Tomohiro Harano

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.

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.

Direct effects of polyandry on female fitness in Callosobruchus chinensis

In many insect species with high levels of polyandry, females benefit directly from remating. The effects of remating on female fitness have generally been examined by comparing the fitness of females in multiple-mating and single-mating treatments. In this standard approach, females in the multiple-mating group that refuse to remate are often excluded from the analysis. We investigated the effects of remating in the adzuki bean beetle, Callosobruchus chinensis, a species with low levels of polyandry. Females that refused to remate when given an opportunity to do so were less fecund and shorter lived than females that accepted remating. In this case, excluding females that refuse to remate from the multiple-mating treatment biases the composition of the two treatment populations, and is thus problematic. When we included such females, we found no difference in fecundity, fertility and longevity between females given an opportunity to remate and those that were not. In addition, when we compared females that were allowed to complete remating naturally and those whose remating was interrupted before sperm transfer we found significantly negative effects of female remating on fecundity, suggesting that remating reduces the fitness of polyandrous females in C. chinensis, which is inconsistent with many studies on polyandrous species.

Interpopulation variation in female remating is attributable to female and male effects in Callosobruchus chinensis

The evolution of female multiple mating is best understood by consideration of male and female reproductive perspectives. Females should usually be selected to remate at their optimum frequencies whereas males should be selected to manipulate female remating to their advantage. Female remating behavior may therefore be changed by variation of male and female traits. In this study, our objective was to separate the effects of female and male strains on female remating for the adzuki bean beetle, Callosobruchus chinensis, for which there is interstrain variation in female remating frequency. We found that interstrain variation in female remating is primarily attributable to female traits, suggesting genetic variation in female receptivity to remating in C. chinensis. Some interstrain variation in female remating propensity was attributable to an interaction between female and male strains, however, with the males of some strains being good at inducing nonreceptivity in females from one high-remating strain whereas others were good at inducing copulation in nonvirgin females from the high-remating strain. There is, therefore, interstrain variation in male ability to deter females from remating and in male ability to mate successfully with nonvirgin females. These results suggest that mating traits have evolved along different trajectories in different strains of C. chinensis.

Intralocus sexual conflict and offspring sex ratio.

Males and females frequently have different fitness optima for shared traits, and as a result, genotypes that are high fitness as males are low fitness as females, and vice versa. When this occurs, biasing of offspring sex-ratio to reduce the production of the lower-fitness sex would be advantageous, so that for example, broods produced by high-fitness females should contain fewer sons. We tested for offspring sex-ratio biasing consistent with these predictions in broad-horned flour beetles. We found that in both wild-type beetles and populations subject to artificial selection for high- and low-fitness males, offspring sex ratios were biased in the predicted direction: low-fitness females produced an excess of sons, whereas high-fitness females produced an excess of daughters. Thus, these beetles are able to adaptively bias sex ratio and recoup indirect fitness benefits of mate choice.

Negative relationship between ambient temperature and death-feigning intensity in adult Callosobruchus maculatus and Callosobruchus chinensis

Abstract Although the effects of temperature on insect behaviours are studied frequently, few studies report on the relationship between temperature and anti‐predator behaviours. A negative relationship between ambient temperature and the intensity of death‐feigning is found in adults of two seed beetle species, Callosobruchus maculatus (F.) and C. chinensis (L.) (Coleoptera: Bruchidae). Two traits representing the intensity of immobility, the frequency and the duration of death‐feigning, are measured at different temperatures. Almost all adults feign death at 15 °C, but the frequency of death‐feigning decreases at higher temperatures in C. maculatus, whereas all C. chinensis adults show this behaviour at 15 and 20 °C and almost all show it at 25 °C, but the frequency of death‐feigning decreases at 30 and 35 °C. The difference between the two species might be due to the specific strain of each species used in the experiment. The duration of death‐feigning is correlated negatively with the increase in ambient temperature in both species. The frequency at which adults feigned death is higher in females than in males in both species, but the duration of death‐feigning is higher in females than in males only in C. maculatus. The relationships between temperature and death‐feigning behaviours are discussed from physiological and ecological viewpoints.

Inbreeding depression in development, survival, and reproduction in the adzuki bean beetle (Callosobruchus chinensis)

Inbreeding depression of an aspect of fitness is observed in many insects, but the traits that are of importance for inbreeding depression of fitness remain poorly understood. Here the magnitude of inbreeding depression of fitness-related traits in the development and adult stages was measured in a captive population of the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). Beetles produced by full-sib matings had 8% lower survival in the development stage than did beetles produced by unrelated matings. Although inbred and outbred offspring did not differ in body size after emergence, inbred offspring took 2–3% longer to develop to emergence. This indicates inbreeding depression of growth rate. At the adult stage, inbreeding had no significant effect on longevity, however lifetime offspring production was reduced by 11%. Thus, the magnitude of inbreeding depression was relatively large for offspring production. This suggests inbreeding depression of fitness manifests, to a particularly significant extent, in reduced productivity. This study shows the C. chinensis population, which has been in captivity for more than 100 generations, harbors genetic loads.

No genetic correlation between the sexes in mating frequency in the bean beetle, Callosobruchus chinensis

Female multiple mating, which is common in animals, may have evolved not in response to fitness advantages to females but as a genetic corollary to selection on males to mate frequently. This nonadaptive hypothesis assumes a genetic correlation between females and males in mating frequency, which has received a few empirical investigations. We tested this hypothesis by observing the correlated response in male mating frequency in the adzuki bean beetle, Callosobruchus chinensis to artificial selection on female propensity to remate. Compared to control females, females from lines selected for increased or decreased female propensity to remate had, respectively, higher or lower mating frequency measured by the number of mating within a given period. This indicates that female receptivity to remating is genetically correlated with female mating frequency, and thus the artificial selection for female propensity to remate influenced female mating frequency. In contrast, males from the selected lines that diverged in female mating frequency did not vary significantly in their mating frequency. These results indicate that there is no genetic correlation between the sexes in mating frequency in C. chinensis. This study shows that the reason why females in C. chinensis remate despite suffering fitness costs cannot be explained by indirect selection resulting from selection on males to mate multiple times.

Independence of genetic variation between circadian rhythm and development time in the seed beetle, Callosobruchus chinensis

A positive genetic correlation between periods of circadian rhythm and developmental time supports the hypothesis that circadian clocks are implicated in the timing of development. Empirical evidence for this genetic correlation in insects has been documented in two fly species. In contrast, here we show that there is no evidence of genetic correlation between circadian rhythm and development time in the adzuki bean beetle, Callosobruchus chinensis. This species has variation that is explained by a major gene in the expression and period length of circadian rhythm between strains. In this study, we found genetic variation in development time between the strains. The development time was not covaried with either the incidence or the period length of circadian rhythm among the strains. Crosses between strains suggest that development time is controlled by a polygene. In the F(2) individuals from the crosses, the circadian rhythm is attributable to allelic variation in the major gene. Across the F(2) individuals, development time was not correlated with either the expression or the period length of circadian rhythm. Thus, we found no effects of major genes responsible for variation in the circadian rhythm on development time in C. chinensis. Our findings collectively give no support to the hypothesis that the circadian clock is involved in the regulation of development time in this species.

Bidirectional selection for female propensity to remate in the bean beetle, Callosobruchus chinensis.

The evolution of female multiple mating, or polyandry, is difficult to comprehend and thus has been the subject of a large number of studies. However, there is only a little evidence for genetic variation in polyandry, although the evolution of a trait via selection requires genetic variation that enables the trait to respond to selection. We carried out artificial selection for increased and decreased female propensity to remate as a measure of polyandry to investigate whether this trait has a genetic component that can respond to selection in the adzuki bean beetle, Callosobruchus chinensis. Artificial selection produced responses in both directions and divergence between the selection lines in the female propensity to remate. Although the experimental design adopted in this study selected jointly for female receptivity to remating, which is a trait of females, and male ability to inhibit female remating—both of which are associated with female propensity to remate—the observed response to selection was attributable only to the female receptivity to remating. This study indicates that the female receptivity to remating has significant additive genetic variation and can evolve according to whether remating is advantageous or disadvantageous to females in C. chinensis.