Test of the negative feedback hypothesis of colony size sensing in social insects.

Social insects can sense colony size-even without visual information in a dark environment. How they achieve this is yet largely unknown. We empirically tested a hypothesis on the proximate mechanism using ant colonies. In Diacamma colonies, the monogynous queen is known to increase the effort devoted to queen pheromone transmission behaviour (patrolling) as the colony grows, as if she perceives colony size. The negative feedback hypothesis assumes that, through repeated physical contact with workers, the queen monitors the physiological state (fertility) of workers and increases her patrolling effort when she encounters more fertile workers. Supporting this hypothesis, we found that the queen increased her patrolling effort in response to a higher ratio of fertile workers under the experimental condition of constant colony size. Furthermore, chemical analyses and bioassays suggested that cuticular hydrocarbons have queen pheromone activity and can mediate the observed queen-worker communication of fertility state. Such a self-organizing mechanism of sensing colony size may also operate in other social insects living in small colonies.

Molecular species profiles of plasma ceramides in different clinical types of X-linked adrenoleukodystrophy.

X-linked adrenoleukodystrophy (X-ALD) is a genetic disorder associated with peroxisomal dysfunction. Patients with this rare disease accumulate very long-chain fatty acids (VLCFAs) in their bodies because of impairment of peroxisomal VLCFA ?-oxidation. Several clinical types of X-ALD, ranging from mild (axonopathy in the spinal cord) to severe (cerebral demyelination), are known. However, the molecular basis for this phenotypic variability remains largely unknown. In this study, we determined plasma ceramide (CER) profile using liquid chromatography-tandem mass spectrometry. We characterized the molecular species profile of CER in the plasma of patients with mild (adrenomyeloneuropathy;AMN) and severe (cerebral) X-ALD. Eleven X-ALD patients (five cerebral, five AMN, and one carrier) and 10 healthy volunteers participated in this study. Elevation of C26:0 CER was found to be a common feature regardless of the clinical types. The level of C26:1 CER was significantly higher in AMN but not in cerebral type, than that in healthy controls. The C26:1 CER level in the cerebral type was significantly lower than that in the AMN type. These results suggest that a high level of C26:0 CER, along with a control level of C26:1 CER, is a characteristic feature of the cerebral type X-ALD. J. Med. Invest. 70 : 403-410, August, 2023.

A real-time feedback system stabilises the regulation of worker reproduction under various colony sizes.

Social insects demonstrate adaptive behaviour for a given colony size. Remarkably, most species do this even without visual information in a dark environment. However, how they achieve this is yet unknown. Based on individual trait expression, an agent-based simulation was used to identify an explicit mechanism for understanding colony size dependent behaviour. Through repeated physical contact between the queen and individual workers, individual colony members monitor the physiological states of others, reflecting such contact information in their physiology and behaviour. Feedback between the sensing of physiological states and the corresponding behaviour patterns leads to self-organisation with colonies shifting according to their size. We showed (1) the queen can exhibit adaptive behaviour patterns for the increase in colony size while density per space remains unchanged, and (2) such physical constraints can underlie the adaptive switching of colony stages from successful patrol behaviour to unsuccessful patrol behaviour, which leads to constant ovary development (production of reproductive castes). The feedback loops embedded in the queen between the perception of internal states of the workers and behavioural patterns can explain the adaptive behaviour as a function of colony size.

Population genetic structure of the globally introduced big-headed ant in Taiwan.

Global commerce and transportation facilitate the spread of invasive species. The African big-headed ant, Pheidole megacephala (Fabricius), has achieved worldwide distribution through globalization. Since the late 19th century, Taiwan has served as a major seaport because of its strategic location. The population genetic structure of P. megacephala in Taiwan is likely to be shaped by international trade and migration between neighboring islands. In this study, we investigated the population genetics of P. megacephala colonies sampled from four geographical regions in Taiwan and elucidated the population genetic structures of P. megacephala sampled from Taiwan, Okinawa, and Hawaii. We observed a low genetic diversity of P. megacephala across regions in Taiwan. Moreover, we noted low regional genetic differentiation and did not observe isolation by distance, implying that long-distance jump dispersal might have played a crucial role in the spread of P. megacephala. We sequenced the partial cytochrome oxidase I gene and observed three mitochondrial haplotypes (TW1-TW3). TW1 and TW3 most likely originated from populations within the species' known invasive range, suggesting that secondary introduction is the predominant mode of introduction for this invasive ant. TW2 represents a novel haplotype that was previously unreported in other regions. P. megacephala populations from Taiwan, Okinawa, and Hawaii exhibited remarkable genetic similarity, which may reflect their relative geographic proximity and the historical connectedness of the Asia-Pacific region.

Resilience of native ant community against invasion of exotic ants after anthropogenic disturbances of forest habitats.

The positive association between disturbances and biological invasions is a widely observed ecological pattern in the Anthropocene. Such patterns have been hypothesized to be driven by the superior competitive ability of invaders or by modified environments, as well as by the interaction of these factors. An experimental study that tests these hypotheses is usually less feasible, especially in protected nature areas. An alternative approach is to focus on community resilience over time after the anthropogenic disturbance of habitats. Here, we focused on ant communities within a forest to examine their responses after disturbance over time. We selected the Yanbaru region of northern Okinawa Island, which is a biodiversity hotspot in East Asia. We compared ant communities among roadside environments in forests where the road age differed from 5 to 25 years. We also monitored the ant communities before and after disturbance from forest thinning. We found that the species richness and abundance of exotic ants were higher in recently disturbed environments (roadsides of 5-15 years old roads), where the physical environment was warmer and drier. In contrast, the roadsides of 25-year-old roads indicated the potential recovery of the physical environment with cooler and moister conditions, likely owing to regrowth of roadside vegetation. At these sites, there were few exotic ants, except for those immediately adjacent to the road. The population density of the invasive species Technoymex brunneus substantially increased 1-2 years after forest thinning. There was no evidence of the exclusion of native ants by exotic ants that were recorded after disturbance. Our results suggest that local ant communities in the Yanbaru forests have some resilience to disturbance. We suggest that restoration of environmental components is a better strategy for maintaining native ant communities, rather than removing exotic ants after anthropogenic disturbance.

Exploring New Functional Aspects of HTLV-1 RNA-Binding Protein Rex: How Does Rex Control Viral Replication?

After integration to the human genome as a provirus, human T-cell leukemia virus type 1 (HTLV-1) utilizes host T cell gene expression machinery for viral replication. The viral RNA-binding protein, Rex, is known to transport unspliced/incompletely spliced viral mRNAs encoding viral structural proteins out of the nucleus to enhance virus particle formation. However, the detailed mechanism of how Rex avoids extra splicing of unspliced/incompletely spliced viral mRNAs and stabilizes them for effective translation is still unclear. To elucidate the underlying molecular mechanism of Rex function, we comprehensively analyzed the changes in gene expression and splicing patterns in Rex-overexpressing T cells. In addition, we identified 81 human proteins interacting with Rex, involved in transcription, splicing, translation, and mRNA quality control. In particular, Rex interacts with NONO and SFPQ, which play important roles in the regulation of transcription and splicing. Accordingly, expression profiles and splicing patterns of a wide variety of genes are significantly changed in Rex-expressing T cells. Especially, the level of vPD-L1 mRNA that lacks the part of exon 4, thus encodes soluble PD-L1 was significantly increased in Rex-expressing cells. Overall, by integrated analysis of these three datasets, we showed for the first time that Rex intervenes the host gene expression machinery throughout the pathway, probably to escort viral unstable mRNAs from transcription (start) to translation (end). Upon exerting its function, Rex may alter the expression level and splicing patterns of various genes, thus influencing the phenotype of the host cell.

Exotic Ants of the Asia-Pacific: Invasion, National Response, and Ongoing Needs.

Human activity has facilitated the introduction of many exotic species via global trade. Asia-Pacific countries comprise one of the most economically and trade-active regions in the world, which makes it an area that is highly vulnerable to invasive species, including ants. There are currently over 60 exotic ant species in the Asia-Pacific, with the red imported fire ant, Solenopsis invicta, among the most destructive. Exotic ants pose many economic and ecological problems for the region. Countries in the Asia-Pacific have dealt with the problem of exotic ants in very different ways, and there has been an overall lack of preparedness. To improve the management of risks associated with invasive ants, we recommend that countries take action across the biosecurity spectrum, spanning prevention, containment, and quarantine. The creation of an Asia-Pacific network for management of invasive ants should help prevent their introduction and mitigate their impacts.

Alternative reproductive tactics in male freshwater fish influence the accuracy of species recognition.

Sexual conflict can result in coercive mating. Because males bear low costs of heterospecific mating, coercive males may engage in misdirected mating attempts toward heterospecific females. In contrast, sexual selection through consensual mate choice can cause mate recognition cues among species to diverge, leading to more accurate species recognition. Some species show both coercive mating and mate choice-associated courtship behaviors as male alternative reproductive tactics. We hypothesized that if the selection pressures on each tactic differ, then the accuracy of species recognition would also change depending on the mating tactic adopted. We tested this hypothesis in the guppy (Poecilia reticulata) and mosquitofish (Gambusia affinis) by a series of choice experiments. Poecilia reticulata and G. affinis males both showed imperfect species recognition and directed all components of mating behavior toward heterospecific females. They tended to direct courtship displays more frequently toward conspecific than heterospecific females. With male P. reticulata, however, accurate species recognition disappeared when they attempted coercive copulation: they directed coercions more frequently toward heterospecific females. We also found that heterospecific sexual interaction had little effect on the fecundity of gravid females, which suggests that prepregnancy interactions likely underpin the exclusion of G. affinis by P. reticulata in our region.

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.

Population genetic structure and evolution of Batesian mimicry in Papilio polytes from the Ryukyu Islands, Japan, analyzed by genotyping-by-sequencing.

Batesian mimicry is a striking example of Darwinian evolution, in which a mimetic species resembles toxic or unpalatable model species, thereby receiving protection from predators. In some species exhibiting Batesian mimicry, nonmimetic individuals coexist as polymorphism in the same population despite the benefits of mimicry. In a previous study, we proposed that the abundance of mimics is limited by that of the models, leading to polymorphic Batesian mimicry in the swallowtail butterfly, Papilio polytes, on the Ryukyu Islands in Japan. We found that their mimic ratios (MRs), which varied among the Islands, were explained by the model abundance of each habitat, rather than isolation by distance or phylogenetic constraint based on the mitochondrial DNA (mtDNA) analysis. In the present study, this possibility was reexamined based on hundreds of nuclear single nucleotide polymorphisms (SNPs) of 93 P. polytes individuals from five Islands of the Ryukyus. We found that the population genetic and phylogenetic structures of P. polytes largely corresponded to the geographic arrangement of the habitat Islands, and the genetic distances among island populations show significant correlation with the geographic distances, which was not evident by the mtDNA-based analysis. A partial Mantel test controlling for the present SNP-based genetic distances revealed that the MRs of P. polytes were strongly correlated with the model abundance of each island, implying that negative frequency-dependent selection interacting with model species shaped and maintained the mimetic polymorphism. Taken together, our results support the possibility that predation pressure, not isolation by distance or other neutral factors, is a major driving force of evolution of the Batesian mimicry in P. polytes from the Ryukyus.

Deformed Wing Virus in Two Widespread Invasive Ants: Geographical Distribution, Prevalence, and Phylogeny.

Spillover of honey bee viruses have posed a significant threat to pollination services, triggering substantial effort in determining the host range of the viruses as an attempt to understand the transmission dynamics. Previous studies have reported infection of honey bee viruses in ants, raising the concern of ants serving as a reservoir host. Most of these studies, however, are restricted to a single, local ant population. We assessed the status (geographical distribution/prevalence/viral replication) and phylogenetic relationships of honey bee viruses in ants across the Asia-Pacific region, using deformed wing virus (DWV) and two widespread invasive ants, Paratrechina longicornis and Anoplolepis gracilipes, as the study system. DWV was detected in both ant species, with differential geographical distribution patterns and prevenance levels between them. These metrics, however, are consistent across the geographical range of the same ant species. Active replication was only evident in P. longicornis. We also showed that ant-associated DWV is genetically similar to that isolated from Asian populations of honey bees, suggesting that local acquisition of DWV by the invasive ants may have been common at least in some of our sampled regions. Transmission efficiency of DWV to local arthropods mediated by ant, however, may vary across ant species.

Mimicry genes reduce pre-adult survival rate in Papilio polytes: A possible new mechanism for maintaining female-limited polymorphism in Batesian mimicry.

Batesian mimicry, in which harmless organisms resemble unpalatable or harmful species, is a well-studied adaptation for predation avoidance. The females of some Batesian mimic species comprise mimetic and nonmimetic individuals. Mimetic females of such polymorphic species clearly have a selective advantage due to decreased predation pressure, but the selective forces that maintain nonmimetic females in a population remain unclear. In the swallowtail butterfly, Papilio polytes, female polymorphism is controlled by the H (mimetic) and h (nonmimetic) alleles at a single autosomal locus. Here, we examined whether the dominant H allele has a deleterious effect on the pre-adult survival rate (egg-to-adult emergence rate). We repeated an assortative mating-like treatment-that is breeding of males and females whose mothers had the same phenotype (mimetic or nonmimetic)-for three consecutive generations, while avoiding inbreeding. Results showed that pre-adult survival rate decreased over generations only in lines derived from mothers with the mimetic phenotype (hereafter, mimetic-assorted lines). This lowered survival was due to an increased mortality at the final instar larval stage and the pupal stages. Interestingly, the pre-adult mortality in the mimetic-assorted lines seemed to be associated with a male-biased sex ratio at adult emergence. These results suggest that the dominant H allele displays a mildly deleterious effect that is expressed more strongly in females and homozygous individuals than in heterozygous individuals. We propose that this cost of mimicry in larval and pupal stages contributes to the maintenance of female-limited polymorphism in P. polytes.

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.

Evidence for frequency-dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, Japan.

Batesian mimicry is a well-studied adaptation for predation avoidance, in which a mimetic species resembles an unpalatable model species. Batesian mimicry can be under positive selection because of the protection gained against predators, due to resemblance to unpalatable model species. However, in some mimetic species, nonmimetic individuals are present in populations, despite the benefits of mimicry. The mechanism for evolution of such mimetic polymorphism remains an open question. Here, we address the hypothesis that the abundance of mimics is limited by that of the models, leading to mimetic polymorphism. In addition, other forces such as the effects of common ancestry and/or isolation by distance may explain this phenomenon. To investigate this question, we focused on the butterfly, Papilio polytes, that exhibits mimetic polymorphism on multiple islands of the Ryukyus, Japan, and performed field surveys and genetic analysis. We found that the mimic ratio of P. polytes was strongly correlated with the model abundance observed on each of the five islands, suggesting negative frequency-dependent selection is driving the evolution of polymorphism in P. polytes populations. Molecular phylogenetic analysis indicated that the southern island populations are the major source of genetic diversity, and the middle and northern island populations arose by relatively recent migration. This view was also supported by mismatch distribution and Tajima's D analyses, suggesting a recent population expansion on the middle and northern islands, and stable population persistence on the southern islands. The frequency of the mimetic forms within P. polytes populations is thus explained by variations in the model abundance rather than by population structure. Thus, we propose that predation pressure, rather than neutral forces, have shaped the Batesian mimicry polymorphism in P. polytes observed in the Ryukyus.

Inbreeding tolerance as a pre-adapted trait for invasion success in the invasive ant Brachyponera chinensis.

Identifying traits that facilitate species introductions and successful invasions of ecosystems represents a key issue in ecology. Following their establishment into new environments, many non-native species exhibit phenotypic plasticity with post-introduction changes in behaviour, morphology or life history traits that allow them to overcome the presumed loss of genetic diversity resulting in inbreeding and reduced adaptive potential. Here, we present a unique strategy in the invasive ant Brachyponera chinensis (Emery), in which inbreeding tolerance is a pre-adapted trait for invasion success, allowing this ant to cope with genetic depletion following a genetic bottleneck. We report for the first time that inbreeding is not a consequence of the founder effect following introduction, but it is due to mating between sister queens and their brothers that pre-exists in native populations which may have helped it circumvent the cost of invasion. We show that a genetic bottleneck does not affect the genetic diversity or the level of heterozygosity within colonies and suggest that generations of sib-mating in native populations may have reduced inbreeding depression through purifying selection of deleterious alleles. This work highlights how a unique life history may pre-adapt some species for biological invasions.

Ultraviolet exposure has an epigenetic effect on a Batesian mimetic trait in the butterfly Papilio polytes.

Wing polymorphism of butterflies provides a good system in which to study adaptation. The Asian Batesian mimic butterfly Papilio polytes has unmelanized, putative mimetic red spots on its black hind wings. The size of those red spots is non-heritable but it is highly polymorphic, the adaptive significance of which is unknown. We hypothesized that under strong ultraviolet (UV) irradiation, butterflies develop a wider melanized black area to protect the wings from UV damage, and as a result express smaller mimetic red spots. Our field survey on Okinawa Island revealed a negative relationship between the sizes of the red spot and the black area in the wings. The size varied seasonally and was negatively correlated with the intensity of solar UV radiation at the time of capture. Laboratory experiments revealed that the size was reduced by strong UV irradiation not only of the eggs and larvae, but also of their mothers through a putative epigenetic mechanism. The flexible phenotypic expression of the red spots in P. polytes suggests a trade-off between protection against UV damage and predation avoidance, and provides a new insight into the evolution of Batesian mimicry.

Author Correction: Controlling invasive ant species: a theoretical strategy for efficient monitoring in the early stage of invasion.

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Controlling invasive ant species: a theoretical strategy for efficient monitoring in the early stage of invasion.

Invasion by the red imported fire ant, Solenopsis invicta Buren, has destructive effects on native biodiversity, agriculture and public health. This ant's aggressive foraging behaviour and high reproductive capability have enabled its establishment of wild populations in most regions into which it has been imported. An important aspect of eradication is thorough nest monitoring and destruction during early invasion to prevent range expansion. The question is: How intense must monitoring be on temporal and spatial scales to eradicate the fire ant? Assuming that the ant was introduced into a region and that monitoring was conducted immediately after nest detection in an effort to detect all other potentially established nests, we developed a mathematical model to investigate detection rates. Setting the monitoring limit to three years, the detection rate was maximized when monitoring was conducted shifting bait trap locations and setting them at intervals of 30 m for each monitoring. Monitoring should be conducted in a radius of at least 4 km around the source nest, or wider-depending on how late a nest is found. For ease of application, we also derived equations for finding the minimum bait interval required in an arbitrary ant species for thorough monitoring.

Social enforcement depending on the stage of colony growth in an ant.

Altruism is a paradox in Darwinian evolution. Policing is an important mechanism of the evolution and maintenance of altruism. A recently developed dynamic game model incorporating colony demography and inclusive fitness predicts that, in hymenopteran social insects, policing behaviour enforcing reproductive altruism in group members depends strongly on the colony growth stage, with strong policing as the colony develops and a relaxation of policing during the reproductive phase. Here, we report clear evidence supporting this prediction. In the ant Diacamma sp., reproduction by workers was suppressed by worker policing when the colony was small, whereas in large, mature colonies worker policing was relaxed and worker-produced males emerged. Conditional expression of traits can provide strong empirical evidence for natural selection theory if the expression pattern is precisely predicted by the theory, and our results illustrate the importance of intracolony population dynamics in the evolution of social systems.