Annu. Rev. Entomol. 2002. 47:733–71
Copyright c ? 2002 by Annual Reviews. All rights reserved
THE ECOLOGY AND EVOLUTION OF ANT
ASSOCIATION IN THE LYCAENIDAE (LEPIDOPTERA)
Naomi E. Pierce,1Michael F. Braby,1Alan Heath,2
David J. Lohman,1John Mathew,1Douglas B. Rand,1
and Mark A. Travassos1
1Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts
02138; e-mail: firstname.lastname@example.org; email@example.com;
firstname.lastname@example.org; email@example.com; doug firstname.lastname@example.org;
2Department of Zoology, University of Cape Town, Rondebosch 7700, South Africa;
myrmecophily, parasitism, butterfly, symbiosis, biogeography
of all Papilionoidea. The majority of lycaenids have associations with ants that can be
pae employ complex chemical and acoustical signals to manipulate ants. Cost/benefit
of obligately associated groups. Parasitism typically arises from mutualism with ants,
and entomophagous species are disproportionately common in the Lycaenidae com-
pared with other Lepidoptera. Obligate associations are more common in the Southern
has played in the evolution of the Lycaenidae.
The estimated 6000 species of Lycaenidae account for about one third
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 734
Variation in Lycaenid-Ant Associations: Definition of Terms . . . . . . . . . . . . . . . . . 734
Entomophagy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 737
MECHANISMS OF INTERACTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 737
Chemical Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 738
Acoustic Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 743
COSTS AND BENEFITS OF LYCAENID-ANT INTERACTIONS . . . . . . . . . . . . . 745
Effects of Ant Association on Host Plant Choice . . . . . . . . . . . . . . . . . . . . . . . . . . . 746
Ants as a Template for Butterfly Diversification . . . . . . . . . . . . . . . . . . . . . . . . . . . . 747
ENTOMOPHAGY AND ANT ASSOCIATION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 748
PIERCE ET AL.
Phylogenetic Distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 748
From Mutualism to Parasitism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 753
Evolutionary Constraints on Entomophagy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 753
BIOGEOGRAPHIC DISTRIBUTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 754
Zoogeographical Patterns in Ant Association . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 754
Phylogenetic Patterns in Ant Association . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 755
Origin and Evolution of Ant Association . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 758
CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 759
The estimated 6000 species of Lycaenidae account for about one third of all
Papilionoidea (1,55,208,226). Full or partial life histories have been recorded
for about 20% of these species, and of those whose full life histories are known,
about 75% [(N=665 (Table 1)] associate with ants (95,139,181). These associa-
associations), to complex obligate associations in which larvae are always tended
by ants, often by only a single species (30%) (Table 1). Even when lycaenids
are not myrmecophilous, they may be protected against ant aggression by a suite
of ant-associated adaptations. The Lycaenidae are additionally characterized by
striking life history diversity. Herbivorous species consume an unusually wide
array of different plant families (10,80), and a small number of lycaenids (∼3%
of all associations or 12% of obligate ant associations) are parasitic or predatory
ticularly amenable to comparative studies of life history evolution. Colonel John
N. Eliot laid the groundwork for such research in 1973 by providing what he des-
cribed as a “tentative arrangement” of the higher classification of the Lycaenidae
(83). He later revised this scheme to comprise the five subfamilies we recog-
nize in our treatment here: the Riodininae, Curetinae, Poritiinae, Miletinae, and
Lycaeninae (44,84; Figure 1). A molecular study by Campbell and colleagues
(35) corroborated the broad outlines of Eliot’s hypothesis. The Riodininae form a
monophyletic group and are sometimes considered a separate family (124); they
are the sister taxon to the remaining four subfamilies, which together are mono-
phyletic relative to outgroups from the Nymphalidae (35). For convenience, we
refer to the latter collectively as Lycaenidae sensu stricto (s.s.).
Variation in Lycaenid-Ant Associations: Definition of Terms
Various workers (77,95,104,139,153,154,181) have categorized the degree of
lycaenid-ant associations into three broad types: obligate, facultative, and non-
ant associated. Gray areas between these categories occur, and interpretations
of facultative and obligate have varied. For clarity, we define these interactions
ant-associated species within each lycaenid taxonomic group
(subfamilies and tribes)
The number and proportion (in parentheses) of
Taxonomic groupN Obligate FacultativeNone
Records compiled primarily from (17,21,22,24,39,41,43,44,48,53,70,74,77,79,89,
183,190,195,199,203,205,236,238), and numerous journal articles of single taxa. Doubtful
and hypothetical records such as predictions based on associations of closely related species
are excluded, and information for Riodininae are not included (see text).
as follows and use the term entomophagy to describe the feeding behaviors of
with ants during at least some portion of the life cycle and are dependent on ants
for survival under field conditions. These include both mutualistic and parasitic
only a single species or genus of ant.
Facultative associations are those in which lycaenid larvae are found only in-
termittently associated with ants, either spatially or temporally, and do not require
attendant ants for survival under field conditions. Associations are nonspecific:
Larvae of a particular lycaenid may associate with ants from numerous species,
each partner benefiting from the presence of the other. However, a few species
are facultatively predaceous, occasionally consuming the ants that normally tend
them (e.g., 130).
PIERCE ET AL.
Non-ant-associated, or mymecoxenous, lycaenids are characterized by the ab-
sence of apparent associations with ants. The term myrmecoxenous underscores
the notion that, unlike most lepidopterans, larvae of these lycaenids possess ant-
related adaptations that protect them against aggression, even if they are not ac-
tively tended. Kitching & Luke (153) coined the term to describe species lacking
a specific ant-associated organ, the dorsal nectary organ (see below), but we use
it in a broader sense to describe lycaenids not tended by ants. Chemical defense
from exocrine glands, hairiness, thickness of larval cuticle, and/or construction of
Like other Lepidoptera, the great majority of lycaenid larvae feed exclusively on
living plant tissue. However, some use insect-derived food resources during all or
part of their development. These include (a) ant eggs, larvae and pupae (myrme-
cophagy), (b) ant regurgitations (trophallaxis), (c) Homoptera (homopterophagy),
(d) homopteran honeydew, and (e) other lycaenid larvae (facultative cannibalism
too general when applied to species that supplement an otherwise phytophagous
diet with a nonplant resource or that switch from phytophagy to aphytophagy
between instars. Carnivory is likewise a limited descriptor, as it excludes food
sources such as regurgitations from trophallaxis and homopteran honeydew. We
instead use the term entomophagous for any species that depends on some insect-
derived resource other than plant tissue at some point during its larval phase.
MECHANISMS OF INTERACTION
Ant association has exerted strong selection on lycaenid larval morphology. Pre-
sumably as a defense against ant bites, the cuticle of lycaenid larvae can be up to
20 times thicker than that of larvae from other lepidopteran families, and the head
can be retracted under a sclerotized prothoracic plate (164,165). Lycaenid larvae
also have a much reduced thrashing response in the presence of ants (164,165).
provoke the attention and aggression of ants (240).
DeVries (59) called the strategic deployment of ant-associated organs “entice-
← − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − − −
Phylogeny of the Lycaenidae as proposed by Eliot (83), modified in ac-
cordance with Eliot’s subsequent taxonomic revisions (44), and including Harvey’s
treatment of the Riodininae (taxonomic ranks adjusted; dashed lines indicate groups
not thought to be monophyletic) (124) with modification from Penz & DeVries (177).
PIERCE ET AL.
and maintaining ant associations. Most of these adaptations are found in larvae
and pupae, but adults also engage in complex interactions with ants. Lycaenids
manipulate ant behavior in at least three ways: suppression of ant aggression,
maintenance of a “standing guard,” and ant-mediated defensive measures. In ad-
dition to more general adaptations, lycaenids possess two highly specialized sets
of organs used in interactions with ants: those involved in chemical mediation and
those involved in acoustical mediation. For simplicity, we discuss each of these
separately, recognizing that they typically function in concert with each other.
Pore cupola organs
(PCOs) are found on the larvae of every lycaenid species yet examined, except
ficially resemble the much smaller lenticles found on some hesperiid caterpillars
(116), there is little evidence of structural or functional homology. Lycaenid PCOs
may secrete substances to pacify ants that might otherwise attack the soft-bodied
abled ancestral lycaenids to benefit from enemy-free space in the presence of ants
Single-celled epidermal glands called pore cupola organs
the eighth abdominal segment secretes volatile substances that attract and alert
ants if a caterpillar is alarmed (11,38,95,106,132). These organs are also found
in the Curetinae where they are enlarged, occur more centrally on the dorsum, and
may confer mechanical defense (56). In the Miletinae, only species in the genus
Aslauga possess TOs.
In the Lycaeninae, an eversible pair of tentacle organs (TOs) on
organ (DNO) on the seventh abdominal segment produces nutritious secretions
for ants and plays a critical role in the maintenance of ant/lycaenid mutualisms
(11,160,174). It has been called the honeydew gland by analogy with the excre-
ment of homopterans, but it is in fact a specialized exocrine gland (165).
Apparent losses of TOs and the DNO are found throughout the Lycaenidae
and are often correlated with reduced ant association. For example, larvae in the
entomophagous subfamily Miletinae lack a DNO, and all but those in the genus
Aslauga lack TOs as well. They are nonetheless ignored by the ants tending the
Homoptera on which they feed, suggesting that the PCOs may appease ants in this
group (48) and perhaps in the whole family.
Restricted to species in the Lycaeninae, the dorsal nectary
function is unknown. (b) Dish organs: Clark & Dickson (41) described saucer-like
glands located dorsally on the fifth segment of the final instar larvae of Spindasis
et al. (67) noted that the larvae of species of Curetis possess unusual epidermal
organs of unknown function located laterally on the first thoracic segment and the
unusual structures on the larva of the miletine Allotinus major and, in particular,
noted the presence of ovoid flattened organs scattered along the central axis of the
larva and clustered in groups of 20 or more on lateral discs near the posterior end.
Ants showed great interest in these areas, and Kitching proposed that these organs
might be of special significance in the Miletinae.
Riodinine ant organs
been described from three relatively derived ant-associated subtribes [Eurybiiti,
Lemoniiti, and Nymphidiiti (63,124)]. Recent phylogenetic work by Penz &
DeVries (177), however, shows that the Lemoniiti are rooted within the
Nymphidiiti, so the three groups collapse to two, the Eurybiiti and Nymphidiiti.
Nutritious droplets are secreted from paired tentacle nectary organs (TNOs) on
the eighth abdominal segment, while paired anterior tentacle organs (ATOs) on
the third thoracic segment presumably emit volatile compounds (63). Differences
in the location and structure of ant-associated glands between riodinines and their
sister taxa have been cited as evidence for convergence of both form and function
(61). In view of the evolutionary importance of tagmatization in arthropods, how-
ever, and the ease of switching between segment identities, it is possible that these
organs are homologous (34).
Ant associations in the Riodininae have traditionally
SUPPRESSION OF ANT AGGRESSION
some data (3,132,134) suggest that lycaenid larvae suppress ant aggression in
part by mimicking aspects of the pheromones of ant brood. Attendant ants lick
and antennate lycaenid larvae much as they do their own brood. The substance(s)
responsible in both cases is widely dispersed over the cuticle and relatively non-
volatile, persisting for several days after death (27,106,113,182,234). The larvae
of parasitic inquiline lycaenids are often deposited by workers in the brood cham-
ber of the ant nest alongside the immature ants (217,219).
Henning (132,134) showed that the lycaenids Aloeides dentatis and Lepido-
chrysops ignota chemically mimic the brood of their respective attending ants
(3) demonstrated that larvae of the lycaenid Maculinea rebeli produce a profile of
hydrocarbon compounds sufficiently similar to that of Myrmica schencki ant lar-
vae to induce M. schencki workers to carry M. rebeli larvae into their nests, where
the caterpillars eat the brood. They showed that after seven days inside the nest,
became nearly perfect chemical mimics of the ant brood.
Much discussion (48,88,106,164,182) and
PIERCE ET AL.
Some authors nevertheless doubt the existence of brood pheromones in ants
(169,224). Ants can clearly differentiate brood from workers and discriminate
among different types of brood (e.g., worker-biased larvae, queen-biased larvae,
worker pupae) (161). The experimental problem is to distinguish between a feed-
ing response in which an object is carried into the brood chamber from a simi-
lar response elicited by an object coated with brood pheromone. This remains a
weakness of all published studies on lycaenids (3,132,134). Nevertheless, recent
studies (156,221) have demonstrated that cuticular hydrocarbons communicate
colony membership in worker ants, and hydrocarbons may serve a related purpose
in labeling ant brood in some as-yet-unknown way.
Even if cuticular hydrocarbon matching is responsible for suppressing ant ag-
gression toward lycaenid immatures, it remains to be seen whether PCOs are
involved in their production. While PCOs are unique to lycaenid immatures, cu-
ticular hydrocarbons are ubiquitous among insects as they serve essential roles in
waterproofing and osmoregulation (120,172).
MAINTENANCE OF A “STANDING GUARD” OF ANTS
tending caterpillars may depend on the mode of appeasing ant aggression (such
as ant brood chemical mimicry) but may also relate more directly to the quantity
and quality of nutritive rewards offered to ants. Lycaenids producing particularly
valuable secretions would be expected to maintain a larger cadre of dominant,
aggressive attending ants than those producing less valuable secretions, as seen in
The nutritive rewards secreted by immatures of several lycaenid species have
been analyzed chemically. Maschwitz et al. (167) found carbohydrates (13–19%)
and trace amounts of methionine from the DNO secretion of the facultative ant
associate, Lysandra hispana. Pierce (182,188) also found carbohydrates to be an
important component of the DNO secretions of the Australian lycaenid, Jalmenus
evagoras, making up about 10% dry weight. These secretions also contained at
least 14 different free amino acids, particularly serine, in concentrations ranging
from 20 to 40 mM, depending on the time of day (188). DeVries found that
TNO secretions from the riodinine Thisbe irenea contain at least 18 amino acids,
with glutamine and glycine predominating, and small amounts of sugars (<0.5%)
Behavioral assays indicate that host plant quality can affect the secretions from
the field than counterparts feeding on low-quality unfertilized plants, and females
also preferred to lay eggs on these high-quality plants.
Lycaenid larvae can manipulate their attendant ants by strategically varying the
defenses in plants (2). When under a perceived threat (a pinch from forceps),
The persistence of ants in at-
larvae of both Polyommatus icarus (160) and Plebejus acmon (2) secrete more
rewards and/or attractants from the DNO and thereby attract a greater number of
attendant ants. Individual larvae of J. evagoras also regulate secretions depending
each does when alone (12). Beyond a threshold number of ant guards, the benefit
from producing metabolically expensive secretions may have diminishing returns
Wada and colleagues (228) found that the DNO secretions of the parasitic
larvae of Niphanda fusca fed by worker trophallaxis in the nest contain high titres
of glucose and glycine. Recordings from the taste receptors of the attendant ant
glycine when combined with glucose made these solutions much more attractive
to attendant ants.
Eavesdropping on ant trail pheromones has been demonstrated in the behav-
ior of Euliphyra mirifica and Euliphyra leucyana, which are parasites of arbo-
real weaver ants, Oecophylla longinoda (54). Adult females of a close relative,
L. brassolis, typically lay eggs on foliage adjacent to established nests of Oeco-
phylla smaragdina. The first instars probably locate the ant nests by following ant
trail pheromones. Larvae must also move between nests after they have consumed
the brood within a nest or whenever host ants abandon old nests and construct new
ANT-MEDIATED DEFENSE TACTICS
behavior following this signal is similar to that released by ant alarm pheromone.
Mimicry of an ant’s alarm pheromone has been documented in the Australian
spider Habronestes bradleyi, which uses the chemical to disorient its ant prey,
Iridomyrmex purpureus (5).
and often the same chemical provokes an alarm response in species from different
mimic might communicate the need for protection with multiple ant species. Ant
alarm pheromones and TO/ATO pheromones are highly volatile, which makes
pheromone collection for chemical analysis difficult. Henning (132), however,
succeeded in extracting the posterior half of Aloeides dentatis (which contains the
TOs) in dichloromethane, and these extracts elicited an alarm response from at-
tending ants in bioassays. These ants responded similarly when presented with
dichloromethane extracts from conspecific mandibular glands, which produce
alarm pheromones in several ant species (25,142).
Myrmecophilous lycaenid caterpillars can sig-
philous Lycaenidae, or if they do, treat them much as they would any insect
prey. For example, among species of Chrysoritis and Thestor, adults are killed
Ant workers frequently do not interact with the adults of myrmeco-
PIERCE ET AL.
and eaten if they fail to escape from their corral or byre on eclosion. Species
that eclose inside ant shelters are frequently cloaked in “eclosion wool,” a layer
of deciduous scales that slough off in an ant’s mandibles and tarsi, enabling
the teneral adult to slip away. Nevertheless, several observations suggest that
chemical interactions between adults and ants may be more complex than cur-
rently appreciated, and some adults may appease ants that would otherwise attack
of Anoplolepis longipes tending larvae of Curetis regula were keenly interested in
the adults, palpating them with their antennae and appearing to feed near the base
of the butterfly’s extended proboscis. Larvae of the Australian species Ogyris gen-
teneral adults harden their wings in this shelter without harassment (75). Oviposit-
ant, Oecophylla smaragdina, but workers cease attacking once a female has begun
laying eggs perhaps because the eggs release an appeasement pheromone (109).
ants may also be used as mating and oviposition cues. Males of the Australian
species J. evagoras use ants as cues in finding available females (82). The females
of a number of myrmecophilous lycaenids use attendant ants as oviposition cues
(9,108,109,132,185,209,232). The great majority of these are species with obli-
gate ant association (e.g., 185), although some are facultatively associated (232).
Significantly from the point of conservation practices, experiments have failed
to find ant-dependent oviposition not only among females of facultative species
ever, analyses taking into account host plant phenology, intraspecific competition
in egg deposition, and location of ant nests show that ant-dependent oviposition
may occur in at least one species, Maculinea alcon, but simply be difficult to de-
tect experimentally (225). Differences in adoption times depending on ant hosts
have been measured for caterpillars from separate populations of M. alcon (6),
and genetically differentiated populations of this species are suggestive of host ant
Females from populations of J. evagoras show a remarkable degree of speci-
ficity in ant-dependent oviposition, preferring to lay eggs in response to cues
from their natal ant population rather than other populations of ants of the same
infested host plants (82,117,185). A number of ant-associated insects locate ants
through ant trail pheromones (4,33,54), which the chemosensory structures in the
antennae and ovipositors of adult female lycaenids may likewise be capable of
Most sound production in the Lepidoptera has evolved in response to selection on
sexual or defensive traits (90); juvenile sound production in the Lycaenidae also
mediates associations with ants.
PUPAL SOUND PRODUCTION: MECHANISMS AND DISTRIBUTION
produce sound by a mechanism that is widespread among lepidopteran pupae:
stridulation, the act of grating a file lined with teeth against a hardened plate
(71). In lycaenids, the file-and-scraper organ is found in the intersegmental region
between abdominal segments 4–5, 5–6, or 6–7.
Lycaenid pupae can give three distinct signals (73,141). A primary signal,
often produced by stimulation of the pupa, is detectable without amplification. A
secondary signal is of lower amplitude, consisting of a set of clicks produced in
A pupal stridulatory organ has been found in every lycaenid pupa examined
(72,81), including both ant-associated and non-ant-associated taxa. This includes
ten species of riodinine pupa in the tribe Hamearini and five subtribes of the
Riodinini. Each of these riodinine pupae possesses two sets of file-and-scraper
stridulatory organs, located between abdominal segments 4–5 and 5–6.
PUPAL SOUND PRODUCTION: FUNCTION
turbed, and Downey & Allyn (73) concluded that calls act primarily as a deterrent
to predators and parasites. Travassos & Pierce (222) showed that pupal calling
is also involved in ant recruitment. In pairs of pupae of J. evagoras, where one
guard than their silent counterparts. Eastwood & King (78) observed that pupae
of the myrmecophage, Arhopala wildei, emitted a prolonged “burr” lasting sev-
eral seconds upon reintroduction to the ant nest. The pupae also oscillated with a
rapid dorso-ventral movement of the anterior end in a frequency that matched the
frequency with which the host ants tapped the substrate when alarmed.
DeVries (60) surveyed 26 species of pupae in the Riodininae but found no
evidence of pupal sound production. However, experiments conducted by Ross
(197) on Lemonia caliginea (=Anatole rossi) suggest that sound production in
organs, L. caliginea pupae possess a pair of glands on the metathoracic segment
that may produce a chemical attractive to ants (196). Ross found that a fast-drying
lacquer applied to either the paired metathoracic organs or the stridulatory organs,
that the stridulatory organs and metathoracic glands work in concert to attract and
maintain attendant ants.
Calls are induced when pupae are dis-
PIERCE ET AL.
LYCAENID SENSU STRICTO LARVAL SOUND PRODUCTION
(60), although larvae of Hemiargus isola have been recorded to start calling in
the second instar (D. Wagner, personal communication). In general, these calls
resemble a slow drumming compared with the faster chirps of the riodinines.
They travel primarily through the substrate, although they also have an airborne
component (60,201). DeVries (60) first noted that some lycaenid calls have two
signals: a low background sound accompanied by a constant pulse. Travassos &
Pierce (222) found that J. evagoras larvae produce three signals that differ in
acoustic properties and amplitudes: the grunt, drum, and hiss.
Hill (138) localized rapid trembling to abdominal segments five and six of
Arhopala madytus and described a file of teeth found on the posterior margin of
the fifth abdominal segment that rubs against an opposing plate on the anterior
margin of the sixth abdominal segment. A. madytus larvae thus produce calls with
a stridulatory organ similar to that found in lycaenid pupae, although the position
segments 4–7 when producing calls.
Because the organs for sound production in lycaenids remain poorly charac-
terized, we cannot determine how widespread they may be within the family. In
his sound production survey, DeVries (59,60) found that only myrmecophilous
lycaenids produce calls, and several non-ant-associated members of the Eumaeiti
are silent. However, since then, several non-myrmecophilous lycaenids have been
Caleta manovus (100), and Cheritra freja (98). Callophrys rubi, Curetis bulis, and
Curetis santana also produce sound, but accounts of whether ants attend these
species conflict (26 versus 113 and 56 versus 112). Fiedler (97) suggested that
the ability to produce calls may be universal in the Lycaenidae: Whereas non-
ant-tended lycaenids produce simple calls in response to a disturbance, ant-tended
lycaenids have calls of greater complexity that are produced more often.
DeVries (58), Fiedler (98), and D. Wagner (personal communication) observed
that lycaenid larvae produce sounds when disturbed, suggesting a defensive func-
tion. DeVries (60) argued that lycaenid calls, like riodinine calls, attract ants.
Travassos & Pierce (222) found that two calls produced by larvae of the lycaenid,
Moreover, the calls of Maculinea larvae and the stridulations of the Myrmica ants
they parasitize share the same pulse length and dominant frequency, suggesting
a convergence of caterpillar calls on those produced by host ants (66). Lycaenids
that form obligate associations with different ant species may have evolved dif-
ferent acoustic signals. Attendant ants are widely distributed phylogenetically,
including representatives from the subfamilies Myrmicinae, Dolichoderinae, and
Formicinae (77). Of these, only myrmicines are known to produce calls via stridu-
lation, whereas some dolichoderine and formicine ants produce vibratory signals
by drumming body parts on the substrate (142,166).
Lycaenids (s.s.) typically
LARVAL SOUND PRODUCTION IN RIODININAE
different mechanisms than from those of the Lycaenidae (s.s). Some riodinine
larvae have a pair of vibratory papillae on the distal edge of the prothorax, each
one bearing concentric grooves along its length (62). When a caterpillar oscillates
its head, epicranial granulations on the head slide across these grooves, producing
low-amplitude calls that travel solely through the substrate, unlike the airborne
caterpillars of T. irenea with those that had their papillae removed and found that
calling caterpillars were tended by more ants.
Riodinine larvae produce sound by
COSTS AND BENEFITS OF LYCAENID-ANT INTERACTIONS
Early studies of costs and benefits of lycaenid-ant interactions focused on the ben-
efits of the lycaenids, generating two nonexclusive hypotheses. The appeasement
hypothesis is simply that ant-associated lycaenid larvae (excluding those species
parasitic on host ants) benefit from not being attacked by ants. The food rewards
they provide attendant ants can be regarded as a kind of bribery (162,164,165).
The protection hypothesis argues that attendant ants guard lycaenid larvae against
predators and parasites, and in turn they are rewarded with nutritious secretions
in this way, although the importance of ant protection varies among species
(61,107,111,184,186,187,197,198,206,229–231; but see 178). This does not
preclude the possibility that ant-tended lycaenids also appease otherwise aggres-
sive ants and thereby inhabit enemy-free space (10).
Attendant ants can affect lycaenid development and/or reproductive success
(20,16,49,82,105,110,186,192,229,233). In mutualistic interactions, the cost
for this net benefit is sometimes meted out in terms of adult weight and size.
Larvae and pupae of J. evagoras tended by ants are considerably (25%) lighter
and smaller than experimental counterparts not tended by ants (186). Because size
and weight are determinants of female fecundity and male reproductive success in
J. evagoras (82), this size reduction represents a significant cost. Additional costs
can come in the form of increased apparency: Some parasitoids use chemical cues
from host ants to find their lycaenid prey (140,213).
Other lycaenids, such as the facultative Hemiargus isola (229) and the obli-
gate Paralucia aurifera (49), may compensate for the secretions they give up to
attendant ants. H. isola eclose at a heavier weight when tended by one species of
ant, and P. aurifera develop more quickly and gain more weight when tended by
ants perhaps because they spend more time feeding when tended. Some species
exhibit sex-specific effects during development, wherein one sex supports more of
the cost of the mutualism than the other. Thus, Polyommatus icarus males develop
relatively more quickly than their female counterparts when tended by ants (105),
and males of J. evagoras experience relatively less reduction in size than their
female counterparts when tended by ants (20).
PIERCE ET AL.
portion of their lifetimes have unusually variable development (183). Some have
prolonged developmental times, often overwintering as larvae in the nest (133),
some are variable with respect to overwintering (200), and others vary consider-
ably in final adult size (18,78). Elmes et al. (87) showed that phytopredaceous
lycaenids such as species of Maculinea and other parasites of ants also have un-
usual growth patterns between instars. The small, phytophagous early instars have
regular growth, but the entomophagous final instar has >10 times the growth pre-
patterns are similar to those exhibited by their Myrmica ant hosts.
studied; it has been assumed that ants receive a net nutritional benefit from har-
vesting secretions despite the metabolic cost of protecting caterpillars. However,
sometimes the ants do not benefit, as exhibited most dramatically by species that
parasitize host ants. More subtle forms of manipulation have been demonstrated
by the strategic, or inducible, nature of the rewards offered to ants by different
lycaenid species (2,12,160). Natural selection should favor strategies whereby it
is less expensive metabolically to fool ants into attendance while still receiving a
As described above, attendant ants are rewarded with nutritious secretions
access to lycaenid secretions (49,110,111). Queenright colonies of the attendant
ant Iridomyrmex rufoniger showed net gains in growth rate when their food was
supplemented with secretions from larvae of J. evagoras (171,188).
Effects of Ant Association on Host Plant Choice
Experimental cost/benefit studies of lycaenid-ant interactions have elucidated se-
suggested potential evolutionary repercussions that might be expected among ant-
Pierce (180) investigated whether ant-associated lycaenids that reward ants
with protein-rich secretions are also more likely to feed on legumes and other
protein-rich–host plant species. Similarly, Pierce & Elgar (185) assessed whether
of host plant taxa than those that do not. Fiedler subsequently re-examined these
and other patterns using many additional life history records (95,99,101–103).
With a number of conditional caveats, these two patterns of host plant use appear
to be supported when analyzed with larger data sets (101,99). Leguminous–host
obligately associate with ants use a wider range of host plants than lycaenids that
do not associate with ants.
However, none of these comparative studies has taken into account phylo-
genetic effects, in part because of our limited knowledge of the phylogeny of
the Lycaenidae, making the validity and/or functional significance of these pat-
terns impossible to evaluate. Additional information about the phylogeny of the
Lycaenidae will be necessary to identify appropriate independent contrasts (92) to
test hypotheses about the evolution of ant association and host plant use.
Ants as a Template for Butterfly Diversification
Attendant ants influence many aspects of lycaenid physiology, behavior, and
ecology. In obligately mutualistic lycaenids, overlapping requirements of suit-
able host plants and attendant ants can lead to population fragmentation and
small population sizes, thus promoting genetic divergence among populations
(10,45,46,114,149,179,206,209). The history of ant association may therefore
be reflected in the cladogenesis of ant-associated butterflies, and at least two lines
of evidence suggest that this is the case.
First, phylogenetic studies of four independent lineages of ant-associated ly-
caenids have shown that sister taxa typically share closely related ant associates:
Taxa within the Aphnaeini, Ogyriti, Zesiiti, and Luciiti all show phylogenetic
conservatism with respect to ant association. The genus Chrysoritis (Aphnaeini)
associates largely with Crematogaster ants (Myrmicinae). Other aphnaeines, in-
cluding species of Phasis and Tylopaedia, also associate with myrmicines. In con-
in the subfamily Formicinae, thereby forming distinctive clades within a largely
myrmicine-associated group (191,211).
Most strikingly, the species of the Australian genus Ogyris form several dis-
tinctive clades that correspond well with their ant affiliations. For example,Ogyris
ing Ogyris ianthis, Ogyris iphis, and Ogyris aenone associates with Dolichoderi-
nae; and the clade containing Ogyris oroetes, Ogyris olane, and Ogyris barnardi
has lost or greatly reduced association (N.E. Pierce, A.A. Mignault, G.S. Adelson,
R. Eastwood, D.J. Lohman, M. Blair & T. Itino, manuscript in preparation).
Within the Australian genus Jalmenus, a small group of closely related taxa
with the highly distinctive Iridomyrmex purpureus–species group and its close
A. myrmecophila and A. brisbanensis, associate with ants in the Dolichoderinae.
A speciation event associated with a host-ant shift to Myrmicinae occurred in the
ancestor of the clade containing the sister taxa Acrodipsas cuprea and Acrodipsas
aurata, which further gave rise to the five members of the illidgei species group.
Although the host ants of four species in this group are still unknown, the larvae
of Acrodipsas illidgei itself also feed on ants in the Mymicinae (76).
Just as shifts onto novel host plants may serve as a key adaptation that permits
diversification, shifts by lycaenids to chemically and behaviorally novel clades
PIERCE ET AL.
of ants may facilitate subsequent radiation. Note, however, that this evolutionary
relationship is asymmetrical. Whereas certain lycaenids are obligate in their de-
pendence on attendant ants, the reverse is not true; attendant ants have alternative
food sources in the field. Ants may be regarded as a template against which the
lycaenids have diversified but not vice versa.
A second line of evidence that ant associations may affect patterns of diver-
sification comes from a recent study of the genitalia of ant-associated and non-
ant-associated Lycaenidae. Heath (125) found a strong correlation between the
degree of ant association and the uniformity of male genital features. Species in
highly ant-associated genera have extremely uniform genitalia, whereas species
in non-ant-associated genera have widely divergent genitalia. Explanations of this
pattern include the possibility that myrmecophilous lycaenid species have diver-
sified more recently than their less-myrmecophilous sister groups. Alternatively,
adult male lycaenids may use ant associates as cues for finding mates (82), thus
relaxing any potential lock-and-key selection mechanism affecting their genitalic
complexity. Finally, ant cues may enable adult males of some lycaenid species to
find conspecific pupae so that females are mated immediately on eclosion, thereby
relaxing sexual selection via female choice (8).
ENTOMOPHAGY AND ANT ASSOCIATION
Obligate entomophagy appears throughout the entire subfamily Miletinae and
in small entomophagous clades and occasional species scattered throughout the
Lycaeninae and Riodininae (Table 2).
The Miletinae are entirely aphytophagous: Most species feed on Homoptera.
Exceptions include the obligate myrmecophiles in Liphyra and Euliphyra
(Liphyrini). L. brassolis has a tank-like morphology to repel ant attack and feeds
on the brood of O. smaragdina (48,69,165). E. mirifica subsists on regurgitations
from O. longinoda (54) and possesses a far thinner cuticle than Liphyra, its sister
The genus Thestor (Lachnocnemini), endemic to southern Africa, represents
one of the largest radiations within the Miletinae (∼29 spp.). Some species of
Thestor prey on coccids (40); trophallaxis and detritivory have also been recorded
Anoplolepis custodiens, and it has been suspected that most are likewise affiliated
with A. custodiens. However, it is unlikely that so many sympatric species could
simultaneously parasitize the same ant, leading to the as yet untested hypothesis
that A. custodiens consists of a constellation of sibling species.
A group that seems remarkably specific in its indirect host-ant affiliations is
the Miletini. Fiedler (103,104) proposes that species of Miletus and Logania may
maintain specific associations with ants in the Dolichoderinae and feed only on
ing Taraka, Spalgis, and Feniseca, likewise prey more frequently on homopterans
tended by ants in the Formicinae, although this could be because Formicinae are
more abundant in the habitats where these lycaenids live. Nevertheless, the ant
affiliations of these two clades hint at the possibility of a “ghost of ant-association
past”, and it is possible that associations with specific ants may have facilitated
prey location and exploitation by these groups. In contrast, other miletines feeding
only on Homoptera and/or honeydew are associated with a broad taxonomic range
of ants (Table 2).
Widespread entomophagy occurs in three tribes of the subfamily Lycaeninae:
ported by molecular analysis in some cases), there have been at least 20 indepen-
Most of these shifts appear either as single entomophagous species within phy-
tophagous clades or as small entomophagous genera (5–9 spp.) representing lim-
The primarily African tribe Aphnaeini exhibits several independent shifts to
entomophagy. Chrysoritis dicksoni, alone among the numerous species of its
genus, survives exclusively on trophallaxis from Crematogaster ants (41,48,126,
127,130). There are also some older records of trophallaxis by Axiocerces harpax
(146) and Chloroselas pseudozeritis umbrosa (145). Jackson (146) hypothesized
that more species within Axiocerses, Chloroselas, and Spindasis feed via trophal-
laxis or detritivory, based on the relatively small larval mouthparts in these three
genera. To date, however, life history studies have uncovered only one thor-
oughly entomophagous clade within the Aphnaeini. The genus Trimenia contains
five species that lack DNOs in the final instar and appear to be entomophagous
(41,48,129,130). Heath (125) suggests that Argyrospodes argyraspis is sister to
Trimenia and is likely to share similar characteristics.
Although the large (∼50 spp.) genus Aloeides was thought to be wholly phy-
tophagous, recent studies point to at least one shift to entomophagy. Aloeides
pallida grandis, which unlike many Aloeides species lacks a DNO in the final
instar, can survive for up to four months in Lepisiota (Formicinae) nests without
emerging to forage on host plants and can feed on ant eggs (130). A few other
species of Aloeides also lack a final-instar DNO, as does Phasis thero, although
entomophagy has not been directly observed in these species.
Several independent instances of entomophagy are found in different sub-
tribes of the Theclini, and these are concentrated in Australia. Arhopala wildei
genus (∼120 spp.). Larvae feed on the brood of their ant attendants, Polyrhachis
queenslandica, even as they feed the workers with DNO secretions (24, 151, 78).
probable origin of obligate entomophagy within a smaller genus (13 spp.) (24).
Finally, the Australian endemic genus Acrodipsas (Luciiti; 9+ spp.) represents the
only limited radiation of entomophagous theclines known to date. Larvae of five
PIERCE ET AL.
Lycaenid species with entomophagous life histories (24,48,63,65,68,76,95,125,
species (named if <3)
Ant associate (genus)Distribution
Aslauga (9 spp.)
Allotinus (6 spp.)
Lontalius (0 spp.)
Miletus (5 spp.)
L. brimo, L. durbani
T. protumnus, T. yildizae
A. cuprea, A. illidgei,
species (named if <3)
Ant associate (genus)Distribution
Aloeides pallida grandis
acamas, C. [Spindasis]
nyassae, C. [Spindasis]
Camponotus sp. Oriental/
Lepidochrysops (11 spp.)
Maculinea (6 spp.)
aNumber of known and/or presumed entomophagous species/total number of species in genus.
bBro, ant brood; Det, detritus; Eggs, ant eggs; Fung, algae, lichen and fungi; Hom, Homoptera; Hon, homopteran
honeydew; Phy, plants; Tro, ant trophallaxis.
PIERCE ET AL.
species feed on the brood of their dolichoderine or myrmecine ant hosts, and the
remainder are thought to have similar life styles (24,76).
As with the Aphnaeini and Theclini, the Polyommatini include a few phyloge-
netically isolated entomophagous species, as well as three entomophagous genera
that exhibit a uniquely phytopredaceous life history and shift their diet from plants
to ants during larval development: Maculinea, Lepidochrysops, and Phengaris.
The best known phytopredaceous lycaenids are those in the Palearctic genus
Maculinea (Polyommatiti: Glaucopsyche section) (6,42, 85–88, 114,119,200,
213–220, 225,235). The larvae feed on flower buds for the first few instars be-
fore being carried into Myrmica ant nests (or Aphaenogaster japonica in Japanese
populations of Maculinea arionides).
Most Maculinea species feed on ant brood, but two, the sister taxa M. alcon
and M. rebeli, feed from ant regurgitations alone. These “cuckoo” species do not
impose as great a fitness cost to the ant colony as those that prey directly on ant
brood, and it has been hypothesized that they represent a derived feeding strategy
(220,235). A molecular phylogenetic analysis has shown that the two cuckoo
species are the sister group to the rest of their congeners, which themselves form a
myrmecophagous clade (T.D. Als, personal communication). Thus the phylogeny
neither confirms nor refutes the hypothesis that the cuckoo strategy is derived
relative to predation.
Why do larvae of M. rebeli, C. dicksoni (Aphnaeini), and other trophallactic
Thestor and other miletines, presumably entomophagous for longer than their
lycaenine counterparts, offer no such rewards. It may be only a matter of time
before the lycaenine larvae lose their DNOs, as have some species of Aloeides
(130). On the other hand, some of these vestigial-seeming DNO secretions may
by Wada et al. (228) on N. fusca.
Most species of Maculinea are highly specific with respect to their ant asso-
ciates, with highest survivorship in the nests of one particular ant species (217).
Maculinea species (86,114).
Two species of Phengaris, an Oriental genus in the same section and probably
are transported by workers into a Myrmica colony where they grow and pupate.
Phengaris atroguttata formosana uses related plants and ants, and the larvae of
both species feed on ant brood in their later instars (223).
The phytopredaceous life history observed within the genus Lepidochrysops
although further phylogenetic work will be necessary to clarify the relationship.
Species in both genera are similar in lacking TOs and using their DNO secretions
to appease ants before entering the underground entomophagous phase (130).
Restricted to Africa, Lepidochrysops is an unusually large genus. Reliable life
histories have been published for only 11 of the 126 recognized species, with the
remainder assumed to be ecologically similar (37,41,47,131,132,239). A taxo-
nomic revision may reveal considerably fewer than 126 true species in the genus,
and a rigorous phylogeny of Lepidochrysops and its related genus Euchrysops has
yet to be done. The two genera are currently differentiated almost solely on the
basis of life history, with Euchrysops species grouped by their limited myrme-
cophily. A reliable phylogeny of this section combined with more comprehensive
life history accounts could reveal multiple origins of entomophagy rather than one
From Mutualism to Parasitism
In the large subfamily Lycaeninae, entomophagous species are most often dis-
gests a lack of phylogenetic constraint against such shifts. Moreover, parasitic en-
tomophagous species typically emerge from within mutualistically ant-associated
groups, with the exception of Shirozua within the weakly ant-associated Thecliti.
Entomophagy does not appear at all in the largely myrmecoxenous Lycaenini.
The reverse trend, a single phytophagous species occuring within an otherwise
entomophagous clade, is never observed. The Riodininae exhibit a comparable
pattern, although their life histories are much less well known. Entomophagy has
been recorded for only a few species in this subfamily (∼1200 spp. total), but
these species fall within the ant-associated subtribes Eurybiiti and Nymphidiiti
(including Lemoniiti) (63,177).
Evolutionary Constraints on Entomophagy
Although entomophagy occurs frequently in the Lycaenidae, it most often ap-
pears as a species-poor dead end. Of the approximately 160,000 species in the
Lepidoptera, well over 99% are strictly phytophagous as larvae (189). This is
among the highest proportions of phytophagy in a large insect clade, comparable
only to groups such as the Orthoptera (>99% phytophagous), Hemiptera (90.7%),
and Phytophaga [within Coleoptera; >99% (210)]. The larvae of about 500 lep-
idopteran species have been observed or inferred to feed on other arthropods or
arthropod exudates; these species are widely dispersed across the lepidopteran
phylogeny, with few large clades characterized by such a feeding mode (183).
These small phylogenetically disparate groups include ∼200 moth species (183).
as a frequent precondition for lepidopteran entomophagy. Approximately 300 ly-
caenids are known or suspected to be entomophagous. Most of these occur within
the Miletinae and the polyommatine genus Lepidochrysops, leaving only about 40
species of entomophages scattered across the rest of the phylogeny.
PIERCE ET AL.
With the exception of the two radiations described above, Miletinae and
Lepidochrysops, entomophagy seems to be a short-lived evolutionary experi-
ment. Possible causes are problems associated with life cycle complexity and with
phylogenetic/physiological constraint (183). Over one third of the 152 lycaenid
species in the IUCN Red List of Threatened Species (36) are entomophagous.
Although this disproportionately high representation is in part due to heavy listing
of Lepidochrysops and Thestor species, it accords with the phylogenetic pattern.
The phylogeny suggests that entomophagy is an extinction-prone dead end, and
demographic studies seem to confirm this.
The conservation consequences of entomophagy point to ant association as a
double-edged sword for lycaenid butterflies. Association with ants has promoted
rapid rates of diversification in the Lycaenidae, with an overlapping mosaic of ant
and plant distributions yielding small isolated populations—the raw material of
speciation. While population fragmentation may have resulted in a net diversifica-
In the face of anthropogenic disturbance and habitat loss, the balance may be tip-
ping toward ever-higher extinction rates among lycaenid butterflies. This is true
not only for entomophagous species such as the Large Blue (Maculinea arion) in
the United Kingdom, Arionides Blue (M. arionides) in Japan, and the Mangrove
as the Brenton Blue (Orachrysops niobe) in South Africa, and the Karner Blue
(Lycaeides melissa samuelis) in the United States (7). With their highly complex
life histories, it is not surprising that lycaenids are particularly sensitive to pertur-
bations of their environment (173).
Zoogeographical Patterns in Ant Association
A number of lycaenid lineages have their centers of distribution in particular
zoogeographic regions (Table 3). Pierce (181) estimated the prevalence of ant
associations in different zoogeographic regions based on data summarized from
in the Southern Hemisphere than in the Northern Hemisphere.
Subsequent studies have shown that the proportion of facultative ant associates
in Europe and North West Africa may be higher than originally estimated (96).
the Australian, Afrotropical, and Oriental Regions than in the Holarctic (Table 4).
Australia (39%) and southern Africa (59%) have especially high levels of obligate
ant association. By contrast, obligate myrmecophily in the Nearctic is less than
2%, and ant association in general is rare, with over 80% of the species apparently
not associating with ants. Life histories of over half the species in the Oriental
and tribes) within each zoogeographic region
The geographical distribution of the major lycaenid taxonomic groups (subfamilies
Taxonomic group AustralianAfrotropicalOrientalPalaearctic NearcticNeotropical
+, low representation in region (1–4 species); ++, moderate representation (5–30 species); +++, high representation
(31–100 species); ++++, very high representation (>100 species).
Data derived from Eliot (83), DeVries (63), and Fiedler (95). Several authors recognize an additional tribe, Eumaeini,
consisting mainly of subtribes within the Theclini, but in the absence of additional phylogenetic information we have retained
Eliot’s broader definition of Theclini.
Region are presently unknown, but the region appears to be transitional between
the southern and northern regions in the percentage of obligate association. Our
understanding of life histories of Lycaenidae in the Neotropics is poor relative
to other geographic regions, and broad systematic analyses are still forthcoming.
We have therefore not included the Neotropical fauna in most of our discussion
here (but see 13,14,28–32,50,61,63,65,121–124,147,148,170,177,192–194,
and references therein).
At least two nonexclusive factors account for these pronounced biogeograph-
ical differences in obligate ant association. One is the systematic composition of
the major taxonomic groups within each region and concomitant levels of myrme-
cophily. The other concerns ecological factors or selective forces that may have
led to the loss or gain of myrmecophily in particular clades.
Phylogenetic Patterns in Ant Association
Pierce (181) noted that all but one of the recognized tribes of the Lycaenidae
(sensu Eliot 1973) can be found in both the Holarctic and the southern regions,
and most of the tribes contain both ant-associated and non-ant-associated species.
PIERCE ET AL.
major zoogeographic region (comparable data for the Neotropical region not available)
The number and proportion (in parentheses) of ant-associated species in each
Zoogeographical regionN ObligateFacultativeNone Source
128 50 (39) 51 (40)27 (21)(24,77)
16094 (59)28 (17)34 (24)Heatha
60 13 (22)
134Malay Peninsula and Borneo
Europe and NW Africa 82 10 (12)
aUnpublished data; see also reference in Table 4.
Thus a single vicariance event involving ant-associated versus non-ant-associated
lineages could not explain the dichotomy in obligate ant association observed be-
tween the Holarctic and Southern Hemisphere regions. However, an analysis of
lower taxonomic levels (tribes and subtribes) using additional life history records
showed a strong correlation between the degree of ant association and system-
atic group (95; Table 1). The geographically heterogeneous distribution of tribes
with different levels of ant association can explain much of the observed faunal
The correlation between ant association and phylogeny in Australia and south-
ern Africa can be seen more clearly when the lower taxonomic categories (tribes,
subtribes) are analyzed in detail (Table 5). The high degree of obligate associa-
tions in the Australian and Afrotropical regions is associated with the presence
of the Theclini and Aphnaeini, respectively. In contrast, the low level of obligate
associations in the Palaearctic and Nearctic correlates with the preponderance of
the Lycaenini and non-ant-associated subtribes of Theclini, respectively, as well
as the ubiquitous Polyommatini.
groups are more numerous in the Southern Hemisphere, and the question remains
lycaenid taxonomic group (subfamilies, tribes, subtribes) in Australia and Southern Africa
The number and proportion (in parentheses) of ant-associated species within each
Australia Southern Africa
Ant-association (%)Ant-association (%)
Taxonomic groupN ObligateFacultative NoneN Obligate FacultativeNone
15 8 (53)
79 78 (99)
40206 (30)8 (40)6 (30)
Total12850 (39)51 (40)27 (21)16094 (59)28 (17) 38 (24)
Data derived from Eastwood & Fraser (77) and Braby (24) for Australia; Jackson (145,146), Clark & Dickson (41), Schlosz
& Brinkman (199), Heath & Claassens (130), Heath (125), and Heath (unpublished data) for Southern Africa.
as to why this is the case. Are there phylogeographic features that have enhanced
the success of ant-associated lineages in these regions?
Ecological factors undoubtedly influence the extent of ant association within
zoogeographic regions or within clades. In the Western Palaearctic, for example,
the proportion of facultative myrmecophilous species decreases with increasing
latitude, and in the boreal and tundra zones ant association is rare (103). However,
this same pattern of decreasing myrmecophily with increasing latitude was not
observed in Australia (181). The phosphorus-poor soils of southern Africa and
Australia may have played a role in the high incidence of ant-dispersed myrmeco-
chorous plants in these areas (237), and further research might explore the com-
parative phylogeny and biogeography of myrmecochorous plants or of ant plants
in general. For example, whereas the genus Macaranga has a wide distribution
PIERCE ET AL.
in the Old World tropics, the clade containing ant plants seems to be confined to
West Malesian rainforest, a region well known for its phosphorus-poor soils (51).
Origin and Evolution of Ant Association
Hinton (139, pp. 122) noted that “the possession of a dorsal organ appears to be a
primitive feature in the Lycaenidae, and, if this is indeed the case, it follows that
its absence is in all cases secondary.” However, Fiedler (95) argued that because
the putatively ancestral lycaenid lineages (Poritiinae + Miletinae + Curetinae)
are not generally ant associated, myrmecophily is a derived state in the sister clade
Lycaeninae. This assumes that the ant-associated taxa observed in the Riodininae
and myrmecophagous Miletinae have arisen independently. In either case, within
the subfamily Lycaeninae, absence of overt ant association can be found among
have occurred multiple times.
Analyzing the evolution of ant association within and between different lin-
eages of the Lycaenidae remains problematic, and given the numerous gains and
losses that have occurred, we may never know the sequence of events. The pos-
session of PCOs, thought to be used in appeasing and/or otherwise chemically
ing Riodininae (44). A reasonable conclusion is that manipulation of ants was an
important first step in the evolution of myrmecophilous interactions, whether mu-
tualistic or parasitic. It may have been the crucial step necessary for the Miletinae
to evolve homopterophagy through the appeasement of otherwise aggressive ants
and possibly through the use of the ants themselves as cues in finding prey.
Based on consideration of species richness and present-day distributions, Eliot
years ago) and were Gondwanan in origin. The Oriental and Afrotropical Regions
contain the greatest phylogenetic diversity, including the putatively ancestral
Poritiinae, Miletinae, and Curetinae, whereas the vast majority of the Riodininae
occur in the Neotropical Region. In comparison, the Holarctic fauna is system-
atically depauperate and is more recently derived from the Old World (via Asia
and possibly Africa) and possibly South America (but see 148). The origin of
the Oriental fauna and the role of India are uncertain. Eliot (83) suggested that
lycaenids were absent on India during its northward drift from Antarctica and that
the Southeast Asian fauna was derived from Africa through invasion by dispersal,
possibly via India. If the Oriental fauna is older than hitherto believed, and the
Poritiini and Curetinae represent relictual groups, a scenario of secondary radia-
tion after contact with India in the early Tertiary (and later with Australia in the
late Tertiary) seems plausible.
A southern origin of the Papilionoidea is not widely accepted (e.g., 203,204);
however, several studies advocate the presence of butterflies in Gondwana prior
to continental breakup (95,168,176; see also 143). An analysis of the endemic
Theclini subtribes (Luciiti, Ogyriti, and Zesiiti) are temperate in distribution and
specialize on Gondwanan plants. These groups also contain exceedingly high
proportions of obligately ant-associated species.
suggest that the Australian Theclini and the African Aphnaeini may represent an-
cient vicariant myrmecophilous lineages within the Lycaeninae. Together with the
present-day distributions of other major groups, this points toward a southern ori-
gin of the Lycaenidae. As a corollary, the Polyommatini, New World Eumaeiti,
and Lycaenini are possibly more derived, and the latter tribe, which shows re-
duced myrmecophily and does not form obligate associations with ants, may have
originated in the Northern Hemisphere. Such a phylogeographic model is not in-
consistent with the low incidence of obligate myrmecophily in the Palaearctic and
Determining the phylogenetic relationships and monophyly of the major lin-
eages are a priority if we are to understand the evolution of ant association in this
group of butterflies. If, as originally suggested by Eliot, the Holarctic fauna was
derived from the southern areas and loss of myrmecophily is derived, a prediction
is that the Aphnaeini + certain subtribes of Theclini are basal and the Lycaenini
+ Eumaeiti + Polyommatini are derived groups within the Lycaeninae. Critical to
understanding the origin of the Lycaenidae and the evolution of ant associations
will be the elucidation of systematic relationships and larval-ant associations in
South America. The systematics and biology of species in this part of the world
are still poorly known, and the Eumaeiti, of which more than 900 species are en-
demic (95), may be paraphyletic. If a Gondwana faunal split did play a role in the
evolution of the lycaenids, some of these taxa may be highly ant associated and
have close relatives in southern Africa and Australia.
The Lycaenidae provide a model system for studying the evolution of complex
particularly amenable for comparative studies. However, the validity of conclu-
sions drawn from such comparisons is called into question by our poor under-
standing of the evolutionary history of the family at almost every level. A detailed
phylogeny of Lycaenidae and related groups is essential if we are to evaluate these
hypotheses. Without more information regarding their evolutionary history, quan-
titative comparisons of lycaenid behavioral and ecological attributes are at best
difficult to interpret.
The possibility that ant association has both promoted and constrained diver-
sification of the Lycaenidae could be evaluated through additional analysis of
targeted groups. Comparisons of population structure between ant-associated and
non-ant-associated species may reveal mechanisms underlying rates of speciation
PIERCE ET AL.
dominence of obligately myrmecophilous lycaenids in the Southern Hemisphere
remains unexplained, and an understanding of this distribution will require a com-
and natural history of the Neotropical fauna is essential for our understanding of
the origin and evolution of the Lycaenidae and their symbioses with ants.
We thank G.S. Adelson, A.J. Berry, D.L. Campbell, P.J. DeVries, R. Eastwood,
B.D. Farrell, A.M. Fraser, R.L. Kitching, D.R. Nash, C.M. Penz, J.O. Schwartz,
and D. Wagner for their comments; B. H¨ olldobler, E.S. Nielsen, G.E. Robinson,
J.A. Rosenheim and E.O. Wilson for their support and encouragement; and
C.A. Adams and J.K. Mills for their assistance in preparing the manuscript. We
have benefited from support provided by the National Science Foundation, the
Baker Foundation, and the Putnam Expeditionary Fund of the Museum of Com-
contributions of Colonel J.N. Eliot, who laid the groundwork for lycaenid system-
atics, and we dedicate this paper to him.
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