Divergent lines selected artificially for many generations make it possible to answer two questions: (1) whether genetic variation still exists within the selected population; and (2) whether the selection itself is costly for the selected strain. In previous studies, the red flour beetle Tribolium castaneum was divergently selected artificially for duration of death-feigning, and strains selected for longer (L-strain) and shorter (S-strain) durations of death-feigning have been established (Miyatake et al. 2004, 2008). Because the selection experiments have been conducted for more than 27 generations, genetic variation may be eroded. Furthermore, because another previous study reported physiological costs to L-strains, the L-strains selected artificially for longer duration of death-feigning may have suffered more costs than the S-strains. In the present study, therefore, we relaxed the selection pressure after the 27th or 30th generation of S- and L-strains. We also carried out reverse selection during the most recent eight generations of S- and L-strains. The results showed that each strain clearly responded to relaxation of selection and reverse selection, suggesting that (1) additive genetic variation still existed in both strains after long-term selection, and (2) selection for shorter and longer duration of death-feigning was costly. These results suggest that anti-predator behavior is controlled by many loci, and longer or shorter duration of death-feigning is costly in a laboratory without predators.
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This work was supported by the Japan Society for the Promotion of Science Grant-in-Aid for Scientific Grants, KAKENHI 26291091 16K14810 and 17H05976 to T.M., and 16J0445818 to K.M.
Compliance with ethical standards
Conflict of interest
K. Matsumura and T. Miyatake declare that they have no conflict of interest.
All applicable international, national, and institutional guidelines for the care and use of animals were followed. We followed all of the Committee on Publication on Ethics (COPE) guidelines.
Research involving human participants and/or animals
This article does not contain any studies with human participants performed by any of the authors.
Boake CRB (1994) Quantitative genetic studies of behavioral evolution. University of Chicago Press, ChicagoGoogle Scholar
Brodin T, Johansson F (2004) Conflicting selection pressures on the growth/predation-risk trade-off in a damselfly. Ecology 85:2927–2932CrossRefGoogle Scholar
Bult A, Lynch CB (1996) Multiple selection responses in house mice bidirectionally selected for thermoregulatory nest-building behavior: crosses of replicate lines. Behav Genet 26:439–446CrossRefPubMedGoogle Scholar
Cunningham DL, Siegel PB (1978) Response to bidirectional and reverse selection for mating behavior in Japanese quail Coturnix coturnix japonica. Behav Genet 8:387–397CrossRefPubMedGoogle Scholar
Dawson PS (1964) Age at sexual maturity in female flour beetles, Tribolium castaneum and T. confusum. Ann Entomol Soc Am 57:1–3CrossRefGoogle Scholar
Hill WG, Caballero A (1992) Artificial selection experiments. Annu Rev Ecol Syst 23:287–310CrossRefGoogle Scholar
Kiyotake H, Matsumoto H, Nakayama S, Sakai M, Miyatake T, Ryuda M, Hayakawa Y (2013) Gain of long tonic immobility behavioral trait causes the red flour beetle to reduce anti-stress capacity. J Insc Physiol 60:92–97CrossRefGoogle 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 34:97–105CrossRefPubMedGoogle Scholar
Miyatake T (2001) Diurnal periodicity of death-feigning in Cylas formicarius (Coleoptera: Brentidae). J Insect Behav 14:421–432CrossRefGoogle 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 271:2293–2296CrossRefGoogle 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 75:113–121CrossRefGoogle Scholar
Nakayama S, Miyatake T (2009) Positive genetic correlations between life-history traits and death-feigning behavior in adzuki bean beetle (Callosobruchus chinensis). Evol Ecol 23:711–722CrossRefGoogle Scholar
Nakayama S, Miyatake T (2010) A behavioral syndrome in the adzuki bean beetle: genetic correlation among death-feigning, activity, and mating behavior. Ethology 116:108–112CrossRefGoogle Scholar
Ödeen A, Florin A-B (2000) Effective population size may limit the power of laboratory experiments to demonstrate sympatric and parapatric speciation. Proc R Soc B 267:601–606CrossRefPubMedPubMedCentralGoogle Scholar
Ohno T, Miyatake T (2007) Drop or fly? Negative genetic correlation between death-feigning intensity and flying ability as alternative anti-predator strategies. Proc R Soc B 274:555–560CrossRefPubMedGoogle Scholar
Phillips TJ, Shen EH, McKinnon CS, Burkhart-Kasch S, Lessov CN, Palmer AA (2002) Forward, relaxed, and reverse selection for reduced and enhanced sensitivity to ethanol’s locomotor stimulant effects in mice. Alcohol Clin Exp Res 26:593–602PubMedGoogle Scholar
Ritchie MG, Butlin RK (2014) The genetics of insect mating systems. In: Shuker DM, Simmons LW (eds) The evolution of insect mating systems. Oxford University Press, Oxford, pp 59–77CrossRefGoogle Scholar
Roberts RC (1966) The limits to artificial selection for body weight in the mouse. II. The genetic nature of the limits. Genet Res 8:361–375CrossRefPubMedGoogle Scholar
Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals, and mimicry. Oxford University Press, OxfordCrossRefGoogle Scholar
SAS Institute Inc (2015) JMP 12.2.0. SAS Institute Inc., CaryGoogle Scholar
Sokoloff A (1974) The Biology of Tribolium with special emphasis on genetic aspects. Oxford University Press, OxfordGoogle Scholar
Suzuki T, Nakakita H (1991) Tribolium castaneum (HERBEST), T. confusum J. du V., T. freemani HINTON. In: Yushima K, Kamano S, Tamaki Y (eds) Rearing methods of insects. Nihon Shokubutsu-Boueki Kyokai, Tokyo, pp 251–254 (In Japanese)Google Scholar
Van Oers K, Drent PJ, de Goede P, van Noordwijk AJ (2003) Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities. Proc R Soc B 271:65–73CrossRefGoogle Scholar
Wund MA, Baker JA, Golub JL, Foster SA (2015) The evolution of antipredator behaviour following relaxed and reversed selection in Alaskan threespine stickleback fish. Anim Behav 106:181–189CrossRefPubMedPubMedCentralGoogle Scholar
Yoo BH (1980) Long-term selection for a quantitative character in large replicate populations of Drosophila melanogaster. I. Response to selection. Genet Res 35:1–17CrossRefGoogle Scholar