Behavioral Ecology Vol. 13 No. 2: 239-247
© 2002 International Society for Behavioral Ecology
Intracolonial patterns of reproduction in the queen-size dimorphic ant Leptothorax rugatulus
a Zoologie II, Universität Würzburg, Biozentrum, Am Hubland, D-97074 Würzburg, Germany b LS Biologie I, Universität Regensburg, Universitätsstraße 31, D-93040 Regensburg, Germany
Address correspondence to O. Rüppell, who is now at the Department of Entomology, University of California at Davis, 1 Shields Avenue, Davis, CA 95616, USA. E-mail: orueppell{at}ucdavis.edu .
Received 29 November 2000; revised 8 May 2001; accepted 23 May 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Animals that live in genetically heterogeneous groups are faced with a combination of cooperation and conflict. Reproductive skew theory aims to provide a unified theory of the partitioning of reproduction in animal societies by combining genetic, demographic, and environmental factors. Although theoretical elaborations abound, empirical data are rare. Specifically, explicit intraspecific tests are scarce and have provided conflicting results. We present data on reproductive partitioning among queens in the ant Leptothorax rugatulus with special emphasis on relatedness and body size. Relatedness was negatively correlated to skew in sexual offspring and uncorrelated to skew in total offspring. Body size was not correlated to a queen's reproductive share. Thus, we did not find any support for the classic optimal skew models that are based on concessions. In artificial colonies, composed of randomly selected, unrelated workers and queens, reproductive skew was higher than in natural colonies, which suggested that unequal reproduction among queens could arise without nepotism by workers. Again, a queen's body size was not a good indicator of her reproductive share, but egg laying rate was. In colonies that contained large and small queens, small queens produced proportionally more sexual offspring. Although this result is in accordance with the kin conflict over caste determination hypothesis, it is more plausibly explained by an adaptation of the caste ratios to alternative dispersal tactics.
Key words: body size, kin conflict, queen size dimorphism, reproductive skew, selfish microgynes.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Cooperative group living has proven very successful in animal evolution (e.g., Hölldobler and Wilson, 1990
). However, most groups are genetically heterogeneous, and
cooperation and conflict coexist within groups
(Emlen, 1997; Hamilton,
1964a,b;
Heinze et al., 1994;
Keller, 1993b;
Maynard Smith and Szathmáry,
1995; Vehrencamp,
1983a,b).
The central conflict occurs over reproduction among several potential
breeders, and thus reproductive skew theory has been suggested as a general
theory to characterize animal groups
(Johnstone, 2000;
Reeve and Ratnieks, 1993;
Vehrencamp,
1983a,b).
Indices of reproductive skew vary between zero, when reproduction is shared
equally, and one, when only one potential breeder reproduces.
Recently, there has been tremendous interest in reproductive skew theory
(for reviews, see Johnstone,
2000; Reeve and Keller,
2001) due to its broad and unifying taxonomic perspective and its
potential for a comprehensive theory of social evolution
(Reeve and Keller, 2001). The
majority of work has been theoretical, and a large number of models have been
proposed. These models fall into two categories: transactional and compromise
(Johnstone, 2000).
Transactional models assume that the individuals that control reproduction
concede reproduction to subordinates to maintain group stability. In contrast,
compromise models consider reproductive division among group members to be the
outcome of incomplete control by the dominant and differences in the ability
of individuals to claim a share of group reproduction (at the cost of group
productivity). Both models create sets of predictions that depend on various
aspects of the general biology of the focal species
(Johnstone and Cant, 1999b;
Kokko and Johnstone, 1999;
Ragsdale, 1999;
Reeve et al., 1998), and on
parameters such as intragroup relatedness
(Reeve and Keller, 1995;
Johnstone, 2000), group size
(Reeve and Emlen, 2000), and
the benefits of group living (Johnstone et
al., 1999). Despite theoretical elaborations that have created an
array of models, independent, empirical tests are scarce and provide
conflicting results (Reeve and Keller,
2001).
The concession form of transactional skew models (Vehrencamp,
1983a,b)
has received most attention. It predicts a positive association of
reproductive skew and the four factors intragroup relatedness, power
asymmetry, subordinate contribution to colony productivity, and risk
associated with independent breeding. Its most crucial assumptions are that
the dominant breeder has absolute control over reproduction, individual
reproduction can be estimated, subordinates may leave the group for
independent reproduction, and that subordinates benefit the dominant.
In vertebrates, some support for these classic optimal skew models has been
presented (Emlen, 1997;
Jamieson, 1997;
Keller and Reeve, 1994), but
alternative explanations cannot be ruled out
(Clutton-Brock, 1998;
Cooney and Bennett, 2000). In
invertebrates, evidence in favor of transactional models comes mainly from
interspecific comparisons in social Hymenoptera and circumstantial evidence
(Heinze, 1995;
Hoogendoorn and Velthuis,
1999; Keller and Reeve,
1994; Reeve and Keller,
2001). Direct tests at the intraspecific level are less common and
have provided conflicting evidence. For example, many aspects of the
reproductive biology of several wasp species of the genus Polistes
might be explained by reproductive transactions
(Reeve and Keller, 2001;
Reeve et al., 2000), but
another study of this genus found no support for these models
(Field et al., 1998).
Compromise models (Reeve et al.,
1998) have received less attention. Their main assumptions are
incomplete control by the dominant breeder and a struggle for reproduction in
which every breeder chooses to divert some energy to claiming reproduction and
consequently lowering group productivity. Their main predictions are a weak
relation (negative or positive) of reproductive skew and relatedness and a
strong positive association between skew and the inequality between dominant
and subordinate individuals. Furthermore, they predict a negative association
between skew and agonistic interactions.
The most prominent compromise model, the tug-of-war model, is supported by
a field study in meerkats (Clutton-Brock
et al., 2001). It is also supported by the negative correlation
between skew and relatedness found in Polistes
(Field et al., 1998) but is
refuted by another study in the same genus
(Tibbetts and Reeve, 2000).
Circumstantial evidence in other groups sustains arguments for and against
compromise models (e.g., Hoogendoorn and
Velthuis, 1999).
Few studies have reported intraspecific tests within ant species. There was
no support for the prediction of transactional models of a positive
association between skew and relatedness in Myrmica tahoensis
(Evans, 1995), and data from
Formica fusca agrees better with predictions of compromise models
(Hannonen MT and Sundström L, personal communication). In contrast,
Bourke et al. (1997) provided
supportive data for transactional models by comparing two populations of
Leptothorax acervorum.
The genus Leptothorax may prove particularly important for tests
of reproductive partitioning in ants because the relatively small colonies can
be collected completely and maintained under seminatural condition in the
laboratory (Buschinger,
1974a). Leptothorax species exhibit a variety of social
structures (Bourke and Heinze,
1994; Buschinger,
1974b), and remarkable data sets exist on various aspects of their
biology (e.g., Bourke et al.,
1997; Herbers,
1990). Social diversity is also common within Leptothorax
species: in many cases single-queen (monogynous) and multiple-queen
(polygynous) colonies coexist (facultative polygyny;
Bourke and Franks, 1995), which
can be attributed to variation in ecological constraints on independent
founding (Bourke and Franks,
1995; Herbers,
1993). In some cases, variation in reproductive strategies has led
to alternative queen morphs (Buschinger
and Heinze, 1992; Heinze and
Tsuji, 1995; Rüppell and
Heinze, 1999).
For the North American ant Leptothorax rugatulus, a queen size
dimorphism has been documented
(Rüppell et al., 1998).
Besides normal-sized queens (macrogynes), small queens (microgynes) exist as a
quasi-isometric reduction. Queen morphology and social structure are
correlated: while many macrogynes occur in monogynous colonies, microgynes are
found almost always in polygynous colonies. Queen-size dimorphism is related
to alternative reproductive tactics: after mating, microgynes are adopted into
existing colonies, predominantly related ones, while macrogynes are more
likely to start new colonies independently
(Rüppell et al., 2001).
Presumably, adoption of new queens is followed by colony budding (as in other
facultatively polygynous Leptothorax species;
Bourke and Franks, 1995),
though this has not yet been conclusively demonstrated for L.
rugatulus. Although workers are only capable of male production (in the
absence of queens), both macro- and microgynes possess a fully developed
reproductive tract (Rüppell et al.,
1998). Mixed colonies with macro- and microgynes are relatively
rare (13% of all colonies), and a slight genetic differentiation
(FST = 0.09) between morphs has been found
(Rüppell et al., 2001).
The resource allocation to offspring (sex ratio) of colonies is influenced by
social structure, but not by queen morphology per se (Rüppell et al.,
unpublished data).
The highly variable queen body size of Leptothorax rugatulus makes
the investigation of its reproductive pattern in colonies particularly
interesting. On the one hand, the strong differences in body size are expected
to give an advantage to larger queens in competitive ability (that could
include the ability to fight, produce pheromones, or acquire food) and
fertility, as these parameters are generally well correlated with body size
(Clutton-Brock, 1988).
Furthermore, the small body size of microgynes poses a serious constraint on
independent reproduction (Rüppell et
al., 2001). It is therefore predicted that reproductive skew and
variance in queen body size in a colony are positively correlated and that in
mixed colonies, macrogynes claim a disproportionately large reproductive
share. Moreover, according to concession models, subordinate microgynes are
expected to accept a higher reproductive skew because they have no option of
independent reproduction.
On the other hand, it has been suggested that microgynes constitute
intra-specific social parasites (Bourke and
Franks, 1991; Buschinger,
1990; Rüppell and Heinze,
1999). Thus, microgynes may dominate reproduction despite their
smaller body size, as interspecific social parasites do
(Hölldobler and Wilson,
1990). Extending this argument, it was proposed that small body
size in social insect queens results from a selfish larval strategy to develop
into sexuals against the interest of the remaining colony
(Bourke and Ratnieks, 1999;
Nonacs and Tobin, 1992). This
suggests that the relative proportion of sexuals (and specifically gynes) is
expected to be higher in offspring of microgynes than in offspring of
macrogynes. In this case, skew in the production of sexuals might be high
despite similar egg laying rates of queens.
As studies of reproductive distributions in field collected colonies of
Leptothorax have proven difficult due to potentially missing queens
(Bourke et al., 1997), we
investigated the reproductive distribution among cohabiting Leptothorax
rugatulus queens in a controlled laboratory experiment. Specifically, the
influence of intracolonial relatedness and body size of queens on reproductive
partitioning were studied. We used unmanipulated colonies to investigate
naturally occurring skew, as well as randomly assembled colonies to confront
alien queens with each other and control for potential worker nepotism (i.e.,
to exclude the possibility that high skews resulted from workers
nepotistically favoring the reproduction of their own mother). In addition, we
investigated whether queens biased their reproduction toward one particular
offspring type, relative to their nest-mate queens.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Leptothorax rugatulus is widespread in the western United States (Creighton, 1950
). In our
study area (southern Arizona and New Mexico), it mainly nests under stones or
in rock crevices in mixed coniferous forests on mountain ranges. To
investigate the pattern of reproduction among Leptothorax rugatulus
queens, two experimental groups of colonies were established in the
laboratory: unmanipulated colonies and artificially mixed groups. Both groups
comprised colonies with only macrogynes, only microgynes, or both (mixed
colonies).
Experiments
After collection of colonies in August 1996 from various populations in the
Chiricuhua Mountains (Arizona), Huachuca Mountains (Arizona), and Manzano
Mountains (New Mexico), colonies were maintained under standard conditions in
three-chamber nest-boxes and kept in incubators
(Buschinger, 1974a). In June
1997 the following experimental groups were set up: the first group consisted
of 34 original colonies (11 macrogynous, 9 microgynous, and 14 mixed) with 2-7
queens. The second group consisted of 30 artificial colonies (10 macrogynous,
10 microgynous, and 10 mixed) with 4 queens each. These colonies were composed
randomly from a pool of workers and queens from approximately 50 original
colonies. This pool was set up 2 months before the start of the experiment by
mixing the original colonies in one large laboratory arena that contained only
a single nesting cavity. After initial fighting, the colonies settled together
in the nest, and 2 months later no aggression could be observed. Physically
intact individuals were chosen at random from this "super-colony"
to assemble the artificial colonies.
At the start of the experiment, all brood (eggs, larvae and pupae) was completely removed from all colonies in both experimental groups to avoid including brood from past queens. Present queens were randomly paint-marked (Edding 780 paint marker). We determined the primary egg-laying rates of queens 2 weeks later by isolating single queens for 16 h with some workers. The isolation procedure was repeated five times, with queens being returned to their colonies for 32 h of recovery between each period of isolation. For the next 2 years, until the end of the reproductive phase in August 1999, we censused colonies to count the numbers of queens and workers. Direct counts were performed under a Wild stereomicroscope every 3 days during the reproductive season and every 4 weeks during hibernation. All newly emerging off-spring were collected (twice per week in summer, the main reproductive season) and kept frozen at -20°C until DNA extraction. To estimate group productivity, we estimated dry mass production of every colony as a per-year, per-worker value. At the end of the experiment, all queens were killed by freezing, their insemination status was checked by ovarian dissection, and their maximum head and thorax widths were measured. We averaged head and thorax width to give one measure of body size for each individual. Heads and thoraces of queens were then used for DNA extraction.
Genetic analyses
DNA was extracted from individuals by a modification of the Chelex®
protocol (Altschmied et al.,
1997) and seven micro-satellites were adopted from different
species using different polymerase chain reaction (PCR) amplification
protocols (Table 1). The
internally 
-33P-labeled PCR products were separated on
sequencing gels, and their allelic sizes determined by comparison to the
Sequamark® size standard. We calculated queen—queen relatedness in
all experimental colonies using the computer program Relatedness 5.02
(Goodnight and Queller, 1998)
based on the principles of regression relatedness
(Queller and Goodnight, 1989).
Allele frequencies were estimated (with bias correction and weighting by
colony; see Goodnight and Queller,
1998) from an extended data set that comprised 360 additional
queens from colonies not included in this experiment.
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From the initial genotyping of queens, the power of individual microsatellite loci to discriminate between queens as potential mothers was known. On this basis, colonies were chosen that provided, in addition to a relatively high reproductive output, good prospects for unambiguously assigning offspring to mothers. However, analyzed colonies did not have a significantly lower overall relatedness [ranalysed = 0.36 ± 0.27 (SD), romitted = 0.48 ± 0.36, t = -0.93, df = 25, p =.363). Colonies with queens dying during the course of the experiment after the initial 2 weeks were also excluded. We analyzed 12 artificial and 11 unmanipulated colonies. Neither queen number [medianoriginal = 3, 25-75% quartile (Q25-75) = 2-3, medianartificial = 3, Q25-75 = 3-4; Mann-Whitney U11,12 = 48.0, p =.270], nor worker number (medianoriginal = 44, Q25-75 = 33-84; medianartificial = 46, Q25-75 = 43-49; U11,12 = 66.0, p = 1.000) differed significantly between groups.
Starting with the most informative locus, mothers and offspring were genotyped at as many microsatellite loci as necessary for unambiguous mother—offspring assignment. Offspring that could not be assigned unambiguously (overall, 28 males in 4 colonies) were omitted from the subsequent analysis. On average, 27 (range 16-38) offspring per colony were successfully assigned to one of the potential mothers.
We calculated the overall skew index by combining the worker, male, and
gyne offspring, and the sexual skew index was similarly calculated from male
and gyne offspring. The desirable calculation of separate skew indices for
worker, male, and queen offspring was precluded by small sample sizes. Of the
skew indices available (Kokko et al.,
1999), we report here the corrected skew index proposed by Keller
and Krieger (1996). The
hypothesis that queens within groups contribute differentially to worker,
male, and female offspring was tested by chi-square tests with subsequent
Bonferroni correction. At the individual level, relative offspring production
(reproductive share) was investigated as a function of relative queen body
size (individual queen size/average queen size in any given colony) and
relative egg-laying rate (individual egg laying rate/average egg laying rate
in any given colony). We determined significance levels of the correlations by
randomization tests (Manly,
1997) because the relative values were not independent of each
other within colonies. Furthermore, we investigated the influence of relative
body size on reproductive bias toward sexuals. A relative index was calculated
to express this bias with the formula
(xq/nq) /
(xc/nc), where x is the
number of sexuals (gynes and males) and n is the total offspring
number. The subscripts q and c refer to a particular queen and her colony,
respectively.
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RESULTS |
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Colony level
Across all colonies, the expected correlation (due to non-independence of the two calculated indices) between skew in overall and sexual offspring production was found (rs =.65, n = 22, p =.001). The two skew indices and the productivity index are summarized in Table 2, and the raw data for all colonies are given in the Appendix. On average, overall skew and sexual skew were higher in artificial than in original colonies, but only the difference in overall skew was statistically significant (overall skew: medianartificial = 0.15, Q25-75 = 0.06-0.56; medianoriginal = 0.04, Q25-75 = 0.00-0.11; U11,12 = 34.0, p =.049; sexual skew: medianartificial = 0.29, Q25-75 = 0.04-0.47; medianoriginal = 0.05, Q25-75 = -0.07-0.29; U11,11 = 39.0, p =.158). Average productivity was significantly lower in artificial colonies (medianartificial = 0.83, Q25-75 = 0.65-0.98; medianoriginal = 2.24, Q25-75 = 1.47-3.65; U11,12 = 7.5, p <.001).
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As expected, queens were unrelated in all artificially assembled colonies, and consequently no association between relatedness and skew could be tested in this experimental group. Within the sample of original colonies, relatedness was correlated to neither overall skew (rs = -.20, n = 11, p =.555), nor productivity (rs =.08, n = 11, p =.821). Sexual skew was negatively correlated with relatedness (rs = -0.69, n = 11, p =.019: Figure 1). However, the power of the estimation of the underlying within-colony relatedness values was not sufficient for the differences among colonies to be statistically significant. In both experimental groups, neither overall skew nor sexual skew was significantly correlated to variability in queen body size (Figure 2).
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,
artificial groups.
Because predictions of the basic models strictly apply only to two-member groups (assuming nonidentical subordinates), the analyses were repeated with colonies containing only two queens. This reduced the sample size of original colonies to four and the sample size of artificial colonies to three. Although separate analyses of these samples were not statistically meaningful, the pooled analyses led to the following results. Queen relatedness was negatively correlated to overall skew (rs = -.85, n = 7, p =.015) but not significantly to sexual skew (rs = -.58, n = 6, p =.228). There was a nonsignificant, positive association between queen size variability and overall skew (rs =.25, n = 7, p =.589) and sexual skew (rs =.77, n = 6, p =.072).
Colony density and the degree of polygyny in Leptothorax
populations are believed to reflect ecological constraints on independent
colony founding (Bourke and Franks,
1995; Herbers,
1993). Under this assumption, the original colonies were grouped
based on whether they were collected from a population with high or low
ecological constraint, and the skew indices were compared between the two
groups. Populations with >50% polygynous colonies and high colony density
were classified as "high ecological constraint," and the remaining
<50% polygynous colonies and/or low colony density were classified as
"low ecological constraint." The population origin of colonies in
this sample had no significant effect on overall skew
(U6,5 = 13, p =.715) or on sexual skew
(U6,5 = 14, p =.855).
Individual level
The relative size of queens did not significantly affect their reproductive
share in the original colonies (r =.21, n = 31, p
=.061) or in artificial groups (r = -.04, n = 37, p
=.389). The same result was obtained when micro- and macrogynes were compared
in mixed colonies (medianmacro = 0.35, Q25-75 =
0.14-0.63; medianmicro = 0.25, Q25-75 = 0.22-0.38;
U11,11 = 72, p =.450). This is corroborated by
the absence of a correlation between relative body size and relative
egg-laying rate (original colonies: r =.13, n = 31,
p =.255; artificial groups: r =.09, n = 36,
p =.180) and the lack of a difference in relative egg laying rates
between micro- and macrogynes in mixed colonies (medianmacro =
0.40, Q25-75 = 0.33-0.46; medianmicro = 0.29,
Q25-75 = 0.14-0.44; U11,11 = 74.5, p
=.358). A positive trend between primary egg-laying rate and reproductive
share existed (Figure 3) in
original colonies (r =.41, n = 31, p =.132), and a
significant correlation was found in artificial groups (r =.53,
n = 38, p =.001).
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Across both experimental groups, most queens (27) produced workers and gynes; some produced only workers (13), workers and males (10), or all three types of offspring (8); and few specialized in gynes (5) or males only (3), or did not contribute to the investigated offspring at all (3). Thus, co-habiting queens did not contribute evenly to male, female, and worker offspring. The degree of differentiation in offspring production among queens was significant in 8 of the 23 colonies (Table 3). Chi-square values did not differ between original colonies and artificial groups (U12,11 = 72, p =.712), but were significantly higher in groups with microgynes (microgynous and mixed) than purely macrogynous ones (Kruskal-Wallis ANOVA: H2,23 = 6.75, p = 0.34). All groups that were significantly differentiated were either microgynous (three) or mixed (five).
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The differentiation was caused in three colonies by different queen/worker caste ratios, in two colonies by different sex ratios of the individual queen offspring, and in three cases a mixture of both effects. In mixed colonies, microgynes produced relatively more sexuals than macrogynes (U12,11 = 18.0, p =.003; Figure 4). Although this is mainly attributable to the significant difference in gyne production (U12,9 = 17.0, p =.009), microgynes also exhibited a higher relative male production (Figure 4), but this difference was not significant.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Reproductive skew
Johnstone (2000
) called for
comprehensive tests of reproductive skew theory which account for all model
assumptions and study the complete set of predictions generated by any
particular model. Empirical progress, including this study, still falls short
of this demand. Nevertheless, our study is an important contribution as one of
the few explicit tests of skew models within social insects species
(Reeve and Keller, 2001). All
our results contradict predictions of transactional skew models
(Keller and Reeve, 1994;
Reeve and Ratnieks, 1993;
Vehrencamp, 1983a,
b), which are generally
regarded as most applicable to social insects (Reeve et al.,
1998,
2000;
Reeve and Keller, 2001).
The distinction between sexual skew and overall skew is crucial because
skew in worker production does not translate into fitness effects in the
absence of worker reproduction (Bourke, 1988) and within-colony kin
discrimination (Carlin et al.,
1993; DeHeer and Ross,
1997; Keller,
1997). In contrast, differential production of sexuals directly
translates into fitness differences among cohabiting queens. Although
mechanisms are unknown, some evidence exists that ant queens differ in the
caste ratios that they produce (Pamilo and
Seppä, 1994; Ross,
1988). Consequently, skew in overall offspring production is not
necessarily equivalent to skew in sexual offspring. This has also been found
in our study, even though both skew indices were reasonably correlated across
all colonies.
A further subdivision of overall skew into male, queen, and worker skew would have been appropriate in our analysis but was precluded by the small sample size. However, the cues that ant queens use for determining their relative reproductive share and for adjusting their behavior accordingly are currently unknown. Until egg laying as a probable cue is ruled out, it is important to report the skew over all offspring classes because it might reflect the queens' reproductive decision rules.
Multiple-queen groups in Leptothorax ants seem to fulfill the
assumptions of the classic, transactional skew model and consequently have
served as key evidence for their support (Reeve and Keller,
1995,
2001;
Reeve et al., 1998). The
existence of functionally monogynous species, in which only one of several
potential queens reproduces in any given colony and linear dominance
hierarchies are formed, demonstrates that recognition of individual status is
possible and that one queen can fully inhibit the reproduction of remaining
queens (Heinze and Lipski,
1990; Ortius and Heinze,
1999). It has also been demonstrated that assessment of individual
reproductive output is possible (Ortius
and Heinze, 1999). Although the assumption of a direct increase in
reproduction by the presence of additional queens is not necessarily fulfilled
[Bourke, 1991;
Evans and Pierce, 1995; in
L. rugatulus, queen number had a positive effect on productivity of
field colonies in only three out of six studied populations (Rüppell et
al., unpublished data)], there may be other cooperative benefits, such as
increased genetic diversity in colonies
(Cole and Wiernasz, 1999) or
"assured fitness returns" due to prolonged colony longevity
(Gadagkar, 1990; for a further
discussion of benefits, see Bourke and
Heinze, 1994). Furthermore, the cost of a subordinate queen
departing is high when workers accompany her during colony budding
(Bourke and Franks, 1995).
In clear contrast to the prediction of the transactional skew model, our study found a negative association between relatedness and sexual skew and no relation between relatedness and overall skew. However, it is important to note that the differences among colonies of the underlying relatedness estimates were not significant, and, thus, our conclusion is weakened by the possible inaccuracy of these estimates. Given this provision, our results comply with the prediction of compromise models, although it is at present uncertain how well L. rugatulus meets the assumptions of these models.
On one hand, we have argued above that full control in Leptothorax
colonies is at least theoretically possible. On the other hand, the
correlation between relative egg-laying rate and relative reproduction found
in this study suggests that high egg-laying rates are perhaps linked to
indiscriminate egg cannibalism (Bourke,
1994). This behavioral scenario is a plausible mechanism for
reproductive sharing according to compromise models. The artificially mixed
colonies display higher reproductive skew, coupled with lower productivity,
than natural colonies. This might also be interpreted as support for
compromise models because they predict more conflict among less related
individuals, which leads to lowered overall group productivity
(Reeve et al., 1998). However,
the low productivity might also be due to the mixing of the workers, which
could result in inefficient division of labor or less cooperation among the
workers.
Both transactional and compromise models of reproductive skew predict that
macrogynes should dominate reproduction for various reasons. Body size is
regarded as a good indicator of power across taxa
(Andersson, 1994;
Roff, 1992), and it also
determines the outcome of conflicts among queens in some ant species (e.g.,
Nonacs, 1990). Therefore,
microgynes should receive smaller peace incentives
(Reeve and Ratnieks, 1993),
provided that there is the risk of physical conflict. Additionally, they
should receive smaller staying incentives because they are less likely to
leave the colony and reproduce independently. Compromise models predict body
size to be important for different reasons: body size is crucial for
parameters that influence resource access and usage (nutrient storage,
metabolism, pheromone production, and physical power). However, size did not
influence the division of overall reproduction in L. rugatulus, and
macrogynes actually incurred a fitness disadvantage in mixed colonies (see
below). Body size did not influence the reproductive skew in the wasp
Polistes bellicosus either (Field
et al., 1998). Yet for both species, the significance of body size
for competitive ability remains to be demonstrated.
Provided that subordinates differ in features such as competitive ability,
relatedness to dominants, and so on, predictions of skew models can become
more complex in multi-member groups
(Johnstone et al., 1999; Reeve
and Emlen, 1999) than in groups with only two members. For this reason, we
reduced our sample for additional analyses to colonies that only contained two
queens. However, no new conclusions emerged from these analyses, perhaps due
to our small sample size.
With an average skew index of 0.19 in sexual offspring and 0.06 in overall offspring, natural colonies of Leptothorax rugatulus display low reproductive skew compared to other social Hymenoptera. We found that reproductive skew was significantly higher in the randomly composed colonies. This suggests that strong reproductive biasing (relative to naturally occurring skew) is possible in L. rugatulus when individuals perceive others as alien. It is unlikely that workers were responsible for the reproductive skew by favoring one related queen (nepotism) because all queens were equally unrelated to the workers in this setup. Thus, our results favor the view that queens could be directly responsible for differences in their reproduction and not workers. Although we presented the ants with an extreme, artificial situation and mortality was high during the initial 2 weeks after their mixing, colonies seem to function during the experimental period: they successfully raised sexual and worker brood, and mortality after the establishment phase was comparable to unmanipulated colonies. However, we cannot exclude the possibility that the treatment itself affected the reproductive patterns in these randomly composed colonies.
To realistically explain reproductive (sexual) skew in Leptothorax
regatulus, one could conceivably build a more complex model to integrate
the species' general biology and our present results. Species-specific skew
models would be the next logical step from the proliferating refinements and
variations of skew models in the literature. However, with an increasing
number of models, skew theory risks losing its general predictive power and
thus its main scientific appeal (Keller
and Reeve, 1994). Johnstone
(2000) claimed that the
different skew models were only variants of the same underlying principle, but
the question arises what generality skew theory conveys beyond the theory of
kin selection (Hamilton,
1964a,b).
Sexual bias
In 30% of all colonies, individual queens differed significantly in their
tendency to produce male, worker, and young queen (gyne) offspring. This was
partly explained by microgynes producing relatively fewer workers and more
gynes than macrogynes, although some microgynes also overproduced males. No
significant differentiation among macrogynes was observed.
Exclusive male production by inseminated queens could be due to unviable
sperm or mate incompatibility (Godfray,
1990). Alternatively, queens may refrain from fertilizing their
eggs to increase their relative sexual production and thus their contribution
to the future gene pool. So far, this potential form of selfishness in the
social Hymenoptera has received little attention.
A differential contribution of individual queens to gyne and worker
production has only been reported for the ants Solenopsis invicta
(Ross, 1988,
1993) and Formica
sanguinea (Pamilo and Seppä,
1994). However, in neither case could these differences be related
to proximate or ultimate reasons. In L. rugatulus, different caste
ratios of macro- and microgyne off-spring were mainly responsible for
differential queen contributions. A reduced body size to favor development as
gynes has been found in socially parasitic ant species
(Aron et al., 1999;
Nonacs and Tobin, 1992), and
it has also been predicted in the intraspecific context of kin conflict over
caste determination (Bourke and Ratnieks,
1999).
However, in our laboratory-reared, mixed colonies, daughter queens of
macrogynes were not significantly larger than daughter queens of microgynes
(data not shown). Even though similar in size, female larvae derived from
microgynes developed more often into gynes than female larvae from macrogynes
in the same physical and social environment. This suggests that caste
determination in Leptothorax rugatulus is, at least partly,
determined by mother queens. The influence could be maternal (blastogenic) or
genetic. Furthermore, the size similarity between offspring of macrogynes and
microgynes suggests that the higher gyne/worker ratio produced by microgynes
is not due to selfish caste determination of the larvae facilitated by their
smaller body size (Bourke and Ratnieks,
1999). Rather, the difference in caste ratios between macro- and
microgynes could be an adaptation to their different reproductive tactics.
Macrogynes, mainly founding independently, have to produce workers for colony
growth before producing sexuals. Microgynes, in contrast, mainly readopting
into their mother colonies, can produce sexuals from the onset of their
reproductive life.
Thus, microgynes have a fitness advantage over macrogynes in mixed
colonies, and their usage of the workforce provided by the macrogynes amounts
to intraspecific social parasitism. However, because mixed colonies are rare
in natural populations (Rüppell et
al., 1998), we interpret the evolution of microgynes in L.
rugatulus not as an adaptation to intraspecific social parasitism but
rather as an adaptation to dependent reproduction
(Rüppell et al., 2001).
Overall, colonies with microgynous queens do not produce higher gyne/worker
ratios than colonies with macrogynes (Rüppell et al., unpublished data).
At the colony level, L. rugatulus produces caste ratios that are
comparable to other Leptothorax species (e.g., data in
Chan et al., 1999) and that
are probably worker controlled.
In conclusion, we have to caution that our results might present artifacts
of our experiments because we did not measure lifetime reproduction of queens,
which is a practical problem in social insects in general due to the long life
spans of reproductives (Keller,
1993a; Ross,
1988).
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ACKNOWLEDGEMENTS |
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We are grateful to the South-Western Research Station of the American Museum of Natural History for essential infrastructure and excellent help during the field work. We also thank A.F.G. Bourke, L. Keller, L. Sundström, and two reviewers for valuable comments and M.C. Kalcounis-Rüppell for proofreading the manuscript. Financial support came from the German Scholarship Foundation, the German Science Foundation (SFB 554), the Training and Mobility of Researchers program "Social Evolution" of the European Union, and the American Museum of Natural History.
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