Colony size evolution and the origin of eusociality in corbiculate bees (Hymenoptera: Apinae)

Recently, it has been proposed that the one of the main determinants of complex societies in Hymenoptera is colony size, since the existence of large colonies reduces the direct reproductive success of an average individual, given a decreased chance of being part of the reproductive caste. In this study, we evaluate colony size evolution in corbiculate bees and their relationship with the sociality level shown by these bees. Specifically i) the correlation between colony size and level of sociality considering the phylogenetic relationship to evaluate a general evolutionary tendency, and ii) the hypothetical ancestral forms of several clades within a phylogeny of corbiculate bees, to address idiosyncratic process occurring at important nodes. We found that the level of social complexity in corbiculate bees is phylogenetically correlated with colony size. Additionally, another process is invoked to propose why colony size evolved concurrently with the level of social complexity. The study of this trait improves the understanding of the evolutionary transition from simple to complex societies, and highlights the importance of explicit probabilistic models to test the evolution of other important characters involved in the origin of eusociality.     

Evaluating alternative stem cell hypotheses for adult corneal epithelial maintenance

In this review we evaluate evidence for three different hypotheses that explain how the corneal epithelium is maintained. The limbal epithelial stem cell(LESC)hypothesis is most widely accepted. This proposes that stem cells in the basal layer of the limbal epithelium, at the periphery of the cornea, maintain themselves and also produce transient(or transit) amplifying cells(TACs). TACs then move centripetally to the centre of the cornea in the basal layer of the corneal epithelium and also replenish cells in the overlying suprabasal layers. The LESCs maintain the corneal epithelium during normal homeostasis and become more active to repair significant wounds. Second, the corneal epithelial stem cell(CESC) hypothesis postulates that, during normal homeostasis, stem cells distributed throughout the basal corneal epithelium, maintain the tissue. According to this hypothesis, LESCs are present in the limbus but are only active during wound healing. We also consider a third possibility, that the corneal epithelium is maintained during normal homeostasis by proliferation of basal corneal epithelial cells without any input from stem cells. After reviewing the published evidence, we conclude that the LESC and CESC hypotheses are consistent with more of the evidence than the third hypothesis, so we do not consider this further. The LESC and CESC hypotheses each have difficulty accounting for one main type of evidence so we evaluate the two key lines of evidence that discriminate between them. Finally, we discuss how lineage-tracing experiments have begun to resolve the debate in favour of the LESC hypothesis. Nevertheless, it also seems likely that some basal corneal epithelial cells can act as long-term progenitors if limbal stem cell function is compromised. Thus, this aspect of the CESC hypothesis may have a lasting impact on our understanding of corneal epithelial maintenance, even if it is eventually shown that stem cells are restricted to the limbus as proposed by the LESC hypothesis.     

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.     

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.     

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.     

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 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.     

Evaluating nesting microhabitat for ground-nesting bees using emergence traps

Nesting resources structure native bee communities and the availability of suitable nests may enhance population abundance and persistence. Nesting rates of ground-nesting bees have proven challenging to assess due to a lack of standardized methods. We quantified the abundance of ground-nesting native bees using emergence traps over a seven-month study period. We then compared specimens captured in emergence traps with pan- and net-collected specimens. We hypothesized that ground-nesting bees would be highly similar to bees found foraging within our study site. However, the species assemblage of ground-nesting bees collected from emergence traps was significantly dissimilar from the assemblages collected with aerial nets and pan traps, indicating different sampling methods target different components of the species assemblage. We then examined the importance of nesting resources found at each emergence trap on the abundance of ground-nesting bees collected from emergence traps. Quantification of potential nesting resources, such as percent bare soil, has been proposed as a proxy of nesting habitat for ground-nesting guilds. Sloped ground and soil compaction were the most predictive nesting resources at the community-level. Further, spatial distribution of nesting resources within the study landscape also affected nesting rates, although this varied by species. Bees occurred in 85% of emergence traps, with sampling date strongly affecting the number of bees collected. Emergence traps provide a useful method of sampling the ground-nesting native bee community and investigating nesting incidence.     

A Bayesian approach for discriminating among alternative inheritance hypotheses in plant polyploids: the allotetraploid origin of genus Borderea (Dioscoreaceae)

Polyploidy is a common phenomenon occurring in a vast number of land plants. Investigations of patterns of inheritance and the origins of plants (i.e., autopolyploidy vs. allopolyploidy) usually involve cytogenetic and molecular studies of chromosome pairing, chromosome mapping, and marker segregation analysis through experimental crosses and progeny tests. Such studies are missing for most wild species, for which artificial crosses are difficult, not feasible, or unaffordable. We report here a Bayesian method to discriminate between alternative inheritance patterns in the two extant, tetraploid species of the monocot genus Borderea (Dioscoreaceae), which does not involve progeny array tests. Our approach is based on the screening of a large number of SSR genotypes, which were obtained from successful amplifications of 17 microsatellite regions in individuals of both B. chouardii and B. pyrenaica. We tested for tetrasomic vs. disomic modes of inheritance, using the Bayes factor test. Assignment of genotypes under both alternatives could be unequivocally done for 14 and 11 of the 17 studied microsatellite regions in B. chouardii and B. pyrenaica, respectively, totaling 9502 analyzed genotypes. The comparison of posterior probabilities for the two competing hypotheses across the surveyed loci clearly favored a disomic inheritance pattern. Linkage tests indicated that none of the studied SSR loci were in linkage disequilibrium, thus representing independent samples of the Borderea genome. These results, along with previous allozyme data, support the allotetraploid origin of this paleoendemic genus and reveal the lowest reported chromosome base number for the family of the yams.     

Ctenoplectridae and the origin of long-tongued bees*

The Ctenoplectridae (for the genera Ctenoplectra and Ctenoplectrina) are separated from the Melittidae, in which they have commonly been included. Ctenoplectrids differ from melittids in many characters, and are more closely related to the long-tongued families Fideliidae, Megachilidae, Anthophoridae, and Apidae than to the Melittidae and other short-tongued families. Ctenoplectrids are the sister-group of the long-tongued bees (and could be considered as long as long-tongued bees with labial palpi of short-tongued bees); melittids are the sister-group to the ctenoplectrids plus long-tongued bees. Characters are listed that support these relationships. Ctenoplectra species appear to be oil collectors from flowers of curcurbits. Some behavioural observations are included. Ctenoplectrina is a probable parasite in nests of Ctenoplectra, as it lacks the pollen and oil manipulating apparatus.     

Evaluating hypotheses about dispersal in a vulnerable butterfly

Sound management of species requires reliable estimates of dispersal. Indeed, dispersal of individuals among local populations is a key factor in the biology and persistence of local populations and metapopulations. Here, the small-scale dispersal pattern of a vulnerable species, the endemic Sardinian chalk hill blue butterfly, was studied by applying capture–recapture multistate models and a model selection based on AIC values. Model parameters were survival, capture and movement probabilities. The model selection showed that (a) survival probability of individuals varied between sexes, (b) capture probability varied between sexes and among patches, and (c) movement probability varied with direction. The probability of movement among adjacent local populations was generally low and ranged from 0.009 to 0.212. Movement probabilities were subsequently modeled using data on interpatch distance and donor patch population size or area. The ultrastructural biology-based models turned out to be the most appropriate models for inference, showing that dispersal decreases with increasing interpatch distance and increasing donor patch population size or area, and suggesting that butterfly dispersal is affected by patch geometry and the presence of conspecifics. The application of multistate models, the model selection approach, and ultrastructural modeling allowed testing the validity of some general hypotheses related to dispersal in metapopulations and helped elucidate the butterfly small-scale dispersal pattern.     

A test of alternative hypotheses for kin recognition in cannibalistic tiger salamanders

The function of kin recognition is controversial. We investigatedtheadaptive significance of kin discrimination in cannibalistictiger salamanderlarvae, Ambystoma tigrinum. Previous laboratoryexperiments show thatcannibals preferentially consume lessrelated individuals. We hypothesizedthat this example of kinrecognition (1) is a laboratory artifact, (2) is aby-productof sibship-specific variation in escape responses, becausecannibalsfrom families with rapid responses may be more likely to cannibalizeslowlyescaping non-kin, (3) is an epiphenomenon of species recognition,(4)functions in disease avoidance, because kin may be moreinfectious thannon-kin, or (5) is favored by kin selection.We evaluated these fivehypotheses by using laboratory and fieldexperiments to test specificpredictions made by each hypothesis.We rejected hypotheses 1-4 above because(1) kin recognitionwas expressed in the wild, (2) escape responses did notreliablypredict whether a cannibal would ingest kin or non-kin, (3)kinrecognition was not most pronounced in populations wheretiger salamandersco-occur with other species of salamanders,and (4) non-kin prey were morelikely than kin to transmit pathogensto cannibals. However, we establishedthat the necessary conditionfor kin selection, Hamilton's rule, was met.Thus, our resultsimplicate kin selection as the overriding reason thatcannibalistictiger salamanders discriminate kin.     

An alternative origin for nanobacteria in kidney stones

Small (50–200 nm), calcium phosphate (apatite)-covered organic particles called nanobacteria or calcifying nanoparticles (CNP) seem to be ubiquitous in kidney stones and are thought to be involved in stone formation. Although initial claims that these particles are the smallest known life forms have been somewhat softened, much controversy remains as to their involvement in kidney stone formation as well as in other pathological calcifications. I suggest that such particles are non-living and may be formed during the normal living activities of bona-fide bacteria which inhabit the kidneys. This hypothesis is based on previous observations that bacteria immersed in a supersaturated fluid produce organic globules which calcify when released to the surrounding fluid, forming CNP-like particles. The possibility that this process is responsible for the formation of CNP associated with pathological calcifications deserves greater scrutiny.     

Endemism in Tasmanian cool temperate rainforest: alternative hypotheses

Endemism in Tasmanian cool temperate rainforest: alternative hypotheseS. Evidence is presented which suggests that hypotheses presented by Kirkpatrick & Brown relating to endemic species in Tasmania are either invalid or of limited importance for woody rainforest species.
In their place three hypotheses are presented to account for the presence of endemic species in Tasmanian cool temperate rainforest on the basis of the fossil record and the distribution of species which are closely related to the endemics. The first two hypotheses relate to the presence of the endemic species in the general Tasmanian region. They are:

• 1. 

  Some species evolved in southeastern Australia during the Tertiary in response to the changing climate. Some of the ancestral species still occur in temperate rainforest at lower latitudes in Australia.
• 2. 

  Some species have remained essentially unchanged in Tasmania during the Tertiary and Quaternary climatic changes.

The third hypothesis relates to the restriction of these cool temperate rainforest species to Tasmania:

• 1. 

  Post-glacial climatic changes (especially a decrease in rainfall) and the human influence (especially land clearing and fire) may have combined to eliminate some cool temperate rainforest species from mainland Australia.

     

Evaluating hypotheses on the origin and evolution of the New Zealand alpine cicadas (Maoricicada) using multiple-comparison tests of tree topology

The statistical testing of alternative phylogenetic trees is central to evaluating competing evolutionary hypotheses. Fleming proposed that the New Zealand cicada species Maoricicada iolanthe is the sister species to the major radiation of both low-altitude and montane Maoricicada species. However, using 1,520 bp of mitochondrial DNA sequence data from the cytochrome oxidase subunit I, tRNA aspartic acid, and the ATPase subunit 6 and 8 genes, we inferred that both M. iolanthe and another low-altitude species, Maoricicada campbelli, are nested within the montane Maoricicada radiation. Therefore, we examined the stability of the inferred phylogenetic placement of these two species using the newly developed Shimodaira-Hasegawa test (SH test) implemented in a maximum-likelihood framework. The SH test has two advantages over the more commonly used Kishino-Hasegawa (KH) and Templeton tests. First, the SH test simultaneously compares multiple topologies and corrects the corresponding P: values to accommodate the multiplicity of testing. Second, the SH test is correct when applied to a posteriori hypotheses, unlike the KH test, because it readjusts the expectation of the null hypothesis (that two trees are not different) accordingly. The comparison of P: values estimated under the assumptions of both the KH test and the SH test clearly demonstrate that the KH test has the potential to be misleading when the issue of comparing of a posteriori hypotheses is ignored and when multiple comparisons are not taken into account. The SH test, in combination with a variety of character-weighting schemes applied to our data, reveals a surprising amount of ambiguity in the phylogenetic placement of M. iolanthe and M. campbelli.     

Evaluating phylogenetic hypotheses of carpoids using stratigraphic congruence indices

Fossil carpoids possess a unique anatomy that is difficult to interpret; as a result, there are a number of competing phylogenetic hypotheses for carpoid taxa. Stratigraphic congruence indices provide a quantitative means of evaluating alternative cladograms where character coding is contentious; trees that show a statistically significant fit between stratigraphy and phylogeny are better supported by the fossil record. We here test the agreement between stratigraphic and cladistic data for 27 carpoid cladograms (24 have previously been published, three are novel). The results demonstrate that in analyses of subsets of carpoid taxa, the stratigraphic congruence of trees is not strongly affected by the interpretative model followed. However, when studying the relationships of carpoids with other deuterostomes, assuming that carpoids should be interpreted by reference to chordates/hemichordates (rather than echinoderms) leads to a poorer fit with the known stratigraphic ranges of taxa. Thus, the disputed calcichordate hypothesis (carpoids interpreted as stem and crown-group chordates and stem-group hemichordates) is much less congruent with stratigraphy than alternative models interpreting carpoids as stem or crown-group echinoderms.     

An alternative strategy for maintenance of eusociality after nest destruction: new nest construction in a primitively eusocial wasp

Although nests are central to colonial life in social insects, nests are sometimes damaged by predators or natural disasters. After nest destruction, individuals usually construct new nests. In this case, a sophisticated mechanism like the scent trail pheromone used in large insect colonies that recruit individuals to new nest sites would be important for the maintenance of eusociality. In independent-founding Polistes wasps, it is well known that queens enforce workers physiologically on the natal nests even if evidence of trail pheromone use has not been exhibited. We investigated the effect of the queen on an alternative strategy for the maintenance of eusociality by first females after nest destruction in the primitively eusocial wasp Polistes chinensis. We predicted that the first females in queen-absent colonies have various behavioral options after nest destruction. Even if the females construct new nests cooperatively with other individuals, the new nest construction should be conducted more smoothly in queen-present colonies because the queens regulate the behavior of wasps. We made wasps construct new nests by removing the entire brood from existing nests. The presence of the queen did not cause variation in the alternative strategy of the first females, as the first females (workers) usually constructed new nests cooperatively irrespective of the queen-presence. Thus, the workers in the queenpresent colonies affiliated to the new nest construction more smoothly and constructed new nests more efficiently than workers in the queen-absent colonies. Our results suggest that the presence of the queen is important for maintaining eusociality in primitively eusocial wasps after nest destruction. Received 8 February 2005; revised 5 October 2005; accepted 17 October 2005.     

Enfleurage, lipid recycling and the origin of perfume collection in orchid bees

Enfleurage, the extraction of elusive floral scents with the help of a lipophilic carrier (grease), is widely used in the perfume industry. Male neotropical orchid bees (Euglossini), which accumulate exogenous fragrances as pheromone analogues, use a similar technique. To collect fragrances, the bees apply large amounts of straight-chain lipids to odoriferous surfaces from their cephalic labial glands, which dissolve the volatiles, and the mixture is then transferred to voluminous hind-leg pockets. Here, we show that males do in fact operate a lipid conveyor belt to accumulate and concentrate their perfume. From the hind-leg pockets of caged male Euglossa viridissima, deuterated derivatives of carrier lipids were consecutively sequestered, shuttled back to the labial glands and reused on consecutive bouts of fragrance collection. Such lipid cycling is instrumental in creating complex perfume bouquets. Furthermore, we found that labial glands of male orchid bees are strikingly similar to those of scent-marking male bumblebees in terms of size, form and structure. This, and a prominent overlap in secretory products, led us to propose that perfume collection evolved from scent-marking in ancestral corbiculate bees.