Behavioral Ecology Vol. 14 No. 6: 870-875
© 2003 International Society for Behavioral Ecology
Reproductive sharing among queens in the ant Formica fusca
Department of Ecology and Systematics, University of Helsinki, FIN-00014 Helsinki, Finland
Address correspondence to M. Hannonen, who is now at the Turku Centre for Biotechnology, P.O. Box 23, FIN-20521 Turku, Finland.E-mail: minttu.hannonen{at}btk.utu.fi.
Received 8 August 2001; revised 30 December 2002; accepted 23 January 2003.
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ABSTRACT |
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Reproductive sharing among cobreeders, in which reproductive shares may vary from equal contribution (low reproductive skew) to reproductive dominance by one individual (high reproductive skew), is a fundamental feature of animal societies. Recent theoretical work, the reproductive skew models, has focused on factors affecting the degree to which reproduction is skewed within a society. We used the parameters provided by skew models as a guideline to study determinants of reproductive sharing in polygyne ants. As a model system we used two-queen laboratory colonies of the ant Formica fusca in which the reproductive shares of each queen was assessed from offspring by using allozymes and DNA microsatellites. We tested how the different variables included in reproductive skew models (queen-queen relatedness, potential fighting ability, productivity, and worker relatedness reflected by queen number in the colony of origin) affect reproductive sharing among queens. The results showed that the relatedness among queens explained 26% of the variation in reproductive skew. The size difference between queens (reflecting potential fighting ability), colony productivity, and worker relatedness did not have an effect on reproductive partitioning among cobreeders. To our knowledge, this is the first study to test for the effects of various determinants of skew in an experimental setting.
Key words: ant, Formica fusca, multiple queens, reproductive skew.
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INTRODUCTION |
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In many vertebrate and invertebrate taxa, related individuals come to share reproduction and cooperatively rear offspring (see Krebs and Davies, 1997
). This often occurs at the expense of the personal reproduction of some individuals in the group, to the benefit to other group members. Such reproductive division of labor can eventually become manifest as differential reproductive potential among members of the society. For example, in most vertebrate societies and some invertebrate societies, all group members have the potential to reproduce, whereas in many invertebrate societies, most notably in social Hymenoptera, only some individuals have retained their full reproductive capacity.
Among the social Hymenoptera, ants provide an interesting case of a rerun of the evolution of sociality. Individuals of the worker caste are usually effectively sterile, and reproduction is monopolized by the queen caste (Bourke and Franks, 1995; Hölldobler and Wilson, 1990). Hence, workers in single-queen societies help raise their full siblings and so gain inclusive fitness returns from their helping behavior. However, ant colonies commonly have multiple queens that represent offspring females that are recruited back to their natal colony (secondary polygyny; Bourke and Franks, 1995; Hölldobler and Wilson, 1977). Such polygyny can be considered as a second round of social evolution (Rosengren and Pamilo, 1983), as these queens are by definition cobreeders and contribute collectively to the worker force of the colony. Nevertheless, these queens also compete for reproductive shares within a colony of limited resources. An increase in queen number is generally associated with a decrease in individual reproductive output (Bourke and Franks, 1995; Keller and Vargo, 1993; but see Walin et al., 2001). Kin selection provides a framework for analyzing rules by which reproductive sharing among cobreeding groups can evolve (Hamilton, 1964a,b). In short, the theory holds that a reduced personal reproduction can be outweighed by the inclusive fitness benefits gained through the increased reproduction of the cobreeding relative sharing similar genes.
Models of reproductive skew build on the foundation provided by inclusive fitness principles and seek to generate predictions concerning the partitioning of reproduction in societies with multiple reproductive individuals (Cant 1998; Cant and Johnstone, 1999; Johnstone, 2000; Johnstone and Cant, 1999a,b; Johnstone et al., 1999; Keller and Reeve, 1994; Kokko and Johnstone, 1999; Reeve, 2000; Reeve and Emlen, 2001; Reeve and Keller, 2001; Reeve and Ratnieks, 1993; Reeve et al., 1998; Vehrencamp 1983a,b). The term reproductive skew describes how reproduction is shared among cobreeding individuals, such that high skew stands for uneven reproduction, and low skew stands for equal reproduction. The models can be divided into two main groups based on the assumptions on the nature of dominance among group members (Johnstone, 2000; Reeve and Keller, 2001). The "transactional models" assume that either the dominant (concession models; see Reeve and Ratnieks, 1993) or the subordinate (restraint model; Johnstone and Cant, 1999b) has total control over reproductive sharing in the group. In contrast, "tug-of-war models" (Reeve et al., 1998), assume that dominants and subordinates both have limited control over the reproductive allocation, and thus, both face a trade-off between maximizing overall group productivity versus their own share of reproduction. The models yield specific sets of predictions concerning the effects that factors such as environmental constraints, relatedness, fighting ability, and group productivity are expected to have on the degree of reproductive skew (Table 1). However, as Johnstone (2000) pointed out, the relevant model to be tested cannot be selected unless the assumptions on which the predictions of the models are based have been confirmed for the study species.
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Both transactional and tug-of-war models are developed for societies in which cobreeders have the option to reproduce independently and in which the decision on reproductive shares is made among the individuals directly involved in reproduction. However, these scenarios may not necessarily apply in polygyne ant societies. First, queens have lost their wings and so do not have the option to leave the colony and begin independent breeding unless colonies can reproduce by budding. Second, the workers may act as an independent party with their own reproductive interests.
In the present study, we use the parameters provided by reproductive skew models as a guideline for factors that may determine reproductive sharing in polygyne ants. The models cannot be tested as such, as the assumptions the models are based on have not been confirmed in our study system. The aim is to estimate the effect of four potential determinants of reproductive skew in the ant Formica fusca, a species known to be weakly polygyne (Rosengren et al., 1993; this study). We measured three key parameters most commonly used in reproductive skew models: (1) relatedness among cobreeding queens, a variable included in all skew models (Johnstone, 2000); (2) total production, which is included in both transactional and tug-of war models (Johnstone and Cant, 1999b; Reeve and Ratnieks, 1993; Reeve et al., 1998;); and (3) queen size as an indicator of her potential fighting ability (Field et al., 1998; Reeve and Ratnieks, 1993), as queens of F. fusca are observed to coexist amicably within association (Hannonen and Sundström, 2002). In addition, we included a fourth parameter, the effective number of queens in the colony of origin as reflected by the relatedness among workers. Different decision rules may apply depending on the number of queens present in a colony, and more queens (represented by more independent haploid genomes, sensu Pamilo, 1983) may translate into reduced abilities to selectively favor the offspring of one particular queen, or the ability to suppress fellow queens (see also skew models for multimember groups by Johnstone et al., 1999; Reeve and Emlen, 2000). To our knowledge, this is the first study to test for the effects of various determinants of skew in an experimental setting.
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METHODS |
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Laboratory cultures
Entire F. fusca colonies were excavated in April–May 1997 (56 colonies) and 1999 (81 colonies) from two populations located about 1 km apart on a bog and in a logged area in southwest Finland. At the time of collection, the snow had melted, and the ants aggregated close to the surface attracted by the heat of the sun. None of the queens had started laying eggs at the time of collection. About 30% of the field colonies contained two or more queens, so we constructed 41 (24 in 1997, 17 in 1999) laboratory colonies, each with two queens and 300 ± 50 workers originating from the same field colony. We used plastic trays (30 x 40 x 15 cm) as nest-boxes, with peat and material from the field colony as nest material. Each next-box also contained a 15 x 15-cm bathroom tile, under which the ants built their nest, as well as Sphagnum sp. to keep in the humidity.
The colonies were watered and fed daily, with a Bhatkar-Whitcomb diet (Bhatkar and Whitcomb, 1970), and the temperature followed the ambient outdoor temperature. Within approximately a week, all queens had started to lay eggs. Under the prevailing conditions, only worker brood is produced. In both years, the brood and the queens were frozen when the brood had pupated. All queens were dissected for the presence of yellow bodies and to ascertain that they were mated (an opaque spermatheca indicates that a queen is mated). After dissection, the spermathecae were stored separately in alcohol for later DNA-microsatellite analysis. We assigned the total production of each laboratory nest into three classes: class 1 (less than 50 pupae), class 2 (50–100 pupae), class 3 (more than 100 pupae). In total, 30 colonies (19 in 1997, 11 in 1999) produced enough pupae (more than 30) for the study purpose, and those colonies were used in subsequent analyses.
We measured queen size by measuring the widest part of the head capsule to the nearest 0.01 mm (wild x40 with a x10 ocular with a built-in scale). We then calculated the size difference for each pair of queens by using the equation of Field et al. (1998), in which the size difference is given by the equation (queen 1-queen 2)/(mean for the pair).
Genotyping methods
Queens, their spermathecae (analyzed with DNA-microsatellites only), and 30–100 pupae per nest were genotyped at one allozyme (1997 only; 6pgd, Seppä, 1992) and seven DNA-microsatellite loci (FL12, FL20, FL21, Chapuisat, 1996; FE13, FE17, FE19, FE21, Gyllenstrand et al., 2002. DNA was extracted from two legs (queens) or entire pupae in 200 ml 5% Chelex, or in 75 ml 5% Chelex (spermathecae) and incubated for 2 x 15 min at 95°C (vortexed between the two incubation periods). PCR amplification was carried out in10-ml reaction volume comprising 1.5 ml DNA template, 0.5 pmol primers, x1 Dynazyme PCR-buffer, 1.5 mM MgCl2, 0.2 U enzyme (Dynazyme II, Finnzymes), 75 mM each dA/T/GTP, and 6 mM dCTP nucleotides. The amplified fragments were internally labeled with a 32P-dCTP (0.2 mCi/reaction). The PCR profile comprised an initial denaturation step for 5 min at 94°C, 30 cycles of 1 min at 94°C, 30 s at the primer-specific annealing temperature (for FL12, Fl20, FE13, FE19: 55°C and for FL21, FE17, FE21: 50°C), 30-s extension at 72°C, and then a final extension step of 5 min at 72°C. The PCR products were separated in 6% denaturing polyacrylamide sequencing gels (Sequagel, National Diagnostics) at 55 V/gel and visualized by autoradiography.
Relatedness estimates, maternity shares, and the measure for reproductive skew
The population-wide allele frequencies and the relatedness between each pair of queens were estimated from multilocus data by using Relatedness 4.2. (Queller and Goodnight, 1989). SEs for estimates were received by jackknifing over the colonies. Although we had several highly polymorphic loci, the SEs for the relatedness estimates between queens are necessarily wide, as there were only two queens per nest. However, the estimate is unbiased (Lynch and Ritland, 1999), so chance deviations in either direction will only increase scatter but not result in a systematic error. For each pair of queens, one or more diagnostic loci were selected, such that the offspring could be assigned to one queen based either on alleles carried by the queens or the sperm in her spermatheca. In most colonies (17 of 19 colonies in 1997, and nine of 11 colonies in 1999), all offspring could be assigned based on one locus; for the remaining ones, we combined information from two loci.
As a measure of reproductive skew, we used the proportion of offspring that was assigned to the queen with majority production. This measure takes values between 0.5 and 1, so that when a single individual produces all the offspring, skew is one, and when reproduction is equal, skew is 0.5. The use of proportions is reasonable here, as the number of offspring is high (no correction for sampling errors is necessary) and because the number of queens always was two. Hence, the problems associated with measuring skew within groups with variable numbers of cobreeders and overall productivity (Kokko et al., 1999; Nonacs, 2000) do not arise.
Statistical methods
All independent test variables were normally distributed (Wilk-Shapiro test for normality, w > 0.9). We were able to measure queen-queen relatedness, total production, and worker relatedness from all 30 colonies. The size ratio could be calculated only for 23 colonies. Hence, queen size ratio was not included in the ANCOVA, and its effect on skew was tested separately with linear regression.
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RESULTS |
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Queen number, relatedness estimates, and size ratio within pairs of queens
Queen number varied from one to 26 per field colony (Figure 1), and deviated from a Poisson distribution (p <.001 in both 1997 and 1999), such that there was an excess of colonies with few queens. The harmonic mean number of queens, as estimated from the observed distributions in the entire material, was slightly lower in the population sampled in 1997 (harmonic mean ± SD = 1.38 ± 4.11) than that sampled in 1999 (harmonic mean ± SD = 1.82 ± 4.71). The relatedness among nest-mate queens, corrected for inbreeding (Pamilo, 1985
), was significantly higher in the 1997 population (0.53 ± 0.09; mean ± SE) than in the 1999 population (0.34 ± 0.10; I = 2.51, df = 28, p =.019). The average inbreeding-corrected (Pamilo, 1985) relatedness among workers in the experimental (i.e., polygyne) colonies was 0.36 ± 0.03 in 1997 and 0.09 ± 0.06 in 1999.
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Queen sizes were similar in both populations (mean ± SD, 1997 = 1.49 ± 0.10 mm, 1999 = 1.43 ± 0.12 mm). Interestingly, the size differences within colonies, as estimated according to Field et al. (1998)
, were extremely small (1997 = 0.004 ± 0.05 mm, 1999 = -0.005 ± 0.02 mm). Conversely, the variation in queen size between colonies was significantly larger than within colonies (ANOVA F ratio = 10.76, df = 22, p <.001). The CV was also larger among all queens (CV = 0.075) than within queen pairs (mean CV = 0.026).
Determinants of reproductive skew
All queens had yellow bodies in their ovaries and an opaque spermatheca, indicating that they were mated and had laid eggs. The total production varied among colonies, but most produced more than 100 pupae (Table 2). In 1997, on average, 61 ± 20 (mean ± SD) offspring per colony were genotyped, and in 1999, 53 ± 18 offspring per colony were genotyped. The average degree of reproductive skew did not differ between populations (1997: median skew = 0.66; lower and upper quartiles = 0.61and 0.81, respectively; 1999: median skew = 0.65; lower and upper quartiles = 0.58 and 0.9, respectively; t = -0.628, df = 28, p =.535). In half of the colonies, the queens contributed unequally to the brood (binomial test, threshold p =.0016 after a Bonferroni correction) (Figure 2).
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The effects of year (population), worker relatedness, total production, and queen-queen relatedness were entered as independent variables in an ANCOVA to test for their effects on reproductive skew. A stepwise backward elimination procedure was used to find the significant effects in the model. The only significant effect was the relatedness between queens, which explained 26% of the variation in reproductive skew among queens (Table 3). The higher the relatedness between queens, the lower the skew in both study populations (Figure 3). None of the other variables—year, worker relatedness, and total production (given in the order of backward elimination)—had any effect on the degree of skew. Queen size ratio did not have any effect on skew (r2 =.07, N = 23, p =.22).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The results show that among the factors analyzed here, the relatedness among nest-mate queens is the most important determinant of the degree of reproductive skew in F. fusca. The higher the relatedness between cobreeding queens is, the more equally they share reproduction in both study populations. By contrast, factors such as fighting ability, as reflected by size differences, or the productivity of the group had no effects on the degree of skew. In addition, the fact that the effective number of queens, expressed through worker relatedness, was not associated with skew suggests that the genetic affinity between queens, rather than the general kin structure of the colony dictates skew.
As reproductive skew was estimated from worker pupae instead of sexual offspring, one could argue that the results only reflect "nonreproductive skew" (following the method of Reeve and Ratnieks, 1993), with no evolutionary consequences. However, in a companion paper, we show that cobreeding queens have similar representation among female sexual and contemporary worker brood (Hannonen M and Sundström L, in preparation). Hence, our results based on worker offspring most likely reflect the true reproductive success of queens in F. fusca.
Our result of negative association between relatedness and reproductive skew is consistent with the predictions of two different skew models. The restriction model (Johnstone and Cant, 1999b) predicts that when relatedness between cobreeders increases, the more the subordinate individual is able to claim reproduction for herself without being evicted by the dominant, which emerges as a negative association between skew and relatedness. However, the model assumption is not relevant for our study species, as there are no observations on social dominance hierarchy within F. fusca queen associations (Hannonen and Sundström, 2002). Moreover, the queens are not under a threat of being evicted from the colony by the dominant member.
The tug-of-war model (Reeve et al., 1998) holds that when relatedness among cobreeders increases, skew either decreases or shows no change as both the dominant and the subordinate individual reduce their efforts to claim reproduction for themselves. However, dominance hierarchy and fighting ability among cobreeders play a crucial role in this model. Again, neither dominance hierarchies nor fights between queens have been found in F. fusca. Indeed, in a companion paper we show that queens from the same field colony coexist amicably (Hannonen and Sundström, 2002), suggesting that fighting does not play any role as a determinant of reproductive skew in F. fusca.
In ants, the power of decision may also lie with the colony workers as they are in a position to control the number of queens (Keller and Vargo, 1993; see also Reeve and Keller, 2001). Hence, they may selectively execute aggressive queens and so promote the peaceful coexistence of queens. This begs the question to what extent and how the workers affect the reproductive shares of queens. Indeed, if fighting increases with size differences between coexisting queens, such worker intervention may result in smaller differences in queen size than otherwise would be expected. Our results are consistent with this interpretation, as the average size differences between coexisting queens were much smaller than the range of size variation in the population.
Recent extensions to the traditional reproductive skew models incorporate the effect of workers, defined as the "collective" dominant, as distinct from the queens, one of which may become the "virtual" dominant, (Reeve and Keller, 2001; Reeve and Jeanne, 2003). Hence, the workers may be the party in control and exert their reproductive interests by favoring the queen they are more closely related to. The predictions of this model are otherwise identical to those given by the basic concession model, but the behaviorally dominant queen may not be the reproductively dominant one if worker relatedness to the behaviorally subordinate queen exceeds that to the behaviorally dominant one. Hence, a behaviorally subordinate queen may become a virtual dominant.
The virtual dominant scenario might actually explain our result of negative correlation between skew and relatedness among queens. If cobreeding queens are full sisters, most workers will be more equally related to both queens and will have no kin-selected incentive to favor one queen over the other, which would result in low skew. However, when queens are unrelated or of low relatedness, most workers may be more related to one of the queens. If workers favor the queen of closest kin, high skew would ensue. As a result, a negative association between relatedness and reproductive skew would arise, being consistent with the virtual dominant scenario (Reeve and Keller, 2001; Reeve and Jeanne, 2003). Indeed, we have addressed this question in a companion paper (Hannonen and Sundström, 2003).
Given that the degree of reproductive skew is the result of largely nonaggressive interaction involving both workers and queens, and that the effect of one party on the other may be indirect, the question arises how information is conveyed between the parties. An obvious candidate is chemical communication. Chemicals, such as pheromones, may act either directly on queen fecundity, or the workers may tend queens based on their chemical signals (Keller and Nonacs, 1993; Reeve and Keller, 2001). Direct chemical control seems unlikely, because a queen producing a pheromone inhibiting reproduction in a competitor is likely to inhibit her own reproduction as well (Keller and Nonacs, 1993). By contrast, evidence for chemical signaling was found in a study by Ortius and Heinze (1999), in which queens in polygyne colonies of the ant Leptothorax sp A influence the behavior of both competing queens and workers by signaling their fecundity. In F. fusca, pheromonal profiles of highly related queens may be hard to discriminate, so the workers may treat such queens and their offspring more equitably than queens of lower relatedness. As a result, the degree of skew would be lower in colonies with closely related queens and higher in colonies with more distantly related queens. The effect of workers on reproductive sharing among queens should be further studied by getting data on how workers behave toward queens with different levels of fecundity and relatedness.
Differences in queen reproductive shares may also arise if phenotypic traits or age correlate with the intrinsic fecundity of queens (Keller 1993; Keller and Ross, 1993). Differences in fitness have been demonstrated in a large number of organisms, and there is generally a strong genetic component underlying phenotypic differences. This explanation predicts that skew should be lower in colonies in which queens are genetically more similar because they are highly related. This interpretation is also consistent with our results. As nothing is known about queen fecundity and reproductive success during previous reproductive seasons in F. fusca, it is possible that differences in fecundity, as represented by the time window of this study, are associated with differences in queen age (Bourke, 1991; Brian, 1988; Keller, 1993). A high rate of queen turnover, which has been demonstrated in several species of polygynous ants (Bourke et al., 1997; Evans, 1996; Seppä, 1994; see also Heinze and Keller, 2000), leads to the coexistence of queens from different age cohorts within a same colony. Given a high rate of queen turnover, queens of the same age may have the same mother and thus may be more closely related compared with queens from different age cohorts, which most likely have different mothers. If queen fecundity reflects her age, then queen associations comprising queens of similar age will have similar fecundity and, consequently, will share reproduction more equally (low reproductive skew) than in associations in which queens belong to different age cohorts. Thus, age-specific fecundity may also lead to a negative association between relatedness and reproductive skew among queens, as shown in the present study.
In conclusion, our results highlight the importance of further experimental exploration into the events during egg-laying and offspring rearing. New predictions may develop when the detailed assumptions are changed. There is also need for further studies on two aspects. First, the effect of queen age on the fecundity and on reproductive skew within polygyne colonies deserves exploration, which will require long-term data on the same colonies and also tools to age the queens. Second, more detailed experimental studies based on the virtual dominant scenario are needed. Studies of communication between cobreeding queens and workers in polygyne ant colonies might shed light on the proximate mechanisms determining reproductive skew within queen associations.
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ACKNOWLEDGEMENTS |
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We thank H. K. Reeve and R. L. Jeanne for access to an unpublished manuscript; H. Kokko, H. K. Reeve, and two anonymous referees for comments; K. Bargum, K. Eloranta, H. Helanterä, C. Henricson, T. Honkasalo, K. Lindqvist, L. Saarikoski, and K. Trontti for help during fieldwork; and Tvärminne Zoological station for providing working facilities. This paper was funded by the Academy of Finland (grant no. 42725).
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Bhatkar A, Whitcomb WH, 1970. Artificial diet for rearing various ant species. Fla Entomol 53:229-232.[CrossRef]
Bourke AFG, 1991. Queen behaviour, reproduction and egg-cannibalism in multiple queen colonies of the ant Leptothorax acervorum. Anim Behav 42:295-310.[CrossRef]
Bourke AFG, Franks NR, 1995. Social evolution in ants. Princeton, New Jersey: Princeton University Press.
Bourke AFG, Green HAA, Bruford MW, 1997. Parentage, reproductive skew and queen turnover in a multiple-queen ant analysed with microsatellites. Proc R Soc Lond B 264:277-283.[Medline]
Brian MV, 1988. Variation in the social behaviour and fecundity of queens in the polygyne ant Myrmica rubra L. Insect Soc 33:118-131.[CrossRef]
Cant MA, 1998. A model for the evolution of reproductive skew without reproductive suppression. Anim Behav 55:163-169.[CrossRef][ISI][Medline]
Cant MA, Johnstone RA, 1999. Costly young and reproductive skew in animal societies. Behav Ecol 10:178-184.
Chapuisat M, 1996. Characterization of microsatellite loci in Formica lugubris B and their variability in other ant species. Mol Ecol 5:599-601.[CrossRef][Medline]
Evans JD, 1996. Queen longevity, queen adoption, and posthumous indirect fitness in the facultatively polygnous ant Myrmica tahoensis. Behav Ecol Sociobiol 39:275-284.
Field J, Solis CR, Queller DC, Strassmann JE, 1998. Social and genetic structure of paper wasp cofoundress associations: tests of reproductive skew models. Am Nat 151:545-563.[CrossRef]
Gyllenstrand N, Gertsch PJ, Pamilo P, 2002. Polymorphic microsatellite DNA markers in the ant Formica exsecta. Mol Ecol Notes 2:67-69.[CrossRef]
Hamilton WD, 1964a. The genetical evolution of social behaviour: I. J Theor Biol 7:1-16.[CrossRef][ISI][Medline]
Hamilton WD, 1964b. The genetical evolution of social behaviour: II. J Theor Biol 7:17-52.[CrossRef][ISI][Medline]
Hannonen M, Sundström L, 2002. Proximate determinants of reproductive skew in polygyne colonies of the ant Formica fusca. Ethology 108:961-973.[CrossRef]
Hannonen M, Sundström L, 2003. Worker nepotism among polygynous ants. Nature 421:910.[CrossRef][Medline]
Heinze J, Keller L, 2000. Alternative reproductive strategies: a queen perspective in ants. Trends Ecol Evol 15:508-512.[CrossRef][Medline]
Hölldobler B, Wilson EO, 1977. The number of queens: sn important trait in ant evolution. Naturwissenschaften 64:8-15.[CrossRef][ISI]
Hölldobler B, Wilson EO, 1990. The ants. Cambridge, Massachusetts: Belknap Press of Harvard University Press.
Johnstone RA, 2000. Models of reproductive skew: a review and synthesis. Ethology 106:5-26.
Johnstone RA, Cant MA, 1999a. Reproductive skew and indiscriminate infanticide. Anim Behav 57:243-249.[CrossRef][ISI][Medline]
Johnstone RA, Cant MA, 1999b. Reproductive skew and the threat of eviction: a new perspective. Proc R Lond Ser B 266:275-279.[CrossRef]
Johnstone RA, Woodroffe R, Cant MA, Wright J, 1999. Reproductive skew in multi-member groups. Am Nat 153:315-331.[CrossRef][ISI]
Keller L, 1993. The assessment of reproductive success of queens in ants and other social insects. Oikos 67:177-180.[CrossRef]
Keller L, Nonacs P, 1993. The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787-794.[CrossRef]
Keller L, Reeve HK, 1994. Partitioning of reproduction in animal societies. Trends Evol Ecol 9:98-102.[CrossRef]
Keller L, Ross KG, 1993. Phenotypic basis of reproductive success in social insects: genetic and social determinants. Science 260:1107-1110.
Keller L, Vargo EL, 1993. Reproductive structure and reproductive roles in colonies of social insects. In: Queen number and sociality in insects, 1st ed (Keller L, ed). Oxford: Oxford University Press;16–44.
Kokko H, Johnstone RA, 1999. Social queuing in animal societies: a dynamic model of reproductive skew. Proc R Soc Lond Ser B 266:1-8.[Medline]
Kokko H, Mackenzie A, Reynolds JD, Lindström J, Sutherland WJ, 1999. Measures of inequality are not equal. Am Nat 154:358-382.[CrossRef][Medline]
Krebs JR, Davies NB, 1997. Behavioural ecology: an evolutionary approach. Cambridge: Cambridge University Press.
Lynch M, Ritland K, 1999. Estimation of pairwise relatedness with molecular markers. Genetics 152:1753-1766.
Nonacs P, 2000. Measuring and using skew in the study of social behavior and evolution. Am Nat 156:577-589.[CrossRef]
Ortius D, Heinze J, 1999. Fertility signaling in queens of a North American ant. Behav Ecol Sociobiol 45:151-159.[CrossRef]
Pamilo P, 1983. Genetic differentiation within subdivided populations of Formica ants. Evolution 37:1010-1022.[CrossRef][ISI]
Pamilo P, 1985. Effect of inbreeding on genetic relatedness. Hereditas 103:195-200.[ISI][Medline]
Queller DC, Goodnight KF, 1989. Estimating relatedness using genetic markers. Evolution 43:258-275.[CrossRef][ISI]
Reeve HK, 2000. A transactional theory of within-group conflict. Am Nat 155:365-382.[CrossRef][Medline]
Reeve HK, Emlen ST, 2001. Reproductive skew and group size: anN-person staying incentive model. Behav Ecol 11:640-647.
Reeve HK, Emlen ST, Keller L, 1998. Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behav Ecol 9:267-278.
Reeve HK, Jeanne RL, 2003. From individual control to majority rule: extending transactional models of reproductive skew in animal societies. Proc R Soc Lond Ser B 270:1041-1045.[Medline]
Reeve HK, Keller L, 2001. Tests of reproductive-skew models in social insects. Annu Rev Entomol 46:347-385.[CrossRef][ISI][Medline]
Reeve HK, Ratnieks FLW, 1993. Queen-queen conflict in polygynous societies: mutual tolerance and reproductive skew. In: Queen number and sociality in insects, 1st ed (Keller L, ed). Oxford: Oxford University Press; 45–85.
Rosengren R, Pamilo P, 1983. The evolution of polygyny and polydomy in mound building Formica. Acta Ent Fenn 42:65-77.
Rosengren R, Sundström L, Fortelius W, 1993. Monogyny and polygyny in Formica ants: the result of alternative dispersal strategies. In: Queen number and sociality in insects, 1st ed (Keller L, ed). Oxford: Oxford University Press; 308–333.
Seppä P, 1992. Genetic relatedness of worker nestmates in Myrmica ruginoidis (Hymenoptera: Formicidae) populations. Behav Ecol Sociobiol 30:253-260.[CrossRef]
Seppä P, 1994. Sociogenetic organization of the ants Myrmica ruginodis and Myrmica lobicornis: number, relatedness and longevity of reproducing individuals. J Evol Biol 7:71-95.
Vehrencamp SL, 1983a. A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667-682.[CrossRef][ISI]
Vehrencamp SL, 1983b. Optimal degree of skew in cooperative societies. Am Zool 23:327-335.
Walin L, Seppä P, Sundström L, 2001. Reproductive allocation in the polygynous, polydomous ant Myrmica rubra. Ecol Entomol 26:1-10.[CrossRef]
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