Molecular phylogeny and historical biogeography of the large carpenter bees, genus Xylocopa (Hymenoptera: Apidae)

The biogeographical history of major groups of bees with worldwide distributions have often been explained through hypotheses based on Gondwanan vicariance or long distance dispersal events, but until recently these hypotheses have been very difficult, if not impossible, to distinguish. New fossil data, comprehensive information on Mesozoic and Cenozoic coastline positions and the availability of phylogenetically informative DNA markers now makes it feasible to test these hypotheses for some groups of bees. This paper presents historical biogeographical analyses of the genus Xylocopa Latreille, based on phylogenetic analyses of species belonging to 22 subgenera using molecular data from two nuclear genes, elongation factor-1α (EF-1α) and phosphoenolpyruvate carboxykinase (PEPCK), combined with previously published morphological and mitochondrial data sets. Phylogenetic analyses based on parsimony and likelihood approaches resulted in several groups of subgenera supported by high bootstrap values (>85%): an American group with the Oriental/Palaearctic subgenera Nyctomelitta and Proxylocopa as sister taxa; a geographically diverse group (Xylocopa s.l); and a group consisting of African and Oriental subgenera. The relationships among these three clades and the subgenus Perixylocopa remained unresolved. The Oriental subgenus Biluna was found to be the sister group of all other carpenter bee subgenera included in this study. Using a relaxed molecular clock calibrated using fossil carpenter bees, we show that the major splits in the carpenter bee phylogeny occurred well after the final breakup of Gondwanaland (the separation of South America and Africa, 100 Mya), but before important Miocene fusion events. Ancestral area analysis showed that the genus Xylocopa most likely had an Oriental-Palaearctic origin and that the present world distribution of Xylocopa subgenera resulted mainly from independent dispersal events. The influence of Pleistocene glaciations on carpenter bee distributions is also discussed. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 249–266.

[1]  Jonathan P. Bollback,et al.  Bayesian Inference of Phylogeny and Its Impact on Evolutionary Biology , 2001, Science.

[2]  W. Bruno,et al.  Performance of a divergence time estimation method under a probabilistic model of rate evolution. , 2001, Molecular biology and evolution.

[3]  M. Schwarz,et al.  Molecular phylogeny of the large carpenter bees, genus Xylocopa (Hymenoptera: apidae), based on mitochondrial DNA sequences. , 2000, Molecular phylogenetics and evolution.

[4]  D. Cutler,et al.  Estimating divergence times in the presence of an overdispersed molecular clock. , 2000, Molecular biology and evolution.

[5]  A. Rokas,et al.  A Bayesian guide to tree felling. , 2000, Trends in ecology & evolution.

[6]  B. Emerson,et al.  COLONIZATION AND DIVERSIFICATION OF THE SPECIES BRACHYDERES RUGATUS (COLEOPTERA) ON THE CANARY ISLANDS: EVIDENCE FROM MITOCHONDRIAL DNA COII GENE SEQUENCES , 2000, Evolution; international journal of organic evolution.

[7]  Mark P. Simmons,et al.  Gaps as characters in sequence-based phylogenetic analyses. , 2000, Systematic biology.

[8]  J. Huelsenbeck,et al.  A compound poisson process for relaxing the molecular clock. , 2000, Genetics.

[9]  R. Leys A revision of the Australian carpenter bees, genus Xylocopa Latreille, subgenera Koptortosoma Gribodo and Lestis Lepeletier & Serville (Hymenoptera : Apidae) , 2000 .

[10]  L. Packer,et al.  Phylogeny of the bee genus Halictus (Hymenoptera: halictidae) based on parsimony and likelihood analyses of nuclear EF-1alpha sequence data. , 1999, Molecular phylogenetics and evolution.

[11]  G. Voelker DISPERSAL, VICARIANCE, AND CLOCKS: HISTORICAL BIOGEOGRAPHY AND SPECIATION IN A COSMOPOLITAN PASSERINE GENUS (ANTHUS: MOTACILLIDAE) , 1999, Evolution; international journal of organic evolution.

[12]  U. Sorhannus,et al.  Testing for Equality of Molecular Evolutionary Rates: A Comparison Between a Relative-Rate Test and a Likelihood Ratio Test , 1999 .

[13]  F. Sperling,et al.  Interaction of process partitions in phylogenetic analysis: an example from the swallowtail butterfly genus Papilio. , 1999, Molecular biology and evolution.

[14]  H. Kishino,et al.  Estimating the rate of evolution of the rate of molecular evolution. , 1998, Molecular biology and evolution.

[15]  R. Minckley A Cladistic Analysis and Classification of the Subgenera and Genera of the Large Carpenter Bees, Tribe Xylocopini (Hymenoptera: Apidae) , 1998 .

[16]  A. Rambaut,et al.  Estimating divergence dates from molecular sequences. , 1998, Molecular biology and evolution.

[17]  B. Danforth,et al.  Elongation factor-1 alpha occurs as two copies in bees: implications for phylogenetic analysis of EF-1 alpha sequences in insects. , 1998, Molecular biology and evolution.

[18]  Michael J. Sanderson,et al.  A Nonparametric Approach to Estimating Divergence Times in the Absence of Rate Constancy , 1997 .

[19]  C. Cunningham,et al.  Can three incongruence tests predict when data should be combined? , 1997, Molecular biology and evolution.

[20]  Fredrik Ronquist,et al.  Dispersal-Vicariance Analysis: A New Approach to the Quantification of Historical Biogeography , 1997 .

[21]  K. Strimmer,et al.  Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies , 1996 .

[22]  Sudhir Kumar,et al.  Continental breakup and the ordinal diversification of birds and mammals , 1996, Nature.

[23]  D. Wagner,et al.  A nuclear gene for higher level phylogenetics: phosphoenolpyruvate carboxykinase tracks mesozoic-age divergences within Lepidoptera (Insecta). , 1996, Molecular biology and evolution.

[24]  F. Ronquist,et al.  Phylogeny and historical biogeography of the cynipoid wasp family Ibaliidae (Hymenoptera) , 1996 .

[25]  P. Oromí,et al.  Phylogeny of the genus Hegeter (Tenebrionidae, Coleoptera) and its colonization of the Canary Islands deduced from Cytochrome Oxidase I mitochondrial DNA sequences , 1996, Heredity.

[26]  P. Oromí,et al.  Mitochondrial DNA phylogeny and sequential colonization of Canary Islands by darkling beetles of the genus Pimelia (Tenebrionidae) , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  E. M. Friis,et al.  The origin and early diversification of angiosperms , 1995, Nature.

[28]  Ziheng Yang Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: Approximate methods , 1994, Journal of Molecular Evolution.

[29]  C. Bult,et al.  TESTING SIGNIFICANCE OF INCONGRUENCE , 1994 .

[30]  John C. Avise,et al.  Molecular Markers, Natural History and Evolution , 1993, Springer US.

[31]  J. C. Regier,et al.  Nuclear gene sequences for higher level phylogenetic analysis: 14 promising candidates , 1992 .

[32]  Wayne P. Maddison,et al.  Macclade: Analysis of Phylogeny and Character Evolution/Version 3 , 1992 .

[33]  Roy Haines-Young,et al.  Biogeography , 1992, Vegetatio.

[34]  B S Weir,et al.  Testing for equality of evolutionary rates. , 1992, Genetics.

[35]  J. Oliver,et al.  The general stochastic model of nucleotide substitution. , 1990, Journal of theoretical biology.

[36]  K. Bremer THE LIMITS OF AMINO ACID SEQUENCE DATA IN ANGIOSPERM PHYLOGENETIC RECONSTRUCTION , 1988, Evolution; international journal of organic evolution.

[37]  W. Li,et al.  Evidence for higher rates of nucleotide substitution in rodents than in man. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[38]  C. Michener Biogeography of the Bees , 1979 .

[39]  J. A. Wolfe A Paleobotanical Interpretation of Tertiary Climates in the Northern Hemisphere , 1978 .

[40]  平嶋 義宏 Hurd, Paul D., Jr. and J. S. Moure, 1963, A classification of the large carpenter bees (Xylocopini)(Hymenoptera : Apoidea), University of California Publications in Entomology, Vol.29 , 1964 .

[41]  J. Proudfoot,et al.  Noise , 1931, The Indian medical gazette.

[42]  D. Maddison,et al.  MacClade 4: analysis of phy-logeny and character evolution , 2003 .

[43]  Ramakant Sharma,et al.  Phylogeny Estimation and Hypothesis Testing using Maximum Likelihood , 2003 .

[44]  M. L.,et al.  Morphology , Molecules , and the Phylogenetics of Cetaceans , 2003 .

[45]  D. Swofford PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[46]  William H. Press,et al.  Numerical recipes in C , 2002 .

[47]  Ziheng Yang,et al.  Phylogenetic Analysis by Maximum Likelihood (PAML) , 2002 .

[48]  M. Engel A MONOGRAPH OF THE BALTIC AMBER BEES AND EVOLUTION OF THE APOIDEA (HYMENOPTERA) , 2001 .

[49]  M. Engel The first large carpenter bee from the Tertiary of North America, with a consideration of the geological history of Xylocopinae (Hymenoptera: Apidae) , 2001 .

[50]  B. Danforth,et al.  Elongation Factor-1 a Occurs as Two Copies in Bees : Implications for Phylogenetic Analysis of EF1 a Sequences in Insects , 2000 .

[51]  B. Larget,et al.  Markov Chain Monte Carlo Algorithms for the Bayesian Analysis of Phylogenetic Trees , 2000 .

[52]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[53]  C. Michener The Bees of the World , 2000 .

[54]  H. Wiering The bees of the world , 2000 .

[55]  Hurst,et al.  Mitochondrial DNA phylogeny of Brimstone butterflies (genus Gonepteryx) from the Canary Islands and Madeira , 1998, Biological journal of the Linnean Society. Linnean Society of London.

[56]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[57]  B. Funnell,et al.  Atlas of Mesozoic and Cenozoic Coastlines , 1994 .

[58]  William H. Press,et al.  Numerical Recipes in C, 2nd Edition , 1992 .

[59]  J. Doyle,et al.  Isolation of plant DNA from fresh tissue , 1990 .

[60]  J. Zhang New fossil species of Apoidea (Insecta, Hymenoptera). , 1990 .

[61]  D. Roubik,et al.  Ecology and natural history of tropical bees: Extant families, subfamilies, tribes, genera, and subgenera of the Apoidea: a partial checklist , 1989 .

[62]  C. Michener,et al.  A Trigona from late Cretaceous amber of New Jersey (Hymenoptera, Apidae, Meliponinae). American Museum novitates ; ; no. 2917. , 1988 .

[63]  C. Eardley A Taxonomic Revision of the Genus Xylocopa Latreille (Hymenoptera: Anthophoridae) in Southern Africa , 1983 .

[64]  M. Mckenna Holarctic Landmass Rearrangement, Cosmic Events, and Cenozoic Terrestrial Organisms , 1983 .

[65]  W. Hamilton Cretaceous and Cenozoic History of the Northern Continents , 1983 .

[66]  F. E. Zeuner,et al.  A monograph on fossil bees (Hymenoptera: Apoidea) , 1976 .

[67]  M. A. Lieftinck Revision of the Carpenter-bees (Xylocopa Latreille) of the Moluccan Islands, with notes on other Indo-Australian species , 1956 .

[68]  B. Gardiner,et al.  The Linnean Society of London , 1960, Nature.