Skip to main content
SpringerLink
Log in

Morphological Asymmetry of Antennae and Behavioral Grooming Asymmetries in the Cockroach Periplaneta americana L.

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

To memory of Dmitriy V. Lychakov

Abstract

Animal behaviors are often characterized by functional asymmetry, or lateralization, which is at least in part due to morphological asymmetry of the body and/or brain. To test the hypothesis that functional asymmetry of grooming is associated with morphological asymmetry of the antennae in the cockroach Periplaneta americana, we measured the morphological parameters of the antennae and their segments (total antenna length, scape diameter, pedicel diameter and length, flagellomeral diameter and length) on either side of the body and analyzed behavioral changes induced by the presentation of the sex pheromone component periplanone B. The data obtained indicate a statistically significant lateralization of antennal morphology: the length of each segment is greater in the left antennae, while the width is greater in the right antennae, except for a short region near the antenna base. Correlation analysis revealed the following relationships: the longer right antenna matches longer time spent on its cleaning; the larger diameter of the right scape correlates with antennal grooming frequency; segment asymmetry does not affect grooming asymmetry. Sex pheromone presentation at a suprathreshold dose increased antennal grooming asymmetry, while the asymmetry of leg cleaning was generally intact. Thus, antennal grooming asymmetry, resulting at least in part from morphological asymmetry, changes significantly in the presence of a biologically important olfactory stimulus, the sex pheromone.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

REFERENCES

  1. Weissburg M (1991) Morphological correlates of male claw asymmetry in the fiddler crab Uca pugnax (Smith) (Decapoda, Brachyura). Crustaceana 61(1): 11–20. https://doi.org/10.1163/156854091X00461

    Article  Google Scholar 

  2. Hart NS, Partridge JC, Cuthill IC (2000) Retinal asymmetry in birds. Curr Biol 10(2): 115–117. https://doi.org/10.1016/S0960-9822(00)00297-9

    Article  CAS  PubMed  Google Scholar 

  3. Tobo S, Takeuchi Y, Hori M (2012) Morphological asymmetry and behavioral laterality in the crayfish, Procambarus clarkii. Ecol Res 27(1): 53–59. https://doi.org/10.1007/s11284-011-0867-7

    Article  Google Scholar 

  4. Malashichev YB (2006) One-sided limb preference is linked to alternating-limb locomotion in anuran amphibians. J Comp Psychol 120(4): 401. https://doi.org/10.1037/0735-7036.120.4.401.

    Article  PubMed  Google Scholar 

  5. Palmer AR (2009) Animal asymmetry. Curr Biol 19(12): R473–R477. https://doi.org/10.1016/j.cub.2009.04.006

    Article  CAS  PubMed  Google Scholar 

  6. Udalova GP, Karas’ AY, Zhukovskaya MI (1990) Asymmetry of the direction of movement in gammarus (Gammarus oceanicus) in the open field test. Zhurnal vysshei nervnoi deyatelnosti imeni IP Pavlova 40(1): 93–101. (In Russ).

    CAS  Google Scholar 

  7. Udalova GP, Zhukovskaya MI, Karas AY (1992) Spatial-motor asymmetry in ants with multiple modifications of the labyrinth skill. Vestnik SPbGU 3(1): 67–75. (In Russ).

    Google Scholar 

  8. Moroz KO (2010) Functional asymmetry of invertebrates’ nervous system on the example of spatial orientation of the Tentyriini tribe beetles. Biosystems Diversity 18(2): 39–45. (In Ukr).

    Article  Google Scholar 

  9. Niven JE, Frasnelli E (2018) Insights into the evolution of lateralization from the insects. Progress in brain research 238: 3–31. https://doi.org/10.1016/bs.pbr.2018.06.001

    Article  PubMed  Google Scholar 

  10. Kostylev MA, Malashichev YB (2007) Correlation of the shoulder girdle asymmetry with the limb skeleton asymmetry in Xenopus laevis. Dokl Biol Sci Springer Nature BV 416(1): 374. https://doi.org/10.1134/S0012496607050146

    Article  CAS  Google Scholar 

  11. Frasnelli E, Anfora G, Trona F, Tessarolo F, Vallortigara G (2010) Morphofunctional asymmetry of the olfactory receptors of the honeybee (Apis mellifera). Behav Brain Res 209: 221–225. https://doi.org/10.1016/j.bbr.2010.01.046

    Article  CAS  PubMed  Google Scholar 

  12. Frasnelli E, Vallortigara G, Rogers LJ (2010) Response competition associated with right-left antennal asymmetries of new and old olfactory memory traces in honeybees. Behav Brain Res 209: 36–41. https://doi.org/10.1016/j.bbr.2010.01.014

    Article  PubMed  Google Scholar 

  13. Sreng L (2003) Sensory asymmetries in the olfactory system underlie sexual pheromone communication in the cockroach Nauphoeta cinerea. Neurosci Lett 351: 141–144. https://doi.org/10.1016/S0304-3940(03)00909-1

    Article  CAS  PubMed  Google Scholar 

  14. Møller AP, Swaddle JP (1997) Asymmetry, developmental stability and evolution. Oxford University Press, UK.

    Google Scholar 

  15. Vallortigara G (2000) Comparative neuropsychology of the dual brain: a stroll through animals’ left and right perceptual worlds. Brain and Language 73: 189–219. https://doi.org/10.1006/brln.2000.2303

    Article  CAS  PubMed  Google Scholar 

  16. Güntürkün O, Diekamp B, Manns M, Nottelmann F, Prior H, Schwarz A, Skiba M (2000) Asymmetry pays: visual lateralization improves discrimination success in pigeons. Curr Biol 10(17): 1079–1081. https://doi.org/10.1016/S0960-9822(00)00671-0

    Article  PubMed  Google Scholar 

  17. Toki W, Togashi K (2011) Exaggerated asymmetric head morphology of female Doubledaya bucculenta (Coleoptera: Erotylidae: Languriinae) and ovipositional preference for bamboo internodes. Zool Sci 28(5): 348–354. https://doi.org/10.2108/zsj.28.348

    Article  Google Scholar 

  18. Frasnelli E (2017) Lateralization in Invertebrates. In Lateralized Brain Functions. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6725-4_6

    Book  Google Scholar 

  19. Zakharov VM (2001) Ontogeny and population: Developmental stability and population variation. Russ J Ecol 32(3): 146–150. https://doi.org/10.1023/A:1011397725175

    Article  Google Scholar 

  20. Zakharov VM, Trofimov IE (2014) Homeostatic mechanisms of biological systems: Development homeostasis. Russ J Dev Biol 45(3): 105–116. https://doi.org/10.1134/S1062360414030096

    Article  CAS  Google Scholar 

  21. Lychakov DV (2013) Behavioral lateralization and otolith asymmetry. J Evol Biochem Phys 49: 441–456. https://doi.org/10.1134/S0022093013040099

    Article  Google Scholar 

  22. Trubyanov AB, Glotov NV (2010) Fluctuating asymmetry: Trait variation and the left-right correlation. Dokl Biol Sci Springer Nature BV 431(1): 103. https://doi.org/10.1134/S0012496610020092

    Article  CAS  Google Scholar 

  23. Schafer R, Sanchez TV (1973) Antennal sensory system of the cockroach, Periplaneta americana: Postembryonic development and morphology of the sense organs. J Comp Neurol 149: 335–353. https://doi.org/10.1002/cne.901490304

    Article  CAS  PubMed  Google Scholar 

  24. Toh Y (1981) Fine structure of sense organs on the antennal pedicel and scape of the male cockroach, Periplaneta americana. J Ultrastruct Res 77(2): 119–132. https://doi.org/10.1016/S0022-5320(81)80036-6

    Article  CAS  PubMed  Google Scholar 

  25. Baba Y, Comer CM (2008) Antennal motor system of the cockroach, Periplaneta americana. Cell Tissue Res 331: 751–762. https://doi.org/10.1007/s00441-007-0545-9

    Article  PubMed  Google Scholar 

  26. Böröczky K, Wada-Katsumata A, Batchelor D, Zhukovskaya M, Schal C (2013) Insects groom their antennae to enhance olfactory acuity. Proc Natl Acad Sci USA 110(9): 3615–3620. https://doi.org/10.1073/pnas.121246611

    Article  PubMed  PubMed Central  Google Scholar 

  27. Zhukovskaya MI (2011) Odorant-dependent changes in surface cuticular secretions on the antennae of the cockroach Periplaneta americana. Sensory systems 25(1): 78–86. (In Russ).

    Google Scholar 

  28. Zhukovskaya MI (2014) Grooming behavior in American cockroach is affected by novelty and odor. Scientific World J 2014: 329514. https://doi.org/10.1155/2014/329514

    Article  Google Scholar 

  29. Zhukovskaya MI, Lychakov DV (2014) Asymmetry of antennal grooming in the cockroach (Periplaneta americana). Russ J Physiol 100(7): 829–840. (in Russ).

    Google Scholar 

  30. Novikova ES, Zhukovskaya MI (2015) Octopamine, the insect stress hormone, alters grooming pattern in the cockroach Periplaneta americana. J Evol Biochem Physiol 51(2): 160. https://doi.org/10.1134/S0022093015020118

    Article  Google Scholar 

  31. Martinez AS, Hardie J (2009) Hygroreception in olfactometer studies. Physiol Entomol 34(3): 211–216. https://doi.org/10.1111/j.1365-3032.2009.00675.x

    Article  Google Scholar 

  32. Kapitsky SV, Zhukovskaya MI (1994) Behaviour of male American cockroaches as a response to structural analogs of the sex pheromone. J Evol Biochem Physiol 30: 558–566. (In Russ).

    CAS  Google Scholar 

  33. De Souza AR, Ribeiro B, José N, Prezoto F (2012) Paint marking social wasps: an evaluation of behavioural effects and toxicity. Entomol Exp Appl 144: 244–247. https://doi.org/10.1111/j.1570-7458.2012.01285.x

    Article  Google Scholar 

  34. Zhukovskaya MI, Kapitsky SV (2006) Activity modulation in cockroach sensillum: the role of octopamine. J Insect Physiol 52(1): 76–86. https://doi.org/10.1016/j.jinsphys.2005.09.005

    Article  CAS  PubMed  Google Scholar 

  35. Gavrikov DE (2012) Analysis of asymmetry in the natural population of Drosophila melanogaster. Izd-vo Vost-sib gos akademii obraz, Irkutsk. (In Russ).

    Google Scholar 

  36. Zakharov VM, Shadrina EG, Trofimov IE (2020) Fluctuating Asymmetry, Developmental Noise and Developmental Stability: Future Prospects for the Population Developmental Biology Approach. Symmetry 12: 1376. https://doi.org/10.3390/sym1208137

    Article  Google Scholar 

  37. Bell ATA, Niven JE (2016) Strength of forelimb lateralization predicts motor errors in an insect. Biol Lett 12: 20160547. https://doi.org/10.1098/rsbl.2016.0547

    Article  PubMed  PubMed Central  Google Scholar 

  38. Cooper R, Nudo N, Gonzales JM, Vinson SB, Liang H (2011) Side-dominance of Periplaneta americana persists through antenna amputation. J Insect Behav 24(3): 175–185. https://doi.org/10.1007/s10905-010-9246-4

    Article  Google Scholar 

  39. Letzkus P, Ribi WA, Wood JT, Zhu H, Zhang SW, Srinivasan MV (2006) Lateralization of olfaction in the honeybee Apis mellifera. Curr Biol 16(14): 1471–1476. https://doi.org/10.1016/j.cub.2006.05.060

    Article  CAS  PubMed  Google Scholar 

  40. Hunt ER, Dornan C, Sendova-Franks AB, Franks NR (2018) Asymmetric ommatidia count and behavioural lateralization in the ant Temnothorax albipennis. Sci Rep 8(1): 1–11. https://doi.org/10.1038/s41598-018-23652-4

    Article  CAS  Google Scholar 

  41. Knebel D, Rigosi E (2021) Temporal and structural neural asymmetries in insects. Cur Opin Insect Sci 48: 72–78. https://doi.org/10.1016/j.cois.2021.10.002

    Article  Google Scholar 

  42. Pascual A, Huang K-L, Neveu J, Preat T (2004) Brain asymmetry and long-term memory. Nature 427: 605–606. https://doi.org/10.1038/427605a

    Article  CAS  PubMed  Google Scholar 

  43. Wolff T, Rubin GM (2018) Neuroarchitecture of the Drosophila central complex: A catalog of nodulus and asymmetrical body neurons and a revision of the protocerebral bridge catalog. J Comp Neurol 526(16): 2585–2611. https://doi.org/10.1002/cne.24512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Phillips-Portillo J, Strausfeld NJ (2012) Representation of the brain’s superior protocerebrum of the flesh fly, Neobellieria bullata, in the central body. J Comp Neurol 520(14): 3070–3087. https://doi.org/10.1002/cne.23094

    Article  PubMed  PubMed Central  Google Scholar 

  45. Polilov AA (2015) Small is beautiful: features of the smallest insects and limits to miniaturization. Annu Rev Entomol 60: 103–121. https://doi.org/10.1146/annurev-ento-010814-020924

    Article  CAS  PubMed  Google Scholar 

  46. Polilov AA (2016) Features of the structure of Hymenoptera associated with miniaturization: 1. Anatomy of the fairyfly Anaphes flavipes (Hymenoptera, Mymaridae). Entomological Review 96(4): 407–418. https://doi.org/10.1134/S0013873816040035

    Article  Google Scholar 

  47. Shvetsov AV, Lopatina NG (2015) Molecular genetic basis of long-term memory lateralization in the honeybee Apis mellifera L. Journal of Asymmetry 9(4): 18–25. https://doi.org/10.18454/ASY.2015.34.733

    Article  Google Scholar 

  48. Strunov A, Schneider DI, Albertson R, Miller WJ (2017) Restricted distribution and lateralization of mutualistic Wolbachia in the Drosophila brain. Cellular Microbiology 19(1): e12639. https://doi.org/10.1111/cmi.12639

    Article  CAS  Google Scholar 

  49. Fokin VF, Ponomareva NV (2004) Dynamic characteristics of functional interhemispheric asymmetry. Functional Interhemispheric Asymmetry 17: 349. (In Russ).

    Google Scholar 

  50. Zhukovskaya MI (2008) Selective regulation of sensitivity to odours of different behavioural significance in the American cockroach, Periplaneta americana. Physiol Entomol 33(2): 162–166. https://doi.org/10.1111/j.1365-3032.2008.00615.x

    Article  Google Scholar 

Download references

Funding

This work was implemented within the state assignment to the IEPhB RAS no. 075-0152-22-00.

Author information

Authors and Affiliations

  1. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia

    M. I. Zhukovskaya & E. S. Novikova

Authors
  1. M. I. Zhukovskaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. S. Novikova
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization and experimental design (M.I.Zh.); data collection and processing (M.I.Zh., E.S.N.); writing and editing the manuscript (M.I.Zh., E.S.N.).

Corresponding author

Correspondence to E. S. Novikova.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

All applicable international, national and/or institutional guidelines for the care and use of animals were observed.

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest.

Additional information

Translated by A. Polyanovsky

Russian Text © The Author(s), 2023, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2023, Vol. 59, No. 2, pp. 112–120https://doi.org/10.31857/S0044452923020079.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhukovskaya, M.I., Novikova, E.S. Morphological Asymmetry of Antennae and Behavioral Grooming Asymmetries in the Cockroach Periplaneta americana L.. J Evol Biochem Phys 59, 350–358 (2023). https://doi.org/10.1134/S0022093023020047

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093023020047

Keywords:

Search

Navigation