The scaling of growth, reproduction and defense in colonies of Amazonian Termites

Pedro A. C. L. Pequeno, Elizabeth Franklin

Abstract


Phenotypes can evolve through life-history tradeoffs. Termites have been the first eusocial insects on Earth, prompting life history evolution at the colony level. Despite this, termite life-history allocation strategies are poorly known. Here, we addressed this issue using novel data on three common species from the diverse, yet understudied Amazonian termite fauna: Neocapritermes braziliensis, Labiotermes labralis and Anoplotermes banksi. Using Oster and Wilson’s optimal caste ratio theory and Higashi et al.’s termite caste allocation theory as frameworks, we assessed how termite colonies should invest in growth (immatures), reproduction (alates) and defense (soldiers) as they accumulate workers. We also examined whether soldier loss in soil-feeding Apicotermitinae (A. banksi) may have affected allocation strategies. We found that: (1) the scaling of immature number was isometric in the three species, contrary to the leveling off expected under resource limitation; (2) colonies of all sizes were equally likely to produce any number of alates, rather than having a size threshold for reproduction; (3) the scaling of soldier number was unrelated to alate production, but varied from isometry in N. braziliensis to negative allometry in L. labralis despite their similar defense strategies; (4) A. banksi had more immatures per worker and a higher maximum alate number per worker than the other species, suggesting that soldier loss may have allowed higher relative investment in colony growth and, possibly, reproduction. Termites can provide novel insights into life-history allocation strategies and their relation to social evolution, and should be better incorporated into sociobiological theory.


Keywords


adaptive demography; caste allocation; inclusive fitness; optimal caste ratio; resource limitation; social insect

Full Text:

PDF

References


Beekman, M., Lingeman, R., Kleijne, F.M. & Sabelis, M.W. (1998). Optimal timing of the production of sexuals in bumblebee colonies. Entomologia Experimentalis et Applicata, 88: 147–154. doi: 10.1023/A:1003401628843

Billick, I. (2001). Density dependence and colony growth in the ant species Formica neorufibrabis. Journal of Animal Ecology, 70: 895–905. doi: 10.1046/j.0021-8790.2001.00562.x

Bourguignon, T., Leponce, M. & Roisin, Y. (2011). Are the spatio-temporal dynamics of soil-feeding termite colonies shaped by intra-specific competition? Ecological Entomology, 36: 776–785. doi: 10.1111/j.1365-2311.2011.01328.x

Bourguignon, T., Šobotník, J., Dahlsjö, C.A.L. & Roisin, Y. (2016). The soldierless Apicotermitinae: insights into a poorly known and ecologically dominant tropical taxon. Insectes Sociaux, 63: 39–50. doi: 10.1007/s00040-015-0446-y

Bouwma, A.M., Nordheim, E. V. & Jeanne, R.L. (2006). Per-capita productivity in a social wasp: No evidence for a negative effect of colony size. Insectes Sociaux, 53: 412–419. doi: 10.1007/s00040-005-0886-5

Cole, B. (2009). The ecological setting of social evolution: the demography of ant populations. In Gadau, J. & Fewell, J. (Eds.), Organization of insect societies: from genome to sociocomplexity (pp. 74–104). Cambridge: Harvard University Press.

Cristaldo, P.F., Almeida, C.S., Cruz, N.G., Ribeiro, E.J.M., Rocha, M.L.C., Santos, A.A., et al. (2017). The role of resource density on energy allocation in the Neotropical termite Nasutitermes aff. coxipoensis (Termitidae: Nasutitermitinae). Neotropical Entomology. doi: 10.1007/s13744-017-0525-z

Dornhaus, A., Powell, S. & Bengston, S. (2012). Group size and its effects on collective organization. Annual Review of Entomology, 57: 123–141. doi: 10.1146/annurev-ento-120710-100604

Engel, M.S., Barden, P., Riccio, M.L. & Grimaldi, D.A. (2016). Morphologically specialized termite castes and advanced sociality in the early cretaceous. Current Biology, 26: 522–530. doi: 10.1016/j.cub.2015.12.061

Higashi, M., Yamamura, N. & Abe, T. (2000). Theories on the sociality of termites. In Abe, T., Bignell, D. & Higashi, M. (Eds), Termites: Evolution, Sociality, Symbioses, Ecology (pp. 169–188). Dordrecht: Kluwer Academic Press.

Hölldobler, B. & Wilson, E.O. (2009). The superorganism. New York: W. W. Norton & Company. 522 p

Hothorn, T., Bretz, F. & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal 50: 346–363. doi: 10.1002/bimj.200810425

Kaspari, M. (1996). Testing resource-based models of patchiness in four Neotropical litter ant assemblages. Oikos, 76: 443–454. doi: 10.2307/3546338

Kaspari, M. & Byrne, M.M. (1995). Caste allocation in litter Pheidole: lessons from plant defense theory. Behavioral Ecology and Sociobiology, 37: 255–263. doi: 10.1007/BF00177405

Korb, J. & Thorne, B. (2017). Sociality in termites. In Rubenstein, D.R. & Abbot, P. (Eds), Comparative social evolution (pp. 124-153). Cambridge: Cambridge University Press.

Kramer, B.H., Scharf, I. & Foitzik, S. (2014). The role of per-capita productivity in the evolution of small colony sizes in ants. Behavioral Ecology and Sociobiology, 68: 41–53. doi: 10.1007/s00265-013-1620-8

Lepage, M. & Darlington, J.P.E.C. (2000). Population dynamics of termites. In Abe, T., Bignell, D. & Higashi, M. (Eds), Termites: Evolution, Sociality, Symbioses, Ecology (pp. 333–361). Dordrecht: Kluwer Academic Press.

Maki, K. & Abe, T. (1986). Proportion of soldiers in the colonies of a dry wood termite, Neotermes koshunensis (Kalotennitidae, Isoptera). Physiology and Ecology Japan. 23: 109-117.

Martius, C. & Ribeiro, J.A. (1996). Colony populations and biomass in nests of the Amazonian forest termite Anoplotermes banksi Emerson (Isoptera: Termitidae). Studies on Neotropical Fauna and Environment, 31: 82–86.

McGlynn, T.P. (2006). Ants on the move: Resource limitation of a litter-nesting ant community in Costa Rica. Biotropica, 38: 419–427. doi: 10.1111/j.1744-7429.2006.00153.x

Naug, D. & Wenzel, J. (2006). Constraints on foraging success due to resource ecology limit colony productivity in social insects. Behavioral Ecology and Sociobiology, 60: 62–68. doi: 10.1007/s00265-005-0141-5

Oster, G.F. & Wilson, E.O. (1978). Caste and ecology in the social insects. Princeton: Princeton University Press, 352 p

Pequeno, P.A.C.L., Franklin, E., Venticinque, E.M. & Serrão Acioli, A.N. (2013). The scaling of colony size with nest volume in termites: A role in population dynamics? Ecological Entomology, 38: 515–521. doi: 10.1111/een.12044

Pequeno, P.A.C.L., Franklin, E., Venticinque, E.M. & Acioli, A.N.S. (2015). Linking functional trade-offs, population limitation and size structure: Termites under soil heterogeneity. Basic and Applied Ecology, 16: 365–374. doi: 10.1016/j.baae.2015.03.001

Pequeno, P.A.C.L., Baccaro, F.B., Souza, J.L.P. & Franklin, E. (2017). Ecology shapes metabolic and life history scalings in termites. Ecological Entomology, 42: 115–124. doi: 10.1111/een.12362

Poitrineau, K., Mitesser, O. & Poethke, H.J. (2009). Workers, sexuals, or both? Optimal allocation of resources to reproduction and growth in annual insect colonies. Insectes Sociaux, 56: 119–129. doi: 10.1007/s00040-009-0004-6

R Development Core Team (2016). R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

Reznick, D. (2014). Evolution of life histories. In Losos, J.B., Baum, D.A., Futuyma, D.J., Hoekstra, H.E., Lenski, R.E., Moore, A.J., Peichel, C.L., Schluter, D. & Whitlock, M.C. (Eds.), The Princeton guide to evolution (pp. 268-275). Princeton: Princeton University Press.

Rivera-Marchand, B., Giray, T. & Guzmán-Novoa, E. (2008). The cost of defense in social insects: Insights from the honey bee. Entomologia Experimentalis et Applicata, 129: 1–10. doi: 10.1111/j.1570-7458.2008.00747.x

Roux, E.A., Roux, M. & Korb, J. (2009). Selection on defensive traits in a sterile caste – caste evolution: A mechanism to overcome life-history trade-offs? Evolution and Development, 11: 80–87. doi: 10.1111/j.1525-142X.2008.00304.x

Shik, J.Z. (2008). Ant colony size and the scaling of reproductive effort. Functional Ecology, 22: 674–681. doi: 10.1111/j.1365-2435.2008.01428.x

Smith, A.R., Wcislo, W.T. & O’Donnell, S. (2007). Survival and productivity benefits to social nesting in the sweat bee Megalopta genalis (Hymenoptera: Halictidae). Behavioral Ecology and Sociobiology, 61: 1111–1120. doi: 10.1007/s00265-006-0344-4

Thomas, M.L. (2003). Seasonality and colony-size effects on the life-history characteristics of Rhytidoponera metallica in temperate south-eastern Australia. Australian Journal of Zoology, 51: 551–567. doi: 10.1071/ZO03037

Tian, L. & Zhou, X. (2014). The soldiers in societies: Defense, regulation, and evolution. International Journal of Biological Sciences, 10: 296–308. doi: 10.7150/ijbs.6847

Walker, J. & Stamps, J. (1986). A test of optimal caste ratio theory using the ant Camponotus (Colobopsis) impressus. Ecology, 67: 1052–1062. doi: 10.2307/1939828

Watanabe, D., Gotoh, H., Miura, T. & Maekawa, K. (2014). Social interactions affecting caste development through physiological actions in termites. Frontiers in Physiology, 5: 1–12. doi: 10.3389/fphys.2014.00127




DOI: http://dx.doi.org/10.13102/sociobiology.v65i1.1786

Refbacks

  • There are currently no refbacks.


JCR Impact Factor 2016: 0.699