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Phylogeny of eusocial Lasioglossum reveals multiple losses of eusociality within a primitively eusocial clade of bees (Hymenoptera: Halictidae).

We performed a phylogenetic analysis of the species, species groups, and subgenera within the predominantly eusocial lineage of Lasioglossum (the Hemihalictus series) based on three protein coding genes: mitochondrial cytochrome oxidase I, nuclear elongation factor 1alpha and long-wavelength rhodopsin. The entire data set consisted of 3421 aligned nucleotide sites, 854 of which were parsimony informative. Analyses by equal weights parsimony, maximum likelihood, and Bayesian methods yielded good resolution among the 53 taxa/populations, with strong bootstrap support and high posterior probabilities for most nodes. There was no significant incongruence among genes, and parsimony, maximum likelihood, and Bayesian methods yielded congruent results. We mapped social behavior onto the resulting tree for 42 of the taxa/populations to infer the likely history of social evolution within Lasioglossum. Our results indicate that eusociality had a single origin within Lasioglossum. Within the predominantly eusocial clade, however, there have been multiple (six) reversals from eusociality to solitary nesting, social polymorphism, or social parasitism, suggesting that these reversals may be more common in primitively eusocial Hymenoptera than previously anticipated. Our results support the view that eusociality is hard to evolve but easily lost. This conclusion is potentially important for understanding the early evolution of the advanced eusocial insects, such as ants, termites, and corbiculate bees.

Animals↗

Evolution of sociality in a primitively eusocial lineage of bees.

Eusociality is a major evolutionary innovation involving alterations in life history, morphology, and behavior. Advanced eusocial insects, such as ants, termites, and corbiculate bees, cannot provide insights into the earliest stages of eusocial evolution because eusociality in these taxa evolved long ago (in the Cretaceous) and close solitary relatives are no longer extant. In contrast, primitively eusocial insects, such as halictid bees, provide insights into the early stages of eusocial evolution because eusociality has arisen recently and repeatedly. By mapping social behavior onto well-corroborated phylogenies, I show that eusociality has arisen only three times within halictid bees (contrary to earlier estimates of six or more origins). Reversals from eusocial to solitary behavior have occurred as many as 12 times, indicating that social reversals are common in the earliest stages of eusocial evolution. Important attributes of social complexity (e.g., colony size, queen/worker dimorphism) show no obvious association with phylogeny, and some reversals to solitary nesting are related to host-plant switches (from polylecty to oligolecty). These results provide a glimpse of social evolution in its earliest stages and provide insights into the early evolution of advanced eusocial organisms.

Animals↗

Recent and simultaneous origins of eusociality in halictid bees.

Eusocial organisms are characterized by cooperative brood care, generation overlap and reproductive division of labour. Traits associated with eusociality are most developed in ants, termites, paper wasps and corbiculate bees; the fossil record indicates that each of these advanced eusocial taxa evolved in the Late Cretaceous or earlier (greater than 65 Myr ago). Halictid bees also include a large and diverse number of eusocial members, but, in contrast to advanced eusocial taxa, they are characterized by substantial intra- and inter-specific variation in social behaviour, which may be indicative of more recent eusocial evolution. To test this hypothesis, we used over 2400 bp of DNA sequence data gathered from three protein-coding nuclear genes (opsin, wingless and EF-1a) to infer the phylogeny of eusocial halictid lineages and their relatives. Results from relaxed molecular clock dating techniques that utilize a combination of molecular and fossil data indicate that the three independent origins of eusociality in halictid bees occurred within a narrow time frame between approximately 20 and 22 Myr ago. This relatively recent evolution helps to explain the pronounced levels of social variation observed within these bees. The three origins of eusociality appear to be temporally correlated with a period of global warming, suggesting that climate may have had an important role in the evolution and maintenance of eusociality in these bees.

Animals↗

Evaluating alternative hypotheses for the origin of eusociality in corbiculate bees.

We use a likelihood-based statistical test to evaluate the extent to which the available molecular data sets can be used to falsify alternative phylogenetic hypotheses describing the inter-relationship among corbiculate bee tribes. Based on the results of this test, we explore three alternative models of behavioural character state evolution and evaluate the support each model has for single-origin versus dual-origin hypotheses for 'highly' eusocial behaviour. We show that only one of four data sets could statistically reject any of the 15 possible outgroup-rooted phylogenetic hypotheses. However, a cytochrome b data set rejected all but three alternative topologies. Using this information, a simple model of behavioural character state evolution, in which transitions between solitary/communal, 'primitively' eusocial, and 'highly' eusocial are unconstrained, supports single-origin hypotheses for 'highly' eusocial behaviour, in spite of phylogenetic uncertainty. By contrast, an ordered model, in which 'highly' eusocial is constrained to be an evolutionarily terminal state, supports a dual-origins hypothesis. Our results show that the molecular phylogenetic evidence favouring a dual-origins hypothesis for 'highly' eusocial behaviour is, at present, conditional on information from one gene (cyt b) and on specific, though likely realistic, assumptions regarding the nature of eusocial evolution.

Animals↗

High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips.

Within the haplodiploid eusocial gall-inducing thrips, a species-level phylogeny combined with genetic data for five eusocial species enables an inference of levels of relatedness and inbreeding values for lineages at the origin of eusociality. Character optimization using data from five eusocial species indicates that the lineage or lineages where eusociality is inferred to have originated exhibit relatedness of 0.64-0.92, and F(IS) of 0.33-0.64. The high inbreeding coefficients found in these eusocial thrips have increased relatedness among and within both sexes and have reduced the haplodiploidy-induced relatedness asymmetries [Hamilton, W. D. (1964) J. Theor. Biol. 7, 1-52]. These results indicate that unusually high relatedness is associated with the origin of eusociality, and they suggest a role for inbreeding in the evolution of bisexual helping.

Acacia↗

A novel social polymorphism in a primitively eusocial bee.

Halictine sweat bees (Hymenoptera, Halictidae) are model organisms for the evolution of altruism, reproductive castes, and eusocial colony organization. Halictine social behavior is not only extremely variable, but also ecologically and evolutionarily labile. Among social species, colony social organization ranges from communal societies of egalitarian females to eusocial and semisocial ones with reproductive queens and more or less sterile workers. A striking aspect of halictine social variation is the mutual exclusivity of communal and eusocial types of colony social organization within the same species, these two types of social behavior being characteristic of different genera and subgenera. We report a recently discovered exception to this rule in a population of Halictus sexcinctus (Fabricius) at Daimonia-Pyla in southern Greece, that contained both communal and eusocial colonies. Moreover, communal and eusocial females exhibit morphological differences that imply a preimaginal developmental switch, which could also underlie the two types of social behavior. That the communal and eusocial forms are not merely cryptic sister species with different social behavior is indicated by the comparison of mitochondrial DNA sequences of two sections of cytochrome oxidase I, which indicate that Greek specimens of both social types are more similar than they are to conspecifics from elsewhere in Europe. The phylogenetic position of Halictus sexcinctus suggests that this unusual communal/eusocial polymorphism may represent an unstable intermediate step in an evolutionary reversal from eusocial to solitary behavior.

Animals↗

Monophyly and extensive extinction of advanced eusocial bees: insights from an unexpected Eocene diversity.

Advanced eusociality sometimes is given credit for the ecological success of termites, ants, some wasps, and some bees. Comprehensive study of bees fossilized in Baltic amber has revealed an unsuspected middle Eocene (ca. 45 million years ago) diversity of eusocial bee lineages. Advanced eusociality arose once in the bees with significant post-Eocene losses in diversity, leaving today only two advanced eusocial tribes comprising less than 2% of the total bee diversity, a trend analogous to that of hominid evolution. This pattern of changing diversity contradicts notions concerning the role of eusociality for evolutionary success in insects.

Animals↗

Juvenile hormone in adult eusocial Hymenoptera: gonadotropin and behavioral pacemaker.

Studies on the role of juvenile hormone (JH) in adult social Hymenoptera have focused on the regulation of two fundamental aspects of colony organization: reproductive division of labor between queens and workers and age-related division of labor among workers. JH acts as a gonadotropin in the primitively eusocial wasp and bumble bee species studied, and may also play this role in the advanced eusocial fire ants. However, there is no evidence that JH acts as a traditional gonadotropin in the advanced eusocial honey bee or in the few other ant species that have recently begun to be studied. The role of JH in age-related division of labor has been most thoroughly examined in honey bees. Results of these studies demonstrate that JH acts as a "behavioral pacemaker," influencing how fast a worker grows up and makes the transition from nest activities to foraging. Hypotheses concerning the evolutionary relationship between the two functions of JH in adult eusocial Hymenoptera are discussed.

Age Factors↗

Testing kin selection with sex allocation data in eusocial hymenoptera

Sex allocation data in eusocial Hymenoptera (ants, bees and wasps) provide an excellent opportunity to assess the effectiveness of kin selection, because queens and workers differ in their relatedness to females and males. The first studies on sex allocation in eusocial Hymenoptera compared population sex investment ratios across species. Female-biased investment in monogyne (= with single-queen colonies) populations of ants suggested that workers manipulate sex allocation according to their higher relatedness to females than males (relatedness asymmetry). However, several factors may confound these comparisons across species. First, variation in relatedness asymmetry is typically associated with major changes in breeding system and life history that may also affect sex allocation. Secondly, the relative cost of females and males is difficult to estimate across sexually dimorphic taxa, such as ants. Thirdly, each species in the comparison may not represent an independent data point, because of phylogenetic relationships among species. Recently, stronger evidence that workers control sex allocation has been provided by intraspecific studies of sex ratio variation across colonies. In several species of eusocial Hymenoptera, colonies with high relatedness asymmetry produced mostly females, in contrast to colonies with low relatedness asymmetry which produced mostly males. Additional signs of worker control were found by investigating proximate mechanisms of sex ratio manipulation in ants and wasps. However, worker control is not always effective, and further manipulative experiments will be needed to disentangle the multiple evolutionary factors and processes affecting sex allocation in eusocial Hymenoptera.

Journal Article↗

Eusociality: origin and consequences.

In this new assessment of the empirical evidence, an alternative to the standard model is proposed: group selection is the strong binding force in eusocial evolution; individual selection, the strong dissolutive force; and kin selection (narrowly defined), either a weak binding or weak dissolutive force, according to circumstance. Close kinship may be more a consequence of eusociality than a factor promoting its origin. A point of no return to the solitary state exists, as a rule when workers become anatomically differentiated. Eusociality has been rare in evolution, evidently due to the scarcity of environmental pressures adequate to tip the balance among countervailing forces in favor of group selection. Eusociality in ants and termites in the irreversible stage is the key to their ecological dominance and has (at least in ants) shaped some features of internal phylogeny. Their colonies are consistently superior to solitary and preeusocial competitors, due to the altruistic behavior among nestmates and their ability to organize coordinated action by pheromonal communication.

Animals↗

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.

Adaptation, Physiological↗

Multiple origins of eusociality among sponge-dwelling shrimps (Synalpheus).

As the most extreme expression of apparent altruism in nature, eusociality has long posed a central paradox for behavioral and evolutionary ecology. Because eusociality has arisen rarely among animals, understanding the selective pressures important in early stages of its evolution remains elusive. Employing a historical approach to this problem, we used morphology and DNA sequences to reconstruct the phylogeny of 13 species of sponge-dwelling shrimps (Synalpheus) with colony organization ranging from asocial pair-bonding through eusociality. We then used phylogenetically independent contrasts to test whether sociality was associated with evidence of enhanced competitive ability, as suggested by hypotheses invoking an advantage of cooperation in crowded habitats. The molecular, morphological, and combined data each strongly supported three independent origins of monogynous, multigenerational (eusocial) colony organization within this genus. Phylogenetically independent contrasts confirmed that highly social taxa, with strong reproductive skew, have significantly higher relative abundance within the host sponge than do less social taxa, a result that was robust to uncertainty in tree topology and varying models of character change. A similar tendency for highly social species to share their sponge with fewer congener species was suggestive, but not significant. Because unoccupied habitat appears to be limiting for many sponge-dwelling shrimp species, these data are consistent with hypotheses that cooperative social groups enjoy a competitive advantage over less organized groups or individuals, where independent establishment is difficult, and that enemy pressure is of central importance in the evolution of animal sociality.

Animals↗

Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae).

Wasps (Vespidae) exhibit a range of social complexity, from solitary living to eusocial colonies, and thus are exemplary for studies of the evolutionary origin and maintenance of social behavior in animals. Integral to the definition of eusociality is the presence of reproductive castes, group members that differ qualitatively in their ability to reproduce in a social setting. Behavioral and morphological evidence suggests that caste determination, the developmental process by which differences in fecundity are established, occurs to a large extent before adult emergence (pre-imaginally) in many species of Vespidae, in both basal and advanced taxa within the clade (Vespinae+Polistinae), which includes most eusocial species. Pre-imaginal determination has been documented in many taxa (e.g. independent-founding Polistinae) where it was not thought to occur. Correlative and experimental studies indicate that differences in nutrition during larval development are often the basis of pre-imaginal caste determination. Pre-imaginal caste determination has important implications for the roles of subfertility and manipulation by nest mates in the evolution of eusocial behavior.

Journal Article↗

Helping behaviour in facultatively eusocial hover wasps: an experimental test of the subfertility hypothesis.

A candidate explanation for the evolution of eusociality is that helpers are physiologically constrained such that helping is their only realistic option. We tested this subfertility hypothesis in a species of facultatively eusocial hover wasp (Hymenoptera, Stenogastrinae: Liostenogaster flavolineata) by seeing whether helpers that were forced to nest on their own were able to mature their own eggs. One focal helper was left alone on each of 22 nests, from which all other adult wasps (including the dominant) were permanently removed. After 18 days, all but one of the 19 focal helpers that remained on their nests had ovarian development and insemination status characteristic of dominants, and the majority had probably laid eggs. This was in striking contrast to the reproductive status of other helpers removed from the same nests at the start of the experiment. These results provide convincing experimental evidence that females do not become helpers because of some unconditional physiological constraint. There is currently no unequivocal support for the subfertility hypothesis in facultatively eusocial Hymenoptera lacking morphological castes. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

Juvenile hormone accelerates ovarian development and does not affect age polyethism in the primitively eusocial wasp, Ropalidia marginata.

Juvenile hormone modulates post-imaginal reproductive division of labor in primitively eusocial species and promotes the production of queens (e.g., Polistes) while it modulates age polyethism and promotes the production of foragers in highly eusocial species (e.g., the honey bee). Ropalidia marginata is a primitively eusocial wasp that shows both post-imaginal regulation of reproductive division of labor as well as age polyethism. Hence, R.marginata is a particularly interesting model system to study the effect of juvenile hormone. We demonstrate here that a single, topical application of 100 micro g of juvenile hormone-III per female wasp accelerates ovarian development of wasps held in isolation. Similar application to wasps released back on to their natal nests has no effect on their rate of behavioral development as witnessed from the age of first performance of feed larva, build, bring pulp and bring food. We conclude therefore that in R.marginata, juvenile hormone has retained its function of modulating reproductive division of labor and has not acquired the function of modulating age polyethism.

Aging↗

Some conceptual issues in the origin of eusociality.

Certain issues arising in connection with the evolutionary origins of eusociality are discussed. Previous results about when natural selection favours helping behaviour are generlised, and the differing viewpoints of both parents and offspring are considered. Particular attention is given to the evolutionary implications of different patterns of overlapping generations observed in bivoltine insects. As argued by Seger (1983), these patterns imply different conditions under which a daughter is selected to help her mother rear additional siblings in haplodiploid populations. Other factors that can alter the selective advantages of helping behaviour under haplodiploidy are also discussed, including the possibility of sex ratio manipulation and the novel result that helping behaviour may be locally favoured in populations that are spatially patchy with respect to sex-specific fitness. A new hypothesis is also presented: The fact that sisters are selected to aid their mother to parasitise other sisters may have played an important role in the origins of eusociality. A given offspring benefits from having maternally parasitised siblings because such siblings rear additional siblings (to which the given offspring is more closely related) instead of nieces and nephews. Finally, the importance of haploidiploidy in the origins of eusociality is discounted; the virtually unique biology of aculeate Hymenoptera would seem to be of much greater importance.

Animals↗

Social parasitism by male-producing reproductive workers in a eusocial insect.

The evolution of extreme cooperation, as found in eusocial insects (those with a worker caste), is potentially undermined by selfish reproduction among group members. In some eusocial Hymenoptera (ants, bees and wasps), workers can produce male offspring from unfertilized eggs. Kin selection theory predicts levels of worker reproduction as a function of the relatedness structure of the workers' natal colony and the colony-level costs of worker reproduction. However, the theory has been only partially successful in explaining levels of worker reproduction. Here we show that workers of a eusocial bumble bee (Bombus terrestris) enter unrelated, conspecific colonies in which they then produce adult male offspring, and that such socially parasitic workers reproduce earlier and are significantly more reproductive and aggressive than resident workers that reproduce within their own colonies. Explaining levels of worker reproduction, and hence the potential of worker selfishness to undermine the evolution of cooperation, will therefore require more than simply a consideration of the kin-selected interests of resident workers. It will also require knowledge of the full set of reproductive options available to workers, including intraspecific social parasitism.

Aggression↗

Evolution of eusociality in termites.

A model is presented that demonstrates that asymmetries in relatedness such that individuals are more closely related to siblings than to offspring develop in diploid pedigrees under conditions of inbreeding. Given also certain incestuous conditions, the model predicts that eusocial-type helping behavior can be favored by natural selection. Three cases of the model are discussed along with implications for termite eusociality. Several aspects of termite biology, particularly the existence of replacement reproductives, are interpreted as evidence that termite eusociality may have arisen under the special conditions specified in the models.

Journal Article↗