Reproductive Adaptations of Eusocial Ant Colonies

ABSTRACT

	In the past decade, many entomologists have noticed that the social organization of some ant 
colonies is quite varied.  It has been found that in the more primitive species, such as in the Ponerine 
family, the reproductive duties are diverse.  There may be a queen present, or there may not.  These 
two distinctions can further be divided into whether or not the queen is the sole reproducer or if some 
of the worker ants are reproductive as well.  These fertile workers are referred to as gamergates.  
Relatedness of ants in a colony is directly related to whether or not they all come from one ant or a 
variety of gamergates. 

	There are dominance structures that go along with each of the above mentioned socio-
reproductive arrangements.  If there is only one reproductive ant, either a queen or a sole gamergate, 
then a hierarchical social structure is maintained.  The dominant ant keeps her reign through aggressive 
behavior such as antennal boxing and pulling of mandibles, inhibiting the reproduction of males, and, 
more simply, by her ability to reproduce.  In colonies where many reproductive ants co-exist, there is 
often no social control or inhibition by reproducers toward subordinates.  Instead, insemination controls 
reproduction.  Regardless of which type of structure exists, the role of regulating reproduction is 
important in keeping the division labor at an  optimal level for prime colony functioning.

	Behavioral characteristics, some of which were mentioned above, come into play here as well.  
Most reproductive ants stay underground (intranidal), but others, including those who aren't able to 
reproduce, are extranidal.  A colony with a sole reproducer tends to have aggressive workers who 
protect her and help her maintain her status.  In colonies with multiple reproducers, the ants with 
developed ovaries are attacked more often than others.  Additionally, younger ants are more 
aggressive than older ones.  Finally, there may be further distinction by age and size.

INTRODUCTION

	The organization of ant colonies is quite variable (Sommer et. alt., 1994).  Reproductive 
arrangements are one way that colonies differ from one another.  There is an enormous amount a 
variation within the primitive ant family, Ponerine, as well as in some fire ant species.  Sommer and 
Holldobler (1992) explain why Ponerine ants are considered primitive.  In this family, each worker 
possesses a spermatheca and therefore, has the potential for reproduction.  Whereas, in more advanced 
ant species, workers either have no ovaries or they are at least reduced.  This is important because, in 
eusocial colonies, reproductive capabilities influence social status.

	  Within these eusocial species, there are generally three types of colony arrangements.  Each 
arrangement is defined according to the number and type of reproducer(s).  According to Herbers and 
Stuart (1996), the variation in queen numbers is the result of a "complex interplay between genetic 
and ecological factors" (p. 161).  The first type of colony found is a queenright, monogynous colony in 
which one morphologically different female ant is the only reproducer.  The second colony arrangement 
is a monogynous, worker reproductive colony in which a single female controls reproduction, but she is 
not morphologically different from her nestmates. Finally, the third type of colony is a polygynous one.  
In this colony, varying numbers of workers share reproductive responsibilities (Ward, 1983).     

	These three arrangements vary from nest to nest, making each colony unique.  For example, 
Ward (1983) found that with some groups queens and mated workers never live in the same nest 
together (Rhytidoponera impressa  group).  In this group, the colonies with worker reproduction are 
smaller and have more males, whereas the queenright colonies are opposite.  Additionally, in the 
queenright colonies of this group, there may be more than one ant with reproductive capabilities 
(dealate), but only the queen is ever inseminated (Ward, 1983).  In contrast, the Pachycondyla 
tridentata  group occurs both with and without queens (Sommer and Holldobler, 1994).  In this group, 
both queens and gamergates compete equally for reproductive status, and the number of gamergates 
per colony varies. 

DISCUSSION

MORPHOLOGY/ SIZE & AGE DISTINCTIONS

	There are three primary morphological differences in reproductive ants.  Queens are different 
because they have vestigial wings.   These ants can dimorphise into wingless queens, also called 
ergatoid queens, as well.  Finally, there can be reproductive workers, or gamergates, which are found 
in polygynous colonies.  When looking at these morphological differences in terms of evolution, the 
reproductive workers are most primitive with winged queens being the most evolutionarily advanced.

	Colony makeup is based on the number and size of the colony inhabitants.  Queenright colonies 
tend to have bigger workers and males.  They also generally have more workers, and produce larger 
offspring (Ward, 1983).  On the other hand, polygynous colonies are the opposite.  Peeters (1987) says 
that gamergates lack morphological specialization and thus, reproduce slower.  Additionally, there are 
larger eggs in worker-reproductive colonies when compared with queenright colonies of the same group 
(Peeters and Crewe, 1985) even though queenright colonies produce larger offspring.

	Division of labor behavior distinctions can be looked at from the ages of the ants.  For example, 
as Villet (1991) explains, newly hatched adults rest for two weeks.  Then they tend to other cocoons.  
Next, they carry eggs and tend to them.  Interestingly, this occurs when the ants' ovaries are most 
physiologically active.  After this, they take care of the nest, and finally, perform tasks outside the 
nest.  Therefore, labor is divided up according to age, not size as one might think.

BEHAVIOR: General

	According to Villet (1991), behavior is affected by seasonal change, colony size, and the 
presence of a queen.  Queenright colonies usually have more sophisticated foraging and recruitment 
strategies than polygynous nests.  Tsuji (1988) also differentiates ants' behavior by whether or not 
they are active inside the nest (intranidal) or outside (extranidal).  Intranidal ants are those who stay 
under ground.  They are bigger than extranidal, have less behavioral differentiation, and have well 
developed ovaries.  Extranidal ants are those who work above ground.  Their behavior is differentiated, 
and their ovaries are less developed which usually keeps them from reproducing.  

	Villet (1991) found over 40 different behaviors when he studied the polygynous Platythyrea cf. 
cribrinodis  group.  Mated workers performed 14 of these, males performed 13, and non-reproductive 
workers performed the remaining.  Villet (1991) divides these behaviors into four major categories  
which include: care of eggs, care of larvae, care of cocoons, and personal and social behaviors.  Within 
these four categories, he found a large degree of task swapping among workers except for in a few 
specialized areas.  Two of these specialized areas include the brood nurses, who focused their 
activities on the care of eggs and newly hatched ants, and the mated workers who spend their time 
resting, caring for their brood, nest maintenance, and other miscellaneous, personal-oriented 
behaviors.  According to Ward (1983), mated workers stay close to the broods, are groomed by non-
reproductive workers, and never forage.  Therefore, non-reproductive workers have a variety of 
duties, and task swapping indicates that a great variety of behaviors are performed by each individual 
ant.  There is no morphological explanation for these divisions, and it is believed to occur because many 
tasks can be combined together for efficiency on achieving a common goal (Villet,1991). 

BEHAVIOR: Dominance

	According to Sommer et. alt. (1994) there are two primary forms of aggressive behavior: 
antennal boxing, where one dominant ant antennates another with rapid movements, and the pulling of 
an opponent's mandibles.  Antennal boxing is performed mainly by mated workers toward other mated 
workers (Ward, 1983), but mandible pulling is performed by all ants.  

	There are also dominant behaviors associated with reproduction.  For example, when Oliveria 
and Holldobler (1990) compared monogynous and polygynous colonies, they found that queens and 
wingless (ergatoid), dominant ants control by mutilation.  In contrast, gamergates of polygynous 
colonies do not control their nestmates.  In  polygynous colony arrangements, aggressive behavior is 
rarely displayed among reproductives (Evans, 1996), but there are conflicts between workers as they 
jockey for higher rank.

	Ponerine ants have both hierarchical and linear dominance arrangements.  Hierarchical 
arrangements are found with monogynous colonies.  Colonies with either a queen or only one ergatoid 
gamergate show signs of control by the dominant single reproductive ant through removal of the 
vestigial wings of newly hatched female adults.  The removal of the vestigial wings produces a 
phermonal change which enables the queen to then reign over her children without force.  Removing the 
wings is only possible because workers hold the newborns captive while their mother mutilates them 
(Peeters and Higashi, 1989).  It has been shown that unmutilated callows behave aggressively, while 
those mutilated are timid (Peeters and Higashi, 1989).  When the queen leaves, a new worker will 
mutilate the others to stake her claim.  Finally, if eggs are produced by another ant in a monogynous 
colony, the queen promptly eats them.  

	According to Oliveira and Holldobler (1990), workers in monogynous colonies compete for 
higher status by attacking one another.  They found that a worker could endure an attack for up to an 
hour, and that during an attack, the subordinate ant usually remained submissive.  The attacks did not 
cause any physical injury, and, if the queen was present, the attacks decreased.  They were 
"extremely" common in her absence because this is the way the ants form new dominance hierarchies.

	In colonies with multiple gamergates, social control and inhibition are absent (Peeters and 
Higashi, 1989).  Instead, linear dominance arrangement are found.  In these arrangements, gamergates 
do not interact with other nestmates very often (Peeters and Crewe, 1985).  Additionally, gamergates 
are not given preferential treatment at feeding times (Peeters and Crewe, 1985).  In polygynous 
colonies, varying numbers of ants, but not necessarily a morphological queen, occupy top positions 
(Sommer and Holldobler, 1994).  But, all top positions are held by ants with well-developed ovaries.  In 
fact, those who are subordinate but have well-developed ovaries are attacked more often than non-
reproductive ants (Sommer et. alt.,1994).  Sommer et. alt. (1994) state that "non-reproductive ants 
are much more aggressive towards foreign ants" (p. 180).  Finally, Ward (1983) found that in these 
nest arrangements, reproductive workers, regardless of whether or not they are mated , behave 
timidly".  

	Age may also influence dominant behavior patterns.  For example, Balas and Adams (1996) 
found workers from incipient colonies to be less aggressive toward conspecific non-nestmates that are 
workers from reprodutively mature (older) colonies.  Additionally, newly hatched workers, called 
callows, are more aggressive than older workers (Sommer et. alt., 1994). Therefore, as a colony 
ages, or if it is infiltrated by older ants, aggressive behavior is diminished.

BEHAVIOR: Reproductive control

	Reproductive  regulation is important for maintaining a cohesive division of labor (Villet, 
1991).  Monogynous and polygynous colonies have different ways of controlling reproduction.  For 
example, there is no social control over the number of reproductives when gamergates reign, but 
queens efficiently control the numbers of reproductives (Peeters and Crewe, 1985).  Not only do they 
control the numbers, but they also control what sex offspring will be.  

	The female queen should control the number of haploid and diploid eggs produced in a ratio that 
maximizes her fitness.  Since a queen's best fitness is achieved by  producing an even ratio of males 
and females, one would assume that even haploid and diploid production would occur (Keller et. alt., 
1996).  But, Keller (1996) only found this to be the case if the colony was likely to fragment.  
Otherwise the queen produced fewer male eggs.  Additionally, workers had partial control by eating 
male eggs before they hatched.  Workers do this because their best fitness is achieved if the sex ratio 
is female biased, but it seems that they know not to destroy male eggs if colony fission or 
fragmentation is eminent.

	In polygynous colonies, insemination controls reproduction (Peeters and Higashi, 1989).  
Insemination triggers egg laying and influences behavior.  It triggers ovarian activity (Peeters and 
Crewe, 1984) and therefore, it alone controls reproduction.  Additionally, insemination alters the 
phermones of the ant, thus altering their behavior.  An example of this is seen in rare instances when 
extranidal ants become inseminated and then shift into intranidal (Peeters and Crewe, 1984).  There is 
also a seasonal fluctuation in gamergate numbers which can regulate reproduction (Peeters and Crewe, 
1985).  As the number of mated workers increases, the number of oocytes produced by each declines.  
Thus, reproductive output is shared fairly equally (Ward, 1983).  

	Another control of reproduction can be seen in the Ophthalmopone group, which Peeters and 
Crewe (1984) discuss.  In this group males are only active for a few months, and will only mate inside 
the nest.  Therefore, those ants who remain underground for various reasons have a high likelihood of 
becoming inseminated.  This means that the numbers of ants allowed to reproduce are not regulated.  
Instead, insemination results by chance--from the number of male visits and the number of young ants 
present underground at the time of the male visits.   

	Colony fission and the need to found new colonies may also contribute the the number of eggs 
that are fertilized.  Keller et alt. (1996) found that there are more haploid eggs laid in polygynous 
colonies than monogynous because it is a way to achieve higher reproductive success when the colony 
loses all its queens through the founding of new colonies.  On top of this, Sasaki et. alt. (1996) found 
that in cofoundress colonies, cooperative behavior is often exhibited, and that reproductives do not 
aggregate with sisters preferentially as one might suspect. 

RELATEDNESS

	Ward (1983) explains that parental offspring control is looked at as an evolutionary 
advancement for eusociality because it works in concert with kin selection.  This is displayed with 
queenright colonies in which monogyny is proved because there are no more than two genotypes present 
(Ward, 1983).  Even so, Evans (1996) found that queens do not alter their egg laying behavior in 
accordance with relatedness.

	In contrast, there is a high genotypic diversity in worker reproduced colonies due to the fact 
that more than one ant is inseminated.  The result, sister and cousin ants are produced (Ward, 1983).  
In fact, not all of the offspring can even be guaranteed to be related because of colony fission (Ward, 
1983).  This can affect nestmate recognition, which is important for social integrity (Peeters and 
Crewe, 1985) as well tolerance amongst nestmates themselves (Sommer and Holldobler, 1992).

STARTING A NEW COLONY/WHY DIFFERENT EUSOCIAL ARRANGEMENTS EXIST

	Ward (1983) comments that queenright colonies are found in rainforests, but that they are 
rarely found in open woodlands.  This is because these areas are subject to fires, floods, and droughts.  
Therefore, in these habitats, founding new colonies may be needed, making polygyny more appropriate. 
 
	When looking at queenright nests, queens are seen as "expensive" (Sommer and Holldobler, 
1992) because they are an energy burden.  If there is only one queen, her energy goes solely to 
reproduction (Banschbach and Herbers, 1996).  Therefore, one must investigate what might happen 
when a queen dies.  Villet (1991) says that either the first ant to mate assumes control, or many ants 
may mate and then break off to form new colonies.  Ward (1983) also thinks that fission may occur 
when colony relatedness drops below a certain level.

	Sommer and Holldobler (1992) state that when alternative dispersal strategies are used by a 
colony, there is often a correlation with having two reproductive entities within that colony.  This 
supports what Ward (1983) thinks when he describes how worker reproduction may be due to orphaned 
queenright colony fragments who need to reproduce to survive.  Or, as Tsuji (1988) states, polygyny 
may occur because of the need to maintain large colonies due to a  nomadic lifestyle.  Tsuji (1996) 
further explains that there are two types of polygyny.  The first is an adaptation to short-lived 
habitats.  In these environments, colony fragmentation is common.  Second, patchy habitats use 
polygyny in expanding their colonies by filling in the patches through fission.  Either way, polygyny is 
adaptive because fission, colony fragmentation, no ceiling on egg production, no energy waste, and 
avoiding parasitism of a vulnerable queen are all achieved (Tsuji, 1988). 

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