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 (2016) 34:97–105 DOI 10.1007/s10164-015-0452-6 ARTICLE Correlated responses in death-feigning behavior, activity, and brain biogenic amine expression in red flour beetle Tribolium castaneum strains selected for walking distance Kentarou Matsumura1 • Ken Sasaki2 • Takahisa Miyatake1 Received: 12 July 2015 / Accepted: 14 November 2015 / Published online: 8 December 2015 Ó Japan Ethological Society and Springer Japan 2015 Abstract Dispersal ability may influence antipredator and mating strategies. A previous study showed a tradeoff between predation avoidance and mating success in strains of the red flour beetle Tribolium castaneum selected for walking distance. Specifically, beetles derived from strains selected for longer walking distance suffered higher predation pressure and had higher male mating success than their counterparts derived from strains selected for shorter walking distance. In the study reported here, we compared the locomotor activity, biogenic amine expression in the brain, and death-feigning behavior of the red flour beetle strains selected for walking distance. The results indicated that individuals genetically predisposed to longer walking distance had higher locomotor activity and lower intensity of deathfeigning behavior than those genetically predisposed to shorter walking distance. However, no significant differences were found in the expression of biogenic amines in the brain among strains selected for walking distance, although the level of dopamine in the brain differed from that of the strains divergently selected for duration of death-feigning behavior. The relationships between walking speed, activity, death-feigning behavior, and brain biogenic amines in T. castaneum are discussed. & Takahisa Miyatake 1 Laboratory of Evolutionary Ecology, Graduate School of Environmental and Life Science, Okayama University, Tsushima-Naka, Okayama City, Okayama, Japan 2 Department of Bioresource Science, Tamagawa University, Machida, Tokyo, Japan Keywords Artificial selection
Biogenic amine
Deathfeigning behavior
Dispersal ability
Genetic correlation
Locomotor activity Introduction The dispersal of animals is an essential feature of survival (Clobert et al. 2009; Bonte et al. 2012). In many animals, dispersal ability is closely related to a suite of other traits, referred to collectively as the dispersal syndrome (Frazzetta 1975; Clobert et al. 2009). For example, in some insect species with wing size dimorphism, individuals with longer wings and greater flight ability show lower reproductive success because more resources are invested in wing size than in ovary size. In contrast, short-winged individuals invest their resources in increasing ovary size, resulting in an increase in reproductive success (Roff and Fairbairn 2007). Both dispersal and non-dispersal types are frequently found in natural populations due to a resource allocation trade-off, and this can help to explain the maintenance of variation in dispersal ability within a population (reviewed in Roff and Fairbairn 2007; Bonte et al. 2012). Predation is a major selection pressure in shaping prey behavior (Lima and Dill 1990), and because natural selection favors individuals that successfully avoid predators, evolution should favor the adaptive antipredator behavior of prey. Dispersal often increases the risk of predation due to the increased frequency of encounter with predators (e.g., Aukema and Raffa 2004; Korb and Linsenmair 2002; Srygley 2004; Matsumura and Miyatake 2015), which suggests that prey should evolve antipredator strategies that are dependent on its own dispersal ability. When a prey perceives danger, it often uses two alternative tactics to survive—flight or fight, or running or death-feigning (e.g., 123 98 Martin and Lopez 2000; Lehtiniemi 2005; Wasson and Lyon 2005; Ohno and Miyatake 2007). Individuals with higher dispersal ability may adopt a running escape tactic to survive when they encounter a predator because they have a higher ability to move and thus avoid the predator. In contrast, individuals with lower dispersal ability may adopt a death-feigning tactic to survive when they encounter a predator due to their lower ability to move. Death-feigning behavior (sometimes referred to as thanatosis) is considered to be a defense mechanism against predators that has evolved in many animals, and its adaptive significance has been reported in many studies (e.g. Edmunds 1974; Miyatake et al. 2004; Ruxton et al. 2004). Miyatake et al. (2004) carried out artificial selection for duration of death-feigning in the red flour beetle Tribolium castaneum and reported that individuals genetically predisposed for longer duration of death-feigning (LD strain) were more successful in surviving an encounter with the jumping spider Hasarius adansoni than their counterparts with a genetic predisposition for shorter duration of death-feigning (SD strain). These authors also observed that the walking distance of beetles derived from LD strains was shorter than that of SD strains and that the expression of brain dopamine in LD strains was significantly lower than that in SD strains (Miyatake et al. 2008a). Many insect behaviors, including aggressiveness and activity, are controlled by biologically active substances, including biogenic amines (e.g., Evans 1980; Bicker and Menzel 1989; Stevenson et al. 2000). In the sand cricket Gryllus firmus, dispersal ability is controlled in part by juvenile hormone, suggesting that in this species dispersal and physiological mechanism may be closely related to each other (reviewed in Roff and Fairbairn 2007). However, few studies to date have investigated the relationship between dispersal ability and biogenic amines (e.g., Miyatake et al. 2008a). Matsumura and Miyatake (2015) recently performed artificial selection for walking distance, i.e., an indicator of dispersal ability, in the red flour beetle T. castaneum and established strains with longer (LW strain) or shorter (SW strain) walking distances. They also compared the frequency of predation by the assassin bug Amphibolus venator, reporting that LW strain beetles suffered higher predation risk than did SW strain beetles (Matsumura and Miyatake 2015). If dispersal ability is genetically correlated with antipredator strategies, two-way artificial selection for dispersal ability should show correlated responses in the expression of biogenic amines and death-feigning behavior. In the study reported here, we compared deathfeigning and expression of biogenic amines of strains selected for longer or shorter walking distance (LW vs. SW). We also examined the locomotor activity of these two selected strains to test whether walking distance correlates with locomotor activity. 123 J Ethol (2016) 34:97–105 Materials and methods Insect The red flour beetles (Tribolium castaneum) used in this study have been maintained in laboratories for more than 30 years. The beetles were reared (...truncated)