Nestmate Recognition in Social Wasps (Polistes, Hymenoptera: Vespidae)
R. Jason Bishop
Abstract
The more charismatic fauna of the animal kingdom are not alone when it comes
to the need to discriminate between kin and non-kin individuals. Insects also face
this dilemma. The ability to discriminate between nestmate and non-nestmate kin
among social wasps can mean the difference between successful propagation and
usurpation of colony resources. This paper reviews of previously studied aspects of
kin recognition and employs the findings of prominent scientists in the field. The
phenomenon is well studied as there is a need to learn how and why species identify
their own kind. There are several issues which need to be covered when one
considers kin recognition. First, a working definition of kin recognition is needed
so as to be able to identify a given behavior as such. The behavior then needs to
be identified as it is observed in social wasps. Next, it is useful to know the
mechanisms of kin recognition. The mechanism of kin recognition in social wasps is
chemical in nature. The adaptations of the behavior are also discussed. The
adaptations of importance to social wasps involved in nestmate recognition are
primarily centered around the individuals utilizing the behavior as well as those
individuals subjected to recognition activities. The significance of recognition in
each arena will also be discussed. Nestmate recognition is vitally important to the
success of a social wasp colony. Improper identification may have dramatic
ramifications. Specific examples are presented for nestmate and non-nestmate
recognition in social wasps, (Hymenoptera: Vespidae) with special attention paid to
Polistes fuscatus. Examples from other Polistes species are included.
Key words: Polistes, Hymenoptera, Vespidae, nestmate recognition, social wasps
Introduction
Studies show that animal species have remarkable capacities to recognize their
own kind (Grafen 1990). Numerous studies have been done on the behavior
demonstrating the wide array of mechanisms used and responses elicited by either
positive or negative encounters. Eusocial insects, particularly the social wasps,
provide an ideal arena for the study of nestmate recognition. Social wasps of the
genus Polistes can occur in large numbers as they tend build combs in aggregations
(Pfennig 1990). In this context researchers have available interactions between
nestmates, non-nestmates, kin, and non-kin, and the perfect natural setting in which
to observe recognition and discrimination behaviors. Gamboa (1986) provided an
extensive model review of nestmate recognition in social wasps.
A Definition of Kin Recognition
There is some disagreement in the literature as to what exactly constitutes
kin recognition. Grafen (1990) defines the phenomenon as 'a system whose use and
function is to assess the kinship of conspecifics.' Many feel his definition is too
restrictive (Stuart 1991; Gamboa 1991). According to Grafen (1990) all systems of
kin recognition involve only genetically bases cues, implying that recognition of
groups or individuals based on other available cues do not serve to discriminate kin
from non-kin. Gamboa (1991) assesses this definition to be more linked to kin
selection than recognition. Group and individual systems of recognition should be
considered systems of kin recognition provided that the groups or individuals being
scrutinized are consistently kin (Stuart 1991). Stuart goes on even further to
discern nestmate recognition in social wasps as actually being a less highly evolved
form of kin recognition (Stuart 1991). This contention is based on the notion that
nestmate recognition in social insects often involves a group recognition mechanism
and integrates genetic and environmental cues which function as forms of kin
recognition. Grafen (1990) excludes such systems from consideration.
In this paper the term 'nestmate' recognition will be used as this is how it
is most commonly seen in the literature. For the purposes of this paper nestmate
recognition is to be broadly defined as the differential treatment of conspecifics
according to their nest of origin (Gamboa (1986).
In the literature, nestmate recognition activities are primarily identified as
values of tolerance. In the studies which looked at mechanisms of nestmate
recognition researchers consistently measured tolerance among members on the nest as
well as individuals introduced to the nest. Individuals recognized as nestmates
were not only more spatially tolerated, but were also preferentially involved in
cooperative nest building activities (Gamboa 1986). Non-nestmates, recognized to be
harmful intruders were not tolerated on the nest.
Mechanisms of Nestmate Recognition
Expression, Perception, and Action
Gamboa (1986) suggests that a useful definition of nestmate recognition
consists of two distinct components: (1) expression of a recognition cue and (2)
perception of that cue. He later amended this definition to include a third
distinct component which he termed the 'action' component (Gamboa 1988). The
expression component not only involves the nature and production of the recognition
cue, but also includes the acquisition of cues used in the identification of kin
(Gamboa 1986). The perception component involves the development of a template of
the cue, the processing of that cue once perceived and the algorithm used to match a
perceived cue with the template (Gamboa 1986). Finally, the action component refers
to the action taken by an individual once the recognition cue has been assessed
based on its similarity to its template (Gamboa 1986).
It is well known that the recognition cues expressed, perceived, and acted
upon among members of the order Hymenoptera are chemical in nature (Hepper 1991).
Specifically, behavioral studies of the paper wasp, Polistes fuscatus, have
established that nestmate recognition is based on chemoreception (Espelie 1994).
Furthermore, recent studies have shown the chemical cues used by Polistes metricus
to manifest themselves in the form of cuticular hydrocarbons (Singer 1992; Espelie
1994). In fact, cuticular hydrocarbons have been shown to be the basis of
chemoreception in other Polistes species including P. fuscatus (Espelie 1994) and
P. annularis (Espelie 1990).
Acquisition
The acquisition of recognition odors is a critical element of the expression
component of nestmate recognition as it has been defined. Gamboa et al. (1986)
determined that the recognition odor has a significant environmental origin. Later
surveys gave a slight indication that the odors may have a heritable component but
this facet of nestmate recognition in the social wasps is poorly studied. On the
other hand, the environmental origin of the recognition odors has been greatly
scrutinized. It is now known that prior exposure to the nest is required for gynes
in Polistes in order for recognition to occur (Shellman 1982). This phenomenon was
evidenced in the observation that gynes isolated from their natal nest immediately
following emergence failed to recognize their nestmates (Shellman 1982). The amount
of time newly emerged adults spend on the nest directly after emergence is also
important to the acquisition of the odors. Pfennig (1983b) showed the learning of
recognition cues to be very rapid. Recognition cues are in fact learned in the
adult stage and can be learned in as little as one after of emergence (Pfennig
1983a). Pfennig (1983a) also determined that recognition cues were not learned from
other adults or the emerged adults themselves, rather the odors were learned from
the natal nest and/or brood within the nest
An understanding of the acquisition of recognition odors now gives one insight
into the expression as well as perception component of nestmate recognition.
Expression of the chemical cue now seems to be a simple "wearing" of the odor which
has been previously shown to be a cuticular hydrocarbon acquired in the natal nest.
Perception of the cue can now be said to be a matter of first learning the odor from
the natal nest after emergence followed by a recognition of said odor on and
encountered individual (Gamboa 1986a, Pfennig 1983a). The action component of
nestmate recognition is the critical step for social wasps as it details which
individuals recognize what, as well as the results of recognition, whether they be
positive or negative. The action component is identified by the adaptations of
nestmate recognition as they appear in social wasps.
Adaptations of Nestmate Recognition
At this point it would be useful to employ a change in terminology. As one
discusses the adaptations of the behavior at hand it might prove more useful to
qualify observed actions as discriminations rather than recognitions. Although the
literature does not explicitly differentiate the two, in fact the two are often used
interchangeably, it is my estimation that the term 'discrimination' is more
appropriate in the context of application.
Now that the behavior has been observed and its mechanisms determined there
only remains the matter of what use this behavior of nestmate discrimination is to
the social wasps. One can easily determine the benefits of recognizing the origin
of an individual making an appearance on a nest. It would not be difficult to
realize the importance of quickly recognizing potential predators, particularly if
said predator is of another order, family, or genus. The question here is what good
it does for the social wasps to discriminate among conspecifics. It has been well
documented that nestmate discrimination in social wasps occurs among spring
foundresses (Ross 1981), aunts and nieces (Bura 1994), workers (Pfennig 1990), and
males (Ryan 1986). Additionally, foundresses of P. fuscatus can discriminate kin
from non-kin brood (Klahn 1983). The following is a review of the evidence for the
above mentioned recognition abilities along with a discussion of the implications of
these actions.
Spring Foundresses
In a study involving foundresses of Polistes metricus Ross (1981) determined
that overwintered P. metricus gynes have the ability to distinguish former
nestmates (probably sisters) as well as to collaborate with them in nesting efforts.
Nestmates were found to be more tolerant of each other than were non-nestmates.
Results from this study also revealed that foundresses may not have to overwinter
together in order to retain recognition abilities but do require a period of
interaction before accepting each other's presence. Ross did not speculate on any
possible benefits of the ability to discriminate among spring foundresses, however
the action does seem to facilitate associations among sisters. Nestmates spent
significantly less time engaged in agonistic behaviors than did non-nestmates
thereby allowing more productive nest constructing activities (Ross 1981).
Aunts and Nieces
Bura (1994) determined that the relatedness, as well as the caste, of
interactants plays a role in the tolerance of non-nestmate intruders in a study
involving P. fuscatus gynes. This was evidenced by the observation that aunts who
were queens were less tolerant of intruders than were their nieces. Fishwild and
Gamboa (1992) made similar observations. The hypothesis is that queens require a
better match for acceptance than do workers as queens may incur more negative
fitness consequences for accepting non-nestmates than would workers (Bura 1994).
Conspecific intruders kill and/or replace queens, not workers. Proficient
recognition by queens (presumably aunts) then becomes critical to the propagation of
her genes as workers (presumably nieces) do not serve in an adequate recognition
capacity.
Workers
Because of the fact that female Polistes are strongly philopatric, nests tend
to occur within 10 m of the location of their parental nest from the previous year
and usually occur in aggregations (Pfennig 1990). In this context there is
opportunity for interaction between workers from neighboring nests. Pfennig (1990)
examined such interactions involving P. exclamans inhabiting a dense aggregation.
This study reveals that these wasps can not only discriminate nestmates from non-
nestmates but can also discriminate among workers from their own nest and foreign
nests as well as workers from nearby and more distant nests. Much information can
be gleaned from these interactions. Wasps seem to gain information on which nests
to aid and which nests to rob (Pfennig 1990). Pfennig proposes that these findings
support the notion that all conspecifics and nests occurring beyond a certain
distance are treated a foreign.
Pfennig's study also shows how wasps treat orphaned workers from other
colonies. If an orphaned worker is allowed to join the nest the benefits could be
far reaching. The addition of a worker could aid in the foraging and defense
abilities of the nest. On the other hand, acceptance of a worker into the nest
could result in the loss of brood as the intruder may be a mere thief, robbing the
colony of mature larvae for use as food in its own nest (Pfennig 1990).
Conspecific usurpation pressures are intense in related species P. fuscatus
(Gamboa 1992)and P. metricus (Gamboa 1978). It would be reasonable to assume that
many of the same pressures are operating among P. exclamans . Although the
usurpation pressures in the prior two species tend to occur during preworker stages,
it is clear that a poor decision in discrimination could be followed by a nest
containing few advanced larvae in all three, particularly P. exclamans (Pfennig
1990).
Males
Although the phenomenon is poorly documented and the significance of the
interaction is unknown (Gamboa 1986), male P. fuscatus have been shown to recognize
male nestmates (Shellman-Reeve 1985).
A recognition ability is also seen between gynes and male P. fuscatus (Ryan
1986). Again, the phenomenon is poorly documented and findings are unclear as to
the significance of male/female recognition abilities. Experimental results do
document nestmate recognition between males and gynes but do not indicate whether
males, gynes, or both males and gynes have the ability to recognize nestmates of the
opposite sex (Ryan 1986). Implications of mate selection through recognition are
sketchy, but there is evidence from other Hymenoptera of negative fitness
consequences of inbreeding (Ryan 1986).
Kin and Non-kin Brood
Colony-founding Polistes fuscatus queens have been shown to have the ability
to discriminate between brood-filled combs of their sisters and those of less
closely related females (Klahn 1983). The recognition of related brood combs has
been connected with cooperative colony-founding associations among sisters (Pardi
1948). Such associations serve to better the fitness and survival of the broods by
having more adults around to defend and forage for the combs. The recognition of
foreign brood may have even more dramatic effects. A female recognizing a brood
comb of a single foundress has a great opportunity for usurpation. Older brood are
spared and, upon eclosion, are exploited by the usurper to tend her own brood (Klahn
1983). Younger brood are destroyed, yielding three possible advantages to the
usurper: 1) cells are emptied of resident larvae and filled with her own eggs, 2)
competitor's genes are removed, and 3) brood may be eaten by herself or used as food
for her own offspring (Klahn 1983). In any light, the ability to discriminate kin
from non-kin brood has importance significance to the social Polistes .
Final Comments
Nestmate recognition in social insects has been greatly studied in the past
decade and a half, however there remain many issues that are either unresolved or
unexplored (Gamboa 1986). As suggested by Gamboa (1986) a major goal seems to be
the exploration of a possible unified mechanism of recognition among all social
insects. Furthermore, by looking more closely at the dissimilarities, as well as
the similarities, of recognition mechanisms among social insects a better
understanding of the evolution of these behaviors may be at hand (Gamboa 1986).
More specifically, Gamboa (1986) points out that nestmate discrimination has
been widely documented in the social wasps. Research spans six temperate species
from three genera and two subfamilies. According to Gamboa (1986) P. gallicus is
the only species of social wasp in which nestmate discrimination abilities has been
studied but not documented. This is significant because a lack of documentation
does not necessarily indicate a lack of ability, rather an insensitivity in a
particular assay for detection of the behavior (Gamboa 1986). It is clear that many
consistencies are found among social wasps in the behavior of nestmate recognition,
particularly among members of the Polistes paper wasps. It seems reasonable that
documentation of nestmate discrimination in P. gallicus would show the behavior to
manifest itself in ways very similar to those already discussed here. The wasps
apparently use cuticular hydrocarbons as the principal chemical recognition cue.
This cue would most likely be learned only in the presence of the natal nest and
learned within one hour of emergence. Furthermore, it seems likely that P. gallicus
uses the ability to discriminate kin in much the same adaptations as seen in P.
fuscatus, P. metricus, P. exclamans, P. carolina, P. annularis, etc.
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