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Evolutionarily conserved insulin/insulin-like growth factor (IGF) signaling (IIS) has been identified as a major physiological mechanism underlying the nutrient-dependent regulation of sexually selected weapon growth in animals. However, the molecular mechanisms that couple nutritional state with weapon growth remain largely unknown. Here, we show that one specific subtype of insulin-like peptide (ILP) responds to nutrient status and thereby regulates weapon size in the broad-horned flour beetle Gnatocerus cornutus. By using transcriptome information, we identified five G. cornutus ILP (GcorILP1-5) and two G. cornutus insulin-like receptor (GcorInR1, -2) genes in the G. cornutus genome. RNA interference (RNAi)-mediated gene silencing revealed that a certain subtype of ILP, GcorILP2, specifically regulated weapon size. Importantly, GcorILP2 was highly and specifically expressed in the fat body in a condition-dependent manner. We further found that GcorInR1 and GcorInR2 are functionally redundant but that the latter is partially specialized for regulating weapon growth. These results strongly suggest that GcorILP2 is an important component of the developmental mechanism that couples nutritional state to weapon growth in G. cornutus. We propose that the duplication and subsequent diversification of IIS genes played a pivotal role in the evolution of the complex growth regulation of secondary sexual traits.

Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-specific predation on an exaggerated sexually selected male trait (the mandibles), while also testing for effects on female lifetime reproductive success. We find that populations subjected to male-specific predation evolve smaller sexually selected mandibles and this indirectly increases female fitness, seemingly through intersexual genetic correlations we document. Predation solely on females has no effects. Our findings support fundamental theory, but also reveal unforseen outcomes—the indirect effect on females—when natural selection targets sex-limited sexually selected characters. Natural and sexual selection can be in opposition favouring different trait sizes, but disentangling these processes empirically is difficult. Here Okada et al. show that predation on males shifts the balance of selection in experimentally evolving beetle populations, disfavoring a sexually-selected male trait but increasing female fitness.

In theory, a male should change the allocation of fighting and mating efforts in relation to his age. Thus, the consequences of sexual selection may be complicated by changes in the male resource allocation due to aging. However, previous studies have focused on changes in female mate choice and male-male competition with aging separately, and the impact of aging on the relationship between mate choice and male competition is unknown. Here, we examined how male competitiveness and attractiveness and their relationship changes over male lifespan in Gnatocerus cornutus. In this species, males perform courtship displays and fight rival males for mates. Older males are more competitive in male fighting and aggressive toward females than younger males. The aggression is also directed toward females. Almost all older males who attacked a female failed to copulate, while younger males never attacked the females. As a result, copulation success decreased with age. When an older male did not mistake a female for a male, he exhibited more frequent courtship. However, mating with older males imposed direct costs on females in terms of both fecundity and lifespan, with no offsetting indirect benefits for her offspring. The courtship behavior of older males does not supply females with cues for mate-choice benefits but are used to coerce females into mating. Our results suggest that male–male competition constrains female preference for older males. Thus, female choice and male–male competition may not be reinforcing in older G. cornutus males.

For understanding the evolutionary mechanism of sexually selected exaggerated traits, it is essential to uncover its molecular basis. By using broad-horned flour beetle that has male-specific exaggerated structures (mandibular horn, head horn and gena enlargement), we investigated the transcriptomic and functional characters of sex-biased genes. Comparative transcriptome of male vs. female prepupal heads elucidated 673 sex-biased genes. Counter-intuitively, majority of them were female-biased (584 genes), and GO enrichment analysis showed cell-adhesion molecules were frequently female-biased. This pattern motivated us to hypothesize that female-biased transcripts (i.e. the transcripts diminished in males) may play a role in outgrowth formation. Potentially, female-biased genes may act as suppressors of weapon structure. In order to test the functionality of female-biased genes, we performed RNAi-mediated functional screening for top 20 female-biased genes and 3 genes in the most enriched GO term (cell-cell adhesion, fat1/2/3 , fat4 and dachsous ). Knockdown of one transcription factor, zinc finger protein 608 (zfp608) resulted in the formation of male-like gena in females, supporting the outgrowth suppression function of this gene. Similarly, knockdown of fat4 induced rudimental, abnormal mandibular horn in female. fat1/2/3 RNAi , fat4 RNAi and dachsous RNAi males exhibited thick and/or short mandibular horns and legs. These cell adhesion molecules are known to regulate tissue growth direction and known to be involved in the weapon formation in Scarabaeoidea beetles. Functional evidence in phylogenetically distant broad-horned flour beetle suggest that cell adhesion genes are repeatedly deployed in the acquisition of outgrowth. In conclusion, this study clarified the overlooked functions of female-biased genes in weapon development.

The genus Monomorium is an important phylogenetic group, notable for its taxonomic complexity and the presence of several well-known tramp species. In this study, we present a description of M. brachypterum sp. nov. from southern Japan along with an updated key to the Japanese species of the genus based on the worker caste. Molecular phylogenetic analysis using 13 protein-coding genes of the mitochondrial genome indicated that this new species is most closely related to M. intrudens . Within their overlapping distributions, analyses based on partial sequences of the mitochondrial COI gene showed that the two species are phylogenetically distinct. The queens of M. brachypterum are distinguished from those of M. intrudens by degenerated wings, suggesting contrasting dispersal strategies between the two sister species. In addition, a phylogenetic analysis performed for the Japanese Monomorium species provides support for the repeated evolution of diverse reproductive systems within this genus. The present study highlights a wide variety of evolutionary trends in the nest-level reproductive system, even among closely related species.

Nutritional conditions during early development influence the plastic expression of adult phenotypes. Among several body modules of animals, the development of sexually selected exaggerated traits exhibits striking nutrition sensitivity, resulting in positive allometry and hypervariability distinct from other traits. Using de novo RNA sequencing and comprehensive RNA interference (RNAi) for epigenetic modifying factors, we found that histone deacetylases (HDACs) and polycomb group (PcG) proteins preferentially influence the size of mandibles (exaggerated male weapon) and demonstrate nutrition- dependent hypervariability in the broad-horned flour beetle, Gnatocerus cornutus. RNAi-mediated HDAC1 knockdown (KD) in G. cornutus larvae caused specific curtailment of mandibles in adults, whereas HDAC3 KD led to hypertrophy. Notably, these KDs conferred opposite effects on wing size, but little effect on the size of the core body and genital modules. PcG RNAi also reduced adult mandible size. These results suggest that the plastic development of exaggerated traits is controlled in a module-specific manner by HDACs.

Winning or losing contests can impact subsequent competitive behaviour and the duration of these effects can be prolonged. While it is clear effects depend on social and developmental environments, the extent to which they are heritable, and hence evolvable, is less clear and remains untested. Furthermore, theory predicts that winner and loser effects should evolve independently of actual fighting ability, but again tests of this prediction are limited. Here we used artificial selection on replicated beetle populations to show that the duration of loser effects can evolve, with a realized heritability of about 17%. We also find that naive fighting ability does not co-evolve with reductions in the duration of the loser effect. We discuss the implications of these findings and how they corroborate theoretical predictions.

How individual organisms whose behavior is potentially driven by selfish interests cooperate to form a society is a central question in evolutionary biology. Worker reproduction and its suppression in eusocial insects provide an illuminating model of such a conflict resolution. Although many theoretical and empirical studies focus on the nature and evolutionary consequences of this reproductive conflict, little is known about its physiological underpinnings. Here, we hypothesized that the dopaminergic system, which has a gonadotropic function in eusocial Hymenoptera, is controlled by social suppression via the queen presence signal and the worker-worker dominance interactions. In Diacamma sp. from Japan, the queen presence signal is transferred to workers by direct contact, and workerworker dominance interaction occurs commonly in large colonies, even when a queen is present. Using the ant Diacamma sp., we showed that the aggressive interactions among workers suppressed brain dopamine levels of the workers. Moreover, our data suggest that the queen presence signal transmitted by direct contact suppresses the brain dopamine level and the transcription of dopamine synthetic enzyme (ddc) of workers. Our data provide clear empirical evidence that worker brain dopamine is suppressed by both social stimuli directed from dominant workers and the queen.

The morphological diversity of insects is one of the most striking phenomena in biology. Evolutionary modifications to the relative sizes of body parts, including the evolution of traits with exaggerated proportions, are responsible for a vast range of body forms. Remarkable examples of an insect trait with exaggerated proportions are the mandibular weapons of stag beetles. Male stag beetles possess extremely enlarged mandibles which they use in combat with rival males over females. As with other sexually selected traits, stag beetle mandibles vary widely in size among males, and this variable growth results from differential larval nutrition. However, the mechanisms responsible for coupling nutrition with growth of stag beetle mandibles (or indeed any insect structure) remain largely unknown. Here, we demonstrate that during the development of male stag beetles (Cyclommatus metallifer), juvenile hormone (JH) titers are correlated with the extreme growth of an exaggerated weapon of sexual selection. We then investigate the putative role of JH in the development of the nutritionally-dependent, phenotypically plastic mandibles, by increasing hemolymph titers of JH with application of the JH analog fenoxycarb during larval and prepupal developmental periods. Increased JH signaling during the early prepupal period increased the proportional size of body parts, and this was especially pronounced in male mandibles, enhancing the exaggerated size of this trait. The direction of this response is consistent with the measured JH titers during this same period. Combined, our results support a role for JH in the nutrition-dependent regulation of extreme mandible growth in this species. In addition, they illuminate mechanisms underlying the evolution of trait proportion, the most salient feature of the evolutionary diversification of the insects.

Females prefer male traits that are associated with direct and/or indirect benefits to themselves. Male-male competition also drives evolution of male traits that represent competitive ability. Because female choice and male-male competition rarely act independently, exploring how these two mechanisms interact is necessary for integrative understanding of the evolution of sexually selected traits. Here, we focused on direct and indirect benefits to females from male attractiveness, courtship, and weapon characters in the armed bug Riptortus pedestris. The males use their hind legs to fight other males over territory and perform courtship displays for successful copulation. Females of R. pedestris receive no direct benefit from mating with attractive males. On the other hand, we found that male attractiveness, courtship rate, and weapon size were significantly heritable and that male attractiveness had positive genetic covariances with both courtship rate and weapon traits. Thus, females obtain indirect benefits from mating with attractive males by producing sons with high courtship success rates and high competitive ability. Moreover, it is evident that courtship rate and hind leg length act as evaluative cues of female choice. Therefore, female mate choice and male-male competition may facilitate each other in R. pedestris. This is consistent with current basic concepts of sexual selection.