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Phylogeny of the Bee Genus Agapostemon (Hymenoptera: Halictidae)

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Phylogeny of the Bee Genus Agapostemon (Hymenoptera: Halictidae) Systematic Entomology (2003) 28, 101±123 Phylogeny of the bee genus Agapostemon (Hymenoptera: Halictidae) JESSICA JANJIC andLAURENCE PACKER Department of Biology, York University, Toronto, Ontario, Canada Abstract. A phylogeny for genus Agapostemon (Hymenoptera: Halictidae) is reconstructed from morphological characters, using all species, with four repre- sentatives of Agapostemonini as outgroup taxa. Parsimony analysis using 150 unordered characters resulted in eighteen equally parsimonious trees, a strict consensus of which is highly resolved for Agapostemon. Based on this analysis, Agapostemonoides Roberts & Brooks is returned to generic status, and a new subgenus is described: Notagapostemon, which includes the rhopalocerus, heter- urus, atrocaeruleus, erebus, kohliellus, nasutus and intermedius groups of Moure & Hurd. Species groups are proposed for Notagapostemon and revised in A. (Agapost- emon). Agapostemon cockerelli Crawford is synonymized with A. obliquus (Provan- cher), A. epichryseus (Morelos) with A. leunculus Vachal, A. inca Roberts with A. heterurus Cockerell, A. hispaniolicus Roberts female with A. centratus (Vachal) and A. hispaniolicus Roberts male with A. alayoi Roberts. Optimization of known behaviours suggests communal ancestry for the genus and infers the prevalence of this behaviour in Agapostemon. Optimization of geographical range suggests a Central American or Caribbean origin of Agapostemon, with one invasion of North America and multiple invasions of South America and the Caribbean. One invasion of the Caribbean suggests arrival from North America via Florida. Introduction Evolutionary reversals, directly from social to solitary behaviour, have often been inferred from phylogenetic Halictidae are often considered an ideal group for studying results (reviewed by Packer, 1997; Wcislo & Danforth, the evolutionary origin of social behaviour in bees. This 1997; Janjic & Packer, unpublished data). Thus, the family, and in particular subfamily Halictinae, exhibits a assumption of an instinctively logical direction of change wide variety of social behaviours. Solitary, aggregative, (such as from solitary to social) may hinder detection of the communal, parasocial and primitively eusocial (sensu phenomenon that has actually occurred. Furthermore, Michener, 1974) behaviours all occur among Halictinae potentially intermediate behaviours, such as communal (Michener & Lange, 1958; Eickwort & Eickwort, 1969; nesting, are generally not found in the same lineages as Roberts, 1969; Michener, 1974, 2000; Eickwort, 1981, eusociality (Packer, 1993). The result is a lack of any clearly 1988; Martins, 1993). Additionally, when considered in the evident stepwise pathway from solitary to eusocial behav- context of phylogeny and classification, the species exhibit- iour. This is compounded by the suggestion that intermedi- ing these behaviours are not clustered together. Rather, the ate series may play no role at all in the evolution of distribution is such that several behaviours are frequently eusociality (Michener, 1985). Thus, the evolutionary pos- found within one group, even within one genus or one itions of potential intermediates, such as communal behav- population of a species, indicating that in most instances iour, remain uncertain. one or more of these behaviours are likely to be relatively As they are distributed among genera within subfamily recent evolutionary developments (Packer, 1997; Wcislo & Halictinae, understanding the fundamental evolutionary Danforth, 1997). patterns of change among the behaviours will require a subfamily level perspective. This approach requires a hypothesis of the behaviour ancestral to each genus, so Correspondence: Laurence Packer, Department of Biology, that evolutionary reversals and innovations within a genus York University, 4700 Keele Street, Toronto, Ontario, M3J 1P3, are not mistaken as plesiomorphic. With the ancestral Canada. E-mail: [email protected] behaviour inferred, the genera can then be viewed as # 2003 The Royal Entomological Society 101 102 Jessica Janjic and Laurence Packer terminals in a subfamily phylogeny, onto which behavioural forty-one recognized species. R. W. Brooks (personal com- changes can be optimized according to the interrelation- munication) considers A. inca as a junior synonym of ships of the genera (Bininda-Emonds et al., 1998). A. heterurus, whereas A. Pauly (personal communication) Just as this perspective requires knowledge of the considers the female of A. hispaniolicus Roberts to belong behaviours at the generic terminals, optimizing these generic to A. centratus, and indicates that the male described as terminals themselves requires species-level information and A. hispaniolicus falls within the range of variation of a degree of phylogenetic resolution of the species interrela- A. alayoi. Both putative synonymies were confirmed by tionships within the genus (Bininda-Emonds et al., 1998). the first author and are validated herein. Thus, to draw a general conclusion as to the pattern of Most Agapostemon species are brilliantly coloured behavioural evolution in the subfamily, one needs first to (Fig. 1), making them more commonly collected than understand the pattern of behavioural evolution within a many bees of similar size. Nonetheless, few have been stud- genus. The necessity of this methodology applies equally to ied in the field and behavioural data are generally lacking studies of geographical distribution, morphology or any for the genus, having been studied for only eight of the other character for which one wishes to determine a forty-one species (Table 1). Although the size of this group higher-level sequence of change. does not prohibit the eventual study of all species, the The agapostemonine group was first recognized only application of the phylogenetic approach to the problem informally as a group of New World halictine bees distinct will indicate those species for which behavioural data will be from Halictus, Lasioglossum and Sphecodes (Eickwort, most informative, thereby directing future research to the 1969a,b). In their discussion of the agapostemonine bees most fruitful path (Packer, 1997). This method, when used of Mesoamerica, Roberts & Brooks (1987) were unable with the appropriate selection of outgroups to root the tree, to find even a single unifying character, and refrained will also permit the optimization of ancestral behavioural from according the group formal tribal status. The agapos- traits for Agapostemon. temonines were thus generally recognized as an informal Communal behaviour, the sharing of a nest entrance and group of New World Halictinae, then consisting of Agapos- tunnels without cooperative provisioning or brood care temon Guerin-Me neville, Agapostemonoides Roberts & (sensu Michener, 1974), has been reported for Agapostemon Brooks, Caenohalictus Cameron, Habralictus Moure, nasutus (Eickwort & Eickwort, 1969), A. kohliellus Paragapostemon Vachal, Dinagapostemon Moure & Hurd (Eickwort, 1988),A.cockerelli(Eickwort, 1981), A. virescens (included as a subgenus of Paragapostemon by Moure & (Abrams & Eickwort, 1980), A. texanus (Roberts, 1969; Hurd, 1987, but assigned generic status by Roberts & Eickwort, 1981), A. angelicus (Eickwort, 1981) and a num- Brooks, 1987, a decision followed by Michener, 2000), ber of the more distantly and ambiguously related Agapos- Pseudagapostemon Schrottky, Rhinetula Friese and temonini and Caenohalictini: Ruizantheda proxima and Ruizantheda Moure. The two subgenera of the last genus R. mutabilis (as Ruizanthedella) (Michener, 1974), R. divaricata were raised to generic status by Cure (1989), thus adding (as P. perzonatus) (Michener & Lange, 1958) and Caenoha- Ruizanthedella Moure to the list. At the same time, Cure also lictus eberhardorum (Michener et al., 1979). Both A. sericeus described a new genus, Oragapostemon,forPseudagapostemon (as A. radiatus, Roberts, 1969; Eickwort, 1981) and divaricatus (Vachal). Oragapostemon and Ruizanthedella A. splendens (Roberts, 1969; Eickwort, 1981) are said to be have subsequently been synonymized with Ruizantheda,which solitary (sensu Michener, 1974), with a single adult bee per now consists of three species, and Agapostemonoides nest. Either quasisociality or semisociality, has been has been reduced to subgeneric status within Agapostemon observed in P. (Neagapostemon) brasiliensis, but the data (Michener, 2000). are insufficient to discern a division of labour (Martins, Despite the unsuccessful attempts of previous authors, 1993). Thus, the behavioural diversity in this group is rela- M.S. Engel (personal communication) has evidence in tively broad, with Agapostemon containing species exhibiting favour of, and formally designated (Engel, 2001a), Agapos- both communal and solitary behaviour and the tribe as temonini, consisting of the majority of the above genera. He a whole probably presenting new origins of solitary and does not include Habralictus in the new tribe, and he places possibly semi-social behaviour. This makes Agapostemonini Caenohalictus within Caenohalictini Michener. Danforth valuable for the study of patterns of behavioural evolution, (2002) has reconstructed a phylogeny for halictid bees with Agapostemon the potential focus for the loss, gain, or based on molecular data, which, although conflicting with both, of the communal habit. Engel (2001a) in tribal resolution, indicates monophyly of Agapostemon are found only in the New World, ranging Agapostemonini in the sense of Roberts & Brooks (1987). coast-to-coast
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