Biological Journal of the Linnean Socicp (1987), 30: 229-243. With 4 figures
Sexual competition during colony reproduction
in army ants
NIGEL R. FRANKS
School of Biological Sciences, University of Bath, Bath B A 2 7 A Y
AND
BERT HOLLDOBLER
Department of Organismic and Evolutionary Biology, Harvard University,
MCZ-Laboratories, Cambridge, Massachusetts 02138, U.S.A.
Received I1 June 1986, accepled for publication I8 N o v m b c r 1986
We review the unusual processes of sexual reproduction and colony fission in army ants and briefly
compare this to reproduction in other ants.
Army ants are a polyphyletic group and are characterized by a syndrome of convergently
evolved traits including large colony size, group foraging for large prey, nomadism, cyclical brood
production and queens who are large and wingless. Because queens are flightless and never leave
their colony, workers are in a position to choose which queen will take over each new colony. Males
fly between colonies and must run the gauntlet of the workers in alien ones before they can
approach the queen. For this reason, workers can also choose which males will inseminate their
queen.
Army ant workers may therefore be involved in choosing both the matriarch and patriarch of
new colonies. We suggest that this unusual form of sexual selection has led to the close resemblance
of conspecific males and females in all the separate lineages of army ants. Males are queen-like in
that they are large and robust, have long cylindrical abdomens, with exocrine glands of similar
form and location to those of females and shed their wings when they enter new colonies.
Furthermore, when males enter new colonies they are followed by a n entourage of workers which
resemble those that accompany queens. We suggest that males resemble queens not as a form of
deceitful mimicry but because under the influence of sexual selection they have come to use the
same channels of communication to demonstrate their potential fitness to the workforce as those
used by queens.
KEY WORDS:-ants
- army ants
pheromones - sexual selection.
-
convergent evolution - exocrine glands - mate choice -
,
CONTENTS
Introduction . . . . . . .
The army ant syndrome . . . .
Colony reproduction . . . . .
Queen selection by workers
. . .
Morphological origin of queen pheromones
Sister’s mate selection . . . . .
Acknowledgements
. . . . .
References.
. . . . . . .
0024-4066/87/030229
+ 15 $03.00/0
. . . . . . . . . . . .
. . . . . . . . . . . .
.
.
.
.
.
.
.
.
.
.
.
.
229
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
230
23 1
23 1
234
236
236
24 1
24 1
0 1987 The Linnean Society of London
230
N. R. FRANKS AND B. HOLLDOBLER
INTRODUCTION
Charles Darwin proposed that many bizarre traits and signals employed by
animals in sexual reproduction evolved by sexual selection. He noted that it is
usually the males of the species that struggle and compete for females, and it is
the female that chooses her mates. Males thus evolved traits which serve in
intrasexual competition and in intersexual courtship. Usually these traits have
nothing to do with ecological adaptations; in fact they might even be a
detriment to survival but they serve in enhancing reproductive success.
Many peculiar features in insect communication can be explained by the
theory of sexual selection (Thornhill & Alcock, 1983; West-Eberhard, 1984).
Recently West-Eberhard (1983, 1984) has suggested that the primary function
of sexual signals is to promote sexual competitive ability and mate choice and
that they serve only secondarily as pre-mating isolation mechanisms.
Entomologists have only recently begun to investigate the diverse mating
tactics among ant species in the light of sexual selection theory (see Holldobler
& Bartz, 1985). In some ant species the females mate with their brothers inside
the nest, while in others the females attract males from distant nests by releasing
sex pheromones. In still other species, males from many colonies gather at
mating sites, and females fly in, from considerable distances, to mate. Finally, in
a few species, the males seek out and enter foreign conspecific colonies in order
to mate with wingless females inside the nest. This latter mode has recently been
documented in the ponerine species Ophthulumopone berthoudi (Peeters & Crewe,
1985); and, although the behaviour differs in some important details, it also
occurs in the doryline and ecitonine army ants.
Army ants reproduce by colony fission, a mode of reproduction that is
relatively uncommon among the social insects. Other than in army ants, where
it is ubiquitous, well-documented cases of reproduction by colony fission occur
only in social wasps, stingless bees and honeybees (Schneirla, 1971; Wilson,
197 1; Michener, 1974). Colony fission is a trait associated with relatively large
colonies that have a single queen (monogynous). Reproduction in such colonies
involves the production of relatively few daughter queens and a large number of
males. The new queens are inseminated by males from other colonies, and
finally leave their parental nest with a large retinue of workers. In this way the
parental colony splits off entirely separate new colonies each of which is headed
by only one queen. The new colonies cease to communicate and essentially are
as hostile to one another as any completley alien colonies would be. Colony
fission is a quite different process to colony budding which typically occurs in
colonies with multiple queens (polygynous) (Holldobler & Wilson, 1977).
Budded nests are also polygynous, typically remain in communication with one
another and are associated with the growth of the parental nest rather than the
creation of entirely independent new societies. Reproduction by colony fission is
of fundamental interest because it involves many of the conflicts between
workers and queen and among the workers themselves that have shaped the
evolution of eusociality in insects in general (Macevicz, 1979).
When a colony divides, two complete and distinct new societies are formed
directly from the old. During this schism a number of critical decisions are
made. Who will be matriarch of the new society? Which workers will
accompany their sister-queen and suffer the fate of raising nieces rather than
sisters? And, who will father the progeny of the new colony?
SEXUAL COMPETITION IN ARMY ANTS
23 1
In this paper we suggest that in army ants, workers participate in all of the
above decisions. Therefore, army ant workers may be involved in an
extraordinary form of sexual selection in which they choose not only their queen
but also her mates.
THE ARMY ANT SYNDROME
Before we consider the choices that workers may make during colony
reproduction, we will briefly examine the life history pattern of typical army
ants that has given rise to a form of colony reproduction in which workers have
such an important role.
The army ant syndrome, chiefly characterized by group predation, large
colony size and frequent nest emigrations has arisen independently at least seven
times, occurs in four subfamilies of ants (Gotwald, 1982), and represents one of
the most extreme examples of convergent evolution among all social insects.
The foraging ecology of army ants has favoured colonies with unusually large
worker populations. Most army ants stage massive raids in pursuit of such prey
as large arthropods or other social insect colonies. Some of these prey can only
be captured by large numbers of workers foraging in concert. However, as such
prey can be locally depleted by such raids the entire army ant colony must
frequently move to new feeding areas. Thus, large colony size facilitates group
raiding and necessitates frequent emigrations (Rettenmeyer, 1963; Topoff,
1984).
Army ant colonies are also unusual in that they tend to produce broods in
discrete generations so that their larvae develop in batches. Consequently the
relatively large queens periodically become extremely physogastric with the
abdomen greatly extended with eggs (see Fig. 1B). They can lay enormous
numbers of eggs within a few days. Eciton burchelli queens, for example, are
known to produce between 60000 and 100000 eggs within a 3-5 day period
(Rettenmeyer, 1963; Franks, 1985). When all these eggs simultaneously hatch
into larvae approximately 10 days after they have been laid, the entire
E . burchelli colony including the queen begins a nomadic phase. During this 15
day period of larval development the colony forages every day to feed its
voracious brood and emigrates to a new bivouac site on almost every night. In
such a nomadic phase the queen, who is no longer physogastric, has to walk a
total of more than 1000 m between the successive bivouac sites (Franks &
Bossert, 1983). At the end of the nomadic phase all the larvae spin pupal cases
and no longer require food with the result that the colony can live in the same
bivouac site for 20 days, foraging locally on only two-thirds of these days
(Schneirla, 1971). This period is called the statary phase and ends when both
the pupae and the next generation of eggs hatch so that the colony has new
cohorts of workers and larvae. Once again it will enter a nomadic phase. These
alternating stationary and migratory phases continue throughout the lives of
Eciton colonies and occur, sometimes in a less stereotyped form, in all other army
ants.
COLONY REPRODUCTION
To maintain this way of life even the smallest, newly formed, army ant
colonies need to be relatively large compared to new colonies of other ant
232
N. R. FRANKS AND B. HOLLDOBLER
Figure 1. Side view of the reproductives of Ecilon. A, Queens of E. rapax, the left one is slightly
physogastric. B, Physogastric E. hamalum queen. C, Ecifon burchclli male.
species. Hence they are established by colony division rather than by individual
queens.
Colony fission imposes severe constraints on the number of new colonies that
a parental colony can produce in its lifetime. Optimization models show that
reproduction by division is most efficient if the parental unit divides (a) into two
units of equal size and (b) at such a size that the combined growth rate of the
daughter units exceeds the growth rate of the parent (Franks, 1985). This
SEXUAL COMPETITION IN ARMY ANTS
233
strategy is exhibited by E. burchelli colonies. Triggered by the beginning of the
Neo-tropical dry season, the largest colonies produce a sexual brood and later
divide equally into two daughter colonies of approximately the optimum size for
most rapid growth (Franks, 1985).
When an army ant colony divides, either one daughter bivouac serves the
original queen while the other is taken over by a daughter queen or the old
queen is rejected so that both new colonies have young queens. Such
reproduction involves the maximum possible investment in the successful new
queens; indeed, the workers that accompany them represent the single greatest
component of the parent colony’s investment in reproduction (Macevicz,
1979).
Reproduction in army ants has been most thoroughly documented in
E. burchelli, and especially on Barro Colorado Island, Panama, where
reproductive colonies have approximately 600 000 workers and raise broods of
about 3000 males and six queens (Schneirla, 1971; Franks, 1985). The sexual
larvae develop over a single nomadic period. When they pupate, always in
synchrony, the colony enters a 20-day statary period. T h e virgin queens emerge
from their cocoons 2-3 days before the end of this phase when the males eclose.
O n the day of the division the colony produces two raid systems in opposite
directions, the queens then emerge from the bivouac and attempt to proceed
down the raid systems. Only two at most, are ever successful. Each is
accompanied by an entourage of workers down one of the raid paths. The
remaining queens are held back at the old bivouac site by clusters of workers
where they are eventually abandoned and left to die. New bivouacs are formed
around the successful queens, one at the end of each raid system. For a
considerable amount of time workers move from one new bivouac to the other
via the site of the old nest. As the males emerge from their cocoons
approximately half go with each daughter colony and eventually, after as many
as 48 hours, the umbilical column of workers breaks and the daughter colonies
go off in their different directions.
Since at most only two new queens will be successful during colony division,
selection on the parental colony (conceivably in the form of local resource
competition (Charnov, 1982) where the limiting resource is the workers who
accompany the new queens) may have led to the reduction in the number of
new queens produced. Allowing for the workers that accompany new queens,
the investment sex ratio is massively female-biased. Marking of queens in the
field has shown that Eciton females can live approximately 6 years
(Rettenmeyer, 1963). Since about one in three of these colonies divide each
year, a colony probably takes 3 years to grow to a size at which it can divide
again. Assuming that established queens retain one-half of their colony at the
first division and give rise to two daughter at the second division, a queen will
give rise to three new daughter colonies and two sets of male broods in her 6year life time. The biomass of males raised in the 35-day cycle before colony
division is almost exactly equivalent to the biomass of workers a nonreproductive colony of a similar size would have raised (Franks, 1985). In 45 35day cycles the colony invests exclusively in daughters (half the workers produced
in the 30 35-day cycles in the first 3 years plus all of the workers produced in the
30 35-day cycles in the second 3 years, giving 15 30 = 45). Investment in males
takes place only in two 35-day cycles. The ratio of investment in males to
+
234
N. R. FRANKS AND B. HOLLDOBLER
females in army ants may therefore be biased to the extent of 1 : 20 or more. The
large number of males that are produced by a colony have wings when they first
emerge as adults and must fly to foreign colonies where they must first be
accepted by the workers before they can gain access to the queens. This
screening of mates by workers occurs because army ant queens never possess
wings and do not leave their colony to seek a mate, instead they are always
guarded by a large workforce.
We will now examine the procedures by which workers may choose first the
queens and second the males.
QUEEN SELECTION BY WORKERS
During colony division, workers should, in theory at least, selfishly select the
queens that would enable them to maximize their own inclusive fitness
(Macevicz, 1979; Franks, 1985). This calculation is complicated by three
factors: (1) workers that accompany sister queens, rather than their mother
queen, suffer the fate of raising nieces and nephews rather than brothers and
sisters; (2) at some stage in the life of a colony, workers have to reject their
maternal queen on the grounds of her senility; (3) virgin queens may not be full
sisters of the workers as army ant queens probably mate more than once in their
lifetime.
If all the virgin queens and all the workers are full sisters, then the workers
should unanimously select the potentially most fertile queens, preferring their
mother to a sister, all else being equal. However, if the maternal queen has
mated more than once in her lifetime, as has been suggested for both Eciton
burchelli (Rettenmeyer, 1963) and Dorylus (Anomma) (Raigner & Van Boven,
1955), then each patrilinial group of workers should prefer their own full sister
to be one of the new queens. However, this alternative would be possible only if
workers can discriminate between full and half-sisters. That degree of kin
recognition has been suggested in honeybees (Getz & Smith, 1983; Page &
Erickson, 1984; Visscher, 1986; but see Page & Erickson, 1986). Also it has been
claimed that colony division in honeybees is associated with the segregation of
workers into sororities (Getz, Brucker & Parisian, 1982). Furthermore, it has
been demonstrated that worker bees can distinguish between individual queens
on the basis of their odours (Boch & Morse, 1974, 1979), while Breed (1981) has
shown that the rate of acceptance of foreign queens is correlated with the degree
of genetic relationship among the queens involved in the transfers.
However, few studies have been conducted on whether ants can discriminate
between individual nestmates, of the same sex, on the basis of their relatedness
and not much can be concluded at the present time (Jutsum, Saunders &
Cherrett, 1979; Carlin & Holldobler, 1983, 1986; Mintzer, 1982; Mintzer &
Vinson, 1985). Furthermore, although army ant queens may mate more than
once they may do so only once each year (Rettenmeyer, 1963), so that it is
possible that new queens and the majority of the worker population are full
sisters. Thus at present we do not know if kinship plays a major part in the
workers choice of new queens. What is clear, however, is that whether workers
are able to recognize their full sisters or not, there will be very strong selection
for workers to discriminate between queens on the basis of their potential
fertility and survivorship.
Army ant queens have to be both exceptionally vigorous and productive. As
SEXUAL COMPETITION IN ARMY ANTS
235
explained earlier, Eciton burchelli queens, for example, may live 6 years during
which time they will produce some 3 million workers in total and walk between
successive bivouacs a total distance of 60 kilometres (Franks, 1985). Due to huge
worker mortalities during foraging, army ant colonies grow relatively slowly and
on average 3 years elapse between bouts of sexual reproduction. The workers
have to choose highly fecund and longlived queens in order to realize any
inclusive fitness at all.
Studies on colony foundation by multiple queens (pleometrosis) in other
species of ants suggest that workers have well-developed abilities to choose the
most fertile and attractive queens, and that kinship is of minor importance in
the rejection of supernumerary queens (Bartz 8.1 Holldobler, 1982). Though
almost nothing is known about the genetic constraints on worker choice of
queens in army ants, a considerable amount is known about the proximate
mechanisms by which workers may discriminate between queens.
Schneirla (1956) observed conflicts between workers who were associated
with different virgin queens even when the latter were still maturing larvae. He
noted that individual queen larvae are often separated by considerable distances
and each larva was surrounded by a cluster of “satellite workers”. Adjacent
worker groups can come into conflict which can even lead to fatalities among
potential queens. This behaviour can be considered an important aspect of
queen competition.
Schneirla (1971) has also documented the attractiveness of both male and
female sexual larvae to the workers. Ant brood is known to produce
characteristic and highly attractive pheromones that elicit care from workers
(i.e. Jaisson, 1972; Walsh & Tschinkel, 1974; Holldobler, 1977). Thus it is
possible that army ant sexual larvae produce a brood pheromone. Once a new
queen ecloses its brood pheromones probably disappear to be replaced by the
true queen pheromones. These new queen odours are probably tolerated in the
presence of the old queen because the reproductive colony is so large that the
old queen’s pheromones do not diffuse to all workers. The increasing production
of new queen pheromones is most likely responsible for the loyal retinue of
workers that builds up around virgin queens. This scenario would explain
another observation of Schneirla (1971) that the first queens to emerge are more
attractive and most likely to be successful. The first young females will have had
longer to produce their pheromones and to win the allegiance of the workers.
That workers may come into conflict over their allegiance to queens does not
necessarily mean that they are forming sororities. Such conflicts may be a
mechanism by which workers can compare the strength of their advocacy for
certain queens and hence the queens’ attractiveness. Therefore such competition
might have resulted purely from colony level selection.
The phenomenon of workers changing their queen-allegiances has been
demonstrated by experiments in which the old queen was removed from the
bivouac when the sexual larvae were mature. Under these circumstances the
parental queen will be readmitted to her colony in an unequivocal manner only
if she is presented to the group of workers previously affiliated with her.
Otherwise she may be segregated in a tight cluster of workers and eventually
abandoned (Schneirla & Brown, 1952; Schneirla, 1956). Schneirla (1956)
suggested that the allegiances between workers and queens were based on
pheromonal cues, characteristic for each individual queen.
236
N. R. FRANKS AND B. HOLLDOBLER
If army ant workers choose their queen on the basis of pheromones, more
than just those workers that immediately accompany the queens may be
involved in the selection process. Queen pheromones are known to be circulated
throughout their colonies, as has been shown by removal experiments. For
example, Eciton colonies will accept workers of alien colonies only if the
transplanted workers have been isolated from their queen for a number of days
(Schneirla, 1971 ) . A colony devoid of its queen will after a number of days fuse
with a colony of the same species with a viable queen. Thus, it is clear that
queen secretions unite and coordinate the huge ant society. Furthermore, the
chemical basis of the queen’s attractiveness and ‘signature’ has been
demonstrated by experiments in which workers were more attracted to paper
discs upon which the queen had been previously sitting than they were to
control discs (Watkins & Cole, 1966).
The way in which these queen pheromones are transmitted throughout the
colony is suggested by the behaviour of the ants that accompany the queen
during emigration. When New World army ant queens move between nests they
are surrounded by an entourage of workers. In Eciton burchelli these queen
retinues are particularly large and such a large number of workers run over the
body of the queen or run with their mouthparts in contact with her gaster that
she is frequently invisible. The workers in the entourage are continuously
changing, with some joining the queen while others leave her to move through
the rest of the colony (Rettenmeyer, Topoff & Mirenda, 1978).
All these observations provide strong circumstantial evidence that army ant
workers can recognize and choose particular queens during colony fission and
that the choice is based on queen attractiveness. In addition the queen’s genetic
relatedness to the workers may also play a role in this selection process.
MORPHOLOGICAL ORIGIN OF QUEEN PHEROMONES
Rettenmeyer (1963) observed worker-queen interactions in Eciton in the
laboratory and recorded the frequency with which workers licked different parts
of the queen’s body. He found that workers rested most frequently with their
mouthparts over the first and second gaster segments and he suggested that the
chemical signals responsible for the attraction to the queen are probably
secreted near this region of the gaster. Whelden (1963) has described
intersegmental exocrine glands in the gaster of Eciton queens, which appear to be
particularly well developed in the first gaster segments. In a more recent
morphological study, Holldobler & Rettenmeyer (in prep.) discovered that, in
fact, the whole gaster of Eciton queens is covered by massive exocrine glands
drained by multiple ducts which penetrate the intersegmental membranes and
the sclerotized cuticle. Apparently large quantities of secretions are produced by
these glands, because during the fixation process, coagulated secretion oozes out
of the glandular openings like toothpaste squeezed out of a tube (Fig. 2).
SISTER’S MATE SELECTION
Once the choice of queen has been made, the parental colony divides and the
daughter colonies are each provisioned with a brood of larval workers that were
SEXUAL COMPETITION IN ARMY ANTS
237
Figure 2. SEM micrographs of the cuticular openings of the exocrine glands on the abdominal
tergites of Eciton hamalum queens. Above: overview illustrating the density of the cuticular openings.
Below: close up of one opening, with secretions oozing out (from Holldobler & Rettenmeyer, in
Prep.)’
produced by the maternal queen in the old bivouac. The daughter colonies then
begin a nomadic phase to feed these larvae. In E. bruchelli this phase lasts 15
days. About 10 days after its completion the queen must lay a batch of eggs to
produce her colony’s new brood of workers. Virgin queens thus have less than 4
weeks, after they eclose as adults, in which to find a mate. But during this period
and indeed throughout the rest of their lives army ant queens are guarded by an
entourage of workers.
238
N. R. FRANKS AND B. HOLLDOBLER
Outbreeding appears to be the rule in army ants; Schneirla (1971) has
suggested that in Eciton, males must fly before they can mate. Males may even
mate with reigning queens in foreign colonies that have not just been through a
colony division (Rettenmeyer, 1963). In any case, males have to enter alien
colonies and break the worker barrier to get to the females. Hence workers are
in a position to choose both the mother and father of their future nestmates.
The reason why workers should be involved in choosing mates for their queen
is that they will later invest in the progeny of these males. Therefore, the
principles of sexual selection and female choice should apply to their preferences
(Williams, 1966; Trivers, 1972; Halliday, 1978; Otte, 1979; Holldobler & Bartz,
1985). In order to maximize their own inclusive fitness the workers should
actively choose males that promise the greatest fertility. Sexual selection theory
suggests that males may demonstrate that they will be donors of highly viable
gene combinations, for example by being themselves large, robust and vigorous.
We now discuss circumstantial evidence suggesting that workers may use
similar criteria to choose males as they used to choose their queen, and that this
form of sexual selection had led to the resemblance of males to queens. We
suggest that worker involvement in sexual selection has favoured males that are
superficially similar in size and shape to their conspecific queen as is the case in
all the polyphyletic lineages of army ants. For example, Dorylus and Anomma
queens are the largest known ants, being up to 50 mm long (Wilson, 1971) and
males of these genera are almost as large (Gotwald, 1982; Barr & Gotwald,
1982), and both sexes have long cylindrical gasters. The unusual robustness of
army ant males is well known. In Africa they are called sausage flies, and
elsewhere they are commonly mistaken for wasps. Indeed the first specimens of
army ant males were classified as Vespa (Linnk, 1764, in Schneirla, 197 1). Even
in the non-doryline army ants such as Cerapachy, Brown (1975) reports that
males are similar to the conspecific queen in size and robustness. In other ant
species, males are often a fraction of the size of the queen and are very lightly
built (Wilson, 1971).
During evolutionary history, the gaster of the male became elongated and
enlarged presumably to house the massive sperm vesicles and the ever increasing
glandular equipment needed to impress the workers. Recently, Holldobler &
Engel-Siege1 ( 1982) discovered that doryline males are unusually well endowed
with abdominal glands, particularly between the tergites of the gaster (Figs 3 &
4). Such glands do not occur in workers, but closely resemble those of the queen
(Whelden, 1963; Holldobler & Rettenmeyer, in prep.). Fierce sexual
competition (consider the highly skewed numerical sex ratios in army ants)
where only a few males succeed, has probably led to the evolution of the rich
glandular equipment in males (convergent to females), because only the most
attractive males were successful. In fact males have retinues of workers that
accompany them like the entourage of queens. It is interesting that workers are
most attracted to the abdominal tergites of the males, as they also devote most
attention to the corresponding parts of the gaster of the queen. Schneirla (1971)
describes such behaviour in Eciton bruchelli and in E. hamatum, and Rettenmeyer
(1963) reports a similar phenomenon in Eciton vagans.
There is one further feature of the army ant syndrome that can be explained
in terms of their unusual form of sexual selection and sexual competition. In
many army ant species males lose their wings upon entering an alien colony.
SEXUAL COMPETITION IN ARMY ANTS
239
Figure 3. SEM micrographs of the gaster of an Eciton Burchelli male. Above: overview. Below: close
up of the posterior area of the fourth abdominal tergite, showing the dense arrangement of
glandular openings.
Dealate males have been found in the Old World, Anomma rubella (Savage, 1849
in Gotwald, 1982) in the New World Labiduspraedalor (Rettenmeyer, 1963) and
in Eciton species (Schneirla, 1971) .
Though the loss of wings further increases the superficial resemblance of males
to queens, this trait is probably also functionally related to the process of wing
muscle histolysis which will provide a male with both energy and metabolic
240
N. R. FRANKS AND B. HOLLDOBLER
Figure 4. A, Schematic drawing of a longitudinal section through the gaster of a Neivamyrmex sp.
male, illustrating the segmental glandular structures. B. Longitudinal section through an
intersegmental complex-gland (between fourth and fifth abdominal segment). C, Longitudinal
section through an intersegmental sternal gland of an Eciton sp. male. A = anus; GC = glandular
cells; P = part of penis with penis gland; R = reservoir; (from Holldobler & Engel-Siege], 1982).
SEXUAL COMPETITION IN ARMY ANTS
24 I
resources probably for spermatogenesis, the production of large quantities of
attractive pheromones and sustenance for the relatively long period it must live
with the new colony before it gains access to the queen.
The remarkable convergence in external morphology of army ant males and
queens (especially in their exocrime glandular structures) may first suggest that
the males mimic queens, in order to be accepted by the workers. There is no
reason, however, for such deceitful sexual mimicry, because army ant workers
would in fact reject additional and foreign queens but must accept males for the
insemination of their queen. We conclude, therefore, that in most army ant
species the males superficially resemble females not as a form of deceitful sexual
mimicry as occurs in many other animals, including fish (Dominey, 1980; Gross,
1985), snakes (Mason ik Crews, 1985) and scorpionflies (Thornhill, 1979), but
because sexual selection acting on both the competitive ability of males and
queens and the discriminatory ability of workers had led to a convergence in the
way in which both sexes demonstrate their potential fertility. We suggest that
this is the reason why males have similar size, shape and morphology to
conspecific queens and furthermore appear to release attractive pheromones
from the same sites on their bodies. Workers in army ants are intimately
involved in all the selection procedures in reproductive colonies. Army ant
colonies are therefore perhaps the most ‘democratic’ of all insect societies.
ACKNOWLEDGEMENTS
We thank Andrew Bourke, Norman Carlin, Jae Choe, Dan Perlman, Carl
Rettenmeyer, Stuart Reynolds, Diana Wheeler, and E. 0. Wilson for reading
and commenting on the manuscript. The field work reported in this paper was
generously supported by the Smithsonian Tropical Research Institute, Panama.
This work was in part supported by Natural Environmental Research Council
and Royal Society Grants to N.R.F. and N.S.F. Grant BNS 82-19060 to B.H.
REFERENCES
BARR, D. & GOTWALD, W. H. Jr., 1982. Phenetic affinities of males of the army ant genus Dorylur
(Hymenoptera: Formicidae: Dorylinae). Canadian Journal of <oology 60: 2652-2658.
BARTZ, S. H. & HOLLDOBLER, B., 1982. Colony founding in Mynnccocystus mimicus Wheeler
(Hymenoptera: Formicidae) and the evolution of foundress associations. Bchauioural Ecology and Sociobiology,
10: 137-147.
BOCH, R. & MORSE, R. A., 1974. Discrimination of familiar and foreign queens by honeybees swarms.
Annals of thc Entomological SocieQ of Amm‘ca, 67: 709-71 1 .
BOCH, R. & MORSE, R. A., 1979. Individual recognition of queens by honeybee swarms. Annals of the
Entomological Society of Ammka, 72: 51-53.
BREED, M. D. 1981. Individual recognition and learning ofqueen odors by worker honeybees. Proceedings of
the National Academy of Sciences, U.S.A., 78: 2635-2637.
BROWN, W. L. Jr., 1975. Contributions toward a Reclassification of the Formicidae. V. Ponerinae, Tribes
Platythyreini, Cerapachyini, Cylindromyrmecini, Acanthostichini, and Aenictogitini. Starch, 5: 1-1 16.
CARLIN, N. F. & HOLLDOBLER, B., 1983. Nestmate and kin recognition in interspecific mixed colonies of
ants. Science, 222: 1027-1029.
CARLIN, N. F. & HOLLDOBLER, B., 1986. The kin recognition system of carpenter ants (Camponotrrsspp.)
I: Hierarchical cues in small colonies. Bchauioural Ecology and Sociobiology, 19: 123-134.
CHARNOV, E. L., 1982. The Thtory of Sex Allocation. Princeton: Princeton University Press.
DOMINEY, W. J., 1980. Female mimicry in male bluegill sunfish-a genetic polymorphism? Nature, 284:
546-548.
4
N.'R. FRANKS AND B. HOLLDOBLER
242
FRANKS, N. R., 1985. Reproduction, foraging efficiency and worker polymorphism in army ants. In B.
Holldobler & M. Lindauer (Eds), Expnimmtal Beavioural Ecology: 91-107. Fortschritte der <oologie, Bd. 31.
Stuttgart: G . Fischer Verlar.
FRANKS, N. R. & BOSSERT, W., 1983. The influence of swarm raiding army ants on the patchiness and
diversity of a tropical leaf litter ant community. In S. L. Sutton, T. C. Whitmore & A. C. Chadwick (Eds),
Tropical Rainforest: Ecology and Management: 151-163. Oxford: Blackwell Scientific Publications.
GETZ, W. M. & SMITH, K. B., 1983. Genetic kin recognition: honey bees discriminate between full and half
sisters. Nature (London), 3 2 : 147-148.
GETZ, W. M., BRUCKER, D. & PARISIAN, T. R., 1982. Kin structure and the Swarming Behaviour of
the Honey Bee Apis mellifna. Behavioural Ecology and Sociobiolog, 10: 265-270.
GOTWALD, W. H. Jr., 1982. Army Ants. In H. Hermann (Ed.), Social Insects, 4: 157-254. New York:
Academic Press.
GROSS, M. R., 1985. Disruptive selection for alternative life histories in salmon. Nature (London), 313: 47-48.
HALLIDAY, T. B., 1978. Sexual selection and mate choice. In J. R.Krebs & N. B. Davies (Eds), Behavioural
Ecology: an Evolutionary Approach: 180-2 13. Oxford: Blackwell Scientific Publications.
HOLLDOBLER, B., 1977. Communication in social Hymenoptera. In Th. A. Sebeok (Ed.), How Animals
Communicate: 41847 I. Blwmington, Indiana: Indiana University Press.
HOLLDOBLER, B. & BARTZ, S. H., 1985. Sociobiology of reproduction in ants. In B. Holldobler & M.
Lindauer (Eds), Expm'mental Behavioural Ecology: 237-257. Fortschritte der <oologie, Bd. 31. Stuttgart:
G. Fischer Verlag.
HOLLDOBLER, B. & ENGEL-SIEGEL, H., 1982. Tergal and sternal glands in male ants (Hymenoptera:
Formicidae). Psyche, 89: 113-132.
HOLLDOBLER, B. & WILSON, E. O., 1977. The number of queens: an important trait in ant evolution.
Naturwissenschaftm, 64: 8-1 5.
JAISSON, P., 1972. Mise en tvidence d'une phkromone d'attractive produite par la jeune ouvritre Formica
(Hymenoptera: Formicidae). Comptes Rendus de I'Acadhnie &s Sciences, series D, 224: 429-432.
JUTSUM, A. R., SAUNDERS, T. S. & CHERRETT, J. M., 1979. lntraspecific aggression in the leafcutting ant Anomyrmex octospinoms. Animal Behaviour, 27: 893-844.
MACEVICZ, S., 1979. Some consequences of Fisher's sex ratio principle for social Hymenoptera that
reproduce by colony fission. American Naturalist, 113: 363-371.
MASON, R. T. & CREWS, D., 1985. Female mimicry in garter snakes. Nature (London), 316: 59-60.
MICHENER, C. D., 1974. The Social Behaviour .f Bees. A Comparative Study. Cambridge: The Belknap Press of
Harvard University Press.
MINTZER, A., 1982. Nestmate recognition and incompatibility between colonies of the acacia ant
Pseudomyrmex f m g i n i a . Behavioural Ecology and Sociobiology, 10: 165-168.
MINTZER, A. & VINSON, S. B., 1985. Kinship and incompatability between colonies of the acacia ant
Pseudomyrmcx f m g i n c a . Behavioural Ecology and Sociobiology, 17: 75-78.
OTTE, D., 1979. Historical development of sexual selection theory. In M. S. Blum & N. A. Blum (Eds), Sexual
Selection and Repoductive Competition in Insects. New York Academic Press.
PAGE, R. E. & ERICKSON, E. H., 1984. Selective rearing of queens by workers of honey bees: kin or
nestmate recognition. Annals of the Entomological Society of America, 77: 578-580.
PAGE, R. E. & ERICKSON, E. H. Jr., 1986. Kin recogition during emergency queen rearing by worker
honey bees (Hymenoptera: Apidae). Annals ofthc Enfomological Socictp of America, 79: 460-467.
PEETERS, C. & CREWE, R., 1985. Worker reproduction in the ponerine ant Ophthalmopone berthoudi: an
alternative form of eusocial organization. Bchavioural Ecology and Sociobiology, 18: 29-37.
RAIGNIER, A. & VAN BOVEN, J. K.A., 1955. Etude taxonomique, biologique et biomttrique des Dotylur
du sous-genre Anomma (Hyrnen0ptera:Formicidae).Annales du mush R y a l du Congo Belge, 2: 1-359.
RETTENMEYER, C. W., 1963. Behavioural studies of army ants. University of Kansas Science Bulletin, 44:
281-465.
RETTENMEYER, C. W., TOPOFF, H. & MIRENDA, J. 1978. Queen retinues of army ants. Annals of thc
Entomological Society of America, 71: 519-528.
SCHNEIRLA, T. C., 1956. A preliminary survey of colony division and related processes in two species of
terrestrial army ants. Insectes Sm'aux, 3: 49-69.
SCHNEIRLA, T. C., 1971. In H.Topoff (Ed.), Army Ants: A Study in Social Organization. San Francisco,
California: Freeman.
SCHNEIRLA, T. C. & BROWN, R. Z., 1952. Sexual broods and the production of young queens in two
species of army ants. .Zoologica, N.Y., 37: 5-32.
THORNHILL, R., 1979. Adaptive female-mimicking behaviour in a scorpionfly. Science, 205: 412414.
THORNHILL, R. & ALCOCK, J., 1983. The Evolution of Insect Mating @stems. Cambridge, Massachusetts:
Harvard University Press.
TOPOFF, H., 1984. Social organization of raiding and emigrations in army ants. Advances in the Study o/
Behaviour, 14: 81-126.
TRIVERS, R. L., 1972. Parental investment and sexual selection. In B. Campbell (Ed.), Sexual Selection and the
Descent of Man: 136-179. Chicago: Aldine Publishing Company.
VISSCHER, K., 1986. Kinship discrimination in queen rearing by honeybees. Behavioural Ecology and
Sociobiology, 18: 453-460.
SEXUAL COMPETITION IN ARMY ANTS
243
WALSH, J. P. & TSCHINKEL, W. R., 1974. Brood recognition by contact pheromone in the red imported
fire ant, Solenopsis inuicta. Animal Behviour, 22: 695-704.
WATKINS, J. F. I1 & COLE, T . W., 1966. The attraction of army ant workers to secretions of their queens.
Texas journal of Science, IS: 254-265.
WEST-EBERHARD, M. J., 1983. Sexual selection, social competition and speciation. Qparterly Review of
Biology, 58: 155-183.
WEST-EBERHARD, M. J., 1984. Sexual selection, competitive communication and species specific signals in
insects. In T . Lewis (Ed.), Insect Communication: 283-324. London: Academic Press.
WHELDEN, R. M., 1963. Anatomy of adult queen and workers of army ants Eciton burchelli Westw. and
E. hamatum Fabr. (Hymenoptera: Formicidae). Journal of the New York Entomological SocieLy, 71: 14-30,
90-115, 158-178, 246-261.
WILLIAMS, G. C., 1966. Adaptation and Natural Selection: a Critique of Some Cunmt Evolutionary Thought.
Princeton: Princeton University Press.
WILSON, E. O., 1971. The Insect Societies. Cambridge, Massachusetts: The Belknap Press of Harvard
University Press.