Behavioral Phylogeny of Corbiculate Apidae (Hymenoptera; Apinae), with Special Reference to Social Behavior

The phylogenetic relationships among the four tribes of corbiculate bees (Euglossini, Bombini, Meliponini, and Apini) are controversial. There is substantial incongruence between morphological and molecular data, and the single origin of eusociality is questionable. The use of behavioral characters by previous workers has been restricted to some typological definitions, such as solitary and eusocial. Here, I expand the term "social" to 42 characters and present a tree based only on behavioral characters. The reconstructed relationships were similar to those observed in morphological and "total evidence" analyses, i.e., Euglossini + (Bombini + (Meliponini + Apini)), all of which support a single origin of eusociality.     

Phylogenetic relationships within the corbiculate Apinae (Hymenoptera) and the evolution of eusociality

We provide a comparison of 520 base pairs of the mitochondrial cytochrome b gene from exemplars of the Meliponini, the Apini, the Bombini and the Euglossini to determine the phylogenetic relationships within the corbiculate Apinae. Our results strongly suggest (91–97% according to bootstrap resampling) that the Meliponini and the Bombini are sister groups. This finding agrees with those of other molecular studies, but is discordant with previous hypotheses based on morphology and the combination of molecular and morphological data. If the Bombini and Meliponini are sister groups and reversal of advanced eusociality is unlikely, then advanced eusociality arose twice within this clade. However, if reversion of eusociality occurred, then it is not possible to discriminate between single or dual origins of advanced eusociality within this group.     

Cladistic analysis of self‐grooming indicates a single origin of eusociality in corbiculate bees (Hymenoptera: Apidae)

Behavioural traits have been used extensively in recent years as an important character source for making phylogenetic inferences. The phylogenetic positions of the members of the Apini subtribe are increasingly being debated, and new characters must be examined. We analysed the presence and absence of certain behavioural patterns, as well as the sequences of some of these patterns, to generate 79 characters. Eleven species comprised the ingroup, and Xylocopini comprised the outgroup. Parsimony analysis showed that the most parsimonious tree was (Euglossina(Bombina(Apina+Meliponina))). This topology is consistent with most studies that use morphological data and the few that use behavioural data, which suggests that advanced eusociality arose only once in a common ancestor of the clade Apina plus Meliponina; however, this hypothesis is inconsistent with our molecular data. Thus we considered behavioural, molecular, and morphological data and recovered the same topology, in which eusociality has a single origin in corbiculate bees.     

Forum: The eusociality continuum

Eusocial societies are traditionally characterized by a reproductivedivision of labor, an overlap of generations, and cooperativecare of the breeders' young. Eusociality was once thought tooccur only in termites, ants, and some bee and wasp species,but striking evolutionary convergences have recently becomeapparent between the societies of these insects and those ofcooperatively breeding birds and mammals. These parallels haveblurred distinctions between cooperative breeding and eusociality,leading to calls for either drastically restricting or expandingusage of these terms. We favor the latter approach. Cooperativebreeding and eusociality are not discrete phenomena, but ratherform a continuum of fundamentally similar social systems whosemain differences lie in the distribution of lifetime reproductivesuccess among group members. Therefore we propose to array vertebrateand invertebrate cooperative breeders along a common axis, representinga standardized measure of reproductive variance, and to dropsuch (loaded) terms as "primitive" and "advanced" eusociality.The terminology we propose unites all occurrences of alloparentalhelping of kin under a single theoretical umbrella (e.g., Hamilton'srule). Thus, cooperatively breeding vertebrates can be regardedas eusocial, just as eusocial invertebrates are cooperativebreeders. We believe this integrated approach will foster potentiallyrevealing cross-taxon comparisons, which are essential to understandingsocial evolution in birds, mammals, and insects.     

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.     

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.     

A conceptual model for the origin of worker behaviour and adaptation of eusociality

In a model based on the wasp family Vespidae, the origin of worker behaviour, which constitutes the eusociality threshold, is not based on relatedness, therefore the origin of eusociality does not depend on inclusive fitness, and workers at the eusociality threshold are not altruistic. Instead, incipient workers and queens behave selfishly and are subject to direct natural selection. Beyond the eusociality threshold, relatedness enables 'soft inheritance' as the framework for initial adaptations of eusociality. At the threshold of irreversibility, queen and worker castes become fixed in advanced eusociality. Transitions from solitary to facultative, facultative to primitive, and primitive to advanced eusociality occur via exaptation, phenotypic accommodation and genetic assimilation. Multilevel selection characterizes the solitary to highly eusocial transition, but components of multilevel selection vary across levels of eusociality. Roles of behavioural flexibility and developmental plasticity in the evolutionary process equal or exceed those of genotype.     

Haplodiploidy and the evolution of eusociality: split sex ratios

It is generally accepted that from a theoretical perspective, haplodiploidy should facilitate the evolution of eusociality. However, the "haplodiploidy hypothesis" rests on theoretical arguments that were made before recent advances in our empirical understanding of sex allocation and the route by which eusociality evolved. Here we show that several possible promoters of the haplodiploidy effect would have been unimportant on the route to eusociality, because they involve traits that evolved only after eusociality had become established. We then focus on two biological mechanisms that could have played a role: split sex ratios as a result of either queen virginity or queen replacement. We find that these mechanisms can lead haplodiploidy to facilitating the evolution of helping but that their importance varies from appreciable to negligible, depending on the assumptions. Furthermore, under certain conditions, haplodiploidy can even inhibit the evolution of helping. In contrast, we find that the level of promiscuity has a strong and consistently negative influence on selection for helping. Consequently, from a relatedness perspective, monogamy is likely to have been a more important driver of eusociality than the haplodiploidy effect.     

Eusociality Shapes Convergent Patterns of Molecular Evolution across Mitochondrial Genomes of Snapping Shrimps

Eusociality is a highly conspicuous and ecologically impactful behavioral syndrome that has evolved independently across multiple animal lineages. So far, comparative genomic analyses of advanced sociality have been mostly limited to insects. Here, we study the only clade of animals known to exhibit eusociality in the marine realm—lineages of socially diverse snapping shrimps in the genus Synalpheus. To investigate the molecular impact of sociality, we assembled the mitochondrial genomes of eight Synalpheus species that represent three independent origins of eusociality and analyzed patterns of molecular evolution in protein-coding genes. Synonymous substitution rates are lower and potential signals of relaxed purifying selection are higher in eusocial relative to noneusocial taxa. Our results suggest that mitochondrial genome evolution was shaped by eusociality-linked traits—extended generation times and reduced effective population sizes that are hallmarks of advanced animal societies. This is the first direct evidence of eusociality impacting genome evolution in marine taxa. Our results also strongly support the idea that eusociality can shape genome evolution through profound changes in life history and demography.     

Advanced eusociality, kin selection and male haploidy

Abstract  The generation-long primacy of kin selection in explaining the evolution of advanced eusociality in social insects has been challenged in recent papers. Does this challenge succeed? I consider three questions: is kin selection still the unchallengeable explanation for the evolution of eusociality; is the male haploidy of Hymenoptera important in this explanation; and, a subsidiary question of why are there no male workers in Hymenoptera? I briefly trace the origins of kin selection back to Darwin and then consider the explanations of mutualism, group selection, parental manipulation, and kin selection and its variant 'green beard' alleles. I stress that in the kin selection equation, however written, relatedness is deeply intertwined with ecology so that both are essential. Kin selection does remain unchallengeable but, for some, the role of male haploidy has lost favour recently despite several modelling efforts all finding that it favours the evolution of eusociality. Sex allocation is deep at the heart of the evolution of hymenopteran advanced eusociality, indicating the interacting roles of population genetics and general biology. Modellers have also found no reason for a lack of male workers, so that a biological superiority of females for this role is indicated for social Hymenoptera.     

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.     

Kinship,parental manipulation and evolutionary origins of eusociality

One of the hallmarks of eusociality is that workers forego their own reproduction to assist their mother in raising siblings. This seemingly altruistic behaviour may benefit workers if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If worker presence is advantageous to mothers, however, eusociality may evolve without net benefits to workers. Indirect fitness benefits are often cited as evidence for the importance of inclusive fitness in eusociality, but have rarely been measured in natural populations. We compared inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusociality is optional. Our results show that workers have significantly lower inclusive fitness than females that found their own nests. In mathematical simulations based on M. genalis field data, eusociality cannot evolve with reduced intra-nest relatedness. The simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when helping behaviour was simulated as the result of maternal manipulation, but not as worker altruism. Thus, eusociality in M. genalis is best explained through kin selection, but the underlying mechanism is likely maternal manipulation.     

The antiquity and evolutionary history of social behavior in bees

A long-standing controversy in bee social evolution concerns whether highly eusocial behavior has evolved once or twice within the corbiculate Apidae. Corbiculate bees include the highly eusocial honey bees and stingless bees, the primitively eusocial bumble bees, and the predominantly solitary or communal orchid bees. Here we use a model-based approach to reconstruct the evolutionary history of eusociality and date the antiquity of eusocial behavior in apid bees, using a recent molecular phylogeny of the Apidae. We conclude that eusociality evolved once in the common ancestor of the corbiculate Apidae, advanced eusociality evolved independently in the honey and stingless bees, and that eusociality was lost in the orchid bees. Fossil-calibrated divergence time estimates reveal that eusociality first evolved at least 87 Mya (78 to 95 Mya) in the corbiculates, much earlier than in other groups of bees with less complex social behavior. These results provide a robust new evolutionary framework for studies of the organization and genetic basis of social behavior in honey bees and their relatives.     

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’).     

TRAIT MAPPING AND SALIENCE IN THE EVOLUTION OF EUSOCIAL VESPID WASPS

The multiple independent origins of eusociality in the insect order Hymenoptera are clustered in only four of more than 80 families, and those four families are two pairs of closely related taxa in a single part of the order. Therefore, although ordinal-level characteristics can contribute to hymenopteran eusocial evolution, more important roles have been played by traits of infraordinal taxa that contain the eusocial forms. Many factors have been proposed and discussed, but assessments of traits' salience to eusocial evolution have heretofore not been joined to phylogenetics. In the present analysis, cladograms of superfamilies and families of Hymenoptera and of the family Vespidae are used to ordinate the appearance of traits that play roles in vespid eusociality. Proximity of traits' first appearance to the origin of eusocial Vespidae is taken as one measure of traits' salience to vespid eusocial evolution. Traits that subtend only eusocial taxa and that are uniquely associated with eusociality have foundations in more general traits that subtend more inclusive taxa. No single trait is uniquely causative of vespid eusocial evolution. High-salience traits that closely subtend vespid eusociality include nesting, oviposition into an empty nest cell, progressive provisioning of larvae, adult nourishment during larval provision malaxation, and inequitable food distribution among nestmates. The threshold characteristic of Polistes-grade eusociality is life-long alloparental brood care by first female offspring who remain, uninseminated, at their natal nest. Traits directly associated with occurrence of such workers are larva-adult trophallaxis, which can foster relatively low larval nourishment early in a colony cycle, and protogyny and direct larval development, which combine to yield restricted mating opportunities for female offspring that are the first to emerge in the colony cycle. Trait mapping suggests no role for asymmetry of relatedness due to haplodiploidy, but it suggests high salience for haplodiploidy as a mechanism enabling the production of all-female clutches of first offspring.     

Evolution of eusociality in diploid species

Haplodiploid species are naturally biased by their genetic structure toward the evolution of sterile worker castes, as shown by W. D. Hamilton (1964. J. Theoret. Biol., 7, 1–16, 17–52). Diploid species do not have this intrinsic genetic bias toward eusociality. Nonetheless, true sociality has evolved in the diploid ancestors of the modern termites, and varying degrees of quasisociality are not uncommon in diploid species, including mammals. A genetic bias toward investment in relatives rather than offspring can arise in a diploid species as a result of inbreeding. The consequences of several regular incestuous breeding systems are analyzed in detail. It is shown that, under certain conditions, there is a natural bias toward an alternation of inbred and outbred generations. As this alternation proceeds, the genetic bias toward eusociality rapidly approaches an asymptotic value of 4(1 + 2f₀)/3(1 + 3f₀), where f₀ is the average coefficient of relationship for the outbreeding pairs. For f₀ close to zero, the genetic bias toward eusociality is close to 1.33, which is even larger than the genetic bias of 1.25 in haplodiploid species. Under other conditions there may be repeated incestuous matings between successive outbreeding generations. In this case the bias toward eusociality can be as large as 2.     

Molecular phylogeny of the carnivora (mammalia): assessing the impact of increased sampling on resolving enigmatic relationships

This study analyzed 76 species of Carnivora using a concatenated sequence of 6243 bp from six genes (nuclear TR-i-I, TBG, and IRBP; mitochondrial ND2, CYTB, and 12S rRNA), representing the most comprehensive sampling yet undertaken for reconstructing the phylogeny of this clade. Maximum parsimony and Bayesian methods were remarkably congruent in topologies observed and in nodal support measures. We recovered all of the higher level carnivoran clades that had been robustly supported in previous analyses (by analyses of morphological and molecular data), including the monophyly of Caniformia, Feliformia, Arctoidea, Pinnipedia, Musteloidea, Procyonidae + Mustelidae sensu stricto, and a clade of (Hyaenidae + (Herpestidae + Malagasy carnivorans)). All of the traditional "families," with the exception of Viverridae and Mustelidae, were robustly supported as monophyletic groups. We further have determined the relative positions of the major lineages within the Caniformia, which previous studies could not resolve, including the first robust support for the phylogenetic position of marine carnivorans (Pinnipedia) within the Arctoidea (as the sister-group to musteloids [sensu lato], with ursids as their sister group). Within the pinnipeds, Odobenidae (walrus) was more closely allied with otariids (sea lions/fur seals) than with phocids ("true" seals). In addition, we recovered a monophyletic clade of skunks and stink badgers (Mephitidae) and resolved the topology of musteloid interrelationships as: Ailurus (Mephitidae (Procyonidae, Mustelidae [sensu stricto])). This pattern of interrelationships of living caniforms suggests a novel inference that large body size may have been the primitive condition for Arctoidea, with secondary size reduction evolving later in some musteloids. Within Mustelidae, Bayesian analyses are unambiguous in supporting otter monophyly (Lutrinae), and in both MP and Bayesian analyses Martes is paraphyletic with respect to Gulo and Eira, as has been observed in some previous molecular studies. Within Feliformia, we have confirmed that Nandinia is the outgroup to all other extant feliforms, and that the Malagasy Carnivora are a monophyletic clade closely allied with the mongooses (Herpestidae [sensu stricto]). Although the monophyly of each of the three major feliform clades (Viverridae sensu stricto, Felidae, and the clade of Hyaenidae + (Herpestidae + Malagasy carnivorans)) is robust in all of our analyses, the relative phylogenetic positions of these three lineages is not resolvable at present. Our analyses document the monophyly of the "social mongooses," strengthening evidence for a single origin of eusociality within the Herpestidae. For a single caniform node, the position of pinnipeds relative to Ursidae and Musteloidea, parsimony analyses of data for the entire Carnivora did not replicate the robust support observed for both parsimony and Bayesian analyses of the caniform ingroup alone. More detailed analyses and these results demonstrate that outgroup choice can have a considerable effect on the strength of support for a particular topology. Therefore, the use of exemplar taxa as proxies for entire clades with diverse evolutionary histories should be approached with caution.The Bayesian analysis likelihood functions generally were better able to reconstruct phylogenetic relationships (increased resolution and more robust support for various nodes) than parsimony analyses when incompletely sampled taxa were included. Bayesian analyses were not immune, however, to the effects of missing data; lower resolution and support in those analyses likely arise from non-overlap of gene sequence data among less well-sampled taxa. These issues are a concern for similar studies, in which different gene sequences are concatenated in an effort to increase resolving power.     

Brood care and social evolution in termites

Cooperative brood care is assumed to be the common driving factor leading to sociality. While this seems to be true for social Hymenoptera and many cooperatively breeding vertebrates, the importance of brood care for the evolution of eusociality in termites is unclear. A first step in elucidating this problem is an assessment of the ancestral condition in termites. We investigated this by determining the overall level of brood care behaviour across four termite species that cover the phylogenetic diversity of the lower termites. Brood care was low in the three species (all from different families) that had an ancestral wood-dwelling lifestyle of living in a single piece of wood that serves as food and shelter. In the fourth species, a lower termite that evolved outside foraging, brood care was more common. Together with data for higher termites, this suggests that brood care in termites only becomes important when switching from a wood-dwelling to a foraging lifestyle. These results imply that early social evolution in termites was driven by benefits of increased defence, while eusociality in Hymenoptera and cooperative breeding in birds and mammals are primarily based on brood care.     

Single "early" action potential cause by Ni2+ ions in true pacemaker cells of the sinoatrial ring of the dace heart

Single "early" action potentials (AP) or "early" postdepolarization (EAD) were recorded in multicellular stripes working in the regimen of true pacemaker cells located in the basis of the sinoatrial valve of the dace (Leuciscus rutilus) heart after Ni2+ (0.3 mM) were added to superfused solution on the 15 th min. The standard microelectrode technique was used. The appearance of single EAD was preceded by increase of AP spike duration almost 1.5-fold due to increase of the duration of a final repolarization phase and of diastolic depolarization. EADs appeared at different levels of repolarization from -20 to -60 mV. EAD's amplitude was lower than the AP proper. The effect is reversible. Nifedipine (2 microM) decreased by 20% the AP duration to 50% repolarization in the cells of atrial type. In case the stripes were primarily subjected to nifedipine effect and then even after a long procedure of washout, the Ni2+ (0.3 mM) did not cause EADs. The hypothesis has been tested of what is the main reason of single EAD appearance in pacemaker cells under the effect of Ni2+; it is either blocking Ca release from the cell by Ni2+, or reactivation of L-type Ca-channels' conductivity. The analysis of the data obtained leads to the conclusion that 30-50% Na-Ca-exchangers block is the basic reason of single EAD appearance in pacemaker cells.     

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

Abstract.— 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.