Skip to main content

Experience-expectant brain plasticity corresponds to caste-specific abiotic challenges in dampwood termites (Zootermopsis angusticollis and Z. nevadensis)

The Science of Nature volume 108, Article number: 57 (2021) Cite this article

Abstract

Hypotheses for adaptive brain investment predict associations between the relative sizes of functionally distinct brain regions and the sensory/cognitive demands animals confront. We measured developmental differences in the relative sizes of visual processing brain regions (optic lobes) among dampwood termite castes to test whether optic lobe investment matches caste differences in exposure to visually complex environments. The winged primary reproductives (Kings/Queens) on mating flights are the only caste to leave the dark nest cavities and as predicted, Kings/Queens showed greater relative investment in optic lobe tissue than nestbound (neotenic) reproductives and soldiers in two dampwood termite species (Zootermopsis angusticollis and Z. nevadensis). Relative optic lobe size spanned more than an order of magnitude among the castes we studied, suggesting the growth of the optic lobes incurs substantial tissue costs. Optic lobe growth was experience-expectant: the optic lobes of Z. angusticollis brachypterous nymphs, which typically develop into Kings/Queens, were relatively larger than the optic lobes of apterous nymphs, which precede neotenics and soldiers, and relative optic lobe size of nestbound brachypterous nymphs was statistically similar to that of Kings/Queens. Experience-expectant brain tissue growth is rarely documented in insects, likely because it entails high potential costs of tissue production and maintenance and relatively low immediate sensory/cognitive benefits. We develop hypotheses for the conditions under which experience-expectant growth in brain regions could be favored by natural selection.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

Data availability

Data will be published as a supplementary file with the paper; to be uploaded after final acceptance.

References

  • Ackman JB, Crair MC (2014) Role of emergent neural activity in visual map development. Curr Opin Neurobiol 24:166–175

    Article  PubMed  CAS  Google Scholar 

  • Bausenwein A, Dittrich AMP, Fischbach KF (1992) The optic lobe of Drosophila melanogaster. Cell Tiss Res 267:17–28

    Article  CAS  Google Scholar 

  • Brent CS (2001) Reproductive maturation in primary and secondary reproductives of the dampwood termite Zootermopsis angusticollis Hagen: the role of social signals and nutrition. PhD dissertation. Boston University

  • Bulova S, Purce K, Khodak P, Sulger E, O’Donnell S (2016) Into the black, and back: the ecology of brain investment in Neotropical army ants (Formicidae: Dorylinae). Sci Nat 103:31

    Article  CAS  Google Scholar 

  • Castle GB (1934) The life history of the common damp-wood termite Zootermopsis angusticollis. PhD dissertation. University of California

  • Cnotka J, Möhle M, Rehkämper G (2008) Navigational experience affects hippocampus size in homing pigeons. Brain Behav Evol 72:233–238

    Article  PubMed  Google Scholar 

  • Corona M, Libbrecht R, Wheeler DE (2016) Molecular mechanisms of phenotypic plasticity in social insects. Curr Opin Ins Sci 13:55–60

    Article  Google Scholar 

  • de Paula DE Jr, de Oliveira MT, Bruscadin JJ, Pinheiro DG, Bomtorin AD, Coelho Júnior VG, Moda LMR, Simões ZLP, Barchuk AR (2021) Caste-specific gene expression underlying the differential adult brain development in the honeybee Apis mellifera. Ins Molec Biol 30:42–56

    Article  Google Scholar 

  • Ehmer B, Gronenberg W (2004) Mushroom body volumes and visual interneurons in ants: comparison between sexes and castes. J Comp Neurol 469:198–213

    Article  PubMed  Google Scholar 

  • Fahrbach SE, Giray T, Robinson GE (1995) Volume changes in the mushroom bodies of adult honey bee queens. Neurobiol Learn Mem 63:181–191

    Article  PubMed  CAS  Google Scholar 

  • Fahrbach SE, Moore D, Capaldi EA, Farris SM, Robinson GE (1998) Experience-expectant plasticity in the mushroom bodies of the honeybee. Learn Mem 5:115–123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fahrbach SE, Farris SM, Sullivan JP, Robinson GE (2003) Limits on volume changes in the mushroom bodies of the honey bee brain. J Neurobiol 57:141–151

    Article  PubMed  Google Scholar 

  • Fischbach KF, Hiesinger PR (2008) Optic lobe development. In: Technau GM (ed) Brain Development in Drosophila melanogaster. Advances in Experimental Medicine and Biology 628. Springer, New York

    Google Scholar 

  • Gaston R (1969) Nervous system and sense organs. In: Krishna K, Weesner FM (eds) Chapter 6, Biology of termites, Vol 1. Academic Press, New York, pp 161–192

    Google Scholar 

  • Golestani N, Zatorre RJ (2004) Learning new sounds of speech: reallocation of neural substrates. Neuroimage 21:494–506

    Article  PubMed  Google Scholar 

  • Greenough WT, Black JE, Wallace CS (1987) Experience and brain development. Child Dev 58:539–559

    Article  PubMed  CAS  Google Scholar 

  • Hartke TR, Baer B (2011) The mating biology of termites: a comparative review. Anim Behav 82:927–936

    Article  Google Scholar 

  • Hasenstaub A, Otte S, Callaway E, Sejnowski TJ (2010) Metabolic cost as a unifying principle governing neuronal biophysics. Proc Nat Acad Sci 107:12329–12334

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayashi Y, Kitade O, Kojima JI (2003) Parthenogenetic reproduction in neotenics of the subterranean termite Reticulitermes speratus (Isoptera: Rhinotermitidae). Entomol Sci 6:253–257

    Article  Google Scholar 

  • Howse PE (1968) On the division of labour in the primitive termite Zootermopsis nevadensis (Hagen). Insect Soc 15:45–50

    Article  Google Scholar 

  • Ilies I, Muscedere ML, Traniello JF (2015) Neuroanatomical and morphological trait clusters in the ant genus Pheidole: evidence for modularity and integration in brain structure. Brain Behav Evol 85:63–76

    Article  PubMed  Google Scholar 

  • Jones TA, Jefferson SC (2011) Reflections of experience-expectant development in repair of the adult damaged brain. Devel Psychobiol 53:466–475

    Article  Google Scholar 

  • Jones TA, Donlan NA, O’Donnell S (2009) Growth and pruning of mushroom body Kenyon cell dendrites during worker behavioral development in the paper wasp, Polybia aequatorialis (Hymenoptera: Vespidae). Neurobiol Learn Mem 92:485–495

    Article  PubMed  Google Scholar 

  • Julian GE, Gronenberg W (2002) Reduction of brain volume correlates with behavioral changes in queen ants. Brain Behav Evol 60:152–164

    Article  PubMed  Google Scholar 

  • Korb J, Hartfelder K (2008) Life history and development-a framework for understanding developmental plasticity in lower termites. Biol Rev 83:295–313

    Article  PubMed  Google Scholar 

  • Korb J, Thorne B (2017) Sociality in termites. In: Rubenstein DR, Abbott P (eds) Comparative social evolution. Cambridge University Press, Cambridge, pp 124–153

    Chapter  Google Scholar 

  • Kotrschal A, Rogell B, Maklakov AA, Kolm N (2012) Sex-specific plasticity in brain morphology depends on social environment of the guppy, Poecilia reticulata. Behav Ecol Sociobiol 66:1485–1492

    Article  Google Scholar 

  • Moczek AP (2010) Phenotypic plasticity and diversity in insects. Phil Trans R Soc B 365:593–603

    Article  PubMed  PubMed Central  Google Scholar 

  • Moran D, Softley R, Warrant EJ (2015) The energetic cost of vision and the evolution of eyeless Mexican cavefish. Sci Adv 1:e1500363

    Article  PubMed  PubMed Central  Google Scholar 

  • Morland AB, Brown HD, Baseler HA (2021) Cortical reorganization: reallocated responses without rewiring. Curr Biol 31:R76–R78

    Article  PubMed  CAS  Google Scholar 

  • Myles TG (1986) Reproductive soldiers in the Termopsidae (Isoptera). Pan-Pac Entomol 62:293–299

    Google Scholar 

  • Nalepa CA, Jones SC (1991) Evolution of monogamy in termites. Biol Rev 66:83–97

    Article  Google Scholar 

  • Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804

    Article  PubMed  CAS  Google Scholar 

  • Noirot C, Thorne BL (1988) Ergatoid reproductives in Nasutitermes columbicus (Isoptera, Termitidae). J Morphol 195:83–93

    Article  PubMed  Google Scholar 

  • Northrop RB, Guignon EF (1970) Information processing in the optic lobes of the lubber grasshopper. J Insect Phys 16:691–713

    Article  Google Scholar 

  • O’Donnell S, Bulova SJ (2017) Development and evolution of brain allometry in wasps (Vespidae): Size, ecology and sociality. Curr Opin Ins Sci 22:54–61

    Article  Google Scholar 

  • O’Donnell S, Clifford MR, Bulova SJ, DeLeon S, Papa C, Zahedi N (2014) A test of neuroecological predictions using paperwasp caste differences in brain structure (Hymenoptera: Vespidae). Behav Ecol Sociobiol 68:529–536

    Article  Google Scholar 

  • Penick CA, Ghaninia M, Haight KL, Opachaloemphan C, Yan H, Reinberg D, Liebig J (2021) Reversible plasticity in brain size, behaviour and physiology characterizes caste transitions in a socially flexible ant (Harpegnathos saltator). Proc R Soc B 288:20210141

    Article  PubMed  CAS  Google Scholar 

  • Rehan SM, Bulova SJ, O’Donnell S (2015) Cumulative effects of foraging behavior and social dominance on brain development in a facultatively social bee (Ceratina australensis). Brain Behav Evol 85:117–124

    Article  PubMed  Google Scholar 

  • Richard G (1969) Nervous system and sense organs. In: Krishna K, Weesner FM (eds) Biology of termites. Academic Press Inc, New York, pp 161–192

    Chapter  Google Scholar 

  • Roat TC, da Cruz LC (2010) Differences in mushroom bodies morphogenesis in workers, queens and drones of Apis mellifera: neuroblasts proliferation and death. Micron 41:382–389

    Article  PubMed  Google Scholar 

  • Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Springer, Dordrecht, pp 95–119

  • Roisin Y, Korb J (2010) Social organisation and the status of workers in termites. In: Bignell D, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 133–164

    Chapter  Google Scholar 

  • Rosengaus RB, Traniello JF (1993) Temporal polyethism in incipient colonies of the primitive termite Zootermopsis angusticollis: a single multiage caste. J Ins Behav 6:237–252

    Article  Google Scholar 

  • Shellman-Reeve JS (1994) Ecology of colony founding in a dampwood termite: Zootermopsis nevadensis. PhD Dissertation, Cornell University, 384 pages

  • Sherry DF (2006) Neuroecology. Ann Rev Psychol 57:167–197

    Article  Google Scholar 

  • Strausfeld NJ (2005) The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arth Struct Devel 34:235–256

    Article  Google Scholar 

  • Strausfeld NJ, Olea-Rowe B (2021) Convergent evolution of optic lobe neuropil in Pancrustacea. Arth Struct Devel 61:101040

    Article  Google Scholar 

  • Thorne BL, Noirot C (1982) Ergatoid reproductives in Nasutitermes corniger (Motschulsky) (Isoptera: Termitidae). Int J Ins Morphol Embryol 11:213–226

    Article  Google Scholar 

  • Thorne BL, Breisch NL, Haverty MI (2002) Longevity of kings and queens and first time of production of fertile progeny in dampwood termite (Isoptera; Termopsidae; Zootermopsis) colonies with different reproductive structures. J Anim Ecol 71:1030–1041

    Article  Google Scholar 

  • Thorne BL, Breisch NL, Muscedere ML (2003) Evolution of eusociality and the soldier caste in termites: influence of intraspecific competition and accelerated inheritance. Proc Natl Acad Sci 100:12808–12813

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weesner FM (1969) External anatomy. In: Krishna K, Weesner FM (eds) Biology of termites. Academic Press Inc., New York, pp 19–45

    Chapter  Google Scholar 

  • Zuberi H (1963) L’anatomie comparée du cerveaux chez les Termites en rapport avec le polymorphisme. Bull Biol France Belg 97:147–207

    Google Scholar 

Download references

Acknowledgements

Thanks to two anonymous reviewers for helpful comments on the manuscript. James Traniello and Rebecca Rosengaus gave advice and insights into the biology of Zootermopsis termites. Barbara Thorne and Nancy Breisch generously provided Z. nevadensis subject termites and made extensive insightful comments on the manuscript.

Funding

This work was funded by Drexel College of Arts and Sciences and NSF grants IBN 0347315 and IOS 0923680.

Author information

Authors and Affiliations

  1. Departments of Biodiversity Earth & Environmental Science and Biology, Drexel University, Philadelphia, PA, 19081, USA

    Sean O’Donnell, Susan Bulova & Meghan Barrett

Authors
  1. Sean O’Donnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susan Bulova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meghan Barrett
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S. O’D.: conceptualization, data curation, statistical analyses, study design, project administration, writing of the original draft, and review and editing; S.B.: data collection and study design; M.B.: data collection, study design, and review and editing. All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Corresponding author

Correspondence to Sean O’Donnell.

Ethics declarations

Ethics approval

Not applicable, because this article solely studies nonvertebrate organisms for which ethical approval is not required.

Consent to participate

Not applicable, because no human subjects were studied.

Consent for publication

Not applicable, because no human subjects were studied.

Competing interests

The authors declare no competing interests.

Additional information

Communicated by: Matthias Waltert

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

O’Donnell, S., Bulova, S. & Barrett, M. Experience-expectant brain plasticity corresponds to caste-specific abiotic challenges in dampwood termites (Zootermopsis angusticollis and Z. nevadensis). Sci Nat 108, 57 (2021). https://doi.org/10.1007/s00114-021-01763-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-021-01763-9

Keywords

  • Optic lobes
  • Retina