Sociality in the phylogenetically basal allodapine bee genus Macrogalea (Apidae: Xylocopinae): implications for social evolution in the tribe Allodapini

Recent phylogenetic studies based on DNA sequence data indicate that the tropical African bee genus Macrogalea is the sister group to the remaining extant allodapine fauna, whereas previously it was thought to be a distal group. This leads to some fundamental changes in our understanding of social evolution in the allodapines. Earlier studies suggested that Macrogalea showed only weak forms of social behaviour and these were not well characterized. However, large samples of Macrogalea zanzibarica presented here show that this species exhibits marked social behaviour. Nearly half of nests collected contained two or more adult females, with up to 10 females per nest. Brood are reared progressively and brood ages within colonies are staggered, giving rise to colonies with very mixed age structures and therefore frequent opportunities for alloparental care. Ovarian dissections indicate non‐simple forms of reproductive partitioning within colonies and most multi‐female colonies show evidence that more than one female has contributed to egg production, though reproductive episodes among colony members are frequently asynchronous. Some females show signs of much higher wing wear than their nestmates, but always show signs of previous reproduction. Reproductive division of labour appears to be temporally marked, ovarian differentiation among nestmates is linked to relative body size, but permanent worker‐like or queen‐like castes appear to be absent. This is similar to the communal, continuously brooded and multivoltine behaviour of some tropical halictine species and may be due to the aseasonal nature of brood development in tropical regions. Patterns of per capita brood production indicate large benefits to multi‐female nest occupancy, and sex allocation is strongly female biased. These findings strongly suggest that the capacity for complex social interactions and alloparental care is an ancestral trait for all of the extant allodapine lineages. Therefore comparisons among extant allodapines are unlikely to throw light on the initial origin of social behaviour, though they may uncover origins of true caste behaviour and reversals to solitary nesting. Sex ratios in Macrogalea and most other allodapine genera, spanning a broad phylogenetic and ecological range, suggest that one or more allodapine traits have provided persistent selection for female‐biased sex allocation.     

Behavioural specialization in pre-reproductive colonies of the allodapine beeExoneura bicolor (Hymenoptera: Anthophoridae)

Summary Exoneura bicolor is a univoltine allodapine bee common in montane forests of southern Australia, where it exhibits a semisocial/quasisocial colony organization. Within-nest behaviour in postemergence autumn nests ofExoneura bicolor was recorded with the aim of studying behavioural specialization in pre-reproductive colonies. Ten complete colonies were transferred to purpose-built observation nests shortly before brood eclosion in late summer. Behaviour within observation nests was recorded for periods of up to 44 days after establishment, covering a period when colonies are preparing for overwintering. Dispersal of females and brood rearing do not occur at this time, although some females may become inseminated. Analyses of data using multivariate techniques indicated four distinguishable behavioural castes, designated here as Guards, Nest Absenters, Nest Modifiers and Non-recruits. This represents a higher degree of behavioural specialization than recorded to date for other allodapines. Behaviours performed by Guards and Nest Absenters are likely to involve considerable risks, but benefit the colony as a whole, so that some nestmates in prereproductive colonies exhibit altruism that frequently aids adult siblings or cousins. The males in our study were fed by females via trophallaxis and two of the males participated in nest maintenance tasks. Our results suggest that autumn colonies ofE. bicolor form well-integrated behavioural units even though brood rearing does not commence until the following spring.     

Reproductive hierarchies in the African allodapine bee Allodapula dichroa (Apidae: Xylocopinae) and ancestral forms of sociality

The social organization of allodapine bees has been described in detail for most genera, although there remains a notable gap for one major lineage, the genus Allodapula . Here, we provide the first detailed study of social organization in Allodapula dichroa . Colony sizes are small and the frequency of cooperative nesting is low compared with other allodapine taxa, but there is very clear evidence for reproductive differentiation among adult nestmates. Reproductively dominant females tend to be larger than their nestmates and have much higher levels of wing wear, suggesting that they perform most foraging activities. Multi-female colonies have: (1) lower rates of complete brood absence, suggesting a substantial benefit to cooperative nesting; and (2) larger numbers of brood, suggesting that the presence of a second adult female leads to a greater reproductive output. These data suggest a major phylogenetic split in the form of social organization within the allodapines. In the genus Macrogalea (sister clade to all other allodapines), body size does not preclude young females from laying eggs, and there appears to be, at most, weak reproductive queues. However, in most other allodapines, reproductive hierarchies are prominent and younger and/or smaller females queue for reproductive opportunities, adopt permanently subordinate roles, or disperse. Interestingly, the most common forms of reproductive hierarchies in allodapines do not involve subordinates undertaking foraging roles before reproduction, but instead involve the delaying of both reproduction and foraging. This has implications for the understanding of suggested developmental ground plans in the early stages of social evolution.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 520–530.     

Molecular phylogenetics of allodapine bees,with implications for the evolution of sociality and progressive rearing

Allodapine bees have long been regarded as providing useful material for examining the origins of social behavior. Previous researchers have assumed that sociality arose within the Allodapini and have linked the evolution of sociality to a transition from mass provisioning to progressive provisioning of brood. Early phylogenetic studies of allodapines were based on morphological and life-history data, but critical aspects of these studies relied on small character sets, where the polarity and coding of characters is problematic. We used nucleotide sequence data from one nuclear and two mitochondrial gene fragments to examine phylogenetic structure among nine allodapine genera. Our data set comprised 1506 nucleotide positions, of which 402 were parsimony informative. Maximum parsimony, log determinant, and maximum likelihood analyses produced highly similar phylogenetic topologies, and all analyses indicated that the tropical African genus Macrogalea was the sister group to all other allodapines. This finding conflicts with that of previous studies, in which Compsomelissa + Halterapis formed the most basal group. Changing the basal node of the Allodapini has major consequences for understanding evolution in this tribe. Our results cast doubt on the previous hypotheses that progressive provisioning and castelike social behavior evolved among lineages leading to the extant allodapine taxa. Instead, our results suggest that mass provisioning in Halterapis is a derived feature and that social behavior is an ancestral trait for all allodapine lineages. The forms of social behavior present in extant allodapines are likely to have resulted from a long evolutionary history, which may help explain the complexity of social traits found in many allodapine bees.     

The biology of Brevineura froggatti and phylogenetic conservatism in Australian allodapine bees (Apidae,Allodapini)

Summary: We present the first data on the social biology of the allodapine bee, Brevineura froggatti. Colony sizes are small, and only 12.5% of nests contained more than two females. Brood rearing occurs throughout the year, including winter, as it does in the other species of Brevineura studied to date. In both Brevineura species, per capita brood production is much higher in multi-female nests than single female nests, raising the question of why more colonies aren't multifemale. The occurrence of small colony sizes, despite large benefits to group living, differs strongly from species of the sister clade Exoneura. These findings, combined with previous allodapine studies, indicate conservatism in voltinism, brood phenology and colony size within, but not between, Australian allodapine genera.     

FEMALE-BIASED SEX RATIOS IN A FACULTATIVELY SOCIAL BEE AND THEIR IMPLICATIONS FOR SOCIAL EVOLUTION

Montane populations of the Australian allodapine bee, Exoneura bicolor, are characterized by high levels of cooperative nesting and strongly female-biased sex ratios. A conspecific population from heathland shows much lower levels of cooperative nesting and lower levels of female bias. In both habitats, sex-ratio bias is greatest in the smallest brood sizes and becomes successively less biased in larger broods. Parity is approached in the largest heathland colonies, but not for any brood-size category in montane areas. Adult intracolony relatedness is moderately high for colonies in both reused and newly founded nests in the montane habitat, but probably low or zero for newly founded nests in heathland. Colony efficiency, measured as the number of brood per adult, increases with colony size in both habitats, suggesting that cooperation between females increases mean female fitness. It is argued that patterns of sex allocation are consistent with nonlinear fitness-return models, in which the mean reproductive value of daughters increases with the number of daughters produced in a brood. Such increases probably arise from a number of social interactions, including cooperative brood defense, increased task efficiency, and lower per capita costs in nest construction. The term “local fitness enhancement” is introduced here to describe these effects collectively. The female-biased ratios should lower selective thresholds for sib-directed altruism, at least in the earlier stages of colony development. It is argued that local fitness enhancement facilitates eusociality in allodapine bees and could also play a role in other haplodiploid taxa, provided cooperative nesting largely involves sisters, colony efficiency increases with colony size, and optimal colony sizes are only achieved after two or more generations after founding.     

昆虫社会行为的进化与生态适应

一、引言昆虫社会行为的进化涉及两大问题:(1)社会行为的起源和进化过程;(2)社会行为的适应意义。这两个问题都曾使达尔文感到困惑。达尔文曾详尽地描述过蜜蜂复杂的造巢行     

Facultative social parasitism in the allodapine bee Macrogalea berentyensis

Previous research on social parasitism has largely ignored allodapine social parasites, which is surprising given the huge potential of these bees to provide a better understanding of social parasitism. Macrogalea berentyensis, a species that was previously suggested to be a social parasite, was collected in nests of M. ellioti, and also in nests consisting of only M. berentyensis. These f＇mdings, along with morphological and phylogenetic evidence, show that this species is a facultative social parasite. In the independently living M. berentyensis nests, brood were present that had been reared to an advanced stage, suggesting that： （i） these parasites may be effective at foraging and caring for their brood; or （ii） these nests may be colonies where all the hosts had died, and these parasites had yet to disperse. Macrogalea berentyensis is the closest relative of the facultative social parasite, M. antanosy, and both these species represent the most recent evolutionary origin of social parasitism within the allodapines. Further behavioral research on both these parasitic species would therefore have important implications for the understanding of the evolution of social parasitism.     

Life history of Kladothrips ellobus and Oncothrips rodwayi: insight into the origin and loss of soldiers in gall-inducing thrips

1. The evolution of eusociality in Australian gall‐inducing thrips cannot be understood without comparisons among closely related solitary species. The life history of two solitary, gall‐inducing thrips, Kladothrips ellobus and Oncothrips rodwayi, was investigated, and data for solitary and eusocial species from previous studies were re‐analysed. Kladothrips ellobus is in a clade that is closely related to the eusocial species. Oncothrips rodwayi is in the same clade as the eusocial species and appears to have undergone an evolutionary loss of eusociality. It is the only galling thrips on Acacia in temperate environments. 2. The brood size of K. ellobus is eight to 23 times larger than broods of foundresses in eusocial species whereas the brood size of O. rodwayi is not significantly different from those of foundresses in eusocial species. 3. In K. ellobus, the mean sex ratio was not significantly different from parity but in O. rodwayi the mean sex ratio was 0.13 male. In O. rodwayi, 77% of females were inseminated by their brothers before dispersal, which is consistent with high levels of inbreeding in eusocial species of the same clade. Sex ratios suggest random mating in K. ellobus whereas female‐biased sex ratios in O. rodwayi are consistent with inbreeding and local mate competition. 4. Comparisons among solitary and eusocial species suggest that large brood size is an ancestral trait for eusociality in thrips, and this trait persists in solitary species as an r‐selection strategy. Soldiers may have evolved in arid environments to minimise the risks of dispersal and the costs of latency to reproduction, and to maximise gall defence. 5. Temperate conditions could have facilitated the evolutionary loss of soldiers in O. rodwayi, as there should be a shorter, safer, more predictable window period between dispersal and gall induction, reducing the period of latency to reproduction following dispersal and lowering risks of dispersal. 6. The loss of soldiers in O. rodwayi is not associated with a reversion to the large brood sizes of solitary species in ancestral lineages.     

Polyphenism ofHalictus (Seladonia) tumulorum (L.) (Hymenoptera,Halictinae)

Summary A population ofHalictus (S.) tumulorum, a species whose biology is poorly known, was studied in eastern France. The polyphenism was evaluated by comparing a sample of foundresses (1991) with two samples of summer females (1991 and 1992).H. tumulorum is a primitively eusocial species with castes differing only slightly in size, but more in function, and producing numerous males in the first brood. The social level of the species appears rather low.     

How brood influences caste aggregation patterns in the dimorphic ant species Pheidole pallidula

Spatial distribution of ant workers and, notably their aggregation/segregation behaviour, is a key-element of the colony social organization contributing to the efficiency of task performance and division of labour. In polymorphic species, specialized worker castes notably differ in their intrinsic aggregation behaviour. In this context, knowing the preponderant role of minors in brood care, we investigate how a stimulus such as brood can influence the spatial patterns of Pheidole pallidula worker castes. In a homogeneous area without brood, it was shown that minors display only a low level of aggregation while majors form large clusters in the central area. Here we find out that these aggregation patterns of both minors and majors can be deeply influenced by the presence of brood. For minors, it nucleates or enhances the formation of a large stable cluster. Such high sensitivity of minors to brood stimuli fits well with their role as main brood tenders in the colony. For majors, interattraction between individuals still remains the prevailing aggregation factor while brood strongly influences the localisation of their cluster. We discuss how the balance between interattraction and sensitivity to environmental stimuli determines the mobility of each worker castes and, consequently, the availability of minors and majors to participate in everyday colony tasks. Moreover, we will evoke the functional value of majors’ cluster location close to the brood, namely with respect to social regulation of the colony caste ratio. Received 30 May 2005; revised 11 January 2006; accepted 13 January 2006.     

Subsociality in halictine bees

To look for the occurrence and the significance of brood care in social evolution, I reared six eusocial halictine bee species in laboratory cages enabling the observation of intranest behaviour: Lasioglossum (Evylaeus) laticeps, L. (E.) pauxillum, L. (E.) nigripes, L. (E.) euboeensis, Halictus (Halictus) scabiosae and L. (E.) fulvicorne. All of them were subsocial, each mother caring for her brood. Brood cells were sealed after oviposition with earthen plugs; they were then reopened, visited and closed again. These observations plus the reports in the literature on eleven eusocial species indicate that seventeen species of eusocial halictine bees provide parental care, i.e. are subsocial. Brood care, subsociality, is strongly associated with eusociality. To study reversal from eusociality to subsociality, I have reared the non-eusocial form of two species within which there are or have been eusocial forms: Halictus (H.) rubicundus and Lasioglossum (E.) fratellum. They are secondarily solitary, having lost worker brood. However, both species still show brood care. This suggests that in transitions to eusociality, brood care antedated eusociality. To further examine this issue I reared two truly solitary species that are not derived from eusocial ancestors: Lasioglossum (E.) villosulum and L. (L.) quadrinotatum. Unlike secondarily solitary species, females of both these species close their brood cells after oviposition and ignore their progeny thereafter. This association strongly suggests that the subsocial route with maternal brood care is the route to eusociality in halictine bees.     

Colony size explains the lifespan differences between queens and workers in eusocial Hymenoptera

Eusocial Hymenoptera show a unique divergence in lifespan of queens and workers; queens belong to the longest lived insects while workers in most eusocial species have significantly shorter lives. The different phenotypes within a colony emerge through reproductive division of labour, which is a characteristic trait of eusocial animals. Division of labour as a measure of organismal complexity increases with colony size in eusocial species similar to the increase of complexity with size that has been shown for the whole range of living organisms. We show that queen and worker lifespan diverge in closely related species representing the transition from solitary to social life and show that queen and worker lifespan are correlated if colony size is taken into account: with increasing colony size the lifespan differential between queen and worker increases, whereas neither queen nor worker lifespan is associated with colony size. Additionally, the lifespan differential is better explained by colony size than by the weight differences between the castes. The divergence of phenotypes found is in line with the increasing specialization of subunits in larger organisms, which leads to increasing complexity. We argue that division of labour is acting to increase colony efficiency, which in turn shapes the investments made into individuals leading to short‐lived workers and long‐lived queens. Additionally, maintenance investments may be shaped due to the variable extrinsic risk faced by different castes. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 710–724.     

A mid-cretaceous origin of sociality in xylocopine bees with only two origins of true worker castes indicates severe barriers to eusociality

The origin of sterile worker castes, resulting in eusociality, represents one of the major evolutionary transitions in the history of life. Understanding how eusociality has evolved is therefore an important issue for understanding life on earth. Here we show that in the large bee subfamily Xylocopinae, a simple form of sociality was present in the ancestral lineage and there have been at least four reversions to purely solitary nesting. The ancestral form of sociality did not involve morphological worker castes and maximum colony sizes were very small. True worker castes, entailing a life-time commitment to non-reproductive roles, have evolved only twice, and only one of these resulted in discrete queen-worker morphologies. Our results indicate extremely high barriers to the evolution of eusociality. Its origins are likely to have required very unusual life-history and ecological circumstances, rather than the amount of time that selection can operate on more simple forms of sociality.     

A modeling approach to swarming in honey bees (Apis mellifera)

Identifying the mechanisms of colony reproduction is essential to understanding the sociobiology of honey bees. Although several proximate causes leading to the initiation of queen rearing – an essential prerequisite to swarming – have been proposed, none have received unequivocal empirical support. Here we model the main proximate hypotheses (colony size, brood comb congestion, and worker age distribution) and show that all proposed swarming triggers occur as a function of the ultimate cause of a colony reaching replacement stability, the point at which the queen has been laying eggs at her maximal rate. We thus present a reproductive optimization model of colony swarming based on evolutionary principles. All models produce results remarkably similar both to each other and to empirically-determined swarming patterns. An examination of the fit between the individual models and swarm-preventing techniques used by beekeepers indicates that the reproductive optimization model has a relatively broad explanatory range. These results suggest that an examination into the behavioral correlates of a queen’s maximum egg laying rate may provide a unified proximate mechanistic trigger leading predictably to colony fission. Generating a predictive model for this very well studied animal is the first step in producing a model of colony fission applicable to other swarm-founding eusocial animals. Received 16 November 2004; revised 31 May 2005; accepted 27 June 2005.     

Sex ratios, local fitness enhancement and eusociality in the allodapine bee Exoneura richardsoni

Previous studies of a facultatively eusocial allodapine bee, Exoneura richardsoni Rayment, indicated that high levels of cooperative nesting among close relatives seem to be maintained by benefits that lead to increases in per capita brood production. These traits could lead to local fitness enhancement, which in turn could select for female-biased sex ratios. We show here that sex investment ratios in this species are female-biased in small colony sizes, becoming progressively male-biased in larger colonies, consistent with expectations for local fitness enhancement, but not explainable by alternative models. Our results support previous suggestions that local fitness enhancement can lead to sex ratio bias in primitively social Hymenoptera, but differ from previous studies by suggesting that patterns of bias could lower selective thresholds for sib-directed altruism in small colonies, but have an opposing effect in large colonies.     

Strong constraints to independent nesting in a facultatively social bee: quantifying the effects of enemies-at-the-nest

Constraints to independent nesting play a key role in the understanding of social evolution in insects, but the source and the magnitude of such constraints are poorly known for many key taxa. In allodapine bees it is known that solitary nesting females have low rates of successful brood rearing and that this drives selection for cooperative nesting. It has been hypothesized that these constraints are due to the presence of enemies-at-the-nest, such as ants, but no direct link has been demonstrated between such enemies and colony failure. We set up an experiment in which solitary founded nests of an Australian allodapine bee, Exoneura nigrescens, were either protected from non-flying predators or left unprotected, and compared the resulting colony survival and brood production rates. We found that protected colonies have much higher rates of survival and that the constraints to independent nesting are extreme, with a mean of less than one offspring per nest at the end of the brood rearing period. This means that cooperative nesting is essential for this species to persist in its habitat. Received 6 July 2007; revised 5 November 2007; accepted 12 November 2007.     

The evolution of eusociality in allodapine bees: workers began by waiting

Understanding how sterile worker castes in social insects first evolved is one of the supreme puzzles in social evolution. Here, we show that in the bee tribe Allodapini, the earliest societies did not entail a foraging worker caste, but instead comprised females sharing a nest with supersedure of dominance. Subordinates delayed foraging until they became reproductively active, whereupon they provided food for their own brood as well as for those of previously dominant females. The earliest allodapine societies are, therefore, not consistent with an 'evo-devo' paradigm, where decoupling of foraging and reproductive tasks is proposed as a key early step in social evolution. Important features of these ancestral societies were insurance benefits for dominants, headstart benefits for subordinates and direct reproduction for both. The two lineages where morphologically distinct foraging worker castes evolved both occur in ecosystems with severe constraints on independent nesting and where brood rearing periods are very seasonally restricted. These conditions would have strongly curtailed dispersal options and increased the likelihood that dominance supersedure occurred after brood rearing opportunities were largely degraded. The origins of foraging castes, therefore, represented a shift towards assured fitness gains by subordinates, mediated by the dual constraints of social hierarchies and environmental harshness.     

Colony size as a species character in massive reef corals

In a study of seven massive, Caribbean corals, I have found major differences in reproductive behavior between species with large maximum colony sizes and species with smaller maximum colony sizes. Four species (Diploria clivosa, D. strigosa, Montastrea cavernosa, Siderastrea siderea) which are large (<1000 cm² in surface area) broadcast gametes during a short spawning season. Their puberty size is relatively large (>100 cm², except M. cavernosa). In contrast, two small massive species (<100 cm², Favia fragum and S. radians), and one medium-sized (100–1000 cm², Porites astreoides) massive species, brood larvae during an extended season (year-round in Panama). The puberty size of the small species is only 2–4 cm². Given these close associations between maximum colony sizes and a number of fundamental reproductive attributes, greater attention should be given to the colony size distributions of different species of reef corals in nature, since many important life history and population characters may be inferred.