Caste ratios affect the reproductive output of social trematode colonies

Intraspecific phenotypic diversification in social organisms often leads to formation of physical castes which are morphologically specialized for particular tasks within the colony. The optimal caste allocation theory argues that specialized morphological castes are efficient at specific tasks, and hence different caste ratios should affect the ergonomic efficiency, hence reproductive output of the colony. However, the reproductive output of different caste ratios has been documented in few species of insects with equivocal support for the theory. This study investigated whether the ratios of nonreproductive and reproductive morphs affect the reproductive output of a recently discovered social trematode, Philophthalmus sp., in which the nonreproductive members are hypothesized to be defensive specialists. A census of natural infections and a manipulative in vitro experiment demonstrated a positive association between the reproductive output of trematode colonies and the ratio of nonreproductive to reproductive morphs in the presence of an intra‐host trematode competitor, Maritrema novaezealandensis. On the contrary, without the competitor, reproductive output was negatively associated with the proportion of nonreproductive castes in colonies. Our findings demonstrate for the first time a clear fitness benefit associated with the nonreproductive castes in the presence of a competitor while illustrating the cost of maintaining such morphs in noncompetitive situations. Although the proximate mechanisms controlling caste ratio remain unclear in this trematode system, this study supports the prediction that the fitness of colonies is influenced by the composition of specialized functional morphs in social organisms, suggesting a potential for adaptive shifts of caste ratios over evolutionary time.     

Differential protein expression in honeybee (Apis mellifera L.) larvae: underlying caste differentiation

Honeybee (Apis mellifera) exhibits divisions in both morphology and reproduction. The queen is larger in size and fully developed sexually, while the worker bees are smaller in size and nearly infertile. To better understand the specific time and underlying molecular mechanisms of caste differentiation, the proteomic profiles of larvae intended to grow into queen and worker castes were compared at 72 and 120 hours using two dimensional electrophoresis (2-DE), network, enrichment and quantitative PCR analysis. There were significant differences in protein expression between the two larvae castes at 72 and 120 hours, suggesting the queen and the worker larvae have already decided their fate before 72 hours. Specifically, at 72 hours, queen intended larvae over-expressed transketolase, aldehyde reductase, and enolase proteins which are involved in carbohydrate metabolism and energy production, imaginal disc growth factor 4 which is a developmental related protein, long-chain-fatty-acid CoA ligase and proteasome subunit alpha type 5 which metabolize fatty and amino acids, while worker intended larvae over-expressed ATP synthase beta subunit, aldehyde dehydrogenase, thioredoxin peroxidase 1 and peroxiredoxin 2540, lethal (2) 37 and 14-3-3 protein epsilon, fatty acid binding protein, and translational controlled tumor protein. This differential protein expression between the two caste intended larvae was more pronounced at 120 hours, with particular significant differences in proteins associated with carbohydrate metabolism and energy production. Functional enrichment analysis suggests that carbohydrate metabolism and energy production and anti-oxidation proteins play major roles in the formation of caste divergence. The constructed network and validated gene expression identified target proteins for further functional study. This new finding is in contrast to the existing notion that 72 hour old larvae has bipotential and can develop into either queen or worker based on epigenetics and can help us to gain new insight into the time of departure as well as caste trajectory influencing elements at the molecular level.     

Nutritional asymmetries are related to division of labor in a queenless ant

Eusocial species exhibit pronounced division of labor, most notably between reproductive and non-reproductive castes, but also within non-reproductive castes via morphological specialization and temporal polyethism. For species with distinct worker and queen castes, age-related differences in behavior among workers (e.g. within-nest tasks versus foraging) appear to result from physiological changes such as decreased lipid content. However, we know little about how labor is divided among individuals in species that lack a distinct queen caste. In this study, we investigated how fat storage varied among individuals in a species of ant (Dinoponera australis) that lacks a distinct queen caste and in which all individuals are morphologically similar and capable of reproduction (totipotent at birth). We distinguish between two hypotheses, 1) all individuals are physiologically similar, consistent with the possibility that any non-reproductive may eventually become reproductive, and 2) non-reproductive individuals vary in stored fat, similar to highly eusocial species, where depletion is associated with foraging and non-reproductives have lower lipid stores than reproducing individuals. Our data support the latter hypothesis. Location in the nest, the probability of foraging, and foraging effort, were all associated with decreased fat storage.     

扩头蔡白蚁消化与生殖系统解剖及其与黑翅土白蚁的比较研究

扩头蔡白蚁Tsaitermes ampliceps(Wang&Li)和黑翅土白蚁Odotoermes formosanus(Shiraki)是分布广泛的食木性昆虫,群居生活,具有复杂的品级分化.本试验研究了低等白蚁扩头蔡白蚁不同品级的消化和生殖系统结构,并与高等白蚁黑翅土白蚁进行了比较.结果显示扩头蔡白蚁的消化、生殖系...     

The definition of eusociality

We describe more precise definitions for the term "eusociality"and other social systems. Our criterion for eusociality is thepresence of castes, which are groups of individuals that becomeirreversibly behaviorally distinct at some point prior to reproductivematurity. Eusocial societies are characterized by two traits:(1) helping by individuals of the less-reproductive caste, and(2) either behavioral totipotency of only the more reproductivecaste (facultative eusociality) or totipotency of neither caste(obligate eusociality). We define "cooperative breeding" asalloparental care without castes. Cooperatively breeding societiesmay comprise two types, semisocial (distribution of lifetimereproductive success bimodal), and quasisocial (distributionof lifetime reproductive success unimodal), but this hypothesisrequires empirical analysis. Our definitions conceptually unifystudies of arthropod and vertebrate sociality.     

Caste Determination in Bombus terrestris: Differences in Development and Rates of JH Biosynthesis between Queen and Worker Larvae

To study the possible role of juvenile hormone in caste determination in Bombus terrestris, we measured development and rates of juvenile hormone biosynthesis in vitro in larvae destined to develop into either workers or queens. Larvae of both castes developed through four instars and had the same growth rates. However, the duration of the instars was longer for queen larvae, and their head width at the third and fourth instars was significantly larger. After validating the well-known radiochemical assay of JH for bumble bee larvae, we show that worker larvae corpora allata exhibited a constant and low rate of JH biosynthesis, never more than 5 pmol JH/h/pair. Queen larvae, in contrast, had two peaks of JH biosynthesis: a small one during the first instar, which has previously been correlated with caste determination; and a large peak, previously undetected, above 40 pmol JH/h/pair, during the second and third instars. We suggest that caste determination in this species is mediated by JH and that the duration of larval instars is a key factor. The possibility that the queen influences caste determination via an effect on instar duration is also discussed. Copyright 1997 Elsevier Science Ltd. All rights reserved     

Differential expressions of nuclear proteomes between honeybee (Apis mellifera L.) Queen and Worker Larvae: a deep insight into caste pathway decisions

Honeybees (Apis mellifera L.) possess individuals (castes) in their colonies, to which specific tasks are allocated. Owing to a difference in nutrition, the young female larvae develop into either a fertile queen or a sterile worker. Despite a series of investigations on the underlying mechanisms of honeybee caste polyphenism, information on proteins and enzymes involved in DNA and RNA regulation in the nucleus is still missing. The techniques of nuclear protein enrichment, two-dimensional electrophoresis, mass spectrometry and bioinformatics were applied to understand the nuclear proteome changes in response to changes in environmental settings (nutrition and time) during the early developmental stages at the third (72 h), fourth (96 h), and fifth (120 h) instars of the two caste intended larvae. A total of 120 differentially expressed nuclear proteins were identified in both caste intended larvae during these developmental stages. The third, fourth and fifth instars of queen prospective larvae expressed 69%, 84%, and 68% of the proteins that had altered expression, respectively. Particularly, the prospective queen larvae up-regulated most of the proteins with nuclear functions. In general, this changing nuclear proteome of the two caste intended larvae over the three developmental stages suggests variations in DNA and RNA regulating proteins and enzymes. These variations of proteins and enzymes involved in DNA and RNA regulation in response to differential nutrition between the two caste intended larvae lead the two caste larvae to pursue different developmental trajectories. Hence, this first data set of the nuclear proteome helps us to explore the innermost biological makings of queen and worker bee castes as early as before the 72 h (3rd instar). Also, it provides new insights into the honeybee's polymorphism at nuclear proteome level and paves new ways to understand mechanisms of caste decision in other eusocial insects.     

A theory of natural selection incorporating interaction among individuate. X. Use of groups consisting of a mating pair together with haploid and diploid caste members

This paper and the previous member of the series, deal with genetical mechanisms responsible for the evolution of eusociality (a level of social organization that includes differentiated sterile castes) among the “social” insects. Eusociality has evolved in a number of different species. Two different types of genetic systems are represented among these species: diplodiploidy (both sexes diploid) and haplodiploidy (haploid males and diploid females). The previous paper examined the evolution of a sterile caste system in the context of diplodiploidy, and the present paper considers the evolution of eusociality in the context of haplodiploidy.The present study demonstrates that selection operating with regard to random groups within the haplodiploid inheritance system cannot result in the evolution of a sterile caste system. Thus haplodiploidy, in itself, is not sufficient for the evolution of eusociality. However, if the sterile caste members are related to the reproductive members of the group, the appropriate caste associate gene effects are included in the function determining gene frequency change (i.e. Δp_i), and therefore, eusociality can evolve. This is true for both haploid and diploid castes.In comparing the two modes of inheritance, it is demonstrated that haplodiploidy provides up to 37·5% increased selection efficiency relative to diplodiploidy in evolving a social caste system in the absence of inbreeding.     

Hybridogenesis through thelytokous parthenogenesis in two Cataglyphis desert ants

Hybridogenesis is a sexual reproductive system, whereby parents from different genetic origin hybridize. Both the maternal and paternal genomes are expressed in somatic tissues, but the paternal genome is systematically excluded from the germ line, which is therefore purely maternal. Recently, a unique case of hybridogenesis at a social level was reported in the desert ant Cataglyphis hispanica. All workers are sexually produced hybridogens, whereas sexual forms (new queens and males) are produced by queens through parthenogenesis. Thus, only maternal genes are perpetuated across generations. Here, we show that such an unusual reproductive strategy also evolved in two other species of Cataglyphis belonging to the same phylogenetic group, Cataglyphis velox and Cataglyphis mauritanica. In both species, queens mate exclusively with males originating from a different genetic lineage than their own to produce hybrid workers, while they use parthenogenesis to produce the male and female reproductive castes. In contrast to single‐queen colonies of C. hispanica, colonies of C. velox and C. mauritanica are headed by several queens. Most queens within colonies share the same multilocus genotype and never transmit their mates' alleles to the reproductive castes. Social hybridogenesis in the desert ants has direct consequences on the genetic variability of populations and on caste determination. We also discuss the maintenance of this reproductive strategy within the genus Cataglyphis.     

Soldier‐biased gene expression in a subterranean termite implies functional specialization of the defensive caste

In a termite colony, reproduction is typically monopolized by a small number of sexuals that are supported by reproductively altruistic soldiers and workers. We expect caste differentiation to be associated with clear‐cut differences in gene expression, and for these differences to reflect caste function and development. Here, we use RNA‐Sequencing to compare the gene expression profiles of sexual nymphs and two non‐reproductive helper castes (i.e., workers and soldiers) of the Eastern subterranean termite Reticulitermes flavipes. We found that of n = 93 genes that are strictly expressed as a function of caste, a majority (78%) show a soldier‐specific pattern. This conspicuous soldier‐bias in genome‐wide expression suggests that this defensively specialized caste is functionally well‐differentiated from both the reproductive and the other non‐reproductive caste of this species, despite a shared developmental program with workers. Gene ontology analysis supports the notion of functional specialization by soldiers, as soldier‐biased gene sets are enriched for novel biological processes. Whether this pattern reflects ancient or more recent bouts of selection for caste novelty at the gene‐regulatory level is not known, but because soldiers are sterile and thus have no direct fitness, any selection for novelty must have been mediated indirectly, through reproducing relatives.     

Social organization in a flatworm: trematode parasites form soldier and reproductive castes

In some of the most complex animal societies, individuals exhibit a cooperative division of labour to form castes. The most pronounced types of caste formation involve reproductive and non-reproductive forms that are morphologically distinct. In colonies comprising separate or mobile individuals, this type of caste formation has been recognized only among the arthropods, sea anemones and mole-rats. Here, we document physical and behavioural caste formation in a flatworm. Trematode flatworm parasites undergo repeated clonal reproduction of ‘parthenitae’ within their molluscan hosts forming colonies. We present experimental and observational data demonstrating specialization among trematode parthenitae to form distinct soldier and reproductive castes. Soldiers do not reproduce, have relatively large mouthparts, and are much smaller and thinner than reproductives. Soldiers are also more active, and are disproportionally common in areas of the host where invasions occur. Further, only soldiers readily and consistently attack heterospecifics and conspecifics from other colonies. The division of labour described here for trematodes is strongly analogous to that characterizing other social systems with a soldier caste. The parallel caste formation in these systems, despite varying reproductive mode and taxonomic affiliation, indicates the general importance of ecological factors in influencing the evolution of social behaviour. Further, the ‘recognition of self’ and the defence of the infected host body from invading parasites are comparable to aspects of immune defence. A division of labour is probably widespread among trematodes and trematode species encompass considerable taxonomic, life history and environmental diversity. Trematodes should therefore provide new, fruitful systems to investigate the ecology and evolution of sociality.     

Reproductive division of labor between hybrid and nonhybrid offspring in a fire ant hybrid zone

Abstract.— Interspecific hybridization can often impose a substantial fitness cost due to reduced hybrid viability or fecundity. In social insects, however, such costs disproportionately impact reproductive offspring, whereas hybrids who become sterile workers can be functional, and even beneficial, colony members. Genomic imprinting of the paternal genome in reproductive, but not worker female offspring has been proposed as a mechanism to avoid genomic incompatibilities in hybrid queens in a hybrid zone between two fire ant species, Solenopsis geminata and S. xyloni. A study of allozyme variation demonstrated differences between the worker caste displaying a hybrid phenotype, and the winged queen caste displaying only the mother's phenotype. In this study, we investigate whether these differences are caused by genomic imprinting or genetic differences between castes by comparing variability of proteins to that of microsatellite markers. Workers and winged queens differed genetically at both classes of marker, indicating that allozyme differences were caused by underlying genetic differences between castes rather than differences in gene expression due to imprinting. Workers were F1 S. geminata X S. xyloni hybrids, whereas nearly all winged queens were of pure S. xyloni ancestry. Thus, S. xyloni within the hybrid zone appears to have evolved social hybridogenesis, in which the loss of worker potential in pure-species offspring necessitates hybridization for worker production, but prevents hybrids from being represented in the reproductive caste.     

熊蜂级型分化研究进展

熊蜂是众多野生植物及农作物的有效授粉昆虫,具有重要的经济和生态价值。熊蜂复杂的生长发育过程及社会性使其成为社会生物学研究的最佳模式生物之一。社会性昆虫的生殖劳动分工具有重要的进化意义,而级型分化是形成生殖劳动分工的基础。蜜蜂级型分化的研究已取得诸多重要成果,其机理也得到了较为深入的阐释,而熊蜂的社会性研究尚未形成系统,与蜜蜂研究相差甚远。近来的研究表明,饲喂频率或者饲喂总量的差异能够引起熊蜂级型分化的发生。保幼激素和蜕皮激素与熊蜂幼虫的发育紧密联系,在熊蜂级型分化的过程中发挥重要作用。一些参与蜜蜂级型分化的基因,在熊蜂级型间也存在差异表达。此外,群体间的相互作用以及蜂王和工蜂间的竞争也是促进熊蜂级型分化发生的重要因素。本文从营养、激素调控、群体发展及相互作用等方面综述熊蜂级型分化机制,并对未来的研究提出可能方向。     

Evidence for Caste Differences in Anal Droplet Alarm Pheromone Production and Responses in the Eusocial Thrips Kladothrips intermedius

Thrips (Thysanoptera) are tiny insects that produce anal secretions when threatened. Several studies have shown that, depending on the species, the droplets may contain alarm pheromones and/or repellents against enemies. In the eusocial gall‐inducing thrips Kladothrips intermedius both larvae and adults produce such droplets. There are two castes of adults in this species, soldiers (the sub‐fertile and gall‐bound defenders) and dispersers (winged and capable of initiating a gall). We tested the proclivity of secreting anal droplets by the two castes and whether the anal droplets induce different behavioural responses in relation to the emitter–receiver's caste in a contact chemoreception bioassay. Although secretion patterns were similar between castes, exposure to anal droplets emitted by different castes elicited different behavioural responses in adults in the bioassay. When exposed to soldiers’ anal droplets, dispersers significantly reduced the distance moved while soldiers significantly increased the distance moved, compared to when they were exposed to hexane control. In contrast, no differences in the distance moved were observed for any caste when exposed to dispersers’ anal droplets versus hexane control. Increased activity in soldiers when exposed to their own anal droplets is a predicted response to enhance the overall defence of the gall when under threat, whereas dispersers should slow down their activity when exposed to such ‘warning signal’. Thus, the behavioural data indicate that the anal droplets emitted by soldiers are likely to contain an alarm pheromone.     

Reproductive skew and the origin of sterile castes

Reproductive skew theory has not heretofore formally addressed one of the most important questions in evolutionary biology: How can whole-life sterile castes evolve? We construct a transactional skew model investigating under what conditions a subordinate in a multimember group is favored to develop into a morphologically specialized worker caste. Our model demonstrates that, contrary to former expectations, the ecological and genetic conditions favoring caste differentiation are far more restrictive than those favoring high skew. Caste differentiation cannot be selected in saturated, symmetrical relatedness groups unless the genetic relatedness among group members is extremely high. In contrast, it can be selected in the saturated, asymmetrical relatedness (parent-offspring) groups with complete skew. If we also consider the future reproduction of subordinates, caste differentiation is possible only after the group size reaches a certain critical point. Most importantly, caste differentiation in a parent-offspring group increases its saturated group size. The positive feedback between group size and the degree of caste differentiation can continue in principle until completely sterile worker castes emerge. Thus, at least in the case of parent-offspring groups, group size but not the degree of reproductive skew may be a better index of the level of social complexity. A scheme for the evolution of sterile worker castes that integrates the role of group size into the framework of reproductive skew theory is proposed.     

蜜蜂蜂王与工蜂级型分化研究进展

蜜蜂ApismekiferaL .是典型的社会性昆虫 ,蜂王和工蜂都是由受精卵发育而来的二倍体成蜂 ,但是在形态、生理、行为等方面有明显的差异 ,属于不同的级型。蜂王和工蜂的级型分化的关键时期发生在幼虫的 4龄末至 5龄止。分化是由分化基因调控的 ,幼虫期食物的质和量是分化的外部决定因子。JH对两级型中卵巢的分化有非常重要的调控作用。蜜蜂脑或其它组织中可能有分泌调控CA的咽侧体调节激素 ,它们通过对CA中JH的合成和分泌的调控而参与了分化的调控。章鱼胺等生物胺也参与了分化调控过程。     

A theory of natural selection incorporating interaction among individuals. IX. Use of groups consisting of a mating pair and sterile diploid caste members

This paper and the next member of the series, deal with genetical mechanisms responsible for the evolution of eusociality (a level of social organization that includes differentiated sterile castes) among the “social” insects. Eusociality has evolved in a number of different species. Two different types of genetic systems are represented among these species: diplodiploidy (both sexes diploid) and haplodiploidy (haploid males and diploid females). The present paper examines the evolution of a sterile caste system in the context of diplodiploidy, and the next paper considers the evolution of eusociality in the context of haplodiploidy.The present study demonstrates that if the sterile diploid caste members are related to the reproductive members of the group, eusociality can evolve. This is true because the caste associate gene effects are included in the function determining gene frequency change (i.e. Δp_i). Also, since the caste gene effects are expressed only through the associate dimension of gene activity, they can cause morphological and behavioral adaptations to occur which are peculiar to the caste members, and need not be expressed in the reproducing members of the group. Thus caste differentiation is possible.     

Detecting selection on morphological traits in social insect castes: the case of the social wasp Vespula maculifrons

Highly social insects dominate terrestrial ecosystems because society members belong to discrete castes that undertake distinct tasks. The distinct functional roles of members of different castes may lead to divergent selective regimes, which may ultimately lead to morphological specialization and differentiation of the castes. This study used morphological and genetic analyses to identify traits that experienced caste‐specific selection in the social wasp Vespula maculifrons (Buysson, 1905). Traits putatively under selection were identified based on their degree of caste dimorphism, levels of variability, strength of correlations with other traits, and patterns of allometric scaling. Analyses of trait characteristics suggested that queen thorax length, thorax width, and possibly mass, have experienced queen‐specific selection. Additionally, trait dimorphism and intercaste phenotypic correlation values were negatively correlated, as expected if some morphological traits were subject to selection, leading to alternate phenotypic optima in the two castes. Overall, our analyses demonstrate how techniques used to identify selection between dimorphic groups can be applied to social species with distinct castes. In addition, our analyses suggest the operation of selection may be stronger in reproductive than in non‐reproductive castes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 93–102.     

Queen,worker, and male yellowjacket wasps receive different nutrition during development

Nutritional variation among developing larvae is a long-standing hypothesis for how a sterile caste could evolve, with larvae deprived of nutrition becoming sterile or not leaving the nest. In this study, we test whether the three castes of the eusocial yellowjacket wasp (Vespula maculifrons) differ in the trophic source of their larval diet, their overall carbon (C) and nitrogen (N) content, as well as the distribution of C and N across body parts. Virgin queens (gynes) assimilated food from a higher relative trophic level compared to males, and workers were the lowest. Gynes, due to their much greater mass compared to the other castes are much more costly in terms of N, but males have the lowest C:N ratio. The variation in C:N is likely due to differences in life history between males and females (gynes and workers), where females invest more in energy storage (e.g., lipids) compared to males which have very short life spans; the major difference is in the abdomen, where fat is stored. The results of this study complement similar results in ants, which evolved a reproductive division of labor independently, and which diverged from vespid wasps near 150 million years ago. Similarities between how wasp and ant caste determination occurs suggest either a conserved mechanism that predates the evolution of eusociality or convergence on the same mechanism for generating alternative phenotypes. Provisioning N-expensive castes with food from a higher trophic level likely increases efficiency of N delivery because of N-enrichment with increasing trophic level.