Takahisa Miyatake

Is death-feigning adaptive? Heritable variation in fitness difference of death-feigning behaviour

The adaptation of death–feigning (thanatosis), a subject that has been overlooked in evolutionary biology, was inferred in a model prey–and–predator system. We studied phenotypic variation among individuals, fitness differences, and the inheritance of death–feigning behaviour in the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). Two–way artificial selections for the duration of death–feigning, over 10 generations, showed a clear direct response in the trait and a correlated response in the frequency of death–feigning, thus indicating variation and inheritance of death–feigning behaviour. A comparison of the two selected strains with divergent frequencies of death–feigning showed a significant difference in the fitness for survival when a model predator, a female Adanson jumper spider, Hasarius adansoni Audouin (Araneomophae: Salticidae), was presented to the beetles. The frequency of predation was lower among beetles from strains selected for long–duration than among those for short–duration death–feigning. The results indicate the possibility of the evolution of death–feigning under natural selection.

Intralocus sexual conflict unresolved by sex-limited trait expression.

Sexually antagonistic selection generates intralocus sexual conflict, an evolutionary tug-of-war between males and females over optimal trait values [1-4]. Although the potential for this conflict is universal, the evolutionary importance of intralocus conflict is controversial because conflicts are typically thought to be resolvable through the evolution of sex-specific trait development [1-8]. However, whether sex-specific trait expression always resolves intralocus conflict has not been established. We assessed this with beetle populations subjected to bidirectional selection on an exaggerated sexually selected trait, the mandible. Mandibles are only ever developed in males for use in male-male combat, and larger mandibles increase male fitness (fighting [9, 10] and mating success, as we show here). We find that females from populations selected for larger male mandibles have lower fitness, whereas females in small-mandible populations have highest fitness, even though females never develop exaggerated mandibles. This is because mandible development changes genetically correlated characters, resulting in a negative intersexual fitness correlation across these populations, which is the unmistakable signature of intralocus sexual conflict [1]. Our results show that sex-limited trait development need not resolve intralocus sexual conflict, because traits are rarely, if ever, genetically independent of other characters [11]. Hence, intralocus conflict resolution is not as easy as currently thought.

Costs of mating and egg production in female Callosobruchus chinensis

Costs of reproduction include the costs of mating and egg production. Specific techniques such as irradiation or genetic mutation have been used to divide the expense into costs of mating and egg production in previous studies. We tried to divide the costs in the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae), which needs some kinds of bean as an oviposition substrate. Mated females that were not allowed to lay eggs had a shorter life span than virgin females, but they had a longer life span than mated females that were allowed to lay eggs. The results showed two independent significant costs, mating and egg production, on the life span in C. chinensis. Costs of mating, however, include the costs of sexual harassment by males and copulation itself, and we need further studies to divide the costs. The present method for dividing the cost of reproduction into costs of mating and egg production can be applied to a broad taxonomic range of insect species, and thus it will be a useful model system for inter-specific comparisons of costs of mating and egg production.

The period gene and allochronic reproductive isolation in Bactrocera cucurbitae

Clock genes that pleiotropically control circadian rhythm and the time of mating may cause allochronic reproductive isolation in the melon fly Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Flies with a shorter circadian period (ca. 22 h of locomotor activity rhythm) mated 5 h earlier in the day than those with a longer circadian period (ca. 30 h). Mate–choice tests demonstrated significant pre–mating isolation between populations with short and long circadian periods. Pre–mating isolation did not occur when the mating time was synchronized between the two populations by photoperiodic controls, indicating that reproductive isolation is due to variations in the time of mating and not any unidentified ethological difference between the two populations. We cloned the period (per) gene of B. cucurbitae that is homologous to the per gene in Drosophila. The relative level of per mRNA in the melon fly exhibited a robust daily fluctuation under light : dark conditions. The fluctuation of per expression under dark : dark conditions is closely correlated to the locomotor rhythm in B. cucurbitae. These results suggest that clock genes can cause reproductive isolation via the pleiotropic effect as a change of mating time.

Correlated Responses to Selection for Developmental Period in Bactrocera cucurbitae (Diptera: Tephritidae): Time of Mating and Daily Activity Rhythms

Comparisons of “time of mating” (the time copulation begins) between lines selected for short and long developmental periods have been made in the melon fly, Bactrocera cucurbitae. These comparisons showed that longer developmental periods were associated with later initiation of mating. Crosses were also made between selected lines to ascertain the genetic basis of developmental period and time of mating. Comparisons of daily activity rhythms for four types of behavior (locomotion, preening, feeding, and wing vibration) between the selected lines showed the following; (1) locomotion and preening occurred in daytime for the short developmental period lines, versus mainly at night for the long developmental period lines; (2) feeding behavior occurred in daytime for both the short and the long developmental period lines; and (3) wing vibration, a component of courtship behavior of males, occurred at dusk for the short developmental period lines and at night for the long developmental period lines.

GENETIC CHANGES OF LIFE HISTORY AND BEHAVIORAL TRAITS DURING MASS-REARING IN THE MELON FLY, BACTROCERA CUCURBITAE (DIPTERA : TEPHRITIDAE)

Quantitative genetic studies for life history and behavioral traits are important in quality control for insect mass-rearing programs. Firstly, a brief history of quality control in mass-reared insects is described. Next, the differentiation of many traits of wild and mass-reared melon flies,Bactrocera cucurbitae, in Okinawa is reviewed, and the factors which have caused variation in these traits are considered. As artificial selection pressures are thought to be more important than inbreeding depression and genetic drift in the mass-reared strain of the Okinawan melon fly, two artificial selection experiments were conducted to evaluate genetic variations and genetic correlations among life history and behavioral traits. These are divergent selections for age at reproduction and for developmental period. The genetic relationship among 5 traits, i.e. longevity, age at reproduction, developmental period, circadian period, and time of mating was clarified and discussed in relation to genetic changes of traits during the mass-rearing. The results suggest that the genetic trade-off relationships between traits should be taken into account in mass-rearing programs.

Heritable variation in polyandry in Callosobruchus chinensis

The evolution of polyandry remains controversial. Various hypotheses that account for its evolution assume heritable variation in polyandry. We compared the frequency of female remating in 10 strains of the adzuki bean beetle, Callosobruchus chinensis, then made crosses between populations of high and low remating frequencies to investigate the mode of inheritance of polyandry. We found significant heritable variation in polyandry between the strains. Lower levels of polyandry were found in populations derived from long-term laboratory cultures than in those from recently established ones, suggesting that a selection pressure favoured monandry in the laboratory cultures. F1 offspring from reciprocal crosses between strains with high and low frequencies of female remating had frequencies similar to that of the strain with a high remating frequency, suggesting that polyandry is inherited with dominance in C. chinensis, unlike any other species reported to date. This study indicates that polyandry can evolve in response to selection in C. chinensis.

Drop or fly? Negative genetic correlation between death-feigning intensity and flying ability as alternative anti-predator strategies.

A prey animal may have the alternative of flying away or feigning death when it encounters predators. These alternatives have a genetic base as anti-predator strategies in the adzuki bean beetle, Callosobruchus chinensis. A negative genetic correlation between death-feigning intensity and flying ability was found in C. chinensis, i.e. lower flying ability is genetically connected to escaping by dropping from a perch and then feigning death, whereas higher flying ability does not correspond to death-feigning behaviour. Two bidirectional artificial selections for death-feigning duration and flying ability were conducted independently in C. chinensis. The strains selected for shorter (longer) duration of death-feigning had higher (lower) flying ability, while the strains selected for lower (higher) flying ability showed longer (shorter) duration of death-feigning. When the two traits were compared in 21 populations of C. chinensis derived from different geographical regions, a significant negative correlation was found between death-feigning intensity and flying ability. Based on these results, the choice between alternative escaping behaviours in animals is discussed from two points of view: phenotypic plasticity, an individual with two tactics; and pleiotropic genetic correlation, different individuals with opposite strategies.

Genetic correlations between life-history and behavioral traits can cause reproductive isolation

Reproductive isolation may often evolve as an indirect (pleiotropic) consequence of populations adapting to different environments or habitats. For example, niches that are temporally or seasonally offset can select for organisms with different developmental characteristics. These developmental differences can inadvertently cause reproductive isolation by a variety of means including shifts in mating activity patterns. Here, we show a genetic correlation between a life‐history trait (developmental period) and a behavioral trait (time of mating) that causes significant premating isolation in the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae). Fly lines selected for short and long developmental periods differ in their preferred times of mating during the evening. This difference translates into significant prezygotic isolation, as measured by mate choice tests. If the time of mating between two populations differed more than one hour, the isolation index was significantly higher than zero. These indicate that premating isolation can be established if the developmental period is divergently selected for. If such genetic correlations are ubiquitous in many organisms, multifarious divergent selection for life‐history traits would often accelerate the evolution of reproductive isolation. We speculate that reproductive isolation may have been evolved via genetic correlations among time‐related traits, for example, developmental period and time of mating, as in other organisms.

Dispersal and ejaculatory strategies associated with exaggeration of weapon in an armed beetle

Weapons used in male fighting can be costly to males and are often reported to trade off with other characters such as wings or spermatogenic investment. This study investigated whether increased investment into weapons can generate evolutionary changes in mating strategy for armed males. Male flour beetles, Gnatocerus cornutus, have enlarged mandibles that are used in male–male competition. We subjected these weapons to 12 generations of bidirectional selection and found trade-offs between weapons and two other male characters: wing and testis size. In addition, probably as a consequence of the observed changes in investment, dispersal ability and ejaculatory volume differ significantly between the lines. This indicates that the exaggeration of a weapon can be associated with dispersal and ejaculatory strategies. Thus, altered investment into weapons can lead to correlated changes in life-history traits.