Caste-specific phenotypic plasticity of Asian weaver ants: Revealing the allometric and non-allometric component of female caste system of Oecophylla smaragdina (Hymenoptera: Formicidae) by using geometric morphometrics

Authors

  • K. V. Mahima University of Calicut, Kerala, India
  • P. P. Anand University of Calicut, Kerala, India
  • S. Seena University of Calicut, Kerala, India
  • K. Shameema University of Calicut, Kerala, India
  • E. M. Manogem University of Calicut, Kerala, India
  • Y. Shibu Vardhanan University of Calicut, Kerala, India

DOI:

https://doi.org/10.13102/sociobiology.v68i2.5941

Keywords:

Asian weaver ant, caste system, Geometric morphometric, polyphenism, Oecophylla smaragdina.

Abstract

In eusocial insects, particularly in ants, caste differentiation is extremely complicated when we rely on traditional taxonomy. In most species, the worker caste does not display any distinct morphological characters neither the caste’s central division according to their morphological size variations. We used a landmark-based geometric morphometric approach to quantify the morphological characteristics of female caste systems (queen, major and minor worker ant) of Oecophylla smaragdina. Our findings suggested that each caste has its unique shape and size. Especially in the worker caste, apart from the size variations, we can use the shape as a prominent tool for distinguishing between them. The O. smaragdina exhibits a triphasic allometry pattern. Studying the allometry and non-allometry components of each caste system revealed a highly complex size and shape relationship in the female caste systems. From the allometric and non-allometric analysis, we concluded that the major worker ants showed a closer relationship with the queen than the minor worker ant. This outcome demonstrated that Asian weaver ant exhibits complex shape variations related to size and is correlated to their functional modular characters. This research sheds new light on caste systems’ taxonomic uncertainties for eusocial hymenopteran groups, especially ants.

Author Biographies

K. V. Mahima, University of Calicut, Kerala, India

Biochemistry & Toxicology Division, Department of Zoology, University of Calicut, Kerala, India 673 635

P. P. Anand, University of Calicut, Kerala, India

Research Scholar, Biochemistry & Toxicology Division, Department of Zoology, University of Calicut, Kerala, India 673 635

S. Seena, University of Calicut, Kerala, India

Research Scholar, Biochemistry & Toxicology Division, Department of Zoology, University of Calicut, Kerala, India 673 635

K. Shameema, University of Calicut, Kerala, India

Biochemistry & Toxicology Division, Department of Zoology, University of Calicut, Kerala, India 673 635

E. M. Manogem, University of Calicut, Kerala, India

Associate Professor, Insect Endocrinology Laboratory, Department of Zoology, University of Calicut, Kerala, India. 673 635

Y. Shibu Vardhanan, University of Calicut, Kerala, India

Associate Professor, Biochemistry & Toxicology Division, Department of Zoology, University of Calicut, Kerala, India 673 635

References

Adams, D.C., Rohlf, F.J. & Slice, D.E. (2013). A field comes of age: geometric morphometric in 21st century. Hystrix, 24: 7-17.

Adams, D.C. (1999). Methods for shape analysis of landmark data from articulated structures. Evolutionary Ecology Research, 1: 959-970.

Alibert, P., Moureau, B., Dommergues, J.L. & David, B. (2001). Differentiation at a microgeographical scale within two species of ground beetle, Carabus auronitens and C. nemoralis (Coleoptera: Carabidae): a geometrical morphometric approach. Zoologica Scripta, 30: 299-311.

Anand, P.P. & Shibu Vardhanan, Y. (2020). Computational modelling of wet adhesive mussel foot proteins (Bivalvia): insights into the evolutionary convolution in diverse perspectives. Scientific Reports, 13: 2612. doi: 10.1038/s41598- 020-59169-y.

Bacaraman, N.B. & Torres, M.A.J. (2016). Mandibular shape variation among different size classes of the Camponotus ant sp. (Hymenoptera: Formicidae). Journal of Biodiversity and Environmental Science, 8(3): 179-186.

Bingham, C.T. (1903). The fauna of British India, Including Ceylon and Burma. Hymenoptera, Volume 2, Ants and Cuckoo wasps. London: Taylor and Francis.

Bookstein, FL (1991). Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge/New York/ Port Chester/ Melbourne/ Sydney. XVIII, 435 S.

Bookstein, FL (1997). Morphometric tools for landmark data: Geometry and Biology. Cambridge: Cambridge University Press.

Chapuisat, M. & Keller, L. (2002). Division of labour influences the rate of ageing in weaver ant workers. Proceedings of the Royal Society of London, Series, B: Biological Sciences, 269: 909-913.

Clyde, W.C. & Gingerich, P.D. (1994). Rates of evolution in the dentition of early Eocene Cantius: comparison of size and shape. Paleobiology, 20: 506-522.

Crozier, R.H., Newey, P.S., Schluns, E.S. & Robson, S. K.A. (2010). A masterpiece of evolution – Oecophylla weaver ants (Hymenoptera: Formicidae). Myrmecological News, 13: 57-71.

Debat, V., Behin, M., Legout, H. & David, J. R. (2003). Allometric and non-allometric components of Drosophila wing shape respond differentially to developmental temperature. Evolution, 57: 2773-2784. doi: 10.1111/j.0014-3820.2003.tb01519.x.

Drake, A.G. & Klingenberg, C. P. (2008). The pace of morphological change: historical transformation of skull shape in St. Bernard dogs. Proceedings of the Royal Society of London B. Biological Sciences, 275: 71-76.

Dryden, I.L. & Mardia, KV (1998). Statistical shape analysis. John Wiley & Sons: New York, 376 pp.

Dzeverin, I. (2008). The stasis and possible patterns of selection in evolution of a group of related species from the bat genus Myotis (Chiroptera, Vespertilliionidae). Journal of Mammalian Evolution, 15: 123-142. doi: 10.1007/s10914-007-9071-5.

Fiedler, K. & Maschwitz, U. (1989). The symbiosis between the weaver ant, Oecophylla smaragdina, and Antene emolus, an obligate myrmecophilous lycaenid butterfly. Journal of Natural History, 23: 833-846.

Fjerdingstad, E.J. & Crozier, R.H. (2006). The evolution of worker caste diversity in social insects. American Naturalist, 167: 390-400.

Fruciano, C. (2016). Measurement error in geometric morpho-metrics. Development Genes and Evolution, 226: 139-158.

Holldobler, B. & Wilson, E.O. (1977). Weaver ants-social esta-blishment and maintenance of territory. Science, 195: 900-902.

Holldobler, B. (1983). Territorial behaviour in the green tree ant (Oecophylla smaragdina). Biotropica, 15: 241-250.

Huang, H.T. & Yang, P. (1987). The antient cultured citrus ant. Bioscience, 37: 665-671.

Hunt, G. (2007). The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages. PNAS, 104: 18404-18408. doi: 10.1073/pnas.0704088104.

Joseph, L.T. & Kotiaho, J.S. (2001). Fluctuating asymmetry. Encyclopedia of Life Science, www.els.net.in.

Katzke, J., Barden, P., Dehon, M., Michez, D. & Wappler, T. (2018). Giant ants and their shape: revealing relationships in the genus Titanomyrma with geometric morphometrics. Peer J, 6: e4242. doi: 10.7717/peerj.4242.

Keller, R.A., Peeters, C. & Beldade, P. (2014). Evolution of thorax architecture in ant castes highlights trade-off between flight and ground behaviors. eLife, 3: e01539.

Kendall, D.G. (1977). The diffusion of shape. Advances in Applied Probability, 9: 428-430. doi: 10.2307/1426091.

Klingenberg, C. P. (2016). Size, shape, and form: concepts of allometry in geometric morphometrics: Development, Genes and Evolution, 226: 113-137.

Klingenberg, C.P. & Zaklan, S.D. (2000). Morphological integration between developmental compartments in the Drosophila wing. Evolution, 54: 1273-1285.

Klingenberg, C.P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology, Evolution and Systematics, 39: 115-132.

Klingenberg, C.P. (2010). Evolution and development of shape: Integrating quantitative approaches. Nature Genetics, 11: 623-635. doi: 10.1038/nrg2829.

Klingenberg, C.P. (2011). Morpho J: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11: 353-357. doi: 10.1111/j.1755-0998.2010.02924.x.

Klingenberg, C.P. (2015). Analysing fluctuating symmetry with geometric morphometrics: concepts, methods and applications. Symmetry, 7: 843-934.

Klingenberg, C.P., Barluenga, M. & Meyer, A. (2002). Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution, 5: 1363-1375.

Langthasa, S., Teron, R. & Tamuli, A.K. (2017). Weaver ants (Oecophylla smaragdina): a multi-utility natural resource in Dima Hasao District, Assam. International Journal of Applied Environmental Science. 12: 709-715.

Londe, S., Monnin, T., Cornette, R., Debat, V., Fisher, B.L. & Molet, M. (2015). Phenotypic plasticity and modularity allow for the production of novel mosaic phenotypes in ants. Evodevo, 6: e36.

Manting, M.M.E. Torres, M.A.J. & Demayo, C.G. (2013). Describing variability in mandible shapes in selected workers of the ant Diacamma rugosum (LeGuillou) 1842. (Hymenoptera: formicidae: Ponerinae). International Research Journal of Biological Science, 2: 8-15.

Molet, M., Wheeler, D.E. & Peeters, C. (2012). Evolution of novel mosaic castes in ants: modularity, phenotypic plasticity, and colonial buffering. The American Naturalist, 180: 328-341.

Mosimann, J.E. (1970). Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. Journal of the American Statistical Association, 65: 930-945.

Nowbahari, B., Feneron, R. & Malherbe, M.C. (2000). Polymorphism and polyphenism in the formicinae ant Cataglyphis niger (Hymenoptera). Sociobiology, 36: 485-496.

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

Peeters, C. & Ito, F. (2001). Colony dispersal and the evolution of queen morphology in social Hymenoptera. Annual Review of Entomology, 46: 601-630.

Peng, R.K. & Christian, K. (2004). The weaver ant, Oecophylla smaragdina (Hymenoptera: Formicidae), an effective biocontrol agent of the red-banded thrips, Selenothrips rubrocinctus (Thysanoptera: Thripidae) in mango crops in the Northern territory of Australia. International Journal of Pest Management, 50: 107-114.

Powell, S. (2016). A comparative perspective on the ecology of morphological diversification in complex societies: nesting ecology and soldier evolution in the turtle ants. Behaviour Ecology and Sociobiology, 70: 1075-1085.

Powell, S., Price, S.L. & Kronauer, D.J. (2020). Trait evolution is reversible, repeatable, and decoupled in the soldier caste of turtle ants. PNAS, 117: 6608-6615.

Premoli, A.C. (1996). Leaf architecture of South American Nothofagus (Nothofagaceae) using traditional and new methods in morphometrics. Botanical Journal of the Linnean Society, 21: 25-40.

Rajkumar, R. et al., (2012). Ancestral developmental potential facilitates parallel evolution in ants. Science, 335(6064): 79-82.

Rohlf, F.J. (1999). Shape statistics: procrustes superimpositions and tangent spaces. Journal of Classification, 16: 197-223. doi: 10.1007/s003579900054.

Rohlf, F.J. (2003). tpsSmall: calculation of shape variation, Version 1.34. Stony Brook, NY: Department of Ecology and Evolution, State University of New York at Stony Brook.

Rohlf, F.J. (2015). The tps series of software. Hystrix, The Italian Journal of Mammalogy, 26: 9-12.

Rohlf, F.J. & L.F. Marcus. (1993). A revolution in morphometrics. Trends in Ecology and Evolution, 8: 129-132.

Savriama, Y. & Klingenberg, C.P. (2011). Beyond bilateral symmetry: geometric morphometric methods for any types of symmetry. BMC Evolutionary Biology, 11: 280.

Scheib, J.E., Gangestad, S.W. & Randy, T. (1999). Facial attractiveness, symmetry and cues of good genes. Proceedings: Biological Sciences, 266: 1913-1917.

Schluns, E., Wegener, B., Schluns, H., Azuma, N., Robson, S. & Crozier, R. (2009). Breeding system, colony and population structure in the weaver ant Oecophylla smaragdina. Molecular Ecology, 18: 156-167.

Seifert, B. (1988). A taxonomic revision of the Myrmica species of Europe, Asia minor and Caucasia. Abhandlungen und Berichte des Naturkundemuseums Gorlitz, 62(3): 1-75.

Seifert, B. (2008). Removal of allometric variation improves species separation in multi-character discriminant functions when species are strongly allometric and exposes diagnostic characters. Myrmecological News, 11: 91-105.

Stanley, S.M. (1979). Macroevolution, pattern and process. San Francisco: W.H. Freeman.

Stanley, S.M. & Yang, X. (1987). Approximate evolutionary stasis for bivalve morphology over millions of years: a multivariate, multilineage study. Paleobiology, 13: 113-139.

Sullivan, R. (2012). Weaver ants use corporate memory to defend nests. https://www.abc.net.au/science/articles/2012/ 03/12/3449920.htm.

Trible, W. & Kronauer, D.J. (2017). Caste development and evolution in ants: its all about size. Journal of Experimental Biology, 220: 53-62.

Tschinkel, W.R., Mikheyev, A.S. & Storz, S.R. (2003). Allometry of worker of the fire Ant, Solenopsis invicta. Journal of Insect Science, 3: 1-11.

Way, M. & Khoo, K.C. (1992). Role of ants in pest management. Annual Review of Entomology. 37: 479-503.

Webster, M. & Sheets, H.D. (2010). A practical introduction to landmark based morphometrics. The Paleontological Society Paper, 16: 163-188.

Wheeler, D.E. (1991). The developmental basis of worker caste polymorphism in ants. American Naturalist, 138: 1218-1238.

Wills, B.D., Powell, S., Rivera, M.D. & Suarez, A.V. (2018). Correlates and consequences of worker polymorphism in ants. Annual Review of Entomology, 63: 575-98.

Wilson, E.O. (1953). The origin and evolution of polymorphism in ants. Quarterly Review of Biology, 28: 136-156.

Wood, A. R., Zelditch, M.L., Rountrey, A.N., Eiting, T.P., Sheets, H.D. & Gingerich, P.D. (2007). Multivariate stasis in the dental morphology of the Palaeocene-Eocene condylarth Ectocian. Paleobiology, 33: 248-260. doi: 10.1666/06048.1.

Yazdi, A.B. (2014). Application of geometric morphometrics to analyse allometry in two species of the genus Myrmica (Hymenoptera: Formicidae). Soil Organisms, 86: 77-84.

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Published

2021-05-31

How to Cite

Mahima, K. V., Anand, P. P., Seena, S., Shameema, K., Manogem, E. M., & Shibu Vardhanan, Y. (2021). Caste-specific phenotypic plasticity of Asian weaver ants: Revealing the allometric and non-allometric component of female caste system of Oecophylla smaragdina (Hymenoptera: Formicidae) by using geometric morphometrics. Sociobiology, 68(2), e5941. https://doi.org/10.13102/sociobiology.v68i2.5941

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Research Article - Ants