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Pharaoh ant colonies dynamically regulate reproductive allocation based on colony demography

  • Michael R. Warner
  • Jessica Lipponen
  • Timothy A. Linksvayer
Original Article

Abstract

The success of social insect colonies is dependent upon efficient and dynamic allocation of resources to alternate queen and worker castes. The developmental and molecular mechanisms regulating the caste fate of individual larvae in response to environmental cues have been the focus of intense study. However, the mechanisms regulating colony-level resource allocation into alternate castes (i.e., caste allocation ratios) are less well studied. Here, we systematically manipulate colony demography to elucidate the social regulatory mechanisms of caste allocation in the ant Monomorium pharaonis. By measuring the effects of demographic manipulation on colony productivity, we infer that caste allocation results from differences in timing and efficiency of culling of very young reproductive-destined larvae, which are always present in colonies. Based on our results, we develop a conceptual model depicting how colonies integrate numerous individual-level caste determination decisions to regulate colony-level caste allocation. We propose that adult workers make decisions about culling larvae based on the ratio of the number of workers to the number of eggs contained in colonies, likely signaled by pheromone present on eggs. This strategy enables the dynamic alteration of colony demography in response to internal and external conditions, which is likely key to the ability of M. pharaonis and similar ants to thrive in disturbed habitats and to become widespread invasive species.

Significance statement

The defining feature of social insect societies is the presence of alternate queen (reproductive) and worker (non-reproductive) castes of individuals. The fitness of social insect colonies is dependent upon efficient allocation of resources to alternate castes, particularly in the case of highly polygynous (multiqueen) societies. However, the mechanisms by which such societies regulate caste allocation are largely unknown. In this study, we perform a range of manipulative studies to disentangle social mechanisms of caste allocation in polygynous ant societies. Based on our results, we develop a model in which colonies manipulate their production of queens (and also males) versus workers according to the present density of eggs in the colony, a reliable indicator of queens’ fertility. Provided egg density is high, colonies kill queen- and male-destined larvae; when egg density falls, colonies begin to rear queens and males. This flexible resource allocation strategy is key to the ability of highly polygynous species to thrive in marginal (often human-associated) habitats.

Keywords

Caste regulation Superorganism Resource allocation Adaptive demography 

Notes

Acknowledgements

We thank Rohini Singh and Justin Walsh for comments on previous drafts of the manuscript. This research was funded by National Science Foundation award IOS-1452520. MRW was funded by National Science Foundation award DGE-1321851.

Supplementary material

265_2017_2430_MOESM1_ESM.bmp (17.2 mb)
Fig. S1 Colonies that were established with similar sizes (~1.2 mL; ~175 adult workers) but different numbers of queens differed in caste allocation. A) Colonies began producing reproductives before queen removal when started with fewer queens. B) Colonies which we observed producing reproductive pupae in the presence of queens contained fewer eggs two weeks prior to the given observation (approximately the developmental time between caste regulation of 1st instar larvae and pupation), demonstrating that number of eggs affects caste regulation (BMP 17578 kb)
265_2017_2430_MOESM2_ESM.bmp (17.2 mb)
Fig. S2 Initially equal-sized (~1.2 mL; ~175 adult workers) colonies differed in colony productivity according to the number of queens they contained at colony creation. At the time of queen removal (6 weeks after colony creation), there was a positive relationship between the number of queens and the number of A) worker pupae, and B) eggs present in colonies, demonstrating that queen number strongly affects colony productivity (BMP 17578 kb)
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Fig. S3 When queens were removed, caste allocation differed between experimental colonies created with two versus four or eight queens. Colonies created with two queens produced higher A) caste ratios (gynes/[gynes + workers]) and B) reproductive ratios ((gynes + males)/(gynes + males + workers)) than those created with four or eight queens. This was the result of increased production of worker pupae in colonies with four and eight queens (B) (BMP 17578 kb)
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Fig. S4 When equal-sized colonies were established with two or eight queens, the number of queens that laid the eggs did not affect production of any caste after queen removal. After removing queens, the number of young brood (eggs and 1st instar larvae) was standardized, such that colonies were demographically equivalent, but differed in the number of queens that laid eggs. This demonstrates that the the shift in caste allocation accompanying increased colony size is not dependent upon a maternal effect (BMP 8789 kb)
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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyUniversity of PennsylvaniaPhiladelphiaUSA

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