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‘Do not go where the path may lead; go instead where there is no path and leave a trail.’

– Ralph Waldo Emerson (1803–1882)

Those whose interest resides among the bees are truly fortunate. Among Hymenoptera, only the ants and some of the social wasps can boast of receiving comparable attention, but even these cannot compete if the full enormity of literature on the honey bee, specifically the western honey bee Apis mellifera L., is taken into consideration. Naturally, this is not to say that bees as a whole have been studied evenly, as is more apparent when the same comparison is made between Apis and the remainder of the bees. Most work has gravitated to the conspicuously social lineages, to which Apis may be joined by its close relatives the bumble bees and stingless bees. Nonetheless, melittologists have a historical intensity of research, even excluding Apis, that is to be envied. In particular, a majestic, comprehensive and current account of the global supraspecific diversity is available (Michener, 2007), supplemented and enhanced by excellent regional treatments (e.g. Michener et al., 1994; Pauly et al., 2001; Silveira et al., 2002; Eardley et al., 2010). Such important guides, alongside annotated checklists for large regions or clades (e.g. Cardale, 1993; Gusenleitner & Schwarz, 2002; Moure et al., 2007; Ungricht et al., 2008; Ascher & Pickering, 2010; Eardley & Urban, 2010), render accessible a fauna that might otherwise be challenging to grasp. Hand-in-hand with these works has been a plethora of phylogenetic studies, rooted in a tradition of detailed comparative work, continually enhancing, expanding and revising the body of available data. Furthermore, bees are of such considerable biological interest and importance that melittological systematics has been enriched further by an organic synthesis with diverse and voluminous investigations into their behaviour, ecology and almost any conceivable aspect of their biology.

It is no surprise then that bee phylogenetics is such a robust and active field. Hardly a season goes by without a new treatment of some component of melittological diversity being considered from a phylogenetic perspective, and revisions or descriptions of new species are continually appearing. Certainly many genera remain to be investigated carefully, and for those already treated new data, studied either in isolation or more frequently with prior analyses, continue to revise perspectives on relationships. Indeed, the familiar corbiculate bees highlight such dynamics as these tribes have received a disproportionate amount of inquiry. But such intense scrutiny has served to improve our estimates of relationships among these four tribes by gradually accumulating numerous diverse sources of data (Cardinal & Packer, 2007). Morphological and molecular studies have together provided several improvements at both broad (e.g. Roig-Alsina & Michener, 1993; Alexander & Michener, 1995; Danforth et al., 2006a) and more constrained (e.g. Fuller et al., 2005; Larkin et al., 2006; Gonçalves, 2010) scales of inquiry, and these complementary forms of data are repeatedly and wisely synthesized for their maximum explanatory power (e.g. Sedivy et al., 2008; Michez et al., 2009). In contrast to most insect groups, if one takes a macroscopic view across the bees there are few major lineages that have not received some degree of phylogenetic inquiry, and some examples seem particularly noteworthy (this list is by no means exhaustive of papers from the last decade): among families (Danforth et al., 2006a, b; Davis et al., 2010), within Colletidae (Michener, 2002; Magnacca & Danforth, 2007; Packer, 2008; Almeida et al., 2008; Almeida & Danforth, 2009; Kuhlmann et al., 2009), within Halictidae (Engel, 2000a; Janjic & Packer, 2003; Coelho, 2004; Danforth et al., 2008; Patiny et al., 2008; Gonçalves & Melo, 2009; Gonçalves, 2010), within Andrenidae (Engel, 2000b; Ascher, 2003; Roig-Alsina & Compagnucci, 2003; Larkin et al., 2006; Ramos & Melo, 2010), within Melittidae (Michez et al., 2009), within Megachilidae (Engel, 2004a; Praz et al., 2008; Sedivy et al., 2008) and among the Apidae (Engel, 2000c, 2001a, b; Schwarz et al., 2003; Camargo & Pedro, 2003a, b; Rightmyer, 2004; Anjos-Silva et al., 2007; Straka & Bogusch, 2007; Rasmussen & Cameron, 2007; Cameron et al., 2007a; Cardinal & Packer, 2007; Dubitzky, 2007; Kawakita et al., 2008; Schaefer & Renner, 2008; Michez et al., 2008a; Ramírez et al., 2010; Rehan et al., 2010). Although relationships among the families have shifted between studies (e.g. Alexander & Michener, 1995; Danforth et al., 2006a, b; Davis et al., 2010), the families themselves have proven relatively well circumscribed, with certain refinements here and there (e.g. demotion of Oxaeidae, removal of the paraphyletic Anthophoridae, proper association of Ctenoplectridae and Fideliidae): authors generally recognize six or seven families (e.g. Engel, 2005; Michener, 2007) (Fig. 1). Bee phylogenetics is assuredly healthier and more robust today than it ever has been.

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Figure 1. Representative diversity of the families of bees (after Grimaldi & Engel, 2005).

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Monophyly of the bees is of little debate. A few authors have considered the bees as polyphyletic (e.g. Robertson, 1904), but melittological monophyly has been recovered repeatedly in studies critically examining myriad forms of data (e.g. Börner, 1919; Michener, 1944; Danforth et al., 2006a; Davis et al., 2010; among many other citations). Contrary to the assertions of some authors (e.g. Börner, 1919; Lanham, 1960, 1979, 1980), the bees are a derived lineage (clade Anthophila) among the Apoidea, a larger group encompassing Anthophila and the grade of apoid wasps formerly known as ‘Sphecoidea’ (or Spheciformes) (Müller, 1872; Ashmead, 1896; Michener, 1944, 2007; Bradley, 1958; Malyshev, 1968; Brothers, 1975, 1999; Königsmann, 1978; Lomholdt, 1982; Alexander, 1992; Brothers & Carpenter, 1993; Alexander & Michener, 1995; Prentice, 1998; Melo, 1999; Engel, 2001b; Danforth et al., 2006a, b; Ohl & Bleidorn, 2006; Pilgrim et al., 2008; Davis et al., 2010). Non-molecular characters supporting Anthophila as a natural group include: the presence of branched or plumose setae (although this also occurs elsewhere in Aculeata); the subantennal sulci internally connected to a fan-shaped sheet of the tentorium; the labrum thickened basally and articulated at the clypeal apical margin; the mesocoxa is dorsoventrally elongate, about equal to the distance from the mesocoxal summit to the hindwing base (hemicryptic in short-tongued bees except melittids); the presence of a mesotibial comb (reversed or vestigial among oxaeines, some melittids and long-tongued bees; Jander, 1976); the presence of the metatibial plate (reversed or frequently vestigial among the bees); the metabasitarsus broader than the subsequent tarsomeres; the absence of the metabasitarsal (posterior) strigil; the cleft pretarsal claws (reversed to simple claws frequently among the bees, and with some minute teeth among apoid wasps); the presence of an alar fenestra cutting across 1 m-cu and not M in the forewing; cu–a shorter than the second abscissa M + Cu (except in Caupolicana) in the hindwing; the mid-dorsal reduction of the female seventh metasomal tergum and formation of lateral hemitergites; the seventh and eighth metasomal sterna in males modified and concealed by the sixth sternum, or with only extreme apical portions exposed; the larva maxilla with a single apical papilla (secondarily reversed in some melittids and apids); the cleaning of the foreleg by drawing it through the flexed midleg at the femorotibial joint; and most notably the consumption by the larva of pollen mixed with nectar or floral oil, or glandular secretions of adults who consume such plant materials [reversed in one derived clade of Trigona (Camargo & Roubik, 1991), and apparently in Lisotrigona and Pariotrigona, which collect mammalian tears, and probably provision their nests with this protein-rich fluid (Bänziger et al., 2009)]. An additional feature discussed at times is the development of a single sperm cell from each spermatocyte (Lomholdt, 1982), but there remains insufficient sampling to determine the validity of this attribute for supporting Anthophila. The sister group to the bees has been controversial but is considered to be the digger wasp family Crabronidae (e.g. Ashmead, 1896; Lomholdt, 1982; Alexander, 1992; Melo, 1999), although monophyly of this family relative to Anthophila is of some question (Ohl & Bleidorn, 2006). It is interesting that among the Crabronidae there exists at least one species, Krombeinictus nordenae Leclercq, that has become independently a ‘bee’, provisioning its brood with pollen and nectar (Leclercq, 1996; Krombein & Norden, 1997a, b; Krombein et al., 1999). It is greatly hoped that investigation of crabronids and other apoid wasps continues to receive intense scrutiny, as it is among these close relatives that the greatest insights into bee origins shall be revealed.

Despite the low number of available specimens relative to other arthropod lineages, palaeomelittology has gradually gained wide acceptance, and has revised phylogenetic, biogeographic and evolutionary behavioural patterns previously established solely on recent species (e.g. Michener, 1982; Michener & Grimaldi, 1988; Rasnitsyn & Michener, 1991; Engel, 1995, 1999a, 2001a, b, 2006; Rozen, 1996a; Camargo et al., 2000; Michez et al., 2007, 2008a; Engel et al., 2009) (Fig. 2). Indeed, the use of insect fossils has been adopted broadly across insect systematics, and has become commonplace in all levels of analysis (Grimaldi & Engel, 2005). Naturally such palaeontological data are used principally for dating clades and regularly for the calibration of molecular estimates of divergence, although caution in the application of such techniques is needed (Ware et al., 2010). Palaeomelittological evidence has generally indicated an origin for bees around 125 Ma, and just prior to the explosive diversification of angiosperms in the early mid-Cretaceous (Engel, 1996, 2001b, 2004b; Ohl & Engel, 2007). The fossil record of apoid wasps has also expanded significantly in the last decade, greatly refining estimates for the wasp–bee divergence, and offering a wealth of data for apoid wasp phylogeny (e.g. Antropov, 2000, 2010; Ohl, 2004; Bennett & Engel, 2006; Ohl & Bennett, 2009; Ohl & Spahn, 2010).

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Figure 2. The fossil corbiculate apine, Melissites trigona Engel (Apinae: Melikertini), in middle Eocene (Lutetian) Baltic amber (after Engel, 2004b).

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Given the robustness of molecular and morphological work on bees and their close relatives, and an abundance of researchers devoted to systematic melittology, obviously the opportunity for the exploration of alternative character systems, new areas of emphasis and the exploitation of new technologies is ripe. Yet despite various deviations from relying solely on adult external morphology and DNA sequences, the use of alternative character systems continues to be modest, and largely the same kinds of techniques are relied upon. Whereas similar suites of data are part of the norm or are being intensely explored in other areas of insect systematics, such work has not generated a corresponding intensity among melittologists. Accordingly, melittology is conservative by comparison, giving solid preference to a restricted set of techniques and available character sources. This is not to criticize the efforts of anyone in the field, and indeed my few contributions to the topic have certainly fallen well within such a traditional scope (indeed, even more narrowly than most of my peers). Perhaps more so than most melittologists, I have held fast to the status quo. Thus, some constructive observations are provided here for what appear to be areas of investigation that have received little attention from the wider community of bee systematists, but that show signs of potential and recent, or even increasing, interest. Naturally, this is not exhaustive, and there are areas in which melittologists have already pushed into understudied domains. Nonetheless, I hope that by highlighting some examples of positive forays away from standard practices, such work might receive increased attention and ideally become part of the modus operandi among the next generation of melittologists.

As in any endeavor, the adoption of new or alternative techniques and sources of data does not mean the cessation of more traditional activities. Indeed, such new or underexploited resources often reach their potential more fully when synergized with those already well tested, and melittologists have largely not fallen victim to the temptation to abandon informative data simply because a particular method or technique was not in vogue. Accordingly, I do not mean to imply that resources or energies have been wasted, or that traditional adult morphology and molecular studies should be pushed aside in favour of any other line of inquiry. Instead, the adoption of new techniques and reinvestment in otherwise marginalized data sources will certainly strengthen an already robust field.

Internal morphology and soft-tissue anatomy

  1. Top of page
  2. Internal morphology and soft-tissue anatomy
  3. Immature bees
  4. Biology and behaviour
  5. New imaging technologies
  6. Sundry natural progressions
  7. Conclusion
  8. Acknowledgements
  9. References

Recently there have been surveys of frequently ignored exoskeletal components that, not surprisingly, have revealed variation pertinent to phylogenetic studies at all levels (e.g. Lanham, 1977; Schönitzer & Renner, 1980; Michener, 1981; Michener & Brooks, 1984; Schönitzer, 1986; Jander & Jander, 2002; Packer, 2003, 2004), and these characters are incorporated increasingly into analyses (e.g. Roig-Alsina & Michener, 1993; Rightmyer, 2004; Cardinal & Packer, 2007; Packer, 2008). Typically, these have concerned merely long-ignored external structures or internalized components of familiar external features, such as the basal sclerites of the sting apparatus. More wholly internalized structures have usually not received detailed examination, despite the fact that the internal morphology of the exoskeleton is certainly familiar to melittologists. Such characters have been discussed in numerous comparative studies (e.g. Michener, 1944), and have been utilized to some degree in taxonomic revisions and analyses of bee phylogenies (e.g. Prentice, 1991; Alexander, 1992; Roig-Alsina & Michener, 1993; Alexander & Michener, 1995; Roig-Alsina, 1997). Thus, in all fairness, melittologists have already been using such information in their attempts to elucidate relationships. Nonetheless, the number of structures examined has been relatively limited, and a thorough systematic survey of internal morphology could prove illuminating. The work by Prentice (1998) on apoid wasps documented a wealth of information on internal as well as external structures, and there is no reason to believe that a critical comparative survey focused specifically on internal morphology across the bees would not enlarge the body of data available for analyses.

Of more novelty is the use of soft-tissue anatomy for phylogenetic data. Again, there are well-known examples of taxonomically informative characters being extracted from bee internal anatomy. Among these perhaps the most familiar is the structure of the ovaries and ovarioles (Iwata, 1955; Iwata & Sakagami, 1966; Rozen, 1986, 2003; Alexander & Rozen, 1987). The number of ovarioles and testicular tubules turns out to be important in supporting the family-level classification of bees. The diverse family Apidae differs from other bees in having a basic number of four (with variation in highly social and cleptoparasitic taxa); in all other families of bees the basic number is three (Michener, 2007). However, several other internal organs have received comparative attention in the past, and histological work that is ongoing has identified informative character suites. For example, investigations of the structure of the salivary glands, proventriculus, cardiac valves, ventral nerve cord, spermatheca, wax glands, scent glands, rectal glands and endophallus, or cytological features of the caste determination system, have discovered discrete character variation that is generally congruent with studies based on other data (Cruz-Landim, 1963, 1967, 1968; Cruz-Landim & Rodrigues, 1967; Cruz-Landim et al., 1972; Kerr, 1987; Roig-Alsina, 1993; Serrão, 2001, 2004, 2005, 2007; Peixoto & Serrão, 2001; Martins & Serrão, 2002). Perhaps one of the most interesting uses of data from the internal tissues investigated the chemical secretions of the Dufour's gland (Cane, 1983a, b). Naturally, the time and complexity involved with a thorough review of even a single species tends to limit the number of taxa surveyed in such analyses. Nonetheless, these innovative studies amply demonstrate the potential value of the internal anatomy and physiology for providing unique data pertinent to sundry analyses of relationship.

Immature bees

  1. Top of page
  2. Internal morphology and soft-tissue anatomy
  3. Immature bees
  4. Biology and behaviour
  5. New imaging technologies
  6. Sundry natural progressions
  7. Conclusion
  8. Acknowledgements
  9. References

Although the utilization of data from immature stages is more commonplace (albeit still reduced relative to the study of adults) in some lineages of insects, it has not received wholesale acceptance among melittologists, despite the diversity of character information available. This may derive from a perceived challenge in obtaining sufficient material for study and inclusion in comparative studies, and indeed the immatures are less easily recovered compared with those of mayflies or caddisflies, in which the systematics of such stages is rather advanced. Among holometabolan insects, the use of immatures in analyses of Coleoptera, Diptera, Lepidoptera, Trichoptera and Neuropterida are more familiar (e.g. Meier & Lim, 2009; see also the virtual issue in Systematic Entomology on ‘Larval Information in Entomological Systematics'), and is increasingly perceived as simply a part of ‘doing business' in the field today. Use of such data among Hymenoptera lags significantly behind that of related orders, and this is largely a result of the relatively simplified morphology of the many endoparasitoid larval stages (although even among these lineages variation is well documented and should receive more detailed examination), and the difficulties in obtaining them. However, among the Aculeata the immature stages are typically more complex in their anatomy, and offer a greater variety of observable traits for study.

Modern detailed study of the structure of bee larvae started around the late 1920s with the many contributions from Grandi (culminating in Grandi, 1961), and the extensive study of bee larvae by Michener (1953). However, recent studies and the systematic documentation and analysis of immature stages have been largely through the efforts of one man (J. G. Rozen, Jr). He, above all others, has demonstrated consistently that the immature stages of bees can be obtained readily if a concerted effort is applied toward their discovery (not to mention the associated wealth of data on the nesting biology of these same species, vide infra). Basically, if the study of immatures is made a priority, then the material and information will be there for the taking. Through these and related studies, data from immatures has been applied regularly towards particular phylogenetic questions, and has proven repeatedly to be of considerable value (e.g. Rozen & McGinley, 1974; Michener, 1977; Rozen et al., 1978; McGinley, 1981; McGinley & Rozen, 1987; Alexander, 1990; Rozen, 1993; Reyes, 1998). Indeed, some of the earliest of Hennigian approaches to relationships among groups of bees came from the application of larval characters (e.g. Rozen, 1966, 1969). A quick perusal of some recent works by Rozen highlights the plethora of information residing in bee pupae, larvae and even eggs (e.g. Rozen, 2000, 2001, 2003; Rozen & Özbek, 2003). Certainly many others have contributed to the study of ‘baby bees', but no one has adopted it as a natural part of ongoing research programmes. Although conflict exists between the patterns implied by adult and immature morphologies (e.g. Michener, 1977; Rozen, 1996b; Rozen et al., 1997), there is also much congruence and no legitimate reasons for not spurring others to build programmes as intensive and successful as the one championed by Rozen. More and more characters from immatures are appearing in cladistic analyses, and it is desirable that this persists. Larval data, in conjunction with molecular work, have revealed lineages that were previously unrecognized from adult morphology (Chenoweth et al., 2008), have suggested alternative patterns in the number of origins of cleptoparasitism among apids (Straka & Bogusch, 2007), have added greater support to relationships among honey bees (Engel & Schultz, 1997), and have reinforced hypotheses among the major groups of Halictidae (Rozen, 2008). In addition, considerable information has been compiled for out-groups among the apoid wasps (e.g. Evans & Lin, 1956a, b; Evans, 1957, 1958, 1959, 1964; Ohl & Linde, 2003). This is an important and frequently underutilized source of information, and one for which melittologists are amply rewarded not only in the enrichment of their data sets but in the biological information simultaneously obtained during the recovery of such material. A continuing and growing emphasis on the developmental stadia of bees will also set the stage for eventual evolutionary developmental studies. For example, the application of molecular and developmental approaches to addressing hypotheses regarding the origin and formation of structural traits associated with cleptoparasitism (e.g. Wcislo, 1999) will require expansion, and will build upon already well-developed phylogenies for groups in which this transition has taken place more frequently and recently (e.g. Danforth, 1999), along with concomitant work on the development of these same species. Considerable strides have already been made, but the next 50 years will not see the same leaps unless this momentum is maintained and accelerated by a continually expanding number of melittologists.

Biology and behaviour

  1. Top of page
  2. Internal morphology and soft-tissue anatomy
  3. Immature bees
  4. Biology and behaviour
  5. New imaging technologies
  6. Sundry natural progressions
  7. Conclusion
  8. Acknowledgements
  9. References

It is widely known and accepted that ecological and behavioural attributes can provide significant suites of characters for phylogenetic analysis (Wenzel, 1992; de Queiroz & Wimberger, 1993; Miller & Wenzel, 1995; Wimberger & de Queiroz, 1996; Proctor, 1996; Rendall & Di Fiore, 2007). This is assuredly no revelation to melittologists, as the study of bee biology and behaviour is extensive, particularly in the area of sociobiology. Similarly, the phylogenetic interpretation of behaviours and ecologies is well established among bee workers, although more typically in the exploration of such traits across topologies derived from other sources (e.g. Raffiudin & Crozier, 2007). Such work has been of considerable importance for understanding social (e.g. Schwarz et al., 2007) and host–plant evolution (e.g. Patiny et al., 2008; Michez et al., 2008b; Sedivy et al., 2008). Moreover, the pre-eminent attribute defining bees is of course the consumption of pollen mixed with nectar and floral oil by the larva, and the concomitant collection of such materials by the adult, a combined suite involving physiological, morphological and behavioural novelties.

There has been no more intensely investigated behaviour in bees than sociality among the corbiculate Apinae. Ethological data found its way into several corbiculate analyses early on, but was oversimplified to solely the degree of sociality observed (e.g. Michener, 1990; Prentice, 1991; Chavarría & Carpenter, 1994). Many behaviours and biological features have been presented for corbiculates in a comparative framework, and frequently discussions of such traits have been formulated in a more-or-less Hennigian manner. For example, several characters of meliponine nest architecture were discussed and even polarized by Wille & Michener (1973), although based on the limited suite no attempt was made to build a phylogeny or revised classification. Similar comparative surveys were provided by Sakagami (1976) in relation to the biology of bumble bees, and by Zucchi et al. (1969) for orchid bees. Jander (1976) and Michener et al. (1978) identified numerous attributes in the repertoires of bee grooming and pollen manipulation that were interpreted in the light of existing phylogenies, but these behaviours could just as easily be coded for analysis with morphology or molecules. Michener (1974) provides a wealth of comparative information on the social bee lineages. The ultimate culmination has been the study by Noll (2002), in which many of the aforementioned studies were distilled and coded for an analysis that provided robust results largely congruent with investigations based on morphological or molecular data. Naturally, behavioural studies continually uncover new information that can be interpreted not only in a phylogenetic framework, but can be built into ethological data matrices. For example, recent discoveries on the occurrence of nectar transfer in corbiculate bees support an Apini-Meliponini clade (Hart & Ratnieks, 2002), alongside the results of Noll (2002). An overview of nomiine behaviour identified diverse traits that were putatively of systematic value for the subfamily (Wcislo & Engel, 1996), and the preliminary survey of the proboscis extension reflex by Vorel & Pitts-Singer (2010) suggests it may support the corbiculates or a larger clade of Apidae relative to megachilids.

Brief phylogenetic considerations based on limited suites of behaviour were also put forward by Lindauer (1956; overviewed by Dyer, 1991), Sakagami & Michener (1962), Hobbs (1964), Rozen (1977), Eickwort & Sakagami (1979), Eickwort et al. (1981) and Pereira-Martins & Kerr (1991), among many others. [Obviously, these are merely a very few examples, and a thorough consideration of the evolutionary biology of bees is well beyond this brief article. Michener (2007) is an excellent entry point into this vast body of literature, as is the extensive work of Iwata (1976).] More relevant have been the analyses that incorporated ethological characters directly into matrices (e.g. Michener, 1977; McGinley & Rozen, 1987; Alexander, 1990; Rozen, 1991; Müller, 1996; Engel & Schultz, 1997; Reyes, 1998), or included analyses based entirely on such character suites (e.g. Drumond et al., 2000; Bosch et al., 2001; Noll, 2002). Behavioural traces such as cut leaves or nest elements can also be preserved, and, even in the absence of body fossils, used to establish minimum clade ages, document the palaeobiogeographic presence of particular lineages or estimate diversity in palaeobiotas (e.g. Elliott & Nations, 1998; Engel, 1999b, 2004b; Genise et al., 2002; Wappler & Engel, 2003; Engel & Perkovsky, 2006; Sarzetti et al., 2008; Wedmann et al., 2009; note that putative Triassic ichnological records of bees have been dismissed conclusively by Lucas et al., 2010). These and the aforementioned studies repeatedly demonstrate the utility to some level of biological and behavioural attributes in the systematic study of bees, and it is hoped that such characters will be found more regularly in investigations to come. Given the considerable interest in bee behaviour and ecology, a steady stream of information should be forthcoming, and it would be unfortunate not to utilize these data thoroughly, and thus encourage future systematic melittologists to carry on traditional original field observations.

New imaging technologies

  1. Top of page
  2. Internal morphology and soft-tissue anatomy
  3. Immature bees
  4. Biology and behaviour
  5. New imaging technologies
  6. Sundry natural progressions
  7. Conclusion
  8. Acknowledgements
  9. References

Whereas traditional comparative morphological investigation remains an immensely useful tool and a natural complement to molecular and other forms of data, the availability of new fine-scale imaging techniques are helping to revive and revolutionize this honoured area of study. In the same way that scanning electron microscopy provided ‘new eyes' through which to see familiar structures, so too are technologies once restricted to the medical and engineering communities. Among the new and increasingly accessible tools the three-dimensional rendering provided by confocal laser scanning microscopy (CLSM) and X–ray computerized microtomography (µ–CT), currently have the greatest potential (Hörnschemeyer et al., 2002; Klaus et al., 2003; Klaus & Schawaroch, 2005; Schawaroch et al., 2005; Friedrich & Beutel, 2008). Each is mentioned briefly, and some examples of their application to the study of insects are provided. These technologies have enhanced the visualization of not only the adult external morphological structures employed by all melittologists, but have complemented the study of soft tissues or immatures (e.g. the larval head capsule) mentioned above.

An application of CLSM to ephydroid fly genitalia (of both males and females), mouthparts and antennae demonstrated the amazing fidelity of this technique (Schawaroch et al., 2005). The minute and frequently cleared sclerites of structures typically examined as slide-mounts with compound or light microscopy, were rendered in their natural three-dimensional configuration with such clarity as to revise some previous morphological interpretations of these very structures. Similar results were obtained in a study of different staining techniques for lepidopteran genitalia (Lee et al., 2009). CLSM cannot observe deeper layers within larger structures or from particularly large insects, and so it is best applied to smaller, isolated components. Among the bees, the study of the labiomaxillary complex or of genitalic sclerites, particularly among the more diminutive species, using CLSM reconstructions could provide a new perspective on otherwise familiar character suites.

Likewise, three-dimensional rendering can be provided by µ–CT. Such scans, even using low-energy desktop models, can produce impressive rendering of the external morphology, again revolutionizing the visualization of even the most traditional of external characters (Friedrich & Beutel, 2008). Perhaps even more tantalizing are the higher level energy scans currently provided by a more restricted set of facilities. The resolution of such data is of a significantly higher density, and permits the discrimination of individual tissues. For example, such techniques visualize the arrangement of muscles, nerves, internal sclerites, or even minute and difficult to discern external sclerotic structures (e.g. axillary sclerites) in various insects. Such rendering, whether produced by a desktop CT-scanner or through a high-energy synchrotron facility, have proven to be of considerable utility in homologizing and identifying phylogenetically informative characters among orders, as well as within particular lineages (e.g. Hörnschemeyer et al., 2002; Beutel et al., 2008; Friedrich et al., 2009; Friedrich & Beutel, 2010). Not surprisingly, given the scale of resolution achievable with µ–CT imaging, it is also becoming widespread in insect palaeontology (e.g. Grimaldi, 2003; Tafforeau et al., 2006; Lak et al., 2008, 2009), and as the technology continues to improve, surely it will become more pervasive. Among the bees the use of µ–CT has been applied only within the context of a brief exploratory account of the stingless bee Trigona carbonaria Smith and an unidentified Amegilla (Greco et al., 2008). The application of µ–CT to morphological studies of bees will surely enhance the information obtained from external and internal structures.

Sundry natural progressions

  1. Top of page
  2. Internal morphology and soft-tissue anatomy
  3. Immature bees
  4. Biology and behaviour
  5. New imaging technologies
  6. Sundry natural progressions
  7. Conclusion
  8. Acknowledgements
  9. References

For much of the past 50 years the emphasis on determining relationships among bees has focused on higher levels. Certainly excellent species-level revisions were, and continue to be, undertaken (e.g. Dathe, 1980; Daly, 1983; McGinley, 1986, 2003; Snelling & Rozen, 1987; Snelling, 1990; Rozen, 1992; Snelling & Stage, 1995a, b; Tadauchi & Xu, 2002, 2003; Rightmyer & Engel, 2003; Whitehead & Eardley, 2003; Coelho, 2004; Exley, 2004; Davies & Brothers, 2006; Pauly, 2008; Rightmyer, 2008; Gonçalves, 2010), but detailed cladistic work within genera was vastly outweighed by the number of discussions and investigations (numerical and otherwise) focused on the ‘bigger’ picture among the bees. Such a bias was certainly necessary as it is vital to ascertain that a particular subfamily, tribe or genus is monophyletic, and to clarify the most pertinent out-groups for any more fine-scale study. Moreover, certain questions in the evolution of bees have necessitated a suprageneric perspective, such as the number of origins of eusociality among corbiculate bees, coarse biogeographic patterns, or timing the divergence of bees from among the apoid wasps. As the supraspecific classification of many groups is becoming more and more finely resolved, the number of analyses delving into species-level relationships is growing. Such finer-scale investigations, along with careful characterizations of behavioural and ecological adaptations, where pertinent, can lead to greater precision and improved evolutionary explanations. Such analyses have revealed historical biogeographic patterns (e.g. Janjic & Packer, 2003; Coelho, 2004; Fuller et al., 2005; Ramos & Melo, 2010), patterns of host–plant usage (e.g. Michez et al., 2008b; Sedivy et al., 2008) and particularly important insights into transitions in social evolution (e.g. Danforth et al., 2003; Schwarz et al., 2007; Tierney et al., 2008).

Just as more finer-scale analyses are a natural progression of the voluminous work being undertaken in systematic melittology, it would be remiss of me not to briefly note the amazing wealth of information garnered from continued advances in molecular systematics. It goes without saying that molecular systematics has been a tremendous asset to phylogenetic research, and an increasing reliance on molecular data has arisen, alongside the continued use of morphological and other forms of data (Bybee et al., 2010), which should continue, given that not everything is encapsulated in the genomic sequences, regardless of how complete they might be (Freudenstein et al., 2003). Already its application to bees has proven to be of considerable interest and of great resolving power, either in isolation or when combined with morphology (e.g. Chenoweth et al., 2008; Michez et al., 2009, or any of the other previously cited works). But even here technological developments will serve to propel DNA sequencing, which has now become routine and rightly part of the regular operation of phylogenetic research, to even greater contributions. Technological advances are making it possible to more easily capture larger and larger sections of the genome from more taxa, in less time and for less cost. Entire genomes are becoming more readily obtained, leading to an era of phylogenomics. Full mitochondrial genome analyses have been explored for various insect orders (e.g. Castro & Dowton, 2005; Cameron et al., 2007b, 2009), and such analyses will become more frequent. As demonstrated in the aforementioned works there are inherent challenges to mitochondrial genomic analyses that can affect the outcomes greatly, and so, as with the evaluation of any set of data, the appropriate means of analysis must be considered. Furthermore, the apparent range of applicability of such genomic data to both ancient and more recent divergences highlights not only its utility for a group as relatively recent as the bees (at least among Holometabola, or even within Hymenoptera), but for simultaneously recovering many levels in the hierarchy (e.g. Cameron et al., 2007b). Molecular data for bees will continue to proliferate in the number of species as well as the diversity of markers sequenced. Accordingly, we will see an inevitable scaling up from the multiple gene phylogenies of today to what can be labeled more truly as phylogenomic analyses, either based on entire mitochondrial genomes or on a greater diversity of markers. Unlike the areas elaborated upon above briefly above, bee phylogenomics, in whatever particular form it manifests itself, is in its most initial stages (e.g. the relatively large number of genes employed by Kawakita et al., 2008). As already alluded to, bee phylogenomics will manifest its greatest utility when unified with large suites of phenotypic information (Freudenstein et al., 2003).

Of course, systematics is more than just the building of evolutionary trees, and the applications of those topologies to evolutionary and ecological questions. Melittology is fortunate in that, along with the increased use of newer methods, classical methods continue to be practiced to great effect. For example, catalogues are among the most important tools that systematists need and use. Gusenleitner & Schwarz (2002) for the Behemoth of a genus, Andrena Fabricius, Moure et al. (2007) for all neotropical bees, Ungricht et al. (2008) for Palaearctic Osmiini, Eardley & Urban (2010) for afrotropical bees and Ascher & Pickering (2010) for the world (albeit not annotated as in the former treatises), are all examples of such vital compendia. They represent our current knowledge of diversity, permit us to understand local and large-scale faunas, and provide access to a vast and historical literature. These are the first resources referenced at the start of any inquiry, and their value is immense. As more such efforts migrate to online resources, their impact will be underscored further, and it is hoped that they may become more interconnected leading ultimately to a fully annotated, world catalogue of the bees, complete with distributions, biologies and aids to identification. Revisional studies of various taxa continue to be prepared (e.g. LaBerge, 2001; Daly & Magnacca, 2003; Coelho, 2004; Thorp & LaBerge, 2005; Dathe, 2006; Pesenko & Pauly, 2009; Engel, 2009, 2010; Gonçalves, 2010; Ramos & Melo, 2010), and remind us continually that descriptive science is as valuable and as relevant today as ever (Grimaldi & Engel, 2007). Excitingly, we are witness to a significant transition in the dissemination of knowledge. In the same way the evolution from scrolls to codices, and from the painstaking copying of monkish scribes to automated printing, radically altered the means, speed and mode of information transmission, current advances in electronic publication and data sharing are thrusting this progression into previously unimagined fora. Searchable online resources such as checklists linked to georeferenced, specimen-level data from collections, permit live mapping of distributions based on museum specimens (e.g. Ascher & Pickering, 2010), and make accessible swaths of data that were once challenging to obtain. Interactive keys make seemingly intractable groups easy to determine (e.g. Stevens et al., 2007). In addition, recent technological advances in electronic publication permit the rapid generation of natural language descriptions from morphological data matrices (although not all characters useful for circumscribing taxa are necessarily coded in matrices), provide links to internet registers and databases, and even facilitate the automated production of species accounts, revisions and online identification keys (a.k.a. cybertaxonomy; e.g. Penev et al., 2009, 2010; Blagoderov et al., 2010). These revisions, whether electronic or in traditional print, with their keys, descriptions and illustrations, make possible, among other things, the accurate identifications of bees. Such identifications are essential for many sorts of applied or ecological investigations, such as pollination studies important in agricultural and natural ecosystems, and the conservation of biotas. Revisions and monographs, whether coupled with cladistic analyses or not, serve great purpose, and make it possible to know what fundamental units must be considered in any phylogenetic treatment. Some identification keys to bees are poorly constructed, are challenging and can lead to immense frustration, but by far the majority are highly accessible. Nonetheless, some systematists wish to increasingly rely on molecular barcodes, partly to save money and time. This method has proved useful for some activities, but is dependent on a minute sample of the genome that may or may not suggest species-level differences, or lack thereof, among populations. As a tool this method has some significant challenges (e.g. Ebach & Holdredge, 2005; Will et al., 2005; Hickerson et al., 2006; Meier et al., 2006; Hołyński, 2010). Even the most limited sampling of morphological attributes alone represents a broader sampling of the genome than a single gene barcode, particularly given that a seemingly simplistic feature can be highly polygenic in nature. Surely a greater sampling of genetic information, either through morphological characters or through the sampling of as many genes as possible, is more informative for the circumscription and identification of species than isolated fragments. The most valuable approach is the continuation of revisionary works, and for particularly troublesome cases in which morphological variation appears limited, to then bring to bear as many other forms of data as can be found, be they multiple gene sequences, behaviour, etc. More and diverse data with increased accuracy should always be preferred to overly simplified, quick answers.

Conclusion

  1. Top of page
  2. Internal morphology and soft-tissue anatomy
  3. Immature bees
  4. Biology and behaviour
  5. New imaging technologies
  6. Sundry natural progressions
  7. Conclusion
  8. Acknowledgements
  9. References

Given that the systematics of Apoidea is quite advanced relative to many groups of Hymenoptera, a growing holistic approach is timely: future students of the subject should be encouraged to seek more than just the tried and true morphological or molecular toolkits. The benefit to the field could be substantial. It will be exciting to watch as the kind of adventurism seen in other insect lineages becomes more pervasive among bee systematists, re-invigorating areas in which some have already trodden, digging into subjects yet unexplored or reaching out to co-opt techniques and technologies originally intended for other purposes. I believe that the initial steps for all of these have been made by the pioneers cited herein, alongside those who have advanced in every way our understanding of bees.

Acknowledgements

  1. Top of page
  2. Internal morphology and soft-tissue anatomy
  3. Immature bees
  4. Biology and behaviour
  5. New imaging technologies
  6. Sundry natural progressions
  7. Conclusion
  8. Acknowledgements
  9. References

I am grateful to Lars Vilhelmsen and Pete Cranston for encouraging me to compose this brief opinion piece for the virtual issue dedicated to ‘Systematic Melittology’, and for their constructive comments. Charles D. Michener, Ismael A. Hinojosa-Díaz, Daniel J. Bennett, Steven R. Davis, Michael Ohl, John S. Ascher, Jaime Ortega-Blanco and an anonymous reviewer provided particularly valuable discussion and input for the ideas expressed herein. This is a contribution of the Division of Entomology, University of Kansas Natural History Museum.

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  1. Top of page
  2. Internal morphology and soft-tissue anatomy
  3. Immature bees
  4. Biology and behaviour
  5. New imaging technologies
  6. Sundry natural progressions
  7. Conclusion
  8. Acknowledgements
  9. References
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