Elsevier

Animal Behaviour

Volume 75, Issue 1, January 2008, Pages 113-121
Animal Behaviour

Pleiotropic antipredator strategies, fleeing and feigning death, correlated with dopamine levels in Tribolium castaneum

https://doi.org/10.1016/j.anbehav.2007.04.019Get rights and content

A prey animal has the alternative of fleeing or feigning death to survive when it encounters predators. We found that fleeing by an artificial threat, locomotion and feigning death are pleiotropically correlated with a genetic factor related to a biogenic amine in the red flour beetle, Tribolium castaneum. Walking distance of adults was significantly lower in strains artificially selected for longer (L strains) than shorter duration (S strains) of death-feigning. Crosses showed that S-strain adults were dominant in the frequency and duration of death-feigning and locomotor activity compared to those of L strains, suggesting that death-feigning and activity have the same genetic basis. S-strain adults fled, but L-strain adults feigned death, when they encounter artificial threat. Not only adults that were directly selected for the duration of death-feigning, but also the larvae of L strains frequently showed tonic immobility, when they were dropped onto the ground: the larvae of S strains showed this behaviour less often. This suggests that chemical modulators of behaviour present in these insects before and after metamorphosis control both general locomotor activity and death-feigning. Brain levels of the candidate neuromodulator dopamine were, in fact, found to be significantly higher in S strains compared to L strains in the two selection replications. Thus, we suggest that two alternative behaviours related to antipredator strategies, fleeing or feigning death, are associated with the pleiotropic effects of a neuroactive substance in T. castaneum.

Section snippets

Insects and Culture

The Tribolium castaneum beetle culture used in this study has been maintained in laboratories for more than 25 years. The beetles were fed wholemeal (Yoshikura Shokai, Tokyo, Japan) enriched with brewer's yeast (Asahi Beer, Toyko, Japan) as the rearing medium and kept in a chamber (Sanyo, Tokyo, Japan) maintained at 25°C and 60% RH under a photoperiod of 16:8 h light:dark cycle (lights on at 0700, light off at 2300).

Observation of Death-feigning

One day before observation, each beetle was placed in a well of a 48-well tissue

Responses to Selection

The duration of death-feigning showed a clear direct response to selection and a steady divergence between the two selection regimes in both selection replications (Fig. 1). After 16 generations of selection, S strain beetles feigned death for 0.1 s, while L strain beetles showed more than 2 min of death-feigning on average.

The frequency of death-feigning behaviour also showed a clear correlated response to selection for the duration of death-feigning (Fig. 2). After 10 generations, almost all L

Discussion

A genetic correlation was found between death-feigning behaviour and the level of running with locomotor activity, which is associated with fleeing in T. castaneum. Beetles derived from strains having less and more death-feigning had longer and shorter travelling distances, respectively. Predator avoidance rates may depend on a prey's travel speed when the prey escapes by fleeing. On the other hand, death-feigning behaviour is adaptive to survival when T. castaneum adults encounter a model

Acknowledgments

The authors thank Dr Mike Speed and two anonymous referees for valuable comments on the manuscript and Yukari Takeda, Atsushi Sugita and Yusuke Nishi for insect rearing, and Dr Akira Matsumoto and Prof. Masaki Sakai for useful advice on neuroactive substances. This work was supported by KAKENHI 19370011 and 19657026, Grant-in-Aid for Scientific Research, JSPS and MEXT to T.M.

References (70)

  • C. Refshauge et al.

    New high performance liquid chromatographic analysis of brain catecholamines

    Life Sciences

    (1974)
  • K. Sasaki et al.

    Distribution and levels of dopamine and its metabolites in brains of reproductive workers in honeybees

    Journal of Insect Physiology

    (2001)
  • K. Sasaki et al.

    Brain tyramine and reproductive states of workers in honeybees

    Journal of Insect Physiology

    (2002)
  • R. Scheiner et al.

    Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees

    Behavioural Brain Research

    (2002)
  • S. Acheampong et al.

    Quiescence in the Colorado potato beetle, Leptinotarsa decemlineata

    Entomologia Experimentalis et Applicata

    (1997)
  • S.A. Adamo et al.

    The role of neurohormonal octopamine during “fight or flight” behavior in the field cricket Gryllus bimaculatus

    Journal of Experimental Biology

    (1995)
  • A. Agresti

    Categorical Data Analysis

    (1990)
  • A.H. Anton et al.

    A study of the factors affecting the aluminum oxide-trihydroxyindole procedure for the analysis of catecholamines

    Journal of Pharmacology and Experimental Therapeutics

    (1962)
  • G. Bicker et al.

    Chemical codes for the control of behaviour in arthropods

    Nature

    (1989)
  • G.L. Brookhart et al.

    Amphetamine and reserpine deplete brain biogenic amines and alter blow fly feeding behavior

    Journal of Neurochemistry

    (1987)
  • J.L. Casagrand et al.

    Biogenic amines modulate synaptic transmission between identified giant interneurons and thoracic interneurons in the escape system of the cockroach

    Journal of Neurobiology

    (1992)
  • N.A. Chentsova et al.

    Stress response in Drosophila melanogaster strain inactive with decreased tyramine and octopamine contents

    Journal of Comparative Physiology B

    (2002)
  • A.P. Davenport et al.

    Changes in haemolymph octopamine levels associated with food deprivation in the locust, Schistocerca gregaria

    Physiological Entomology

    (1984)
  • B.E. Donnelly et al.

    Functional response of Xylocoris flavipes (Hemiptera: Anthocoridae): effects of prey species and habitat

    Environmental Entomology

    (2001)
  • E. Ebermann

    Thanatosis or feigning death in mites of the family Scutacaridae

  • M. Edmunds

    Defense in Animals

    (1974)
  • J.H. Fabre
    (1900)
  • V.P. Fedotov et al.

    Cardiac activity of freshwater crayfish at wakefulness, rest, and “animal hypnosis”

    Journal of Evolutionary Biochemistry and Physiology

    (2006)
  • E.N. Franq

    Behavioral aspects of feigned death in the opossum Didelphis marsupialis

    American Midland Naturalist

    (1969)
  • J.J. Gart et al.

    The effect of bias, variance estimation, skewness and kurtosis of the empirical logit on weighed least squares analyses

    Biometrika

    (1985)
  • R.S. Goldstein et al.

    Different effects of the biogenic amines, dopamine, serotonin and octopamine on the thoracic and abdominal portions of the escape circuit in the cockroach

    Journal of Comparative Physiology A

    (1991)
  • J.B.S. Haldane

    The estimation and significance of the logarithm of a ratio of frequencies

    Annals of Human Genetics

    (1955)
  • K. Harano et al.

    Depression of brain dopamine and its metabolite after mating in European honeybee (Apis mellifera) queens

    Naturwissenchaften

    (2005)
  • H.A. Hofmann et al.

    Flight restores fight in crickets

    Nature

    (2000)
  • J.S. Holmes

    Death-feigning in Ranatra

    Journal of Comparative Neurology and Psychology

    (1906)
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      There is evidence, in insects, that individuals that are active at the time of threat often adopt a fleeing strategy, while inactive individuals more frequently resort to a TI strategy. In T. castaneum, the strain selected for long TI duration had lower levels of locomotor activity (walking distance measured for 15 min by an image tracking system) than in the short duration strain, proving a negative genetic correlation between the intensity of TI and activity levels (Miyatake et al., 2008). The same was found in Tribolium confusum (Nakayama et al., 2010).

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    K. Sasaki is at the Department of Brain and Bioinformation Science, Kanazawa Institute of Technology, Hakusan, Ishikawa, 924-0838, Japan.

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