck, L. 1971. Bodenzoologishe Gliederung und Charakterizierung des ama- Nee, S., and R. M. May. 1997. Extinction and the loss of evolutionary history.
zonishen Regenwaldes. Amazoniana 3:69–132. Science 278:692–694.
Brady, S. G. 2003. Evolution of the army ant syndrome: the origin and long- Nee, S., R. M. May, and P. H. Harvey. 1994. The reconstructed evolutionary
term evolutionary stasis of a complex of behavioral and reproductive process. Philos. Trans. R. Soc. Lond. B 344:305–311.
adaptations. Proc. Natl. Acad. Sci. USA 100:6575–6579. Nee, S., A. O. Mooers, and P. H. Harvey. 1992. The tempo and mode of
Brady, S. G., T. R. Schultz, B. L. Fisher, and P. S. Ward. 2006. Evaluating evolution revealed from molecular phylogenies. Proc. Natl. Acad. Sci.
alternative hypotheses for the early evolution and diversification of ants. USA 89:8322–8326.
Proc. Natl. Acad. Sci. USA 103:18172–18177. Ouellette, G. D., B. L. Fisher, and D. J. Girman. 2006. Molecular systematics
Brown, W. L. 1954. Remarks on the internal phylogeny and subfamily classi- of basal subfamilies of ants using 28S rRNA (Hymenoptera: Formici-
fication of the family Formicidae. Insect. Soc. 30:21–31. dae). Mol. Phylogenet. Evol. 40:359–369.

EVOLUTION NOVEMBER 2009 3029

B R I E F C O M M U N I C AT I O N

Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature Saux, C., B. L. Fisher, and G. S. Spicer. 2004. Dracula ant phylogeny as in-
401:877–884. ferred by nuclear 28S rDNA sequences and implications for ant system-
Paradis, E. 1997. Assessing temporal variations in diversification rates from atics (Hymenoptera: Formicidae: Amblyoponinae). Mol. Phylogenet.
phylogenies: estimation and hypothesis testing. Proc. R. Soc. Lond. B. Evol. 33:457–468.
264:1141–1147. Sanderson, M. J., and M. J. Donoghue. 1994. Shifts in diversification rate with
———. 2003. Analysis of diversification: combining phylogenetic and taxo- the origin of angiosperms. Science 264:1590–1593.
nomic data. Proc. R. Soc. Lond. B 270:2499–2505. Savolainen, V., S. B. Heard, M. P. Powell, T. J. Davies, and A. O. Mooers.
Paradis, E., J. Claude, and K. Strimmer. 2004. APE: analyses of phylogenetics 2002. Is cladogenesis heritable? Syst. Biol. 51:835–843.
and evolution in R language. Bioinformatics 20:289–290. Slowinski, J. B., and C. Guyer. 1993. Testing whether certain traits have
Phillimore, A. B., R. P. Freckleton, C. D. L. Orme, and I. P. F. Owens. 2006. caused amplified diversification: an improved method based on a model
Ecology predicts large-scale patterns of phylogenetic diversification in of random speciation and extinction. Am. Nat. 142:1019–1024.
birds. Am. Nat. 168:220–229. Ward, P. S., and S. G. Brady. 2003. Phylogeny and biogeography of the
Phillimore, A. B., C. D. L. Orme, R. G. Davies, J. D. Hadfield, W. J. Reed, ant subfamily Myrmeciinae (Hymenoptera: Formicidae). Invert. Syst.
K. J. Gaston, R. P. Freckleton, and I. P. F. Owens. 2007. Biogeographical 17:361–386.
basis of recent phenotypic divergence among birds: a global study of Wilson, E. O. 1976. Which are the most prevalent ant genera? Stud. Entomol.
subspecies richness. Evolution 61:942–957. 19:187–200.
Rabosky, D. L., S. C. Donnellan, A. L. Talaba, and I. J. Lovette. 2007. Ex- ———. 1987. Causes of ecological success: the case of the ants. the sixth
ceptional among-lineage variation in diversification rates during the Tansley Lecture. J. Anim. Ecol. 56:1–9.
radiation of Australia’s largest vertebrate clade. Proc. R. Soc. Lond. Ser. ———. 1990. Success and dominance in ecosystems: the case of the social
B 274:2915–2923. insects. Ecology Institute, Oldendorf-Luhe.
Rambaut, A. 2002. PHYL-O-GEN: phylogenetic tree simulator package. Wilson, E. O., and B. Hölldobler. 2005. The rise of ants: a phylogenetic
Version 1.1. Available at: http://evolve.zoo.ox.ac.uk/software.html? and ecological explanation. Proc. Natl. Acad. Sci. USA 102:7411–
id=phylogen 7414.
Raup, D. M. 1993. Extinction: bad genes or bad luck? Oxford Univ. Press,
Oxford. Associate Editor: A. Mooers

3030 EVOLUTION NOVEMBER 2009