Skip to main content
SpringerLink
Log in

Dominance and inheritance patterns of mobility and death feigning in beetle strains selected for moving activity

  • Original Paper
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Reciprocal crossing of different strains is a suitable method to investigate the dominance and inheritance of a focal trait. Herein, we performed reciprocal crossing among strains of Tribolium castaneum exhibiting a genetically high (H strain) and low (L strain) moving activity and investigated the related heritable factors in the F1 and F2 generations. We also evaluated death-feigning behavior, which negatively responded to artificial selection for moving activity in T. castaneum. The results obtained for the F1 generation suggest that low moving activity and short duration of death feigning were dominant. In the F2 generation, movement and death feigning exhibited continuous segregation. The distribution of each trait value in the F2 generation differed from that in the parental generation, and no individuals transgressing the distribution of trait values in the parental generation emerged in the F2 generation. These results suggest that the genetic correlation between movement and death-feigning behavior is controlled in a polygenic manner. Moreover, the examination of the proportions of both behaviors (high vs. low moving activity and long vs. short death-feigning duration) in the F1 generation revealed that the two behaviors may be controlled by the maternal genotype, suggesting that the gene(s) that control movement and death feigning are located on the sex chromosome in T. castaneum.

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
Fig. 6

Similar content being viewed by others

References

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  • Brisson JA, Davis GK, Stern DL (2007) Common genome-wide patterns of transcript accumulation underlying the wing polyphenism and polymorphism in the pea aphid (Acyrthosiphon pisum). Evol Dev 9:338–346

    Article  CAS  Google Scholar 

  • Brisson JA, Ishikawa A, Miura T (2010) Wing development genes of the pea aphid and differential gene expression between winged and unwinged morphs. Insect Mol Biol 19(2):63–73

    Article  CAS  Google Scholar 

  • Campbell JF, Athanassiou CG, Hagstrum DW, Zhu KY (2022) Tribolium castaneum: a model insect for fundamental and applied research. Annu Rev Entomol 67:347–365

    Article  Google Scholar 

  • Clutton-Brock TH, Parker GA (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456

    Article  Google Scholar 

  • Dingle H (2014) Migration: the biology of life on the move. Oxford University Press, USA

    Book  Google Scholar 

  • Dingle H, Drake VA (2007) What is migration? Bioscience 57:113–121

    Article  Google Scholar 

  • Falconer DS (1996) Introduction to quantitative genetics. Pearson Education, India

    Google Scholar 

  • Fox J, Weisberg S (2019) An [R] companion to applied regression. SAGE, Thousand Oaks

    Google Scholar 

  • Froy O, Gotter AL, Casselman AL, Reppert SM (2003) Illuminating the circadian clock in monarch butterfly migration. Science 300:1303–1305

    Article  CAS  Google Scholar 

  • Garland T Jr, Losos JB (1994) Ecological morphology of locomotor performance in squamate reptiles. Ecol Morphol Integr Org Biol 1994:240–302

    Google Scholar 

  • Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366

    Article  Google Scholar 

  • Irschick DJ, Garland T Jr (2001) Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system. Annu Rev Ecol Syst 32:367–396

    Article  Google Scholar 

  • Irschick DJ, Meyers JJ, Husak JF, Le Galliard J-F (2008) How does selection operate on whole-organism functional performance capacities? A review and synthesis. Evol Ecol Res 10:177–196

    Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland

    Google Scholar 

  • Masaki S (1990) Effect of selection on wing dimorphism in the ground cricket Dianemobius fascipes (Walker). Boll San Veg Plagas (fuera De Serie) 20:381–393

    Google Scholar 

  • Matsumura M (1996) Genetic analysis of a threshold trait: density-dependent wing dimorphism in Sogatella furcifera (Horváth)(Hemiptera: Delphacidae), the whitebacked planthopper. Heredity 76:229–237

    Article  Google Scholar 

  • Matsumura K, Miyatake T (2015) Differences in attack avoidance and mating success between strains artificially selected for dispersal distance in Tribolium castaneum. PLoS ONE 10:e0127042. https://doi.org/10.1371/journal.pone.0127042

    Article  CAS  Google Scholar 

  • Matsumura K, Miyatake T (2022) Polygene control and trait dominance in death-feigning syndrome in the red flour beetle Tribolium castaneum. Behav Genet 52:298–305. https://doi.org/10.1007/s10519-022-10108-9

    Article  Google Scholar 

  • Matsumura K, Yasui Y (2022) Genetic link between mobility and sexual attractiveness in male Tribolium castaneum beetles. Anim Behav 188:111–117. https://doi.org/10.1016/j.anbehav.2022.04.010

    Article  Google Scholar 

  • Matsumura K, Sasaki K, Miyatake T (2016) Correlated responses in death-feigning behavior, activity, and brain biogenic amine expression in red flour beetle Tribolium castaneum strains selected for walking distance. J Ethol 34:97–105

    Article  Google Scholar 

  • Matsumura K, Sasaki K, Miyatake T (2022) Responses to artificial selection for locomotor activity: a focus on death feigning in red flour beetle. J Evol Biol 35:855–867. https://doi.org/10.1111/jeb.14012

    Article  Google Scholar 

  • McCulloch GA, Oliphant A, Dearden PK, Veale AJ, Ellen CW, Waters JM (2019) Comparative transcriptomic analysis of a wing-dimorphic stonefly reveals candidate wing loss genes. EvoDevo 10:21

    Article  Google Scholar 

  • Miyatake T (1997) Correlated responses to selection for developmental period in Bactrocera cucurbitae (Diptera: Tephritidae): time of mating and daily activity rhythms. Behav Genet 27:489–498

    Article  CAS  Google Scholar 

  • Miyatake T, Katayama K, Takeda Y, Nakashima A, Sugita A, Mizumoto M (2004) Is death–feigning adaptive? Heritable variation in fitness difference of death–feigning behaviour. Proc R Soc Lond B 271:2293–2296

    Article  Google Scholar 

  • Miyatake T, Tabuchi K, Sasaki K, Okada K, Katayama K, Moriya S (2008) Pleiotropic antipredator strategies, fleeing and feigning death, correlated with dopamine levels in Tribolium castaneum. Anim Behav 75:113–121

    Article  Google Scholar 

  • Naylor AF (1961) Dispersal in the red flour beetle Tribolium castaneum (Tenebrionidae). Ecology 42:231–237

    Article  Google Scholar 

  • Oufiero CE, Garland T Jr (2007) Evaluating performance costs of sexually selected traits. Funct Ecol 21:676–689

    Article  Google Scholar 

  • Pai A, Feil S, Yan G (2007) Variation in polyandry and its fitness consequences among populations of the red flour beetle, Tribolium castaneum. Evol Ecol 21:687–702

    Article  Google Scholar 

  • Parker GA (1978) Evolution of competitive mate searching. Annu Rev Entomol 23:173–196

    Article  Google Scholar 

  • Reppert SM, de Roode JC (2018) Demystifying monarch butterfly migration. Curr Biol CB 28:R1009–R1022

    Article  CAS  Google Scholar 

  • Reppert SM, Gegear RJ, Merlin C (2010) Navigational mechanisms of migrating monarch butterflies. Trends Neurosci 33:399–406

    Article  CAS  Google Scholar 

  • Ridley AW, Hereward JP, Daglish GJ, Raghu S, Collins PJ, Walter GH (2011) The spatiotemporal dynamics of Tribolium castaneum (Herbst): adult flight and gene flow. Mol Ecol 20:1635–1646

    Article  CAS  Google Scholar 

  • Roff DA (1986) The evolution of wing dimorphism in insects. Evolution 40:1009–1020

    Article  Google Scholar 

  • Roff DA, Fairbairn DJ (1991) Wing dimorphisms and the evolution of migratory polymorphisms among the Insecta. Am Zool 31:243–251

    Article  Google Scholar 

  • Sokoloff A (1974) The biology of Tribolium, with special emphasis on genetic aspects. Oxford University Press, USA

    Google Scholar 

  • Tada S, Honma K, Kakizaki M, Fujisaki K, Nakasuji F (1994) Genetic mode of flight muscle dimorphism in a scarabaeid, Heptophylla picea Motschulsky. Appl Entomol Zool 29:303–305

    Article  Google Scholar 

  • Team RC (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Thornhill R, Alcock J (2013) The evolution of insect mating systems. Harvard University Press

    Google Scholar 

  • Xue J, Bao YY, Li BL, Cheng YB, Peng ZY, Liu H, Xu HJ, Zhu ZR, Lou YG, Cheng JA, Zhang CX (2010) Transcriptome analysis of the brown planthopper Nilaparvata lugens. PLoS ONE 5:e14233

    Article  CAS  Google Scholar 

  • Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Anthony Zera Publications

    Book  Google Scholar 

  • Zhan S, Merlin C, Boore JL, Reppert SM (2011) The monarch butterfly genome yields insights into long-distance migration. Cell 147:1171–1185

    Article  CAS  Google Scholar 

  • Zhu H, Yuan Q, Briscoe AD, Froy O, Casselman A, Reppert SM (2005) The two CRYs of the butterfly. Curr Biol CB 15:R953–R954

    Article  CAS  Google Scholar 

  • Zhu H, Sauman I, Yuan Q, Casselman A, Emery-Le M, Emery P, Reppert SM (2008) Cryptochromes define a novel circadian clock mechanism in monarch butterflies that may underlie sun compass navigation. PLoS Biol 6:e4

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by Grant-in-Aid for Japan Society for the Promotion of Science (JSPS) Fellows to KM (no. 20J00383) and a grant from Grant-in-Aid for Scientific Research KAKENHI 21H02568 to TM.

Author information

Authors and Affiliations

  1. Graduate School of Environmental and Life Science, Okayama University, Okayama, Japan

    Kentarou Matsumura & Takahisa Miyatake

Authors
  1. Kentarou Matsumura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takahisa Miyatake
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors conceived and designed the study. K.M. performed the experiment and analyses. All authors contributed to the interpretation of data and drafted the manuscript. All authors approved the final version and agree to be accountable for the content therein.

Corresponding author

Correspondence to Kentarou Matsumura.

Ethics declarations

Competing interests

The authors declare no competing interests.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matsumura, K., Miyatake, T. Dominance and inheritance patterns of mobility and death feigning in beetle strains selected for moving activity. Genetica 151, 1–10 (2023). https://doi.org/10.1007/s10709-022-00174-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-022-00174-6

Keywords

Search

Navigation