Beyond promiscuity: mate-choice commitments in social breeding

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female''s, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.     

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.     

The Soldiers in Societies: Defense,Regulation, and Evolution

The presence of reproductively altruistic castes is one of the primary traits of the eusocial societies. Adaptation and regulation of the sterile caste, to a certain extent, drives the evolution of eusociality. Depending on adaptive functions of the first evolved sterile caste, eusocial societies can be categorized into the worker-first and soldier-first lineages, respectively. The former is marked by a worker caste as the first evolved altruistic caste, whose primary function is housekeeping, and the latter is highlighted by a sterile soldier caste as the first evolved altruistic caste, whose task is predominantly colony defense. The apparent functional differences between these two fundamentally important castes suggest worker-first and soldier-first eusociality are potentially driven by a suite of distinctively different factors. Current studies of eusocial evolution have been focused largely on the worker-first Hymenoptera, whereas understanding of soldier-first lineages including termites, eusocial aphids, gall-dwelling thrips, and snapping shrimp, is greatly lacking. In this review, we summarize the current state of knowledge on biology, morphology, adaptive functions, and caste regulation of the soldier caste. In addition, we discuss the biological, ecological and genetic factors that might contribute to the evolution of distinct caste systems within eusocial lineages.     

The weird eusociality of polyembryonic parasites

Some parasitoid wasps possess soldier castes during their parasitic larval stage, but are often neglected from our evolutionary theories explaining caste systems in animal societies. This is primarily due to the polyembryonic origin of their societies. However, recent discoveries of polyembryonic trematodes (i.e. flatworms) possessing soldier castes require us to reconsider this reasoning. I argue we can benefit from including these polyembryonic parasites in eusocial discussions, for polyembryony and parasitism are taxonomically vast and influence the evolution of social behaviours and caste systems in various circumstances. Despite their polyembryony, their social evolution can be explained by theories of eusociality designed for parent–offspring groups, which are the subjects of most social evolution research. Including polyembryonic parasites in these theories follows the trend of major evolutionary transitions theory expanding social evolution research into all levels of biological organization. In addition, these continued discoveries of caste systems in parasites suggest social evolution may be more relevant to parasitology than currently acknowledged.     

Physiology as a caste-defining feature

Division of labour is a key factor in the ecological success of social insects. Groups of individuals specializing on a particular behaviour are known as castes and are usually distinguished by morphology or age. Physiology plays a key role in both these types of caste, in either the developmental physiology which determines morphology, or the temporal changes in physiology over an insect’s life. Physiological correlates of morphological or temporal caste include differences in gland structure, secretory products, leanness, neuroanatomy and neurochemistry. However, purely physiological castes could also occur. Physiological castes are discrete groups of same-age same-size individuals with particular physiological competencies, or groups of individuals with similar physiology crossing age or size groups. A stable physiological caste occurs in the monomorphic Pharaoh’s ant, where some ants can detect old pheromone trails and retain this specialization over time. These ants differ physiologically from other workers, and the differences arise before eclosion. More temporary physiological castes occur in the ant Ectatomma where brood care specialists have more developed ovarioles than other same-aged workers, and in the honeybee where nurses, wax-workers and soldiers all differ physiologically from same-aged nestmates. Physiology is an important aspect of caste, not only in its contribution to age-related and morphological castes, but also in its own right as a caste grouping factor. While age and morphological differences make caste structures accessible for study, more cryptic physiological castes may play just as important a role in division of labour. Received 19 December 2007; revised 24 July and 18 September 2008; accepted 19 September 2008.     

Building a new research framework for social evolution: intralocus caste antagonism

The breeding and non‐breeding ‘castes’ of eusocial insects provide a striking example of role‐specific selection, where each caste maximises fitness through different morphological, behavioural and physiological trait values. Typically, queens are long‐lived egg‐layers, while workers are short‐lived, largely sterile foragers. Remarkably, the two castes are nevertheless produced by the same genome. The existence of inter‐caste genetic correlations is a neglected consequence of this shared genome, potentially hindering the evolution of caste dimorphism: alleles that increase the productivity of queens may decrease the productivity of workers and vice versa, such that each caste is prevented from reaching optimal trait values. A likely consequence of this ‘intralocus caste antagonism’ should be the maintenance of genetic variation for fitness and maladaptation within castes (termed ‘caste load’), analogous to the result of intralocus sexual antagonism. The aim of this review is to create a research framework for understanding caste antagonism, drawing in part upon conceptual similarities with sexual antagonism. By reviewing both the social insect and sexual antagonism literature, we highlight the current empirical evidence for caste antagonism, discuss social systems of interest, how antagonism might be resolved, and challenges for future research. We also introduce the idea that sexual and caste antagonism could interact, creating a three‐way antagonism over gene expression. This includes unpacking the implications of haplodiploidy for the outcome of this complex interaction.     

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.     

Genetic variation in South Indian castes: evidence from Y-chromosome, mitochondrial, and autosomal polymorphisms

Background

Major population movements, social structure, and caste endogamy have influenced the genetic structure of Indian populations. An understanding of these influences is increasingly important as gene mapping and case-control studies are initiated in South Indian populations.

Results

We report new data on 155 individuals from four Tamil caste populations of South India and perform comparative analyses with caste populations from the neighboring state of Andhra Pradesh. Genetic differentiation among Tamil castes is low (R_ST = 0.96% for 45 autosomal short tandem repeat (STR) markers), reflecting a largely common origin. Nonetheless, caste- and continent-specific patterns are evident. For 32 lineage-defining Y-chromosome SNPs, Tamil castes show higher affinity to Europeans than to eastern Asians, and genetic distance estimates to the Europeans are ordered by caste rank. For 32 lineage-defining mitochondrial SNPs and hypervariable sequence (HVS) 1, Tamil castes have higher affinity to eastern Asians than to Europeans. For 45 autosomal STRs, upper and middle rank castes show higher affinity to Europeans than do lower rank castes from either Tamil Nadu or Andhra Pradesh. Local between-caste variation (Tamil Nadu R_ST = 0.96%, Andhra Pradesh R_ST = 0.77%) exceeds the estimate of variation between these geographically separated groups (R_ST = 0.12%). Low, but statistically significant, correlations between caste rank distance and genetic distance are demonstrated for Tamil castes using Y-chromosome, mtDNA, and autosomal data.

Conclusion

Genetic data from Y-chromosome, mtDNA, and autosomal STRs are in accord with historical accounts of northwest to southeast population movements in India. The influence of ancient and historical population movements and caste social structure can be detected and replicated in South Indian caste populations from two different geographic regions.     

Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis

Understanding how a single genome can produce a variety of different phenotypes is of fundamental importance in evolutionary and developmental biology. One of the most striking examples of phenotypic plasticity is the female caste system found in eusocial insects, where variation in reproductive (queens) and non-reproductive (workers) phenotypes results in a broad spectrum of caste types, ranging from behavioural through to morphological castes. Recent advances in genomic techniques allow novel comparisons on the nature of caste phenotypes to be made at the level of the genes in organisms for which there is little genome information, facilitating new approaches in studying social evolution and behaviour. Using the paper wasp Polistes canadensis as a model system, we investigated for the first time how behavioural castes in primitively eusocial insect societies are associated with differential expression of shared genes. We found that queens and newly emerged females express gene expression patterns that are distinct from each other whilst workers generally expressed intermediate patterns, as predicted by Polistes biology. We compared caste-associated genes in P. canadensis with those expressed in adult queens and workers of more advanced eusocial societies, which represent four independent origins of eusociality. Nine genes were conserved across the four taxa, although their patterns of expression and putative functions varied. Thus, we identify several genes that are putatively of evolutionary importance in the molecular biology that underlies a number of caste systems of independent evolutionary origin.     

Caste morphology and development in Termitogeton nr. planus (Insecta,Isoptera, Rhinotermitidae)

The termite family Rhinotermitidae displays a wide diversity in its patterns of social organization in castes. The genus Termitogeton probably branched off early in the evolution of this family. We studied the developmental pathways of a putative undescribed species from New Guinea, Termitogeton nr planus. The development begins with two white inactive instars (larvae), the second of which possesses small wing buds. These are followed by a relatively homogenous group of active immature stages (pseudergates) among which a biometric study revealed the presence of four instars. The first of these instars possesses wing buds that regress at subsequent molts. The external morphology of older instars resembles that of higher termite workers. Older pseudergates can differentiate into presoldiers and then into soldiers, but they are also able to molt into a unique stage with long wing pads (nymph), preceding the imago. Colony maturity can be reached with about 10(3) individuals. The sex ratio is near 1:1 in all castes except soldiers, among which females are more numerous than males. The caste pattern of T. nr. planus is reminiscent of those of the Kalotermitidae and Termopsidae, and of Prorhinotermes among the Rhinotermitidae. None of these taxa possess a true worker caste, permanently diverted from imaginal development: social tasks are done by unspecialized immatures that retain a full array of developmental options, including that of proceeding to the imago. The most remarkable trait of T. nr. planus is the presence in all second-instar individuals of wing buds that later regress to reappear in the single nymphal stage. We suggest that the traditional definitions of the terms larvae, nymphs, and pseudergates should be revised because they cannot be satisfactorily applied to the castes of Termitogeton.     

Incipient morphological castes in <Emphasis Type="Italic">Polistes gallicus</Emphasis> (Vespidae,Hymenoptera)

The occurrence of a pre-imaginal caste determination represents a sort of “point of no return” to eusociality. In some social insect taxa, including Polistes species, the occurrence of distinct queen and worker castes is still debated. Before this report, no clear morphological differences between reproductive and non-reproductive individuals were known. Here we show that several pre-imaginal morphological differences of the Van der Vecht organ occur between foundresses (queens) and workers. Geometric morphometrics revealed that queens are characterized by shape deformations of this organ, which is responsible for a typical allometric growth of the secretory area. This organ is predicted to be larger in foundresses compared to workers because its secretion is involved in defense against ants, in nestmate recognition and in preventing workers from challenging for direct reproduction. The results presented here indicate the existence of an incipient morphological caste determination Polistes gallicus and suggest that this species may have passed the “point of no return” for eusociality.     

Genomic imprinting and evolution of insect societies

Reproductive division of labor is a hallmark of social insect societies where individuals follow different developmental pathways resulting in distinct morphological castes. There has been a long controversy over the factors determining caste fate of individuals in social insects. Increasing evidence in the last two decades for heritable influences on division of labor put an end to the assumption that social insect broods are fully totipotent and environmental factors alone determine castes. Nevertheless, the genes that underlie hereditary effects on division of labor have not been identified in any social insects. Studies investigating the hereditary effects on caste determination might have overlooked non-genetic inheritance, while transmission to offspring of factors other than DNA sequences including epigenetic states can also affect offspring phenotype. Genomic imprinting is one of the most informative paradigms for understanding the consequences of interactions between the genome and the epigenome. Recent studies of genomic imprinting show that genes can be differentially marked in egg and sperm and inheritance of these epigenetic marks cause genes to be expressed in a parental-origin-specific manner in the offspring. By reviewing both the eusocial Hymenoptera and termites, I highlight the current theoretical and empirical evidence for genomic imprinting in eusocial insects and discuss how genomic imprinting acts in caste determination and social behavior and challenges for future studies. I also introduce the new idea that genomic imprinting plays an essential role in the origin of eusociality.     

Directional migration in the Hindu castes: inferences from mitochondrial, autosomal and Y-chromosomal data

Genetic, ethnographic, and historical evidence suggests that the Hindu castes have been highly endogamous for several thousand years and that, when movement between castes does occur, it typically consists of females joining castes of higher social status. However, little is known about migration rates in these populations or the extent to which migration occurs between caste groups of low, middle, and high social status. To investigate these aspects of migration, we analyzed the largest collection of genetic markers collected to date in Hindu caste populations. These data included 45 newly typed autosomal short tandem repeat polymorphisms (STRPs), 411 bp of mitochondrial DNA sequence, and 43 Y-chromosomal single-nucleotide polymorphisms that were assayed in more than 200 individuals of known caste status sampled in Andrah Pradesh, in South India. Application of recently developed likelihood-based analyses to this dataset enabled us to obtain genetically derived estimates of intercaste migration rates. STRPs indicated migration rates of 1–2% per generation between high-, middle-, and low-status caste groups. We also found support for the hypothesis that rates of gene flow differ between maternally and paternally inherited genes. Migration rates were substantially higher in maternally than in paternally inherited markers. In addition, while prevailing patterns of migration involved movement between castes of similar rank, paternally inherited markers in the low-status castes were most likely to move into high-status castes. Our findings support earlier evidence that the caste system has been a significant, long-term source of population structuring in South Indian Hindu populations, and that patterns of migration differ between males and females.     

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.     

Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation

More than a century ago, William Morton Wheeler proposed that social insect colonies can be regarded as superorganisms when they have morphologically differentiated reproductive and nursing castes that are analogous to the metazoan germ‐line and soma. Following the rise of sociobiology in the 1970s, Wheeler's insights were largely neglected, and we were left with multiple new superorganism concepts that are mutually inconsistent and uninformative on how superorganismality originated. These difficulties can be traced to the broadened sociobiological concept of eusociality, which denies that physical queen–worker caste differentiation is a universal hallmark of superorganismal colonies. Unlike early evolutionary naturalists and geneticists such as Weismann, Huxley, Fisher and Haldane, who set out to explain the acquisition of an unmated worker caste, the goal of sociobiology was to understand the evolution of eusociality, a broad‐brush convenience category that covers most forms of cooperative breeding. By lumping a diverse spectrum of social systems into a single category, and drawing attention away from the evolution of distinct quantifiable traits, the sociobiological tradition has impeded straightforward connections between inclusive fitness theory and the major evolutionary transitions paradigm for understanding irreversible shifts to higher organizational complexity. We evaluate the history by which these inconsistencies accumulated, develop a common‐cause approach for understanding the origins of all major transitions in eukaryote hierarchical complexity, and use Hamilton's rule to argue that they are directly comparable. We show that only Wheeler's original definition of superorganismality can be unambiguously linked to irreversible evolutionary transitions from context‐dependent reproductive altruism to unconditional differentiation of permanently unmated castes in the ants, corbiculate bees, vespine wasps and higher termites. We argue that strictly monogamous parents were a necessary, albeit not sufficient condition for all transitions to superorganismality, analogous to single‐zygote bottlenecking being a necessary but not sufficient condition for the convergent origins of complex soma across multicellular eukaryotes. We infer that conflict reduction was not a necessary condition for the origin of any of these major transitions, and conclude that controversies over the status of inclusive fitness theory primarily emanate from the arbitrarily defined sociobiological concepts of superorganismality and eusociality, not from the theory itself.     

Bigger Helpers in the Ant Cataglyphis bombycina: Increased Worker Polymorphism or Novel Soldier Caste?

Introduction

The mechanisms by which development favors or constrains the evolution of new phenotypes are incompletely understood. Polyphenic species may benefit from developmental plasticity not only regarding ecological advantages, but also potential for evolutionary diversification. For instance, the repeated evolution of novel castes in ants may have been facilitated by the existence of alternative queen and worker castes and their respective developmental programs.

Material and Methods

Cataglyphis bombycina is exceptional in its genus because winged queens and size-polymorphic workers occur together with bigger individuals having saber-shaped mandibles. We measured seven body parts in more than 150 individuals to perform a morphometric analysis and assess the developmental origin of this novel phenotype.

Results

Adults with saber-shaped mandibles differ from both workers and queens regarding the size of most body parts. Their relative growth rates are identical to workers for some pairs of body parts, and identical to queens for other pairs of body parts; critical sizes differ in all cases.

Conclusions

Big individuals are a third caste, i.e. soldiers, not major workers. Novel traits such as elongated mandibles are combined with a mix of queen and worker growth rates. We also reveal the existence of a dimorphism in the queen caste (microgynes and macrogynes). We discuss how novel phenotypes can evolve more readily in the context of an existing polyphenism. Both morphological traits and growth rules from existing queen and worker castes can be recombined, hence mosaic phenotypes are more likely to be viable. In C. bombycina, such a mosaic phenotype appears to function both for defense (saber-shaped mandibles) and fat storage (big abdomen). Recycling of developmental programs may have contributed to the morphological diversity and ecological success of ants.     

Origin and evolution of eusociality: a perspective from studying primitively eusocial wasps

Eusocial insects are those that show overlap of generations, cooperative brood care and reproductive caste differentiation. Of these, primitively eusocial insects show no morphological differences between reproductive and worker castes and exhibit considerable flexibility in the social roles that adult females may adopt. This makes them attractive model systems for investigations concerning the origin of eusociality. The rapidly accumulating information on primitively eusocial wasps suggests that haplodiploidy is unlikely to have an important role in the origin of eusociality. General kin selection (without help from haplodiploidy) could however have been an important factor due to the many advantages of group living. Pre-imaginal caste bias leading to variations in fertility is also likely to have some role. Because workers often have some chance of becoming reproductives in future, mutualism and other individual selection models suggest themselves as important factors. A hypothesis for the route to eusociality which focuses on the factors selecting for group living at different stages in social evolution is presented. It is argued that group living originates owing to the benefit of mutualism (the ‘Gambling Stage’) but parental manipulation and subfertility soon become important (the ‘Manipulation Stage’) and finally the highly eusocial state is maintained because genetic asymmetries created by haplodiploidy are exploited by kin recognition (the ‘Recognition Stage’).     

Resolving the evolution of sterile worker castes: a window on the advantages and disadvantages of monogamy

Many social Hymenoptera species have morphologically sterile worker castes. It is proposed that the evolutionary routes to this obligate sterility must pass through a ‘monogamy window’, because inclusive fitness favours individuals retaining their reproductive totipotency unless they can rear full siblings. Simulated evolution of sterility, however, finds that ‘point of view’ is critically important. Monogamy is facilitating if sterility is expressed altruistically (i.e. workers defer reproduction to queens), but if sterility results from manipulation by mothers or siblings, monogamy may have no effect or lessen the likelihood of sterility. Overall, the model and data from facultatively eusocial bees suggest that eusociality and sterility are more likely to originate through manipulation than by altruism, casting doubt on a mandatory role for monogamy. Simple kin selection paradigms, such as Hamilton''s rule, can also fail to account for significant evolutionary dynamics created by factors, such as population structure, group-level effects or non-random mating patterns. The easy remedy is to always validate apparently insightful predictions from Hamiltonian equations with life-history appropriate genetic models.     

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.