Evolutionary diversification of the gall midge genus Asteromyia (Cecidomyiidae) in a multitrophic ecological context

Molecular Phylogenetics and Evolution

Volumn 54, Issue 1, 2010, Pages 194-210

  Stireman III, John O ^a   Devlin, Hilary ^a   Carr, Timothy G ^b   Abbot, Patrick ^c  

^a WRIGHT STATE UNIVERSITY   (United States)

^b Cornell University ^*  (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Adaptive diversification; Asteraceae; Astereae; Cryptic species; Diptera; Fungal mutualism; Insect plant coevolution; Parasitoid

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; CLASSIFICATION; DNA SEQUENCE; ECOLOGY; FLY; FUNGUS; GENE; GENETICS; HOST PARASITE INTERACTION; MOLECULAR EVOLUTION; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; PLANT; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; SYMBIOSIS;

ANIMALS; DIPTERA; DNA, MITOCHONDRIAL; ECOLOGY; EVOLUTION, MOLECULAR; FUNGI; GENES, INSECT; GENETIC SPECIATION; HOST-PARASITE INTERACTIONS; PHYLOGENY; PLANTS; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS;

ASTERACEAE; ASTEREAE; ASTEROMYIA; CECIDOMYIIDAE; DIPTERA; FUNGI; HEXAPODA;

EID: 70649102111     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2009.09.010     Document Type: Article

References (86)

1. Baldwin B.G., and Sanderson M.J. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl. Acad. Sci. USA 95 (1998) 9402-9406
2. Beck J.B., Nesom G.L., Calie P.J., Baird G.I., Small R.L., and Schilling E.E. Is subtribe solidagininae (Asteraceae) monophylefic?. Taxon 53 (2004) 691-698
3. Bisset J., and Borkent A. Ambrosia galls: the significance of fungal nutrition in the evolution of the Cecidomyiidae (Diptera). In: Pirozynski K.A., and Hawkswork D.L. (Eds). Coevolution of Fungi with Plants and Animals (1988), Academic Press, London 203-225
4. Borkent A., and Bisset J. Gall midges (Diptera: Cecidomyiidae) are vectors for their fungal symbionts. Symbiosis 1 (1985) 185-194
5. Brower A.V.Z. Rapid morphological radiation and convergence among races of the butterfly heliconius-erato inferred from patterns of mitochondrial-DNA evolution. Proc. Natl. Acad. Sci. USA 91 (1994) 6491-6495
6. Camp R.R. Insect-fungus blister galls on Solidago graminifolia and S. rugosa. I. A macroscopic and light microscope study of the host-parasite relationship. Can. J. Bot. 59 (1981) 2466-2477
7. Caterino M.S., Cho S., and Sperling F.A.H. The current state of insect molecular systematics: a thriving Tower of Babel. Annu. Rev. Entomol. 45 (2000) 1-54
8. Condon M., Adams D.C., Bann D., Flaherty K., Gammons J., Johnson J., Lewis M.L., Marsteller S., Scheffer S.J., Serna F., and Swensen S. Uncovering tropical diversity: six sympatric cryptic species of Blepharoneura (Diptera: Tephritidae) in flowers of Gurania spinulosa (Cucurbitaceae) in eastern Ecuador. Biol. J. Linn. Soc. 93 (2008) 779-797
9. Condon M.A., Scheffer S.J., Lewis M.L., and Swensen S.M. Hidden neotropical diversity: greater than the sum of its parts. Science 320 (2008) 928-931
10. Cook J.M., Rokas A., Pagel M., and Stone G.N. Evolutionary shifts between host oak species and host plant organs in Andricus gall waps. Evolution 56 (2002) 1821-1830
11. Craig T.P., Horner J.D., and Itami J.K. Hybridization studies on the host races of Eurosta solidaginis: implications for sympatric speciation. Evolution 51 (1997) 1552-1560
12. Craig T.P., Horner J.D., and Itami J.K. Genetics, experience, and host-plant preference in Eurosta solidaginis: implications for host shifts and speciation. Evolution 55 (2001) 773-782
13. Craig T.P., Itami J.K., Abrahamson W.G., and Horner J.D. Behavioral evidence for host-race formation in Eurosta-solidaginis. Evolution 47 (1993) 1696-1710
14. Crego C.L., Weis A.E., Polans N.O., and Bretz C.K. Sympatric sibling species from three phenotypically distinct Asteromyia (Diptera: Cecidomyiidae) galls on the same host plant species. Ann. Entomol. Soc. Am. 83 (1990) 149-154
15. Desalle R., Freedman T., Prager E.M., and Wilson A.C. Tempo and mode of sequence evolution in mitochondrial-DNA of Hawaiian Drosophila. J. Mol. Evol. 26 (1987) 157-164
16. Dorchin N., Freidberg A., and Mokady O. Phylogeny of the Baldratiina (Diptera: Cecidomyiidae) inferred from morphological, ecological and molecular data sources, and evolutionary patterns in plant-galler relationships. Mol. Phylogenet. Evol. 30 (2004) 503-515
17. Drummond A.J., Ho S.Y.W., Phillips M.J., and Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4 (2006) 699-710
18. Drummond A.J., and Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7 (2007) 214
19. Dugan K.A., Lawrence H.S., Hares D.R., Fisher C.L., and Budowle B. An improved method for post-PCR purification for mtDNA sequence analysis. J. Forensic Sci. 47 (2002) 811-818
20. Farrell B.D., and Mitter C. The timing of insect/plant diversification: might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved?. Biol. J. Linn. Soc. 63 (1998) 553-577
21. Felt E.P. Gall midges of Aster, Carya, Quercus and Salix. J. Econ. Entomol. 3 (1910) 347-356
22. Gagné R.J. A taxonomic revision of the genus Asteromyia (Diptera: Cecidomyiidae). Misc. Publ. Entomol. Soc. Am. 6 (1968) 1-40
23. Gagné R.J. A tribal and generic revision of nearctic Lasiopteridi (Diptera-Cecidomyiidae). Ann. Entomol. Soc. Am. 62 (1969) 1348-1364
24. Gagné R.J. The Plant-feeding Gall Midges of North America (1989), Cornell University Press, Ithaca, New York
25. Gagné R.J. The Gall Midges of the Neotropical Region (1994), Cornell University Press, Ithaca and London
26. Gagné R.J. A catalog of the Cecidomyiidae (Diptera) of the world. Mem. Entomol. Soc. Wash. 25 (2004) 1-408
27. Gagné R.J., and Boldt P.E. The gall midges (Diptera, Cecidomyiidae) of Baccharis Spp. (Asteraceae) in the United-States. Proc. Entomol. Soc. Wash. 97 (1995) 767-778
28. In: Gibson A.P., Huber J.T., and Woolley J.B. (Eds). Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera) National Research Council Research Press (1997), Ottawa, Ontario, Canada
29. Good-Avila S.V., Souza V., Gaut B.S., and Eguiarte L.E. Timing and rate of speciation in Agave (Agavaceae). Proc. Natl. Acad. Sci. USA 103 (2006) 9124-9129
30. Guindon S., and Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 (2003) 696-704
31. Harris M.O., Stuart J.J., Mohan M., Nair S., Lamb R.J., and Rohfritsch O. Grasses and gall midges: plant defense and insect adaptation. Annu. Rev. Entomol. 48 (2003) 549-577
32. Hawkins B.A. Pattern and Process in Host-Parasitoid Interactions (1994), Cambridge University Press, Cambridge
33. Ho S.Y.W., Phillips M.J., Cooper A., and Drummond A.J. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol. Biol. Evol. 22 (2005) 1561-1568
34. Ho S.Y.W., Shapiro B., Phillips M.J., Cooper A., and Drummond A.J. Evidence for time dependency of molecular rate estimates. Syst. Biol. 56 (2007) 515-522
35. Hoberg E.P., and Brooks D.R. A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite system. J. Biogeogr. 9 (2008) 1533-1550
36. Janson E.M., Stireman J.O., Singer M.S., and Abbot P. Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution 62 (2008) 997-1012
37. Jeffries M.J., and Lawton J.H. Enemy-free space and the structure of biological communities. Biol. J. Linn. Soc. 23 (1984) 269-286
38. Jones R.G., Gagné R.J., and Barr W.F. Biology and taxonomy of the Rhopalomyia gall midges (Diptera: Cecidomyiidae) of Artemesia tridentata Nutall (Compositae) in Idaho. Contrib. Am. Entomol. Inst. 21 (1983) 1-76
39. Joy J.B., and Crespi B.J. Adaptive radiation of gall-inducing insects within a single host-plant species. Evolution 61 (2007) 784-795
40. Karban R., and Agrawal A.A. Herbivore offense. Annu. Rev. Ecol. Syst. 33 (2002) 641-664
41. Kim K.J., Choi K.S., and Jansen R.K. Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Mol. Biol. Evol. 22 (2005) 1783-1792
42. Larew H.G., Gagné R.J., and Rossman A.Y. Fungal gall caused by a new species of Ledomyia (Diptera, Cecidomyiidae) on Xylaria-Enterogena (Ascomycetes, Xylariaceae). Ann. Entomol. Soc. Am. 80 (1987) 502-507
43. Legendre P., and Anderson M.J. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol. Monogr. 69 (1999) 1-24
44. Legendre P., Desdevises Y., and Bazin E. A statistical test for host-parasite coevolution. Syst. Biol. 51 (2002) 217-234
45. Lewis P.O. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50 (2001) 913-925
46. Maddison W.P., and Maddison D.R. StochChar: a package of Mesquite modules for stochastic models of character evolution. Version 2 (2006) 5
47. Maddison, W.P., Maddison, D.R., 2008. Mesquite: a modular system for evolutionary analysis. Version 2.5. Available from: .
48. Maddison W.P., Midford P.E., and Otto S.P. Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56 (2007) 701-710
49. Midford P., and Maddison W.P. Diverse package for mesquite. Version 2 (2008) 5
50. Nesom G.L., Suh Y., Morgan D.R., and Simpson B.B. Xylothamia new-genus Aasteraceae Astereae a new genus related to Euthamia. Sida 14 (1990) 101-116
51. Noyes R.D., and Rieseberg L.H. ITS sequence data support a single origin for North American Astereae (Asteraceae) and reflect deep geographic divisions in Aster s.l. Am. J. Bot. 86 (1999) 398-412
52. Nyman T., Bokma F., and Kopelke J.P. Reciprocal diversification in a complex plant-herbivore-parasitoid food web. BMC Biol. 5 (2007) 49
53. Nyman T., Farrell B.D., Zinovjev A.G., and Vikberg V. Larval habits, host-plant associations, and speciation in nematine sawflies (Hymenoptera: Tenthredinidae). Evolution 60 (2006) 1622-1637
54. Panero J.L., and Funk V.A. The value of sampling anomalous taxa in phylogenetic studies: major clades of the Asteraceae revealed. Mol. Phylogenet. Evol. 47 (2008) 757-782
55. Pendleton B.B., and Teetes G.L. Sorghum midge dispersal from sorghum. Southwest Entomol. 19 (1994) 1-9
56. Price P.W. Adaptive radiation of gall-inducing insects. Basic Appl. Ecol. 6 (2005) 413-421
57. Price P.W., Fernandes G.W., and Waring G.L. Adaptive nature of insect galls. Environ. Entomol. 16 (1987) 15-24
58. R Development Core Team, 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: .
59. Rambaut, A., Drummond, A.J., 2007. Tracer v1.4. Available from: .
60. Ronquist F., and Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003) 1572-1574
61. Roskam, H.C., 2005. Phylogeny of gall midges (Cecidomyiidae). In: Raman, A., Schaefer, C.W., Withers, T.M. (Eds.), Biology, Ecology, and Evolution of Gall-inducing Arthropods, Science Publishers Inc., Enfield, NH, pp. 305-319.
62. Semple J.C., and Cook R.E. Solidago. In: Committee F.N.A.E. (Ed). Flora of North America (2006), Oxford University Press, New York 107-166
63. Semple J.C., Heard S.B., and Broulliet L. Cultivated and Native Asters of Ontario (Compositae:Asteraceae) Aster L. (including Asteromoea Blume, Diplactis Raf. and Kalimeris (Cass.) Cass.), Callistephus Cass., Galatella Cass., Doellingeria Nees, Oclemena E.L. Greene, Eurybia (Cass.) S.F. Gray, Canadanthus Nesom, and Symphyotrichum Nees (including Virgulus Raf.). U. Waterloo Biol. Ser. 41 (2002) 1-134
64. Semple, J.C., Ringius, G.S., Zhang, J.J., 1999. The Goldenrods of Ontario: Solidago L. and Euthamia Nutt., third ed. U. Waterloo Biol. Ser., vol. 39. pp. 1-90.
65. Simon C., Frati F., Beckenbach A., Crespi B.J., Liu H., and Flook P. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 87 (1994) 651-701
66. Smith M.A., Rodriguez J.J., Whitfield J.B., Deans A.R., Janzen D.H., Hallwachs W., and Hebert P.D.N. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proc. Natl. Acad. Sci. USA 105 (2008) 12359-12364
67. Smith M.A., Wood D.M., Janzen D.H., Hallwachs W., and Hebert P.D.N. DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proc. Natl. Acad. Sci. USA 104 (2007) 4967-4972
68. Schilling E.E., Beck J.B., Calie P.J., and Small R.L. Molecular analysis of Solidaster cv. Lemore, a hybrid goldenrod (Asteraceae). J. Bot. Res. Inst. Texas 2 (2008) 7-18
69. Smith S.A., and Donoghue M.J. Rates of molecular evolution are linked to life history in flowering plants. Science 322 (2008) 86-89
70. Stireman III J.O., Nason J.D., and Heard S.B. Host-associated genetic differentiation in phytophagous insects: general phenomenon or isolated exceptions? Evidence from a Goldenrod-insect community. Evolution 59 (2005) 2573-2587
71. Stireman III J.O., Nason J.D., Heard S.B., and Seehawer J.M. Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Proc. R. Soc. Lond. B Biol. Sci. 273 (2006) 523-530
72. Stireman J.O., Janson E.M., Carr T.G., Devlin H., and Abbot P. Evolutionary radiation of Asteromyia carbonifera (Diptera: Cecidomyiidae) gall morphotypes on the goldenrod Solidago altissima (Asteraceae). Biol. J. Linn. Soc. 95 (2008) 840-858
73. Stone G.N., and Schonrogge K. The adaptive significance of insect gall morphology. Trends Ecol. Evol. 18 (2003) 512-522
74. Tamura K., Dudley J., Nei M., and Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 (2007) 1596-1599
75. Urbatsch L.E., Anderson L.C., Roberts R.P., and Neubig K.M. Ericameria. In: Committee F.N.A.E. (Ed). Flora of North America (2006), Oxford University Press, New York 50-77
76. Urbatsch L.E., Roberts R.P., and Neubig K.M. Chrysothamnus. In: Committee F.N.A.E. (Ed). Flora of North America (2006), Oxford University Press, New York 187-193
77. Waring G.L., Abrahamson W.G., and Howard D.J. Genetic differentiation among host-associated populations of the gallmaker Eurosta-solidaginis (Diptera, Tephritidae). Evolution 44 (1990) 1648-1655
78. Waring G.L., and Price P.W. Parasitoid pressure and the radiation of a gall-forming group Cecidomyiidae Asphondylia-spp. on creosote bush Larrea-Tridentata. Oecologia 79 (1989) 293-299
79. Weis A.E. Resource utilization patterns in a community of gall-attacking parasitoids. Environ. Entomol. 11 (1982) 809-815
80. Weis A.E. Use of a symbiotic fungus by the gall maker Asteromyia carbonifera to inhibit attack by the parasitoid Torymus capite. Ecology 63 (1982) 1602-1605
81. Weis A.E., Price P.W., and Lynch M. Selective pressures on clutch size in the gallmakers Asteromyia carbonifera. Ecology 64 (1983) 688-695
82. Wolfe K.H., Gouy M.L., Yang Y.W., Sharp P.M., and Li W.H. Date of the monocot dicot divergence estimated from chloroplast DNA-sequence data. Proc. Natl. Acad. Sci. USA 86 (1989) 6201-6205
83. Wool D. Galling aphids: specialization, biological complexity, and variation. Annu. Rev. Entomol. 49 (2004) 175-192
84. Yukawa J. Synchronization of gallers with host plant phenology. Popul. Ecol. 42 (2000) 105-113
85. Yukawa J., and Rohfritsch O. Biology and ecology of gall-inducing Cecidomyiidae (Diptera). In: Raman A., Schaefer C.W., and Withers T.M. (Eds). Biology, Ecology, and Evolution of Gall-inducing Aarthropods (2005), Science Publishers Inc., Enfield, NH 273-304
86. Yukawa J., Uechi N., Tokuda M., and Sato S. Radiation of gall midges (Diptera: Cecidomyiidae) in Japan. Basic Appl. Ecol. 6 (2005) 453-461