Geographical patterns of genetic divergence in the widespread Mesoamerican bumble bee Bombus ephippiatus (Hymenoptera: Apidae)

Molecular Phylogenetics and Evolution

Volumn 64, Issue 1, 2012, Pages 219-231

  Duennes, Michelle A ^a   Lozier, Jeffrey D ^a,b   Hines, Heather M ^a,c   Cameron, Sydney A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ALABAMA   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Color pattern; Mesoamerica; Microsatellites; Phylogeography; Population genetics

Indexed keywords

CASPASE ACTIVATED DEOXYRIBONUCLEASE; DEOXYRIBONUCLEASE; MICROSATELLITE DNA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PRIMER DNA;

ANIMAL; ARTICLE; BAYES THEOREM; BEE; BIOLOGICAL MODEL; CENTRAL AMERICA; DEMOGRAPHY; DNA SEQUENCE; ECOSYSTEM; GENETIC VARIABILITY; GENETICS; MEXICO; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYLOGEOGRAPHY; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; STATISTICAL MODEL;

ANIMALS; BASE SEQUENCE; BAYES THEOREM; BEES; CENTRAL AMERICA; DEMOGRAPHY; DEOXYRIBONUCLEASES; DNA PRIMERS; ECOSYSTEM; EVOLUTION, MOLECULAR; GENETIC VARIATION; LIKELIHOOD FUNCTIONS; MEXICO; MICROSATELLITE REPEATS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PHYLOGENY; PHYLOGEOGRAPHY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

APIDAE; APOIDEA; BOMBUS (GENUS); BOMBUS EPHIPPIATUS; BOMBUS IMPATIENS; HEXAPODA; HYMENOPTERA; IMPATIENS;

EID: 84860556527     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2012.03.018     Document Type: Article

References (69)

1. Altekar G., Dwarkadas S., Huelsenbeck J., Ronquist F. Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 2004, 20:407-415.
2. Anisimova M., Gascuel O. Approximate likelihood ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 2006, 55:539-552.
3. Arbeláez-Cortéz E., Nyári A.S., Navarro-Sigüenza A.G. The differential effect of lowlands on the phylogeographic pattern of a Mesoamerican montane species (Lepidocplaptes affinis, Aves: Furnariidae). Mol. Phylogenet. Evol. 2010, 57:658-668.
4. Barber B.R., Klicka J. Two pulses of diversification across the Isthmus of Tehuantepec in a montane Mexican bird fauna. Proc. Roy. Soc. Lond. B. Biol. 2010, 277:2675-2681.
5. Brower A.V.Z. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patters of mitochondrial DNA evolution. Proc. Natl. Acad. Sci. USA 1994, 91:6491-6495.
6. Cameron S.A., Hines H.M., Williams P.H. A comprehensive phylogeny of the bumble bees (Bombus). Biol. J. Linn. Soc. 2007, 91:161-188.
7. Cameron S.A., Lozier J.D., Strange J.P., Koch J.B., Cordes N., Solter L.F., Griswold T.L. Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. USA 2011, 108:662-667.
8. Campbell J.A. Distribution patterns of amphibians in middle America. Patterns of Distribution of Amphibians: A Global Perspective 1999, 111-210. John Hopkins University Press, Maryland. W.E. Duellman (Ed.).
9. Castoe T.A., Chippendale P.T., Campbell J.A., Ammerman L.K., Parkinson C.L. Molecular systematics of the middle American jumping pitvipers (genus Atropoides) and phylogeography of the Atropoides nummifer complex. Herpetologica 2003, 59:420-431.
10. Castoe T.A., Daza J.M., Smith E.N., Sasa M.M., Kuch U., Campbell J.A., Chippindale P.T., Parkinson C.L. Comparative phylogeography of pitvipers suggests a consensus of ancient Middle American highland biogeography. J. Biogeogr. 2009, 36:88-103.
11. Cockerell T.D.A. Descriptions and records of bees - XLV. Ann. Mag. Nat. Hist. 1912, 10(21):31.
12. Darwin C. The Origin of Species by Means of Natural Selection, or, the Preservation of Favoured Races in the Struggle for Life 1859, Murray, London, UK.
13. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7:214.
14. Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006, 4:e88.
15. Earl D.A., vonHoldt B.M. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 2011, 10.1007/s12686-011-9548-7.
16. Estoup A., Scholl A., Pouvreau A., Solignac M. Monoandry and polyandry in bumble bees (Hymenoptera - Bombinae) as evidenced by highly variable microsatellites. Mol. Ecol. 1995, 4:89-93.
17. Estoup A., Solignac M., Cornuet J.M., Goudet J., Scholl A. Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol. Ecol. 1996, 5:19-31.
18. Evanno G., Regnaut S., Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 2005, 14:2611-2620.
19. Farrell B.D. Evolutionary assembly of the milkweed fauna: cytochrome oxidase I and the age of Tetraopes beetles. Mol. Phylogenet. Evol. 2001, 18:467-478.
20. Franklin H.J. The Bombidae of the New World - Part 2. Species South of the United States. Trans. Am. Entomol. Soc. Phila. 1913, 39:73-200.
21. García-Moreno J., Arctander P., Fjeldså J. Strong diversification at the treeline among Metallura hummingbirds. Auk 1999, 116:702-711.
22. García-Moreno J., Navarro-Sigüenza A.G., Peterson A.T., Sánchez-González L.A. Genetic variation coincides with geographic structure in the common bush-tanager (Chlorospingus ophthalmicus) complex from Mexico. Mol. Phylogenet. Evol. 2004, 33:186-196.
23. García-Moreno J., Cortés N., García-Deras G., Hernández-Baños B. Local origin and diversification among Lampornis hummingbirds: a Mesoamerican taxon. Mol. Phylogenet. Evol. 2006, 38:488-498.
24. Greenbaum E., Smith E.N., de Sá R.O. Molecular systematics of the Middle American genus Hypopachus (Anura: Microhylidae). Mol. Phylogenet. Evol. 2011, 61:265-277.
25. Greenleaf S.S., Kremen C. Wild bee species increase tomato production and respond differently to surrounding land use in Northern California. Biol. Conserv. 2006, 133:81-87.
26. Guidon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
27. Gutiérrez-Rodríguez C., Ornelas J.F., Rodríguez-Gómez F. Chloroplast DNA phylogeography of a distylous shrub (Palicourea padifolia, Rubiaceae) reveals past fragmentation and demographic expansion in Mexican cloud forests. Mol. Phylogenet. Evol. 2011, 61:603-615.
28. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acid. Sci. 1999, 41:95-98.
29. Heinrich B. Bumblebee economics (with a new preface) 2004, Harvard University Press, Cambridge, MA.
30. Hey J., Nielsen R. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 2004, 167:747-760.
31. Hickerson M.J., Stahl E., Lessios H.A. Test for simultaneous divergence using approximate Bayesian computation. Evolution 2006, 60:2435-2453.
32. Hines H.M., Cameron S.A., Williams P.H. Molecular phylogeny of the bumble bee subgenus Pyrobombus (Hymenoptera: Apidae: Bombus) with insights into gene utility for lower-level analysis. Invertebr. Syst. 2006, 20:289-303.
33. Hines H.M. Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus). Syst. Biol. 2008, 57:58-75.
34. Howell T.R. Avian distribution in Central America. Auk 1969, 86:292-326.
35. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
36. Julier H.E., Roulston T.H. Wild bee abundance and pollination service in cultivated pumpkins: farm management, nesting behavior and landspace effects. J. Econ. Entomol. 2009, 102:563-573.
37. Knowles L.L., Maddison W.P. Statistical phylogeography. Mol. Ecol. 2002, 11:2623-2635.
38. Kondo N.I., Yamanaka D., Kanbe Y., Kunitake Y.K., Yoneda M., Tsuchida K., Goka K. Reproductive disturbance of Japanese bumblebees by the introduced European bumblebee Bombus terrestris. Naturwissenschaften 2009, 96:467-475.
39. Kremen C., Williams N.M., Thorp R.W. Crop pollination from native bees at risk from agricultural intensification. Proc. Natl. Acad. Sci. USA 2002, 99:16812-16816.
40. Labougle J.M., Ito M., Okazawa T. The species of the genus Bombus (Hymenoptera: Apidae) of Chiapas, Mexico and Guatemala; with a morphometric and altitudinal analysis. Folia Entomol. Mex. 1985, 64:55-72.
41. Labougle J.M. Bombus of México and Central America (Hymenoptera: Apidae). Univ. Kansas Sci. Bull. 1990, 54:35-73.
42. León-Paniagua L., Navarro-Sigüenza A.G., Hernández-Baños B.E., Morales J.C. Diversification of the arboreal mice of the genus Habromys (Rodentia: Cricetidae: Neotominae) in the Mesoamerican highlands. Mol. Phylogenet. Evol. 2007, 42:653-664.
43. Lozier J.D., Cameron S.A. Comparative genetic analyses of historical and contemporary collections highlight contrasting demographic histories for the bumble bee Bombus pensylvanicus and B. impatiens in Illinois. Mol. Ecol. 2009, 18:1875-1886.
44. Meeus I., Brown M.J.F., de Graaf D.C., Smagghe G. Effect of invasive parasites on bumble bee declines. Conserv. Biol. 2011, 25:662-671.
45. Miller M.J., Bermingham E., Ricklefs R.E. Historical biogeography of the New World solitaires (Myadestes spp.). Auk 2007, 3:868-885.
46. Montalva J., Dudley L., Arroyo M.K., Retamales H., Abrahamovich A. Geographic distribution and associated flora of native and introduced bumble bees (Bombus spp.) in Chile. J. Apicult. Res. 2011, 50:11-21.
47. Morandin L.A., Winston M.L. Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol. Appl. 2005, 15:871-881.
48. Mulcahy D.G., Morrill B.H., Mendelson J.R. Historical biogeography of lowland species of toads (Bufo) across the Trans-Mexican Neovolcanic Belt and the Isthmus of Tehuantepec. J. Biogeogr. 2006, 33:1889-1904.
49. Navarro A.G., Peterson A.T., López-Medrano E., Benítez D.H. Species limits in Mesoamerican Aulacorhynchus toucanets. Wilson Bull. 2001, 113:363-372.
50. Olson D.M., Dinerstein E., Wikramanayake E.D., Burgess N.D., Powell G.V.N., Underwood E.C., D'amico J.A., Itoua I., Strand H.E., Morrison J.C., Loucks C.J., Allnutt T.F., Ricketts T.H., Kura Y., Lamoreux J.F., Wettengel W.W., Hedao P., Kassem K.R. Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 2001, 51:933-938.
51. Peterson A.T., Escalante P., Navarro S.A. Genetic variation and differentiation in Mexican populations of common bush-tanagers and chestnut-capped brush-finches. Condor 1992, 94:244-253.
52. Phillips B.L., Baird S.J.E., Moritz C. When vicars meet: a narrow contact zone between morphologically cryptic phylogeographic lineages of the rainforest skink, Carlia rubrigularis. Evolution 2004, 58:1536-1548.
53. Plath O.E. Bumblebees and their ways 1934, The Macmillan Co., New York, NY.
54. Posada D. JModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
55. Pritchard J.K., Stephens M., Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000, 155:949-959.
56. Rambaut, A., Drummond, A.J., 2007. Tracer v1.4. http://beast.bio.ed.ac.uk/Tracer.
57. Rand A.L. Glaciation, an isolating factor in speciation. Evolution 1948, 2:314-321.
58. Raymond M., Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 1995, 86:248-249.
59. Reber-Funk C.R., Schmid-Hempel R., Schmid-Hempel P. Microsatellite loci for Bombus spp. Mol. Ecol. Resour. 2006, 6:83-86.
60. Ross K., Gotzek D., Ascunce M., Shoemaker D. Species delimitation: a case study in a problematic ant taxon. Syst. Biol. 2010, 59:162-184.
61. Ryan M.E., Johnson J.R., Fitzpatrick B.M. Invasive hybrid tiger salamander genotypes impact native amphibians. Proc. Natl. Acad. Sci. USA 2009, 106:11166-11171.
62. Simmons M.P., Ochoterena H. Gaps as characters in sequence-based phylogenetic analyses. Syst. Biol. 2000, 49:369-381.
63. Sladen F.W.L. The Humble-bee, its Life History and How to Domesticate it, with Descriptions of all the British Species of Bombus and Psithyrus 1912, The Macmillan Co., London, UK.
64. Vergara C.H. Environmental impac of exotic bees introduced for crop pollination. Bee Pollination in Agricultural Ecosystems 2008, 145-165. Oxford University Press, New York. R.R. James, T.L. Pitts-Singer (Eds.).
65. Wild A.L., Maddison D.R. Evaluating nuclear protein-coding genes for phylogenetic utility in beetles. Mol. Phylogenet. Evol. 2008, 48:877-891.
66. Williams P.H. An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bull. Nat. Hist. Mus. Entomol. 1998, 67:79-152.
67. Williams P. The distribution of bumblebee colour patterns worldwide: possible significance for thermoregulation, crypsis, and warning mimicry. Biol. J. Linn. Soc. 2007, 92:97-118.
68. Williams P.H., Osborne J.L. Bumblebee vulnerability and conservation world-wide. Apidologie 2009, 40:367-387.
69. Yoon H.J., Kim S.Y., Lee K.Y., Lee S.B., Park I.G., Kim I. Interspecific hybridization of the bumblebees Bombus ignitus and B. terrestris. Int. J. Ind. Entomol. 2009, 18:45-52.