Primary sex ratio adjustment by ant queens in response to local mate competition

doi:10.1016/j.anbehav.2004.09.005

Animal Behaviour

Volume 69, Issue 5, May 2005, Pages 1031-1035

https://doi.org/10.1016/j.anbehav.2004.09.005 Get rights and content

In the ant Cardiocondyla obscurior, wingless males compete with nestmate males for access to female mating partners, leading to local mate competition (LMC). Queen number varies between colonies, resulting in variation in the strength of LMC. Cremer & Heinze (2002, Proceedings of the Royal Society of London, Series B, 269, 417–422) showed that colonies responded to increasing queen number by producing a less female-biased sex ratio, as predicted by LMC theory. However, the proximate mechanisms responsible for this variation in the sex ratio could not be determined because the study was restricted to adult sex ratios. With LMC, the primary sex ratio (proportion of haploid eggs laid by the queen) is expected to be female biased, which lowers the conflict between queens and workers over sex allocation. We compared the primary sex ratios laid by queens in monogynous and in polygynous experimental colonies of C. obscurior. The proportion of haploid eggs laid by queens was significantly lower in single-queen than in multiple-queen colonies. Furthermore, queens rapidly adjusted their primary sex ratios to changes in colony queen number. This is the first report of an adaptive adjustment of the primary sex ratio in response to LMC by ant queens.

Section snippets

Ant colonies

Eight polygynous colonies of C. obscurior were collected in Bahia, Brazil and cultivated in the laboratory as described elsewhere (Heinze et al. 1998). Permission for collection and export was given by the Brazilian Minister of Science and Technology. No licence was required for import. Each colony was split into one colony fragment containing a single queen (monogynous) and another fragment containing five queens (polygynous), all with an initial number of 20 workers per colony fragment. This

Results

There was a significant difference in the primary sex ratio laid by queens from monogynous and polygynous fragments (logistic regression analysis: χ₁² = 4.66, P = 0.031). Whereas the average proportion of haploid eggs laid by queens in single-queen colony fragments ±SD was 0.08 ± 0.04 (range 0.05–0.14, N = 7), this value increased to 0.18 ± 0.07 (range 0.05–0.25, N = 8) in multiple-queen fragments (Fig. 1). When these polygynous fragments were split into monogynous subunits for an additional 6 weeks (i.e.

Discussion

This study shows that queens of the ant C. obscurior lay a significantly lower proportion of haploid eggs in single-queen than in multiple-queen colonies. The adjustment of the primary sex ratio in response to the changing conditions in the colony (presence/absence of other queens) was relatively rapid, as it occurred within 6 weeks. These results are consistent with the predictions of the LMC theory, because males in monogynous colonies are more closely related and experience a higher local

Acknowledgments

We thank J. S. Pedersen, M. Chapuisat, S. West and two anonymous referees for improving the manuscript. Thanks also to M. Gilbert for his advice with the statistical part of the work. Financial support was provided by the FRIA (L.M.), the DFG (Deutsche Forschungsgemeinschaft: He 1623/12-2) and a Feodor Lynen Fellowship by the Alexander von Humboldt-Foundation (S.C.), and the Belgian National Fund for Scientific Research (Conventions: 2.4597.05, 2.4569.02, 15.174.04) (S.A.).

References (30)

S. Aron et al.
Mode of colony foundation influences the primary sex ratio in ants
Animal Behaviour
(1999)
S. Aron et al.
Queen–worker conflict over sex ratio. A comparison of primary and secondary sex ratios in the Argentine ant, Iridomyrmex humilis
Journal of Evolutionary Biology
(1994)
S. Aron et al.
Evolution of social parasitism in ants: size of sexuals sex ratio and mechanisms of caste determination
Proceedings of the Royal Society of London, Series B
(1999)
S. Aron et al.
Evolution of miniaturisation in inquiline parasitic ants: timing of male elimination in Plagiolepis pygmaea, the host of Plagiolepis xene
Insectes Sociaux
(2004)
M. Beekman et al.
Power over reproduction in social Hymenoptera
Philosophical Transactions of the Royal Society of London, Series B
(2003)
J.J. Boomsma et al.
Analysis of sex ratios in social insects
A.F.G. Bourke et al.
Social Evolution in Ants
(1995)
M. Chapuisat et al.
Testing kin selection with sex allocation data in eusocial Hymenoptera
Heredity
(1999)
S. Cremer et al.
Adaptive production of fighter males: queens of the ant Cardiocondyla adjust the sex ratio under local mate competition
Proceedings of the Royal Society of London, Series B
(2002)
S. Cremer et al.
Stress grows wings: environmental induction of winged dispersal males in Cardiocondyla ants
Current Biology
(2003)

R.H. Crozier et al.

Evolution of Social Insect Colonies. Sex Allocation and Kin Selection

(1996)

E. Hasegawa et al.

Population structure, local mate competition, and sex-allocation pattern in the ant Messor aciculatus

Evolution

(1995)

J. Heinze et al.

Behavior of ergatoid males in the ant Cardiocondyla nuda

Insectes Sociaux

(1993)

J. Heinze et al.

Male competition in Cardiocondyla ants

Behavioral Ecology and Sociobiology

(1998)

L. Keller et al.

Inter-nest sex-ratio variation and male brood survival in the ant Pheidole pallidula

Behavioral Ecology

(1996)

Cited by (18)

Evolution of the scale and manner of brother competition in pollinating fig wasps
2009, Animal Behaviour
Citation Excerpt :
In Cardiocondyla ants, a lack of dispersal is associated with fighting between siblings (Heinze et al. 1998), although the fighting is not directed to dispersing males which have a different scale of competition for matings (Anderson et al. 2003). Also, queens adjust their sex ratio to LMC (Cremer & Heinze 2002; de Menten et al. 2005) and when there is a single queen, the sex ratio is so female biased that fighting has been lost again (Heinze et al. 2005; Schrempf et al. 2005). This last observation is reminiscent of what may have happened with nonfighting pollinators.
Contest competition and male dispersal have evolved a number of times in pollinating fig wasps. Given their highly female-biased sex ratios and high relatedness between competing males, this phenomenon is surprising. Using a comparative approach, we found a significant association between high adult sex ratios (male:female), fighting and dispersal. We conclude that a relatively high proportion of males could have led to the evolution of fighting and to excess males that avoid kin conflict through dispersal. These wasps respond to increased competition between relatives by altering the scale at which they compete, but also by competing more intensely. In support of the new generation of kin selection models, we found that relatedness of competing males has no effect on the likelihood of fighting. Even so, selection at a higher hierarchical level has selected for dispersal and hence a larger scale at which competition occurs. We found that although the sex ratio gives a rough indication of the mating system it fails to be accurate at a finer scale.
Sex allocation conflict in ants: When the queen rules
2006, Current Biology
Citation Excerpt :
The absence of worker control despite strong variation in worker relatedness asymmetry among colonies suggests that F. selysi queens might be particularly effective in controlling sex allocation. Queens can influence colony sex allocation by controlling the fertilization of the eggs they lay [16, 17], which determines the primary proportion of haploid and diploid brood provided to workers. In some species, queens might prevent worker manipulation by limiting the number of diploid eggs, thus forcing workers to rear males [14, 15, 18].
Insect societies are paramount examples of cooperation, yet they also harbor internal conflicts whose resolution depends on the power of the opponents 1, 2, 3, 4. The male-haploid, female-diploid sex-determining system of ants causes workers to be more related to sisters than to brothers, whereas queens are equally related to daughters and sons [1]. Workers should thus allocate more resources to females than to males, while queens should favor an equal investment in each sex. Female-biased sex allocation and manipulation of the sex ratio during brood development suggest that workers prevail in many ant species 1, 2, 5. Here, we show that queens of Formica selysi strongly influenced colony sex allocation by biasing the sex ratio of their eggs. Most colonies specialized in the production of a single sex. Queens in female-specialist colonies laid a high proportion of diploid eggs, whereas queens in male-specialist colonies laid almost exclusively haploid eggs, which constrains worker manipulation. However, the change in sex ratio between the egg and pupae stages suggests that workers eliminated some male brood, and the population sex-investment ratio was between the queens' and workers' equilibria. Altogether, these data provide evidence for an ongoing conflict between queens and workers, with a prominent influence of queens as a result of their control of egg sex ratio.
Queens control caste allocation in the ant Cardiocondyla obscurior
2023, Proceedings of the Royal Society B: Biological Sciences
The indispensable soma of Cardiocondyla obscurior ants
2022, bioRxiv
Laboratory Rearing and Sex Ratio of Apanteles opuntiarum (Hymenoptera: Braconidae), a Potential Biocontrol Agent of Cactoblastis cactorum (Lepidoptera: Pyralidae)
2019, Florida Entomologist
Epigenetic principles of evolution
2018, Epigenetic Principles of Evolution

View all citing articles on Scopus

¹: S. Cremer is now at the Department of Population Biology, Biological Institute, University of Copenhagen, DK-2100 Copenhagen O, Denmark.

²: J. Heinze is at Biology 1, University of Regensburg, Universitätsstrasse 31, D-93040 Regensburg, Germany.

View full text

Primary sex ratio adjustment by ant queens in response to local mate competition

Section snippets

Ant colonies

Results

Discussion

Acknowledgments

Mode of colony foundation influences the primary sex ratio in ants

Animal Behaviour

Queen–worker conflict over sex ratio. A comparison of primary and secondary sex ratios in the Argentine ant, Iridomyrmex humilis

Journal of Evolutionary Biology

Evolution of social parasitism in ants: size of sexuals sex ratio and mechanisms of caste determination

Proceedings of the Royal Society of London, Series B

Evolution of miniaturisation in inquiline parasitic ants: timing of male elimination in Plagiolepis pygmaea, the host of Plagiolepis xene

Insectes Sociaux

Power over reproduction in social Hymenoptera

Philosophical Transactions of the Royal Society of London, Series B

Analysis of sex ratios in social insects

Social Evolution in Ants

Testing kin selection with sex allocation data in eusocial Hymenoptera

Heredity

Adaptive production of fighter males: queens of the ant Cardiocondyla adjust the sex ratio under local mate competition

Proceedings of the Royal Society of London, Series B

Stress grows wings: environmental induction of winged dispersal males in Cardiocondyla ants

Current Biology

Evolution of Social Insect Colonies. Sex Allocation and Kin Selection

Population structure, local mate competition, and sex-allocation pattern in the ant Messor aciculatus

Evolution

Behavior of ergatoid males in the ant Cardiocondyla nuda

Insectes Sociaux

Male competition in Cardiocondyla ants

Behavioral Ecology and Sociobiology

Inter-nest sex-ratio variation and male brood survival in the ant Pheidole pallidula

Behavioral Ecology