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Phylogenetics of Allodapine Bees: a Review of Social Evolution, Parasitism and Biogeography*

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Phylogenetics of Allodapine Bees: a Review of Social Evolution, Parasitism and Biogeography* Apidologie 39 (2008) 3-15 Available online at: © INRA/DIB-AGIB/ EDP Sciences, 2008 www.apidologie.org DOI: 10.1051/apido:2007045 Review article Phylogenetics of allodapine bees: a review of social evolution, parasitism and biogeography* Simon M. TlERNEY1'2, Jaclyn A. SMITH1, Luke CHENOWETH1, Michael P. SCHWARZ1 1 School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, S.A. 5001, Australia 2 Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Balboa, Republic of Panama Received 15 November 2006 - Revised 3 October 2007 - Accepted 3 October 2007 Abstract - It has been assumed that allodapine bees represent early stages in the evolution of social be- haviour. Early studies suggested that sociality evolved from solitary forms, and that the solitary to social transition coincided with a transition from mass to progressive provisioning of brood. Recent studies chal- lenge both of these assumptions, they suggest that: (i) Macrogalea replaces Halterapis + Compsomelissa as the sister group to all other genera; (ii) sociality is plesiomorphic for the tribe; and based on extended Halterapis research, (iii) there are no strictly solitary allodapine species and, therefore, no reversals to soli- tary living. Penalised likelihood dating of Bayesian inferred phylograms show allodapine lineages have an origin older than 40 Mya. The early origin of sociality in this tribe may explain the diverse array of social organization (and social parasitism) found in species across a range of clades, and the age of the group raises curious biogeographic scenarios. social evolution / phylogenetics / alloparental care / brood provisioning / allodapine bees 1. INTRODUCTION cally these two bee groups have provided in- sights on the evolution of social behaviour The Allodapini comprise one of four tribes that studies of more advanced obligate easte- rn the Xylocopinae (Apidae). Allodapines are based insect societies are unable to address (re- unusual among bees in rearing their brood in viewed in Schwarz et al., 2007). an open burrow (with no brood cells) exca- The first detailed studies of allodapines vated in dead plant stems and branches, and were carried out by Charles Michener who ex- the majority of species progressively feed their amined a large number of species from both brood. This extended contact between moth- Africa and Australia and published a wide va- ers and their offspring and the array of fac- riety of monographs and papers covering nest- ultative social nesting species, that appeared ing and social biology (e.g. Michener, 1965, to vary from simple (subsocial) to more so- 1971), social parasitism (Michener, 1970b), phisticated (eusocial) levels of organisation, nesting substrates (Michener, 1970a), adult made the allodapines seem particularly useful and immature morphology (eg. Michener, for uncovering the earliest steps in social evo- 1975a, b, c, d, 1976), and egg-size variation lution. In this sense, they were similar to the (Michener, 1973). Michener (1977) also ear- facultatively social halictine bees that showed ried out the first phenetic classification of al- a range from solitary to eusocial, and histori- lodapines, and contrasted the discordant re- lationships suggested by larval, pupal and Corresponding author: S.M. Tierney, adult characters. This body of work greatly [email protected] influenced studies of insect social evolution * Manuscript editor: Eduardo A.B. Almeida (e.g. Michener, 1974), and allodapines were Article published by EDP Sciences and available at http://www.apidoloqie.orq or http://dx.doi.Org/10.1051/apido:2007045 S.M. Tierney et al. thought to comprise one of the best examples (Michener, 1977; Reyes and Michener, 1992). of the 'subsocial route' to eusociality whereby Contradictions between data sets led to the advanced sociality is thought to have been formation of a consensus phylogeny based on derived from the extended contact between a combination of all data sets, and a heavily mothers and their immature offspring (Lin and weighted reliance on a small number of be- Michener, 1972). havioural traits (e.g. egg laying and brood pro- A second period of allodapine research be- visioning) at crucial nodes of the tree (for a gan in the 1980s with a series of within-nest subsequent cladistic revision see Reyes, 1998). ethological studies by Maeta and co-workers These studies suggested Halterapis + (Maeta et al., 1992; and references therein) fo- Compsomelissa as a holophyletic group that cussing on Asian Braunsapis species, and later formed a sister clade to all other allodap- studies by Australian researchers investigat- ines (based on brood provisioning, male gen- ing colony life-cycles, sex allocation and intra- italia, female terga and larval antennae), and colony relatedness of Australian and African retained some ancestral traits found in the species (reviewed in Schwarz et al., 1997, other tribes of Xylocopinae. Based on knowl- 1998, 2007). More recently, allodapine re- edge of Halterapis natural history at the time search has focused on molecular phylogenet- (the only genus to mass provision brood and ics and inference of ancestral characteristics subsocial colonies, Michener, 1971), the logi- arising from changes in the understanding of cal inference was that progressive provision- generic relationships. The molecular phyloge- ing arose from an ancestral allodapine lin- netic studies, combined with detailed social eage that was mass provisioning. Furthermore, data on species from a wide range of genera, it seemed reasonable to suggest that allodap- are leading to a very different interpretation of ine social behaviour was 'primitive' - of rel- social evolution in the Allodapini. atively recent origin. Given that sociality was largely associated with the progressive provi- sioning taxa it was postulated that true social 2. PRE-MOLECULAR THEORIES behaviour might have arisen from within the ON ALLODAPINE PHYLOGENY extant lineages of the tribe. See Figure 1 for representation of the generic phylogenetic ar- Behavioural traits, have played an influ- rangement as per Michener (1977) and Reyes ential role on allodapine phylogenetics, and (1998). for this reason a brief summary of their im- portance in inferring social evolution is help- ful for understanding more recent outcomes. 3. CURRENT UNDERSTANDING OF The paradigm of how insect societies evolved PHYLOGENY: RELATIONSHIPS has historically revolved around the concept AMONG MAJOR CLADES of a progression from simple to more com- plex forms - subsocial nests gradually attain- A series of molecular phylogenetic stud- ing caste based eusocial organization via a di- ies (Schwarz et al., 2003; Bull et al., 2003; rectional 'step-wise' trajectory. Tierney, 2004; Fuller et al., 2005; Schwarz Initial systematic analyses of the Allodap- et al., 2006) present consistent phylogenetic ini based on adult or immature morphological hypotheses that re-order relationships among and behavioural character sets resulted in dis- the main clades, and counter arguments for parate phylogenetic arrangements (Michener, the holophyly of Halterapis + Compsomelissa 1977). Allodapine larvae show greater mor- (Schwarz et al., 2003; Tierney, 2004). To high- phological diversity than all other bees com- light these differences we include a consen- bined (Michener, 1977, p. 38), and the contrast sus Bayesian chronogram, from a recent study in form is so distinct between genera that iden- (Schwarz et al., 2006), in Figure 2 for com- tification is often more easily keyed by larval parison with the generic relationships in Fig- traits, and taxonomic classification of adults ure 1. The main points to note are that: (i) without con-specific larvae can be problematic Macrogalea is a monophyletic clade that is Phylogenetics of allodapine bees mass provisioned — Ceratina Halterapis Compsornelissa Allodape Braunsapis Allodapula Dallodapula Macrogalea Exoneuridia Exoneurella Exoneura Brevineura Figure 1. Genus level cladogram of Allodapini adapted from Michener (1977) and Reyes (1988). Mass provisioning taxa highlighted in grey box. Biogeographic distribution of taxa denoted at terminal branches: Af - Afrotropical; As - Asia (Indomalaya); Au - Australasia; ME - Middle East (Palaearctic). sister group to all other allodapines. Both lar- of Madagascan taxa (not available to Michener val and adult forms display unique charac- (1977) or Reyes (1998)) raises new questions. ters among the tribe that add credibility to An additional molecular phytogeny from a this rearrangement. Larvae of Macrogalea are study by Smith et al. (2007) is presented, generally simple, showing none of the elab- largely to examine the relationships of so- orate setae or tubercle projections of other cial parasites to their hosts (Fig. 3 - dis- genera, and more closely resemble larvae of cussed below), however this work also in- the sister tribe Ceratinini and the ancestral cludes African and Madagascan taxa absent tribes Manueliini and Xylocopini. The remain- from Figure 2, that are of relevance to the cur- ing allodapines then form two further clades, rent discussion. Species of Halterapis occur in consisting of (ii) the endemic Australian ex- southern Africa and Madagascar, but molecu- oneurine genera; and (iii) the African genera lar studies show this is a paraphyletic arrange- from which the Middle Eastern Exoneuridia ment. and the widespread Braunsapis are derived. Madagascan species form a separate clade What is also surprising from molecular phy- that is sister group to all other African
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