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Encyclopedia of Social Insects

Living Edition
| Editors: Christopher K. Starr

Allodapine Bees

  • Michael P. Schwarz
  • Simon M. TierneyEmail author
Living reference work entry
DOI: https://doi.org/10.1007/978-3-319-90306-4_4-1
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The Allodapini is one of four tribes in the Xylocopinae (Apidae), comprising about 300 described species largely distributed throughout sub-Saharan Africa and Australia, with one genus extending through southern Asia and another restricted to the Middle East. Most species are stem nesters with small colony sizes, but they exhibit the most sophisticated forms of social organization within the subfamily. They have been widely studied for the insights they can provide into social evolution, social parasitism, sex allocation theory, systematics, and historical biogeography. At the same time, these are by no means conspicuous insects. Their small body size, usually very small colonies, and hidden nesting habits ensure that most entomologists are probably unaware of them even in the areas where they naturally occur. It is notable, for example, that they have no generally accepted common name in English.

Nesting Biology

Allodapines are unique among bees in their brood-rearing habit. Regardless of how many females cooperate in using a nest, eggs are laid in a single unpartitioned, unlined nest tunnel, and larvae are progressively provisioned. Larvae require adult females to supply pollen until the post-feeding stage. The lack of cell walls within nests means that brood are totally dependent on adult females for defense against predators and parasites, which leads to extended contact between brood and the adult females that care for them. Such nesting behaviors are likely responsible for a remarkable variation in larval morphology (Fig. 1), displaying more diversity than in all other bees combined [1]. Nest tunnels are usually excavated within dead plant stems with soft or pithy centers (Fig. 2). Alternative nest substrates include Acacia tree thorns and the burrows of wood-boring beetles in hardwood branches. The combination of nest architecture and extensive adult-brood contact throughout the entire immature developmental period is thought to have had a strong impact on social evolution within this tribe [2, 3, 4, 5].
Fig. 1

Larval morphology. Mature larvae of bee tribes Allodapini and Ceratinini. (Adapted from Ref. [1]). Right-facing larvae are allodapines from the Australian exoneurine group. Left-facing larvae are African representatives with the exception of k, which derives from the sister tribe Ceratinini. The numbers 2 and 3 denote second and third larval tubercles and pseudopods. An asterisk denotes an obligate social parasite. (a) Nasutapis straussorum∗; (b) Allodape mucronata; (c) Braunsapis trochanterata; (d) B. natalica; (e) B. simplicipes; (f) B. foveata; (g) B. leptozonia; (h) Compsomelissa (Compsomelissa) stigmoides; (i) C. (Halterapis) nigrinervis; (j) Macrogalea candida; (k) Ceratina dupla; (l) Eucondylops konowi∗; (m) Allodapula (Allodapula) melanopus, a close relative of the host of E. konowi; (n) A. (Dalloapula) acutigera; (o) A. (Allodapulodes) hessei; (p) Exoneura (Inquilina) excavata∗; (q) E. (Exoneura) obscuripes; (r) E. (E.) variabilis; (s) E. (E.) subbaculifera; (t) E. (Brevineura) concinnula; (u) Exoneurella lawsoni

Fig. 2

Stem nests. Three discrete nest entrances of Exoneura robusta excavated in a frond of the tree fern Cyathea australis. The female’s metasoma is used to block the nest entrance

Social Evolution

Because of the extended adult-brood contact, no allodapine species can be regarded as truly solitary. Rather, a single adult female rearing her offspring is categorized as subsocial. Moreover, in all species at least some nests contain more than one adult female during the brood-rearing period, implying that alloparental care occurs in all species. That is, there appears to be a general departure from the habit of solitary bees in which each adult female cares only for her own brood. Multi-female colonies with brood raise interesting questions for understanding social organization, because even if only one of these females feeds brood at any one time, the other, non-provisioning or less-reproductive females are on hand to deter predators or parasites. This nest defense will render fitness benefits to the colony, and inclusive fitness365体育网站 is further augmented if adult females are closely related.

Colonies of allodapines tend to be small, and most species exhibit a modal colony size of fewer than four adult females during brood-rearing periods. Maximum colony sizes during brood rearing rarely exceed eight females, although in the arid-zone Australian species Exoneurella tridentata365体育网站 they can reach up to 56 females per nest. The generally small sizes of allodapine colonies led early researchers to regard this tribe as having only very simple forms of sociality, and it was thought that they represented a very recent transition from subsocial to true social organization. However, studies beginning in the late 1980s have challenged the notion of a recent origin and the “primitive” nature of sociality in this tribe.

Intensive studies of the temperate Australian species Exoneura robusta have demonstrated a sophisticated set of social traits that include (i) kin recognition systems, wherein bees transferred to novel environments with abundant opportunities for independent nesting chose to nest with kin; (ii) well-defined behavioral castes in pre-reproductive colonies without brood; and (iii) reproductive hierarchies modulated by pheromones that were unexpected in such small colony sizes. These combined studies suggest a level of social complexity inconsistent with a very recent origin of sociality [2, 5].

Subsequent investigations of social behavior in a wider array of Australian and African genera revealed broad phylogenetic evidence for age-based queues in egg-laying roles and ample opportunities for alloparental care. At the same time, molecular phylogenetic analyses helped to resolve the apparent mismatch between social complexity and a putatively recent origin of sociality, particularly with the discovery of frequent social nesting in the tropical African genus Macrogalea and its revised phylogenetic position as the sister group to all other allodapines. This is consistent with the hypothesis that group living is an ancestral trait for the tribe. Fossil-calibrated dating analyses showed that the Allodapini have a crown age that extends back to the Eocene and that the subfamily Xylocopinae has a crown age that precedes the K-T boundary [2, 5] and suggest the potential of a Cretaceous origin of sociality in this group.

Reproductive Castes

Inferences of the ancestral form of allodapine social organization using a statistically robust comparative method suggest that at the very beginning of social evolution reproductive differentiation involved serial supersedure of reproductive dominance, whereby younger adult females wait to replace senescent or deceased females that were previously dominant [3]. Such linear hierarchies involving waiting strategies have also been suggested for species of Xylocopa and Ceratina, which implies that this is an ancestral trait for social life in the Xylocopinae. Moreover, reproductively dominant females also engage in foraging to rear brood at the same time as they are laying eggs. This form of sociality is not consistent with “evo-devo” hypotheses which propose that early stages of caste evolution involved a decoupling of foraging and reproductive roles, although the evo-devo models may apply to other social insect groups.

In Exoneura robusta, the first female to reach adult eclosion within a colony assumes reproductive dominance, and dominance hierarchies can be experimentally manipulated by retarding the development of the oldest pupae, destined for dominance, so that they emerge behind younger siblings. As mentioned above, reproductive dominance in Exoneura robusta is pheromonally modulated in the period leading up to commencement of egg laying. Interestingly, a subsequent study showed that nestmate differences in ovarian development in this critical pre-laying period were correlated with pairwise genetic relationships. It is unlikely that such a correlation could be explained by genetic controls for fecundity, body size relationships, or relative age. Females of Exoneura robusta365体育网站 may therefore represent a case of situational assessment of kinship that subsequently influences individual ovarian development.

Another representation of social complexity in allodapines involves Exoneurella tridentata, in which queens are approximately twice the size of workers and exhibit a radically different morphology (Fig. 3). As noted above, this species has the largest colony sizes of any allodapine species, and workers are rarely inseminated but may occasionally produce male eggs. This relatively extreme form of eusociality may be related to their nesting substrate in a harsh xeric environment. While desert hardwoods are much more durable than most allodapine stem nests, which typically last less than three brood-rearing seasons, suitable substrates are also limited, because the bees rely on beetle larvae to make the nest tunnels. The scarcity of suitable nesting substrates may make it very costly for subordinate females to disperse and found independent nests. Similar environmental restrictions apply to Xylocopa pubescens.
Fig. 3

Female castes of Exoneurella tridentata: left, queen; right, worker

Sex Allocation

Allodapines are unique among bees in the near ubiquity of extremely female-biased sex ratios across diverse genera. Numerical sex ratios (proportion of male brood) of <0.15 have been reported in Macrogalea, the sister group of all other allodapines combined, and many species in other genera (e.g., Exoneura and Brevineura) have reported sex ratios of ~0.3 or less.

The most likely source of these female-biased ratios is local resource enhancement [6]. This arises when sisters or other close female relatives cooperate, and this cooperative behavior leads to an increased mean fitness for the colony in the form of improved per capita brood production and decreased mortality from predators and parasites. Local resource enhancement belongs to a family of sex allocation models in which either maternal or paternal fitness is a nonlinear function of resource investment in either males or females.

Social Parasitism

There are many reports of allodapine bees as nest parasites of other allodapine species. In nearly all cases, these social parasites are obligate inquilines that are unable to reproduce outside of their host colonies. However, there are several instances in which parasitism is facultative, although in each case the parasitic lineage is of relatively recent origin [4, 5]. Some inquiline lineages have been accorded generic status even though they are phylogenetically nested within their host genus – such as Effractapis and Nasutapis – which are obligate inquilines of their host genus Braunsapis. At the same time some socially parasitic species of Braunsapis have been assigned the same generic nomen as their hosts. In another lineage, the obligately parasitic Australian genus Inquilina forms a monophyletic sister clade to its host genus, Exoneura. Consequently, for allodapine social parasites, there is a phylogenetically inconsistent assignment of generic status, with multiple cases of paraphyly. Designation of paraphyletic generic status for some allodapine social parasites has been historically driven by extreme adaptations in adult morphology despite conserved larval morphology, and this contrasts with nonparasitic allodapines where larval morphology has been regarded as the most important feature for generic assignment (Fig. 1) [1].

While the bumblebee subgenus Psithyrus is the most speciose group of bee social parasites, the allodapine inquilines are the most phylogenetically diverse among bees with at least 11 (likely 14) independent origins [4, 5] with many more species remaining to be discovered. The abundance of independent origins of social parasitism in allodapines is likely related to the lack of brood cells in this tribe, whereby parasitic species do not need to break into individual brood cells but simply gain access to the communal nest tunnel. Nevertheless, most allodapine social parasites show adaptations for both forced entry to host colonies and resisting ejection, such as enlarged legs and tibial spurs, concave faces, and terminal dentate structures of the metasoma. Interestingly, facultative social parasitism has been reported for the African Braunsapis paradoxa group and some Madagascan species of Macrogalea, and this provides opportunities to study early stages in the evolutionary pathways to obligate parasitism [4].

The loose form of Emery’s rule has sometimes been used to support sympatric speciation models of the origin of social parasitism. The strict form of this rule is that social parasites are sister species of their respective hosts, while the loose form says that hosts and parasites are relatively close phylogenetic relatives or that hosts and parasites form sister clades to each other. While many allodapine host-parasite lineages concord with this loose form of the rule, it has been argued [4] that sympatric speciation is an unlikely evolutionary mechanism, because no obligate parasite-host associations are shown to exhibit immediate sister-species relationships. Allodapine inquilines may be more representative of “spill over” models, whereby highly compatible behavior and chemical communication systems shared by closely related species enable intraspecific cheating, which can subsequently develop into true hetero-specific parasitism.

References

  1. 1.
    Michener, C. D. (1977). Discordant evolution and the classification of allodapine bees. Systematic Zoology, 26, 32–56.
  2. 2.
    Schwarz, M. P., Richards, M. H., & Danforth, B. N. (2007). Changing paradigms in insect social evolution: Insights from halictine and allodapine bees. Annual Review of Entomology, 52, 127–150.
  3. 3.
    Schwarz, M. P., Tierney, S. M., Rehan, S. M., Chenoweth, L., & Cooper, S. J. B. (2011). The evolution of eusociality in allodapine bees: Workers began by waiting. Biology Letters, 7, 277–280.
  4. 4.
    Smith, J. A., Chenoweth, L. B., Tierney, S. M., & Schwarz, M. P. (2013). Repeated origins of social parasitism in allodapine bees indicate the weak form of Emery’s rule is widespread, but no evidence for sympatric speciation. Biological Journal of the Linnean Society, 109, 320–331.
  5. 5.
    Tierney, S. M., Smith, J. A., Chenoweth, L., & Schwarz, M. P. (2008). Phylogenetics of allodapine bees: A review of social evolution, parasitism and biogeography. Apidologie, 39, 3–15.
  6. 6.
    Schwarz, M. P. (1988). Local resource enhancement and sex ratios in a primitively social bee. Nature, 331, 346–348.

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Flinders UniversityAdelaideAustralia
  2. 2.Hawkesbury Institute for the EnvironmentWestern Sydney UniversitySydneyAustralia