Studies in phylogeny and biosystematics of bees: The bee genus Andrena (Andrenidae) and the tribe Anthophorini (Apidae) (Insecta: Hymenoptera: Apoidea).
PhD thesis of Andreas Dubitzky at the Ludwig-Maximilian University Munich
Summary
The present investigation focused on the phylogeny of the short-tongued bee genus Andrena as well as on the phylogeny of the long-tongued bee tribe Anthophorini, in particular the anthophorine genus Habropoda.
The holarctic bee genus Andrena (sandbees) with about 1,500 validly described species represents the largest genus of bees. The phylogeny of Andrena has been insufficiently studied, earlier investigations were restricted to few discrete subgenera or regional elements of Andrena, and did not engage the genus as a whole with all its subgenera. A cladistic analysis based on 162 morphological characters was carried out in the present study which included representatives of 84 of the 99 currently known subgenera of Andrena. The possible evolution of characters with respect to the used character polarity was discussed. Altogether 107 taxa were sampled, five of which were representatives from other Andreninae. A hypothetical ancestor was used as outgroup due to the unclear phylogenetic relationships within the Andreninae.
An unweighted heuristic analysis resulted in six most parsimonious trees (MPTs) of 1875 steps. Seven major clades of Andrena were recognized in the strict consensus tree. The monophyly of Andrena was confirmed by five non-homoplasius apomorphies. Cubiandrena was not a part of Andrena and it is regarded as separate genus. A second analysis using successive character reweighting (a posteriori weighting) resulted in a single cladogram which agrees in some aspects with the results of the heuristic search but also shows clear differences in tree topology. In both analyses 14 groups combined the same taxa, 11 of which had identical tree topologies. Andrena was found in both analyses to be one of the most derived taxa of the Andreninae, and Euherbstia the most ancestral. The holarctic subgenera Larandrena, Micrandrena and Ptilandrena were each polyphyletic in unweighted and the weighted analyses.
The New World is regarded as the place of origin of the Andreninae, however according to the present study Andrena appears to have originated in the Old World, presumably in the Mediterranean region or Central Asia, since most basal subgenera of Andrena are strictly palearctic. The holarctic distribution of Andrena probably is based on dispersal events which occurred during the late Cretaceous and early Tertiary, while the development of subgenera restricted either to the palearctic or nearctic regions may be based on vicariance events caused by the expansion of the Atlantic ocean and the separation of North American and Eurasian landmasses from the middle Eocene onward.
This study also included a molecular study analysing a 758 base pair DNA fragment obtained from the mitochondrial cytochrome oxidase I (COI) in 27 Central European species of Andrena. The species sampled represent 21 different subgenera as well as seven members of the subgenus Micrandrena. Panurgus was sampled as the outgroup. The parsimony analysis of the equally weighted COI data resulted in a single MPT of 1724 steps. Five major lineages of Andrena were recognized in the cladogram. The subgenus Micrandrena, a main focus of this analysis, was clearly polyphyletic.
The following taxa belonging to the genus Andrena were described as new for science: Calcarandrenasubgen. n., Hamandrenasubgen. n., Platygalandrenasubgen. n.; A. (Carandrena) planti sp. n., A. (Euandrena) yangi sp. n., A. (Habromelissa) nantouensissp. n., A. (Larandrena) susanneaesp. n., A. (Leucandrena) chenisp. n., A. (Micrandrena) taiwanensis Dubitzky 2002, A. (Pallandrena) christineaesp. n., A. (Pallandrena) scheuchlisp. n., A. (Simandrena) heinzisp. n. and A. lehmanni Schönitzer & Dubitzky 2002. The following two taxa were raised to specific rank: A. eburnea Warncke, 1975 stat. n. and A. impasta Warncke, 1975 stat. n. The following subgenus was raised to generic rank: Cubiandrena Warncke, 1968 stat. n.
In another part of this study the phylogenetic relationships of the Anthophorini were investigated. This is one of the largest tribes of medium to large-sized, nest-building bees of the subfamily Apinae, and it comprises about 710 species placed into seven genera. The cladistic analysis of Anthophorini was based on 51 morphological characters and included 26 ingroup taxa, representing all known genera and the most important subgenera of the tribe. Centris was used as the outgroup. The analysis obtained two MPTs of 132 steps, yielding the following tree topology at the generic level: ((Habrophorula, Elaphropoda) (Habropoda (Deltoptila (Pachymelus (Amegilla, Anthophora))))). A second tribe, Habropodini, as postulated by some authors, was not recognized since it would represent a paraphyletic taxon. The monophyly of the Anthophorini and each of its genera was confirmed. Based on the present cladistic results and the biogeographic data of Anthophorini the following evolutionary scenario was postulated in which all genera of Anthophorini probably evolved at the time in the late Cretaceous, except Amegilla and Anthophora, which might have been originated in Oligocene. The northern part of Southeast Asia (India to Southeast China) is regarded as the most probable place of origin and radiation of Anthophorini since most of its genera as well as the most basal lineages of the tribe occur in this region. The New World was probably colonized three times independently by Habropoda (upper Cretaceous to Tertiary), by the ancestral lineage of Deltoptila (upper Cretaceous to Tertiary) and by Anthophora (Tertiary to Quaternary). The present distribution of Deltoptila and Pachymelus indicates that the evolution of these genera may be based on vicariance events, while the distribution of all other genera seems to be based on simple dispersal processes, such as expansion (Habropoda, Anthophora, Amegilla) or isolation (Elaphropoda, Habrophorula) due to ecological or abiotic (climatic) factors.
Finally, the genus Habropoda was subjected to a phylogenetic analysis. This genus includes about 60 species in the New and Old Worlds. A cladistic analysis using 25 palearctic and oriental species of Habropoda, reflecting all major lineages of this genus, was conducted based on 41 morphological characters. Three MPTs trees resulted each of 96 steps. The strict consensus tree revealed the following topology: (Fulvohabropoda ((Oculhabropoda, Phyllohabropoda) (Zonhabropoda, Habropoda s. str.))). The main lineages of Habropoda probably evolved in upper Cretaceous in South East Asia. The origin of the Himalayan mountain range in Eocene may have caused a separation of Habropoda into a palearctic (Habropoda s. str., Zonhabropoda) and an oriental lineage (remaining subgenera and isolated species) as well as the initial stages of radiation processes occurring in Fulvohabropoda. That Zonhabropoda inhabits East Asia seems to be secondary and caused by recent dispersal events along the Asian steppes north of the Himalayas. Climatic adaptations during its separation probably prevented Zonhabropoda from reaching the origin place of Habropoda.
The Taiwanese species of Habropoda and the corresponding cleptoparasite Tetralonioidella are revised and the coevolution between the species of these two genera is discussed in consideration of their seasonal and altitudinal distribution patterns.
The following taxa of Habropoda and Tetralonioidella were described as new for science: Fulvohabropoda subgen. n., Oculhabropoda subgen. n., Phyllohabropoda subgen. n., Zonhabropoda subgen. n.; Habropoda (Phyllohabropoda) christineae sp. n., Habropoda (Phyllohabropoda) sinensis taiwana ssp. n. andTetralonioidella heinzi sp. n. Tetralonioidella himalayana formosana stat. n. was transferred to subspecific rank and a lectotype for Habropoda tainanicola tainanicola Strand, 1913 was designated.
