Queen
Number
Sociality
and
in Insects
EDITED
LAURENT
BY
KELLER
Museum of Comparative Zoology,
Harvard University, Cambridge, USA
and Museum of Zoology,
Palais de Rumine, Lausanne, Switzerland
Oxford
OXFORD
New York
UNIVERSITY
1993
Tokyo
PRESS
9
Serial
polygyny
Ropalidia
evolution
in the primitively
marginata:
of sociality
implications
eusocial
wasp
for the
Raghavendra Gadagkar, Krishnappa Chandrashekara, Swarnalatha
Chandran, and SeethaBhagavan
Social insects usually live in colonies comprising one or a small number of
reproductive individuals and a few or large number of sterile individuals.
In termites only, both sexesare represented among the reproductives as
well as among the sterile workers. In other social insects, namely ants,
bees, and wasps, males do not participate significantly in the social life of
colonies, which involves primarily the fertile queens and sterile female
workers (Wilson 1971). The haplodiploid genetic systemfound universally
in the Hymenoptera creates an asymmetry in genetic relatedness such
that a female is more closely related to her full sister (coefficient of
genetic relatedness,r = 0.75) than to her offspring (r = 0.5). This makes
inclusive fitness theory (Hamilton, 19640,b) particularly applicable to the
evolution of sterile worker castesin the social Hymenoptera (Wilson 1971;
Hamilton 1972).
However, two phenomena tend to break down this genetic asymmetry
and decrease the inclusive fitness that workers might have otherwise
gained by rearing siblings instead of their own offspring (Hamilton 1964b).
One is polyandry, or multiple mating by queens. Hymenopteran queens
can mate with several males, store sperm from all of them in their
spermathecae,and use their sperm simultaneously, thus producing several
patrilines of daughters who are half-sisters (r = 0.25). This can lead to
considerable reduction in the relatednessbetweenworkers and their female
siblings. Th~ implication of polyandry for the evolution of sociality has
receivedconsiderableattention (seereviews in Starr 1984; Gadagkar 1985b;
Page 1986). The second is the presence of multiple queens or egg-layers
within a colony (polygyny). Polygyny leads to different matrilines within
a colony but its consequencesfor worker-brood geneticrelatednessdepend
on the number of queens,relatednessamong them, and relatednessbetween
workers and queens (see Queller this volume).
Polygyny can be of two kinds. One involves the simultaneous presence
of multiple egg layers in the colony while the second involves frequent
190
RaghavendraGadagkar et a/.
analysis to study the effects of polyandry and pedigree analysis to study
the effects of serial polygyny.
The primitively
i
:.
eusocial
wasp Ropa/idia
marginata
RopaJidia is a large Old World polistine genus with about 136 known
speciesoccurring in Africa, Southeast Asia, Australia, and the Okinawa
islands of Japan (Vecht 1967). This genus contains both relatively highly
eusocial, swarm-founding, enveloped-nestbuilding specieswith large colony
sizes as well as primitively eusocial, independent-founding, open-nest
building specieswith relatively small colony sizes(Jeanne 1980; Gadagkar
1991a). RopaJidia marginata, a speciesthat belongs to the latter group,
is abundantly distributed in peninsular India. Colonies of R. marginata
may be initiated throughout the year by one or a small group of. females
(Gadagkar ec aJ. 1982). In multiple foundress nests, only one female
becomes the egg layer while others assume the role of workers. Female
offspring may either leave their natal nests to found new single- or
multiple-foundress nests or they may stay and assumethe role of workers
(Gadagkar 1991a). R. marginata exhibits a typical polistine-like colony
cycle with rapid growth in the pre-emergenceand early post-emergence
phases, followed by a declining phase after which, a small number of
females may stay to start another colony cycle on the same nest. In this
manner a series of colony cycles may. be encompassedwithin one nesting
cycle (Gadagkar 1991a; Jeanne 1991; Chandrashekara et aJ. 1990). An
important consequence of such an indeterminate colony cycle is that
colonies often outlive their queens (Gadagkar et aJ. 1990). This provides
opportunities for other adults of the colony to take over the role of
queens. Because such change-over of queens may occur at various times
in the colony cycle, workers who are offspring of one queen often rear
brood that are offspring of another. Apart from such serial polygyny,
R. -marginata exhibits strict monogyny at any given time. This is of
course difficult to prove because it is based on negative evidence. But
in well over 1000 hours of observation of dozens of colonies during the
last 10 years, we have never documented.the simultaneous presence of
two or more egg layers. Some but not all workers in R. marginata are
inseminated. Even the queen may sometimesbe uninseminated at the time
of taking over the role of the queen although she may mate subsequently
(Chandrashekara and Gadagkar 1991).
Data collection
~
Our studies reported in this chapter are based on four colonies of R.
marginata that were established by transplanting four post-emergence
colonies (including the nests and adults) into cageslocated at the Centre
I
L
-
Serial polygyny
in Ropalidia marginata
191
for Ecological Sciences, Indian Institute of Science, Bangalore. These
cages were made of wire mesh which allowed wasps to forage freely
outside but prevented the hornet Vespatropica from attacking the brood.
Long-term studies of R. marginata are almost impossible without such
protection from high rates of V. tropica predation. Colony TOI was
collected from a site 7 km away on 14 September1986and was monitored
for 606 days until it was abandoned on 17 May 1988. This colony had
33 Cggs,25 larvae, 8 pupae, and 4 empty cells when it was collected
and transplanted. Colony T02 was collected from a site 2 km away on
9 February 1987and was monitored for 474 days until it was abandoned
on 24 May 1988. This colony had 14 eggs, 15 larvae, 7 pupae, and 5
empty cells when it was collected and transplanted. Colony T08 was
collected from a site 15 km away on 6 June 1987and was monitored for
315 days till it was abandoned on 15 April 1988. It contained 43 eggs,
17 larvae, and 10 pupae when it was collected and transplanted. Colony
Tll was initiated naturally inside one of our protected cages, by a group
of females who had abandoned their transplanted nest on 5 August 1987,
and was monitored for 272 days till it was abandoned on 2 May 1988.
Starting from the day of transplantation, we maintained a map of
each nest, so that every cell was numbered and its contents noted at
intervals of approximately one to two days. All adults present at the time
of collection and transplantation, as well as those eclosing subsequently,
were marked with unique spots of enamel paint. A census of all the
animals present was made at night at intervals of approximately one to
two days. The identity of the cell from which each animal eclosedwas also
noted. These colonies were under behavioural observation of differing
intensities for other experiments. Consequently, the identity of the egg
layer was known for all nests at all times. A change in the queen of any
colony became known within a day or two of the event.
The system
of serial
polygyny
in Ropalidia
marginata
Figure 9.1 illustrates the indeterminate colony cycle of Ropalidia marginata and shows that the timing of queen replacementsbears no obvious
relation to the phase of the colony cycle. Data in Table 9.1 give a
glimpse of the system of serial polygyny in R. marginata. While the
durations of our studies ranged from 280 to 606 days, the number of
queens seen per colony ranged from 2 to 10. The mean tenure of queens
was about 80 days but it varied enormously, ranging from 7 to 236 days.
The ages of queensalso varied considerably, with values of 4 to 78 days
at the beginning of their tenure and 37 to 262 days at the end of their
tenure. The productivities of different queens were highly variable, as
was the proportion of eggs laid by queens that successfully eclosed as
adults. The maximum value for the latter was only 0.68 indicating that
192
Raghavendra Gadagkar et al.
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Fig. 9.1 Growth and development of the four colonies used in this study. The
survival of these colonies for long periods was associated with possible serial
polygyny. Events of queen turnover are shown by vertical arrows.
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Serial polygyny
in Ropalidia marginata
any social insect species. Note that for colonies TO8 and for Tll,
195
the
relationship between queen 1 and queen 2 was unknown. This is because
both queen 1 and queen 2 were present on the nest at the time of
collection and transplantation. In the analysis, we first make the assumption that queen 2 was the daughter of queen 1 and then repeatthe analysis
assuming that queen 2 was the sister of queen 1. Worker-brood genetic
relatednessfalls to rather low values (see below) even with these assumptions. Therefore, we did not repeat our analysis with assumptions of
even more distant relatednessbetween queen 2 and queen I. The central
messagethat emergesfrom Fig. 9.2 is, once again, that extensivevariation
exists among colonies. The simplest pedigreeis that of colony TO1, where
each queen is the daughter of the previous one, and at the other extreme
is the rather complex pedigree in colony TO8. When the pedigrees of all
four colonies are considered simultaneously, new queens are seento be
daughters, sisters, nieces, or cousins of their immediate predecessorqueens
(Fig. 9.2).
Genetic
relatedness
between
workers
and brood
The pedigrees in Fig. 9.2 lead to temporal and inter-colony variations
in genetic relatedness between workers and brood. The relationships
actually observed depend on the extent of overlap betweenadult offspring
and brood of various queens. The extent of such overlap is shown in
Fig. 9.3. When all colonies are considered, we find brood to be sisters,
brothers, niecesand nephews,cousins,cousins' offspring, mother's cousins,
Table 9.2 Geneticrelationships betweensuccessivequeensand betweenworkers and
brood observed in the four colonies.
Relationship between
Relationship between workers and brooda
queens and their
immediate predecessors
(a) Daughters
(b) Sisters
(c) Nieces
(d) Cousins
(I)
(2)
(3)
(4)
(5)
(6)
(7)
(8)
Sisters (0.75 or 0.53)
Brothers (0.25)
Nieces and nephews (0.375 or 0.265)
Cousins (0.1875 or 0.1325)
Cousins' offspring (0.0938 or 0.0663)
Mother's cousins (0.0938 or 0.0663).
Mother's cousins' offspring (0.0469 or 0.0331)
Mother's cousins' grand-offspring (0.0234 or 0.0165)
a Brood were sisters, brothers, etc., of the workers. Values of relatednessgiven in parenthesisare for single
mating (r for sisters = 0.75 or multiple mating, averager for sisters = 0.53, based on electrophoretic
data from Muralidharan et al. (1986) and Gadagkar (l990a); see the section on genetic relatedness
between workers and brood).
.
196
RaghavendraGadagkaret al.
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Fig. 9.3 The extent of overlap betweenworkers belonging to different matrilines
(WI' W2, etc.) and brood belonging to different matrilines (b I , b 2, etc.) in the four
colonies under study.
mother's cousins' offspring, or mother's cousins' grand-offspring of the
workers. These relationships, along with the appropriate coefficients of
genetic relatedness,are given in Table 9.2. In computing the coefficients
of genetic relatedness,we considered single mating by queens as well as
the possibility of multiple mating. In the caseof multiple mating, we used
the averagerelatednessbetweensisters in a colony of 0.53, obtained from
electrophoretic analysis of colonies with single matrilines (Muralidharan
et at. 1986; Gadagkar 1990a). Thus, the coefficients of genetic relatedness
betweerlworkers and brood ranged from O.~5 to 0.0165.
Variation
in worker-brood
genetic
relatedness
For convenience, all quantitative data analysis was done at weekly intervals. From the nest map and census data, the proportion of workers
belonging to each matriline amongst the total pool of workers present on
any given day was computed. Similarly, the proportion of brood belonging
to each matriline out of the total pool of brood present on any 'given day
was calculated. The mean genetic relatednessbetweenworkers and brood
for any given day was calculated as
n
n
r = ~ ~Wibj rij
i=lj=1
(9.1)
Serial polygyny in Ropaliala marginatE.
197
where, Wi is the proportion of workers that belong to the; th matriline,
hj is the proportion of brood that belongs to the j th matriline, r ij is the
coefficient of genetic relatedness between the workers belonging to the
; th matriline and brood belonging to the j th matriline, and n is the
number of matrilines. Since we had no way of sexing the brood, we
computed two sets of worker-brood relatednessvalues assuming in the
first case that all brood were females, and in the second case that all
brood were males. Although Pamilo and Crozier (1982) have correctly
argued that the appropriate directionality of relatednessis from beneficiary to altruist (in our case, from brood to workers), we shall, in keeping
with common usage in the literature, refer to the conditional probability
that an allele present in the workers is also present in the brood as the
genetic relatednessof workers to brood or simply, worker-brood genetic
relatedness.
Worker-brood genetic relatednessvaries considerably over time in all
four colonies (Figs. 9.4 and 9.5). As expected, th~ relatednessto female
brood drops after queen replacement becauseworkers who are rearing
their sisters will now rear nieces,cousins, or other distantly related female
brood. However, when queens are mated singly, a change in the queen
may lead to an increase in relatednessbetween workers and male brood
TO1
JAN
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1987
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1988
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Fig. 9.4 Variation in mean worker-brood genetic relatednesscomputed at weekly
intervals in the four colonies under study. Vertical arrows indicate eventsof queen
turnover. Queens are assumed to be mated singly. For colonies TO8 and TII,
the upper panel assumesthe unknown relationship betweenqueens (see Fig. 9.2)
to be that of daughters while the lower panel assumesthe relationship to be that
of sisters.
198
RaghavendraGadagkaret a/.
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Fig. 9.5 As in Fig. 9.4 but queens are assumedto be mated multiply such that
the average relatedness between sisters in a colony is 0.53 as determined in a
previous electrophoretic study (Muralidharan et at. 1986; Gadagkar 1990a).
because nephews (r = 0.375) are more closely related to workers than
brothers (r = 0.25). Such cyclical changes in worker-brood genetic relatedness in responseto successivereplacementsof queens are seen most
clearly in colony TOI where there was a considerable time-lag between
queen replacements.
Among the events occurring after a queen replacement, the rate of
egg-laying by the new queen contributes to the initial change in workerbrood relatednesswhile the eclosion of offspring of the previous queen,
the rate of death of workers who are offspring of the previous queen, and
the rate of eclosion of female offspring of the new queen all contribute
to a return to the original level of worker-brood relatedness. In colonies
such as T02 and especially T08, queenreplacementsare so frequent that
the relatednessvalues are uniformly low for long periods of time.
With the assumption of multiple mating, the pattern of variation in
worker-brood genetic relatedness (Fig. 9.5) is qualitatively similar to
that obtained under the assumption of single mating (Fig. 9.4) but it is
quite different quantitatively; the values are uniformly lower in the case
of multiple mating. A striking feature in Fig. 9.5, especially in TOI and
the initial part of T02, is fhe near constancy in worker-male brood
genetic relatedness.This is because, in the multiple mating case, worker
relatednessto nephews (0.53 x 0.5 = 0.265) is nearly the same as that
to brothers (0.25).
Serial polygyny
Evaluating
the observed
in Ropalidia marginata
199
levels of relatedness
Clearly, serial polygyny leads to a reduction in genetic relatedness. But
how significant is this reduction? What are the consequencesof such
reduction for the evolution of worker behaviour? Reducedworker-brood
genetic relatedness values may last for only a very short time or may
occur only when colony sizes are very small, in which case the overall
effect of serial polygyny may be only marginal. We have therefore computed for each colony, a grand mean worker-brood relatednessfrom the
mean relatednesscalculated at weekly intervals by using the equation:
s
=;:==
L; (Wk + Bk)r k
k=l
(9.2)
s
L; (Wk + Bk)
k=I
where, Wk is the total number of workers present on the kth day, B k
is the total number of brood present on the kth day, r k is the mean
worker-brood relatednesson the kth day computed from equation (9.1),
and s is the total number of days for which mean worker-brood genetic
relatedness was computed using equation (9.1). Values of grand mean
worker-brood relatednessfor male and female brood, under single mating
and multiple mating assumptionsare given in Table 9.3. For eachcolony,
the values for female brood range from 0.65 to 0.22 and the values for
male brood range from 0.29 to 0.18.
How low are these values? Are they low enough to permit the conclusion that the advantage of genetic asymmetry created by haplodiploidy
for social evolution is entirely lost on account of serial polygyny and/or
polyandry? A useful way of stating Hamilton's rule (Hamilton 19640)
for social evolution is that a worker allele will be favoured if:
njrj
> noro
(9.3)
where n j is the number of individuals reared by a worker in the colony,
r j is the averagegenetic relatednessbetweenworkers and the brood they
rear, no is the number of offspring that a solitary individual can rear
ar~d r 0 is her genetic relatednessto her offspring (Craig 1979; Gadagkar
19850). Inequality (9.3) can be achieved in two contrasting ways. The
first is if n j > no, even if r i :S r o. The second is if r i > r 0' even if
n j :S no. In other words, when rj > r 0 this may create conditions which
might be sufficient for the evolution of worker behaviour without the
need for any environmentally caused limitations on the productivities
of solitary nest foundresses (Gadagkar 19850, 1990b, 1991b). As mentioned before (Gadagkar 1991b), this is not to deny the importance of~
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Serial polygyny
in Ropalidia marginata
201
environmental factors in social evolution but to test the role of what
can be measured today with some degreeof precision (genetic relatedness,
r i and r 0) by not mixing it up with what cannot be measured precisely
today (differential productivities in the social and solitary modes, n i and
no)'
One way to examine whether haplodiploidy leads to genetic predisposition for the evolution of worker behaviour is to assumethat workers
can skew investment in female and male brood in proportion to their
genetic relatednessto each(Trivers and Hare 1976)and ask if the resultant
weighted mean relatedness between workers and the brood they rear is
greater than 0.5, the value expected for a solitary foundress (Gadagkar
1990b, 1991b). A second way is to argue that, during the origin of social
life, workers may even be selectedto rear an all-female brood and thus
any value of relatednessto female brood greater than 0.5 will be sufficient
to cause genetic predisposition for the evolution of worker behaviour
(Gadagkar 1991b). These arguments yield respectivelytwo possible thresholds in worker-brood relatednessthat can be compared with the values
obtained for the four colonies. One threshold is a weighted mean relatedness to brood of 0.5, taking both female and male brood into consideration and assuming that workers bias investment in female and male
brood in proportion to their relatednessto them. The second, more conservative threshold is simply a value of 0.5 for relatedness to female
brood. If the values obtained are greater than these thresholds, this
would suggest that haplodiploidy results in a genetic predisposition for
the evolution of worker behaviour in R. marginata. If the values obtained
are lower than thesethresholds, thenhaplodiploidy does not causegenetic
predisposition for the evolution of worker behaviour, and we must invoke
other factors to explain the evolution of the worker caste in R. marginata.
The weighted mean relatednessto brood after sex ratio bias is never
greater than 0.5 under multiple mating, and is greater than 0.5 in only
two out of six casesunder single mating (Table 9.3). Similarly, relatedness
to female brood is never greater than 0.5 under multiple mating and is
less than 0.5 for colony T08 even under the assumption of single mating.
Whichever threshold is used, the values obtained are always lower than
the thresholds, under the assumption of multiple mating. Thus, we conclude that the genetic asymmetry, potentially created by haplodiploidy, is
broken down by polyandry and serial polygyny to the extent that the
presenceof a worker caste in this speciescannot be attribut~d solely to
haplodiploidy.
Simulation
models
In an attempt (i) to extend these conclusions from the four colonies
studied to R. marginata in general and to other speciesof social insects
J
202
RaghavendraGadagkaret a/.
exhibiting serial polygyny and (ii) to gain some insight into the mechanism
leading to the observed values of relatedness, we constructed simple
simulation models of serial polygyny. Queens are assumed to lay one
egg every day whose development into adults and subsequentdeath are
monitored in the model. The three parameters used in the model and
their numerical values derived empirically from studies of R. marg;nata
are shown in Table 9.4. In the first model, we have merely consideredthe
mean values of these parameters, a queen tenure of 80 days, a brood
developmentalperiod of 62 days, and a worker life span of 31 days. New
queensare assumedto be either daughters or sisters of their predecessor
queens.As in the case of analysis of empirical data, the model is repeated
for single mating and multiple mating. As before, a mean relatedness
between sisters of 0.53 derived from electrophor{tic data (Muralidharan
et a/. 1986; Gadagkar 1990a) is used in the case of multiple mating.
Variation with time in the mean worker-brood relatednessin the model
(Fig. 9.6) mimics clearly that in the empirical data (Figs. 9.4 and 9.5).
An examination of the grand mean worker-brood relatednessand the
weighted mean relatedness of workers to brood after sex ratio bias
yields results which are similar to those of the empirical analysis. Our
conclusion from the simulation model is therefore identical to that from
the empirical .analysis. By the criteria of either threshold, the evolution
of worker behaviour cannot be attributeq only to genetic predisposition
on account of haplodiploidy, whether new queensare sisters or daughters
of their predecessors(Table 9.5). Serial polygyny in R: marg;nata thus
reduces significantly worker-brood genetic relatedness. Even when polyandry is ignored, haplodiploidy results in a genetic predisposition for the
evolution of worker behaviour only if new queens are daughters of their
predecessorsand only if we use the more conservative threshold, namely
a relatednessto female brood of 0.5. The relatednessvalue corresponding
to this restricted scenario is the only one in Table 9.5 that is greater
than 0.5.
Table 9.4 Parameters used in simulation models of
serial polygyny in R. marginata.
Parameter
Mean :t SE
(Values derived from
natural colonies)
Queen tenure
Brood development period
79.7 :t 15.8 daysa
61.5 :t 1.4 days b
Worker life span
31.2 :t 3.4 daysb
a Data in this chapter.
b
Gadagkar 1990c.
.
Serial polygyny in Ropalidia marginata
203
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+::
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200
300
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100
200
300
Ti me (days)
Fig. 9.6 Variation in worker-brood genetic relatednessderived from a simulation
model using empirically derived meanvalue of 80 days as the queentenure, 62 days
as the brood developmental period and 31 days as the worker life span. Notice
that worker- brood relatednessis zero for the first 62 days when no wQrkershave
yet eclosed. Queens are assumed to mate singly in (a) and (b). In (c) and (d),
queens are assumedto mate multiply, as in Fig. 9.5. New queensare assumedto
be daughters of previous queens in (a) and (c) while they are assumedto be sisters
of previous queens in (b) and (d).
The foregoing analysis ignored the variation seen in the empirically
derived values of the parameters used in the model. Therefore, in the
next model, we attempted to incorporate this variation with the use of
Monte Carlo techniques. To do this, we reconstructed a normal distribution for each of the parameters of the model using the mean and
standard error values in Table 9.4. We then repeated each simulation
1000times, using random values from the normal distribution for eachof
the parameters. This generateda distribution of worker-brood relatedness
values. The results of these simulations indicate that in spite of taking
into consideration the natural variation in queen tenure, brood developmental period, and worker life spans, the entire distribution of the one
thousand 'vorker-brood relatedness values (under multiple mating) is
below the threshold required for haplodiploidy-induced genetic predisposition for the evolution of worker behaviour (Fig. 9.7). This is true
whether we use a weighted mean relatedness to brood (after sex-ratio
bias) of 0.5 as the threshold or the more conservative threshold of
relatednessto female brood of 0.5. In the case of single mating, some
portion of the distribution may lie above the threshold, but even that is
small except when new queens are daughters of their predecessorsand
,
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206
RaghavendraGadagkaret a/.
Threshold values of queen tenure, brood developmental
worker life span
period, and
Next, we explore the effects of varying one of the three parameters at a
time. This allows us to determine the threshold value of each parameter
above which haplodiploidy can cause genetic predisposition for the evolution of worker behaviour. With increase in queen tenure, the relatednessto female brood, as well as the weighted mean relatednessto brood,
increase(Fig. 9.8). In the case of multiple mating, given a brood developmental period of 62 days and a worker life span of 31 days, there is
no value of queen tenure which will yield a weighted mean relatedness
greater than 0.5 (Fig. 9.8(g),(h». There are values of queentenure which
will. yield a relatedness to female brood of 0.5 or more, but these are
very high -465 days if new queens are daughters of their predecessors
(Fig. 9.8(c» and 715 days if new queens are sisters of their predecessors
(Fig. 9.8(d».
Keeping the queen tenure fixed at 80 days and the worker life span
at 31 days, we then explore the consequencesof varying the brood
developmental period. As expected, worker-brood relatednessdecreases
when the brood developmental period increases(Fig. 9.9). Under multiple mating, there is no value of brood developmental period for which
the worker -brood developmental period is higher than either threshold
(Fig. 9.9(c),(d),(g),(h». Similarly, when queen tenure and brood developmental period are held constant at 80 and 62 days respectively, workerbrood relatedness decreaseswith increased worker life span (Fig. 9.10).
Once again under multiple mating, there is no value of worker life span
for which worker-brood relatednessis higher than either threshold (Fig.
9.10(c),(d),(g),(h». These results add to the robustness of our conclusion
that haplodiploidy does not cause the expectedgenetic predisposition for
the evolution of worker behaviour in R. marginata. The values of the
relevant parameters derived emprically for R. marginata are not merely
marginally different from those required for genetic predisposition-they
are very different indeed.
Mapping the parameter space where
genetic predisposition
for the evolution
haplodiploidy
can lead to
of worker behaviour
In an attempt to derive conclusions that may have wider applicability to
other speciesexhibiting serial polygyny, we have delineated regions in the
parameter space where haplodiploidy leads to genetic predisposition for
the evolution of worker behaviour. First, we conducted an extensivesearch
in the entire parameterspaceof queentenure, brood developmentalperiod,
and worker life span, and found that the simulation model can be described
adequately by two parameters, nRmely (i) queen tenure and (ii) the sum
B
Serial polygyny in Ropalidia marginata
Ea
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0.8
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0.6
0.4
04
02
02
0
0
1
30
60
90
I
30
60
90
Worker life span (days)
Fig. 9.10 Variation in worker-brood genetic relatednessas a function of worker
life span in simulation models. See legend to Fig. 9.7 for general explanations.
may be drawn from Fig. 9.11, when queensmate singly, new queensare
daughters of their predecessors,and when a relatednessto female brood
of 0.5 is sufficient to drive social evolution, the sum of brood developmental period and worker life span should be no more than 1.33 times
the queen tenure. Similarly, if all other conditions in the above example
remain unchanged but if a weighted mean relatednessto brood (after
sex-ratio bias) of 0.5 or more is required for worker behaviour to be
selected, then the sum of brood developmental period and worker life
span should be no more than 0.8 times the queen tenure.
Conclusions
Serial polygyny in R. marginata leads to a significant reduction in
worker -brood genetic relatedness. This implies that the evolution of
worker behaviour cannot be attributed solely to haplodiploidy unless, as
Serial polygyny
in Ropalidia marginata
211
argued earlier, two conditions are satisfied: (i) queensmate singly and (ii)
a relatednessvalue to female brood greater than 0.5 is sufficient for such
evolution. An important assumption made in this analysis is that workers
act altruistically towards all brood present in a colony. If workers care
preferentially for brood that belong to their own matriline or patriline,
or in general, for brood that are relatively more closely related to them,
the conclusion drawn here may not be valid. However, our limited present
knowledge suggeststhat, at least in primitively eusocial species,workers
do not show such a care bias (Gadagkar 1985b; Gamboa et of. 1986,
Venkataraman et of. 1988). Another assumption made in this analysis
is that R. morginoto is outbred. This is very likely as mating never
takes place on the nest. Males leave their natal nests within a few days
of eclosion (Gadagkar et of. 1982) and lead a nomadic life, hovering
around vegetation in an apparent attempt to mate with foraging females.
The assumption of outbreeding also appears to be reasonable for most
social insects studied so far (for a compilation of data, see Gadagkar
1991b).
Since we have concluded that the presence of a worker caste in R.
morginoto cannot be attributed to the genetic asymmetries created by
haplodiploidy, it seemsreasonable to end with a brief consideration of
alternative causal factors. Curiously, the very data presented in this
chapter provide a clue. Recall that the average number of adults successfully produced by queens is 76 while most solitary nests fail before producing any adult offspring. Clearly, there is a substantial difference in
the productivities of single-foundress and multiple-foundress nests. This,
coupled with the fact that queen replacements can be quite frequent,
supports strongly the hypothesis that female wasps stay on their natal
nests in the hope of becoming queens in future (Gadagkar 1990c, 19910).
Even if the probability of becoming a queen is quite small for any given
individual, the fitness gained by those who succeedcan be so great that
it offsets the cost incurred by the other, unsuccessful bearers of the
hypothetical 'gambling' allele, which makes its bearers stay in a social
group and await their chances of becoming queens (Gadagkar 1990c,
19910). But why should the productivity of a queen in a multi-female
nestbe so much greater than that of a solitary foundress. Ecological factors
such.as differential sensitivity to predators (such as ants) and parasites
(such as ichneumonid wasps and tachinid flies) are surely important
but quantitative data on these are hard to come by. It ~ becoming
increasingly clear too that a variety of physiological and demographic
factors may interact in complex ways and lead to other kinds of predispositions to the evolution of worker behaviour by boosting the inclusive
fitness of a completely or partially sterile worker relative to that of a
solitary nest foundress (Gadagkar et of. 1988, 1991; Gadagkar 1990d,
1991c).
212
RaghavendraGadagkar et a/.
Summary
Ropa/idia marginata is a tropical Old World primitively eusocialpolistine
wasp with a perennial indeterminate colony cycle. Although colonies have
only one egg layer at any given time, they exhibit serial polygyny due to
frequent queen replacements. In a long term study, the tenure of queens
varied from 7 to 236 days. New queenswere daughters, sisters, nieces, or
cousins of their immediate predecessors.Brood were sisters, brothers,
niecesand nephews,cousins, cousins' offspring, mother's cousins, mother's
cousins' offspring, or mother's cousins' grand-offspring of the workers that
reared them. Electrophoretic analysis showed that queens mate multiply
and use sperm simultaneously from different males, resulting in an average
relatednessbetween sisters of 0.53. When polyandry and serial polygyny
were consideredsimultaneously, the relatednessof workers to female brood
ranged from 0.22 to 0.46 and that to male brood ranged from 0.18 to
0.26. Even if workers invest in female and male brood in proportion to
their relatedness to them, the weighted mean relatednessto brood that
would result ranged from 0.20 to 0.38, values which are much less than
the 0.5 that a solitary foundress would obtain by rearing her own offspring. Simulation models show that the combination of queen tenures,
brood developmental periods, and worker life spans seenin R. marginata
result in the complete breakdown of the genetic asymmetry created by
haplodiploidy. It seemsreasonable to conclude that worker behaviour in
R. marginata must be attributed at least in part to factors other jhan
genetic asymmetry created by haplodiploidy.
Acknowledgements
It is a pleasure to thank Niranjan Joshi, Anindya Sinha, Madhav Gadgil,
Vidyanand Nanjundiah, Kenneth Ross, Robert Jeanne, Mary Jane WestEberhard and Laurent Keller for comments on an earlier version of
this chapter. Supported in part by grants from The Department of Science
and Technology, Government of India and the Ministry of Environment
and Forests, Government of India.
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