Female-limited responses in remating rate and mating duration in the experimental evolution of a beetle Callosobruchus chinensis.

Mating rate optima often differ between the sexes: males may increase their fitness by multiple mating, but for females multiple mating confers little benefit and can often be costly (especially in taxa without nuptial gifts or mala parental care). Sexually antagonistic evolution is thus expected in traits related to mating rates under sexual selection. This prediction has been tested by multiple studies that applied experimental evolution technique, which is a powerful tool to directly examine the evolutionary consequences of selection. Yet, the results so far only partly support the prediction. Here, we provide another example of experimental evolution of sexual selection, by applying it for the first time to the mating behaviour of a seed beetle Callsorobruchus chinensis. We found a lower remating rate in polygamy-line females than in monogamy-line (i.e. no sexual selection) females after 21 generations of selection. Polygamy-line females also showed a longer duration of first mating than monogamy-line females. We found no effect of male evolutionary lines on the remating rate or first mating duration. Though not consistent with the original prediction, the current and previous studies collectively suggest that the observed female-limited responses may be a norm, which is also consistent with the conceptual advances in the last two decades of the advantages and limitations of experimental evolution technique.

Morphology of immatures of the thelytokous ant, Monomorium triviale Wheeler (Formicidae: Myrmicinae: Solenopsidini) with descriptions of the extraordinary last-instar queen larvae.

The ant genus Monomorium is one of the most species-rich but taxonomically problematic groups in the hyperdiverse subfamily Myrmicinae. An East Asian species, M. triviale Wheeler, produces both reproductive queens and sterile workers via obligate thelytokous parthenogenesis. Here, we describe the immature forms of M. triviale based on light and scanning electron microscopy observations, with a note on the striking caste dimorphism in the last larval instar. The last-instar queen larvae were easily recognized by their large size, aphaenogastroid body shape, and rows of doorknob-like tubercles on the lateral and dorsal body surface. This type of queen-specific structure has not been found in ants in general, let alone congeneric species found in Japan. In stark contrast to the queen larvae, worker larvae showed a pheidoloid body shape and a body surface similar to other ants. The worker larvae were estimated to have three instars, consistent with previously described congeners. The pupae of both castes had no cocoon, a characteristic commonly described in other Myrmicinae species. In total, the developmental period from egg to adult worker averaged 59 days under 25C. We discuss possible functions of the tubercles of queen larvae based on previous studies.

The build-up of dominance hierarchies in eusocial insects.

Reproductive division of labour is a hallmark of eusocial insects. However, its stability can often be hampered by the potential for reproduction by otherwise sterile nest-mates. Dominance hierarchy has a crucial role in some species in regulating which individuals reproduce. Compared with those in vertebrates, the dominance hierarchies in eusocial insects tend to involve many more individuals, and should require additional selective forces unique to them. Here, we provide an overview of a series of studies on dominance hierarchies in eusocial insects. Although reported from diverse eusocial taxa, dominance hierarchies have been extensively studied in paper wasps and ponerine ants. Starting from molecular physiological attributes of individuals, we describe how the emergence of dominance hierarchies can be understood as a kind of self-organizing process through individual memory and local behavioural interactions. The resulting global structures can be captured by using network analyses. Lastly, we argue the adaptive significance of dominance hierarchies from the standpoint of sterile subordinates. Kin selection, underpinned by relatedness between nest-mates, is key to the subordinates' acceptance of their positions in the hierarchies. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

The complete mitochondrial genome of a parthenogenetic ant Monomorium triviale (Hymenoptera: Formicidae).

Monomorium is one of the most species-rich yet taxonomically problematic ant genus. An East Asian species, M. triviale Wheeler, W.M., 1906, is reproduced by obligate thelytokous parthenogenesis and performs strict reproductive division of labor. We sequenced the M. triviale mitogenome using next-generation sequencing methods. The circular mitogenome of M. triviale was 16,290 bp in length, consisting of 13 protein-coding genes, two ribosomal RNA genes, 22 transfer RNAs, and a single non-coding region of 568 bp. The base composition was AT-biased (82%). Gene order rearrangements were detected and likely to be unique to the genus Monomorium. We announce the M. triviale mitogenome as additional genomic resources for elucidating phylogenetic and taxonomic problems of Monomorium and comparative genomics of parthenogenetic ant species.

Comprehensive analysis of male-free reproduction in Monomorium triviale (Formicidae: Myrmicinae).

We report comprehensive evidence for obligatory thelytokous parthenogenesis in an ant Monomorium triviale. This species is characterized by distinct queen-worker dimorphism with strict reproductive division of labor: queens produce both workers and new queens without mating, whereas workers are completely sterile. We collected 333 nests of this species from 14 localities and three laboratory-reared populations in Japan. All wild queens dissected had no sperm in their spermathecae. Laboratory observation confirmed that virgin queens produced workers without mating. Furthermore, microsatellite genotyping showed identical heterozygous genotypes between mothers and their respective daughters, suggesting an extremely low probability of sexual reproduction. Microbial analysis detected no bacterial genera that are known to induce thelytokous parthenogenesis in Hymenoptera. Finally, the lack of variation in partial sequences of mitochondrial DNA among individuals sampled from across Japan suggests recent rapid spread or selective sweep. M. triviale would be a promising model system of superorganism-like adaptation through comparative analysis with well-studied sexual congeners, including the pharaoh ant M. pharaonis.

Intraspecific Adaptation Load: A Mechanism for Species Coexistence.

Evolutionary ecological theory suggests that selection arising from interactions with conspecifics, such as sexual and kin selection, may result in evolution of intraspecific conflicts and evolutionary 'tragedy of the commons'. Here, we propose that such an evolution of conspecific conflicts may affect population dynamics in a way that enhances species coexistence. Empirical evidence and theoretical models suggest that more abundant species is more susceptible to invasion of 'selfish' individuals that increase their own reproductive success at the expense of population growth (intraspecific adaptation load). The density-dependent intraspecific adaptation load gives rise to a self-regulation mechanism at the population level, and stabilizes species coexistence at the community level by negative frequency-dependence.

Behavioral responses to colony-level properties affect disturbance resistance of red harvester ant colonies.

Self-organizing biological systems, such as colonies of social insects, are characterized by their decentralized control and flexible responses to changing environments, often likened to swarm intelligence. Although decentralized control is well known to be a product of local interactions among agents, without the need for a bird's-eye view, indirect knowledge of properties that indicate the current states of the entire system also helps each agent to respond to changes, thereby leading to a more adaptive system. In this study, we analyze the rules that govern workers' behavioral responses to colony-level properties and assess whether they contribute to adaptive flexibility in social insect colonies. We focus on task allocation among red harvester ants (Pogonomyrmex barbatus) as a model system and develop an ordinary differential equation model to describe the system of task allocation among workers. We simulate 12 scenarios specifying how workers respond to changes in the colony-level properties of colony size and nutritional state. We found that when workers decrease their contact rates in response to increasing colony size, they enable achievement of a larger colony size, similar to that of P. barbatus colonies in nature, and when workers increase their foraging levels in response to decreasing colony-wide nutritional levels, they increase resilience to environmental disturbances. These negative feedback rules governing the response to colony-level properties are consistent with previous reports on ants and honeybees.

Adaptive switch to sexually dimorphic movements by partner-seeking termites.

How should females and males move to search for partners whose exact location is unknown? Theory predicts that the answer depends on what they know about where targets can be found, raising the question of how actual animals update their mate search patterns to increase encounter probability when conditions change. Here, we show that termites adaptively alternate between sexually monomorphic and dimorphic movements during mate search. When the location of potential mates was completely unpredictable, both sexes moved in straight lines to explore widely. In contrast, when the stray partner was at least nearby, males moved while females paused. Data-based simulations confirmed that these movements increase the rate of successful encounters. The context-dependent switch of search modes is a key to enhance random encounters.

Regulatory mechanism predates the evolution of self-organizing capacity in simulated ant-like robots.

The evolution of complexity is one of the prime features of life on Earth. Although well accepted as the product of adaptation, the dynamics underlying the evolutionary build-up of complex adaptive systems remains poorly resolved. Using simulated robot swarms that exhibit ant-like group foraging with trail pheromones, we show that their self-organizing capacity paradoxically involves regulatory behavior that arises in advance. We focus on a traffic rule on their foraging trail as a regulatory trait. We allow the simulated robot swarms to evolve pheromone responsiveness and traffic rules simultaneously. In most cases, the traffic rule, initially arising as selectively neutral component behaviors, assists the group foraging system to bypass a fitness valley caused by overcrowding on the trail. Our study reveals a hitherto underappreciated role of regulatory mechanisms in the origin of complex adaptive systems, as well as highlights the importance of embodiment in the study of their evolution.

Copy if dissatisfied, innovate if not: contrasting egg-laying decision making in an insect.

The use of conspecific cues as social information in decision making is widespread among animals; but, because this social information is indirect, it is error-prone. During resource acquisition, conspecific cues also indicate the presence of competitors; therefore, decision makers are expected to utilize direct information from resources and modify their responses to social information accordingly. Here, we show that, in a non-social insect, unattractive egg-laying resources alter the behavioural response to conspecific cues from avoidance to preference, leading to resource sharing. Females of the adzuki bean beetle Callosobruchus chinensis avoid laying eggs onto beans that already have conspecific eggs. However, when we provided females with bean-sized clean glass beads with and without conspecific eggs, the females preferred to add their eggs onto the beads with eggs. The glass beads, once coated with water extracts of adzuki beans, enabled the females to behave as if they were provided with the beans: the females preferred bean-odoured glass beads to clean glass beads and they avoided the substrates with eggs. When females are provided with unattractive egg-laying substrates only, joining behaviour (i.e. copying) might be advantageous, as it takes advantage of information about positive attributes of the substrate that the focal animal might have missed. Our results suggest that given only unsatisfactory options, the benefits of copying outweigh the costs of resource competition. Our study highlights the importance of integrating multiple information sources in animal decision making.

The optimal movement patterns for mating encounters with sexually asymmetric detection ranges.

Animals have evolved various sex-specific characteristics to improve the efficiency of mating encounters. One is the sex-specific attracting signal. Signal receivers perform a combination of random search and navigation before and after signal detections. On the other hand, signal senders can also modify their movement patterns to optimize their encounter rates, which invokes a reverse side of random search problems that asks for the most efficient movement patterns of signal senders to be found by signal receivers. In this study, we focused on visual and auditory signals in particular, and quantified the efficiency of mating encounters of individual animals performing a Lévy walk, a special class of random walk, with a variety of speeds before signal detection. We found that signal senders should move more slowly and/or less diffusively than receivers to improve mating encounters. The optimal movement patterns of senders ranged from relatively slow to stationary ones depending on the density of individuals, the effective range of signals, and the ability of receivers to locate senders. By focusing on the optimal movement patterns of individuals that are often assumed to be given targets, the present study provides insights into strategies of effective attraction beyond the case of mate search.

Nature of collective decision-making by simple yes/no decision units.

The study of collective decision-making spans various fields such as brain and behavioural sciences, economics, management sciences, and artificial intelligence. Despite these interdisciplinary applications, little is known regarding how a group of simple 'yes/no' units, such as neurons in the brain, can select the best option among multiple options. One prerequisite for achieving such correct choices by the brain is correct evaluation of relative option quality, which enables a collective decision maker to efficiently choose the best option. Here, we applied a sensory discrimination mechanism using yes/no units with differential thresholds to a model for making a collective choice among multiple options. The performance corresponding to the correct choice was shown to be affected by various parameters. High performance can be achieved by tuning the threshold distribution with the options' quality distribution. The number of yes/no units allocated to each option and its variability profoundly affects performance. When this variability is large, a quorum decision becomes superior to a majority decision under some conditions. The general features of this collective decision-making by a group of simple yes/no units revealed in this study suggest that this mechanism may be useful in applications across various fields.

Radiocarbon analysis reveals expanded diet breadth associates with the invasion of a predatory ant.

Invasions are ecologically destructive and can threaten biodiversity. Trophic flexibility has been proposed as a mechanism facilitating invasion, with more flexible species better able to invade. The termite hunting needle ant Brachyponera chinensis was introduced from East Asia to the United States where it disrupts native ecosystems. We show that B. chinensis has expanded dietary breadth without shifting trophic position in its introduced range. Transect sampling of ants and termites revealed a negative correlation between the abundance of B. chinensis and the abundance of other ants in introduced populations, but this pattern was not as strong in the native range. Both termite and B. chinensis abundance were higher in the introduced range than in native range. Radiocarbon (14C) analysis revealed that B. chinensis has significantly younger 'diet age', the time lag between carbon fixation by photosynthesis and its use by the consumer, in the introduced range than in the native range, while stable isotope analyses showed no change. These results suggest that in the introduced range B. chinensis remains a termite predator but also feeds on other consumer invertebrates with younger diet ages such as herbivorous insects. Radiocarbon analysis allowed us to elucidate cryptic dietary change associated with invasion success.

Anomalous diffusion on the servosphere: A potential tool for detecting inherent organismal movement patterns.

Tracking animal movements such as walking is an essential task for understanding how and why animals move in an environment and respond to external stimuli. Different methods that implemented image analysis and a data logger such as GPS have been used in laboratory experiments and in field studies, respectively. Recently, animal movement patterns without stimuli have attracted an increasing attention in search for common innate characteristics underlying all of their movements. However, it is difficult to track the movements in a vast and homogeneous environment without stimuli because of space constraints in laboratories or environmental heterogeneity in the field, hindering our understanding of inherent movement patterns. Here, we applied an omnidirectional treadmill mechanism, or a servosphere, as a tool for tracking two-dimensional movements of small animals that can provide both a homogenous environment and a virtual infinite space for walking. To validate the use of our tracking system for assessment of the free-walking behavior, we compared walking patterns of individual pillbugs (Armadillidium vulgare) on the servosphere with that in two types of experimental flat arenas. Our results revealed that the walking patterns on the servosphere showed similar diffusive characteristics to those observed in the large arena simulating an open space, and we demonstrated that our mechanism provides more robust measurements of diffusive properties compared to a small arena with enclosure. Moreover, we showed that anomalous diffusion properties, including Lévy walk, can be detected from the free-walking behavior on our tracking system. Thus, our novel tracking system is useful to measure inherent movement patterns, which will contribute to the studies of movement ecology, ethology, and behavioral sciences.

Optimizing mating encounters by sexually dimorphic movements.

All organisms with sexual reproduction undergo a process of mating, which essentially involves the encounter of two individuals belonging to different sexes. During mate search, both sexes should mutually optimize their encounters, thus raising a question of how they achieve this. Here, we show that a population with sexually dimorphic movement patterns achieves the highest individual mating success under a limited lifespan. Extensive simulations found and analytical approximations corroborated the existence of conditions under which sexual dimorphism in the movement patterns (i.e. how diffusively they move) is advantageous over sexual monomorphism. Mutual searchers with limited lifespans need to balance the speed and accuracy of finding their mates, and dimorphic movements can solve this trade-off. We further demonstrate that the sexual dimorphism can evolve from an initial sexually monomorphic population. Our results emphasize the importance of considering mutual optimization in problems of random search.

Public goods dilemma in asexual ant societies.

Cooperation in biological, social, and economic groups is underpinned by public goods that are generated by group members at some personal cost. Theory predicts that public goods will be exploited by cheaters who benefit from the goods by not paying for them, thereby leading to the collapse of cooperation. This situation, described as the "public goods dilemma" in game theory, makes the ubiquity of cooperation a major evolutionary puzzle. Despite this generalization, the demonstration of genetic background and fitness effects of the public goods dilemma has been limited to interactions between viruses and between cells, and thus its relevance at higher levels of organismal complexity is still largely unexplored. Here we provide experimental evidence for the public goods dilemma in a social insect, the ant Pristomyrmex punctatus. In this species, all workers are involved in both asexual reproduction and cooperative tasks. Genetic cheaters infiltrate field colonies, reproducing more than the workers but shunning cooperative tasks. In laboratory experiments, cheaters outcompeted coexisting workers in both survival and reproduction, although a group composed only of cheaters failed to produce offspring. The operations of the public goods dilemma in P. punctatus showed a remarkable convergence with those in microbial societies, not only in fitness consequences but also in behavioral mechanisms. Our study reinforces the evolutionary impact of cheaters on diverse cooperative systems in the laboratory and in the field.

Arms race between selfishness and policing: two-trait quantitative genetic model for caste fate conflict in eusocial Hymenoptera.

Policing against selfishness is now regarded as the main force maintaining cooperation, by reducing costly conflict in complex social systems. Although policing has been studied extensively in social insect colonies, its coevolution against selfishness has not been fully captured by previous theories. In this study, I developed a two-trait quantitative genetic model of the conflict between selfish immature females (usually larvae) and policing workers in eusocial Hymenoptera over the immatures' propensity to develop into new queens. This model allows for the analysis of coevolution between genomes expressed in immatures and workers that collectively determine the immatures' queen caste fate. The main prediction of the model is that a higher level of polyandry leads to a smaller fraction of queens produced among new females through caste fate policing. The other main prediction of the present model is that, as a result of arms race, caste fate policing by workers coevolves with exaggerated selfishness of the immatures achieving maximum potential to develop into queens. Moreover, the model can incorporate genetic correlation between traits, which has been largely unexplored in social evolution theory. This study highlights the importance of understanding social traits as influenced by the coevolution of conflicting genomes.

Intragenomic conflict over queen determination favours genomic imprinting in eusocial Hymenoptera.

Colonies of eusocial Hymenoptera, such as ants, bees and wasps, have long been recognized as candidates for the study of genomic imprinting on the grounds of evolutionary conflicts that arise from close interactions among colony members and relatedness asymmetry owing to haplodiploidy. Although a general kinship theory of genomic imprinting predicts its occurrence under various circumstances of the colony life cycle, new theoretical approaches are required to account for the specifics of real colonies based on recent advances in molecular-level understanding of ants and honeybees. Using a multivariate quantitative genetic model, we examined the potential impact of genomic imprinting on genes that determine the carrier female's propensity to develop into the queen caste. When queen overproduction owing to the increased propensity comes at a colony-level cost, the conflict between maternally and paternally inherited genes in polyandrous (queen multiple mating) colonies favours genomic imprinting. Moreover, we show that the genomic imprinting can occur even under monandry (queen single mating), once incorporating the costs differentially experienced by new males and new queens. Our model predicts the existence of imprinted 'genetic royal cheats' with patriline-specific expression in polyandrous colonies, and seems consistent with the paternal effect on queen determination in monandrous Argentine ants.

A cheater lineage in a social insect: Implications for the evolution of cooperation in the wild.

Biological cooperation is vulnerable to cheaters that exploit the benefits of cooperation without contributing to these benefits, thus the control of cheating is important to maintain cooperative systems. Recently, we reported a cheater lineage in a field population of the Japanese ant Pristomyrmex punctatus. This species is characterized by its asexual reproduction and lack of a division of labor: all females fulfill both reproduction and cooperative tasks in their colonies. Cheaters that originated from cooperators lay more eggs and take little part in cooperative tasks, resulting in lower fitness of their nest mates. This leads to contrasting selection pressures between the individual and group levels, and makes the cheater ants analogous to cheaters in social microbes and cancer cells. The genetic and developmental basis, possible transmission strategies, and evolutionary fate of the cheaters are discussed in the context of the origin and persistence of cheating and cooperation in nature.

Cheater genotypes in the parthenogenetic ant Pristomyrmex punctatus.

Cooperation is subject to cheating strategies that exploit the benefits of cooperation without paying the fair costs, and it has been a major goal of evolutionary biology to explain the origin and maintenance of cooperation against such cheaters. Here, we report that cheater genotypes indeed coexist in field colonies of a social insect, the parthenogenetic ant Pristomyrmex punctatus. The life history of this species is exceptional, in that there is no reproductive division of labour: all females fulfil both reproduction and cooperative tasks. Previous studies reported sporadic occurrence of larger individuals when compared with their nest-mates. These larger ants lay more eggs and hardly take part in cooperative tasks, resulting in lower fitness of the whole colony. Population genetic analysis showed that at least some of these large-bodied individuals form a genetically distinct lineage, isolated from cooperators by parthenogenesis. A phylogenetic study confirmed that this cheater lineage originated intraspecifically. Coexistence of cheaters and cooperators in this species provides a good model system to investigate the evolution of cooperation in nature.