Ecological versus phylogenetic determinants of trophic associations in a plant-leafminer-parasitoid food web

Evolution

Volumn 67, Issue 5, 2013, Pages 1493-1502

  Leppänen, Sanna A ^a   Altenhofer, Ewald ^b   Liston, Andrew D ^c   Nyman, Tommi ^a,d  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b not available   (Austria)

^c SENCKENBERG DEUTSCHES ENTOMOLOGISCHES INSTITUT   (Germany)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Coevolution; Enemy free space; Multitrophic networks; Speciation; Vertical diversification effects

Indexed keywords

COEVOLUTION; DIVERGENCE; FOOD WEB; GENERALIST; HOST PLANT; LEAFMINER; PARASITOID; PHYLOGENETICS; PHYLOGENY; PLANT-HERBIVORE INTERACTION; SPECIATION (BIOLOGY); TRITROPHIC INTERACTION; TROPHIC CASCADE; TROPHIC LEVEL;

AGROMYZIDAE; HETERARTHRINAE; HEXAPODA; SYMPHYTA;

ANIMAL; ARTICLE; ENVIRONMENT; FOOD CHAIN; GENETICS; HERBIVORY; HYMENOPTERA; MOLECULAR EVOLUTION; PARASITOLOGY; PATHOGENICITY; PHYLOGENY; PLANT; PLANT LEAF;

ANIMALS; ENVIRONMENT; EVOLUTION, MOLECULAR; FOOD CHAIN; HERBIVORY; HYMENOPTERA; PHYLOGENY; PLANT LEAVES; PLANTS;

EID: 84876863622     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12028     Document Type: Article

References (66)

1. Altenhofer, E. 2003. Minierende Blattwespen (Hym.: Symphyta): ihre Minenformen, Wirtspflanzen, Ökologie und Biologie. Gredleriana 3:5-24.
2. Althoff, D. M. 2008. A test of host-associated differentiation across the 'parasite continuum' in the tri-trophic interaction among yuccas, bogus yucca moths, and parasitoids. Mol. Ecol. 17:3917-3927.
3. Bailey, R., K. Schönrogge, J. M. Cook, G. Melika, G. Csóka, C. Thuróczy, and G. N. Stone. 2009. Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biol. 7:e1000179.
4. Bernays, E., and M. Graham. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69:886-892.
5. Cagnolo, L., A. Salvo, and G. Valladares. 2011. Network topology: patterns and mechanisms in plant-herbivore and host-parasitoid food webs. J. Anim. Ecol. 80:342-351.
6. Cronin, J. T., and W. G. Abrahamson. 2001. Do parasitoids diversify in response to host-plant shifts by herbivorous insects? Ecol. Entomol. 26:347-355.
7. Desneux, N., R. Blahnik, C. J. Delebecque, and G. E. Heimpel. 2012. Host phylogeny and specialisation in parasitoids. Ecol. Lett. 15:453-460.
8. Digweed, S. C., C. J. K. MacQuarrie, D. W. Langor, D. J. M. Williams, J. R. Spence, K. L. Nystrom, and L. Morneau. 2009. Current status of invasive alien birch-leafmining sawflies (Hymenoptera: Tenthredinidae) in Canada, with keys to species. Can. Entomol. 141:201-235.
9. Eubanks, M. D., C. P. Blair, and W. G. Abrahamson. 2003. One host shift leads to another? Evidence of host-race formation in a predaceous gall-boring beetle. Evolution 57:168-172.
10. Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1-15.
11. Forbes, A. A., T. H. Q. Powell, L. L. Stelinski, J. J. Smith, and J. L. Feder. 2009. Sequential sympatric speciation across trophic levels. Science 323:776-779.
12. Fordyce, J. A. 2010. Host shifts and evolutionary radiations of butterflies. Proc. R. Soc. B Biol. Sci. 277:3735-3743.
13. Gauthier, N., J. LaSalle, D. L. J. Quicke, and H. C. J. Godfray. 2000. Phylogeny of Eulophidae (Hymenoptera: Chalcidoidea) with a reclassification of Eulophinae and the recognition that Elasmidae are derived eulophids. Syst. Entomol. 25:521-539.
14. Godfray, H. C. 1994. Parasitoids: behavioral and evolutionary ecology. Princeton Univ. Press, Princeton, NJ.
15. Grafen, A. 1989. The phylogenetic regression. Phil. Trans. R. Soc. Lond. B. 326:119-157.
16. Hawkins, B. A. 1994. Pattern and process in host-parasitoid interactions. Cambridge Univ. Press, Cambridge, U. K.
17. Heard, S. B., J. O. Stireman III, J. D. Nason, G. H. Cox, C. R. Kolacz, and J. M. Brown. 2006. On the elusiveness of enemy-free space: spatial, temporal, and host-plant-related variation in parasitoid attack rates on three gallmakers of goldenrods. Oecologia 150:421-434.
18. Imada, Y., A. Kawakita, and M. Kato. 2011. Allopatric distribution and diversification without niche shift in a bryophyte-feeding basal moth lineage (Lepidoptera: Micropterigidae). Proc. R. Soc. B Biol. Sci. 278:3026-3033.
19. Ives, A. R., and H. C. J. Godfray. 2006. Phylogenetic analysis of trophic associations. Am. Nat. 168:E1-E14.
20. Janz, N. 2011. Ehrlich and Raven revisited: mechanisms underlying codiversification of plants and enemies. Annu. Rev. Ecol. Evol. Syst. 42:71-89.
21. Jordan, T. 1998. Egg structure and life-history of two species groups of Grypocentrus (Hymenoptera: Ichneumonidae), monophagous parasitoids of spring leaf-mining Eriocrania-moths on birch (Lepidoptera: Eriocraniidae). Entomol. Gen. 22:223-231.
22. Kaartinen, R., G. N. Stone, J. Hearn, K. Lohse, and T. Roslin. 2010. Revealing secret liaisons: DNA barcoding changes our understanding of food webs. Ecol. Entomol. 35:623-638.
23. Karban, R., and de Valpine, P. 2010. Population dynamics of an Arctiid caterpillar-tachinid parasitoid system using state-space models. J. Anim. Ecol. 79:650-661.
24. Kembel, S. W., P. D. Cowan, M. R. Helmus, W. K. Cornwell, H. Morlon, D. D. Ackerly, S. P. Blomberg, and C. O. Webb. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463-1464.
25. Kennedy, C. E. J., and T. R. E. Southwood. 1984. The number of species of insects associated with British trees: a re-analysis. J. Anim. Ecol. 53:455-478.
26. Kitching, R. L. 2006. Crafting the pieces of the diversity jigsaw puzzle. Science 313:1055-1057.
27. Klapwijk, M. J., and O. T. Lewis. 2011. Spatial ecology of multiple parasitoids of a patchily-distributed host: implications for species coexistence. Ecol. Entomol. 36:212-220.
28. Leppänen, S. A., E. Altenhofer, A. D. Liston, and T. Nyman. 2012. Phylogenetics and evolution of host-plant use in leaf-mining sawflies (Hymenoptera: Tenthredinidae: Heterarthrinae). Mol. Phylogenet. Evol. 64:331-341.
29. Lewinsohn, T. M., V. Novotny, and Y. Basset. 2005. Insects on plants: diversity of herbivore assemblages revisited. Annu. Rev. Ecol. Evol. Syst. 36:597-620.
30. Lill, J. T., J. Marquis, and R. E. Ricklefs. 2002. Host plants influence parasitism of forest caterpillars. Nature 417:170-173.
31. Lopez-Vaamonde, C., H. C. J. Godfray, S. A. West, C. Hansson, and J. M. Cook. 2005. The evolution of host use and unusual reproductive strategies in Achrysocharoides parasitoid wasps. J. Evol. Biol. 18:1029-1041.
32. Maddison, W. P., and D. R. Maddison. 2009. Mesquite: a modular system for evolutionary analysis. Version 2.71. Available at http://mesquiteproject.org.
33. Mardulyn, P., M. C. Milinkovitch, and J. M. Pasteels. 1997. Phylogenetic analyses of DNA and allozyme data suggest that Gonioctena leaf beetles (Coleoptera; Chrysomelidae) experienced convergent evolution in their history of host-plant family shifts. Syst. Biol. 46:722-747.
34. Midford, P. E., T. Garland, and W. P. Maddison. 2011. PDAP:PDTREE: a translation of the PDTREE application of Garlands et al.'s Phenotypic Diversity Analysis Programs. Available at http://mesquiteproject.org/pdap_mesquite.
35. Morris, R. J., O. T. Lewis, and H. C. Godfray. 2004. Experimental evidence for apparent competition in a tropical forest food web. Nature 428:310-313.
36. Munro, J. B., J. M. Heraty, R. A. Burks, D. Hawks, J. Mottern, A. Cruaud, J.-Y. Rasplus, and P. Jansta. 2011. A molecular phylogeny of the Chalcidoidea (Hymenoptera). PLoS ONE 6:e27023.
37. Murphy, S. M. 2004. Enemy-free space maintains swallowtail butterfly host shift. Proc. Natl. Acad. Sci. USA 101:18048-18052.
38. Nicholls, J. A., S. Preuss, A. Hayward, G. Melika, G. Csóka, J. L. Nieves-Aldrey, R. R. Askew, M. Tavakoli, K. Schönrogge, and G. N. Stone. 2010. Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes. Mol. Ecol. 19:592-609.
39. Nosil, P., and A. Ø. Mooers. 2005. Testing hypotheses about ecological specialization using phylogenetic trees. Evolution 59:2256-2263.
40. Novotny, V., S. E. Miller, L. Baje, S. Balagawi, Y. Basset, L. Cizek, K. J. Craft, F. Dem, R. A. I. Drew, J. Hulcr, et al. 2010. Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest. J. Anim. Ecol. 79:1193-1203.
41. Noyes, J. S. 2012. Universal Chalcidoidea Database. World Wide Web electronic publication. Available at http://www.nhm.ac.uk/chalcidoids.
42. Nyman, T., F. Bokma, and J.-P. Kopelke. 2007. Reciprocal diversification in a complex plant-herbivore-parasitoid food web. BMC Biol. 5:49.
43. Nyman, T., V. Vikberg, D. R. Smith, and J. L. Boevé. 2010. How common is ecological speciation in plant-feeding insects? A 'Higher' Nematinae perspective. BMC Evol. Biol. 10:266.
44. Pitz, K. M., A. P. G. Dowling, B. J. Sharanowski, C. A. Boring, K. C. Seltmann, and M. J. Sharkey. 2007. Phylogenetic relationships among the Braconidae (Hymenoptera: Ichneumonoidae): a reassessment of Shi et al. (2005). Mol. Phylogenet. Evol. 43:338-343.
45. Price, P. W. 2002. Resource-driven terrestrial interaction webs. Ecol. Res. 17:241-247.
46. Price, P. W., and H. Pschorn-Walcher. 1988. Are galling insects better protected against parasitoids than exposed feeders? A test using tenthredinid sawflies. Ecol. Entomol. 13:195-205.
47. Pschorn-Walcher, H. 1982. Unterordnung Symphyta, Pflanzenwespen. Pp. 4-234 in W. Schwenke, ed. Die Forstschädlinge Europas. 4. Hautflügler und Zweiflügler. Parey, Hamburg, Germany.
48. Pschorn-Walcher, H., and E. Altenhofer. 1989. The parasitoid community of leaf-mining sawflies (Fenusini and Heterarthrini): a comparative analysis. Zool. Anz. 222:37-56.
49. Quicke, D. L. J., N. M. Laurenne, M. G. Fitton, and G. R. Broad. 2009. A thousand and one wasps: a 28S rDNA and morphological phylogeny of the Ichneumonidae (Insecta: Hymenoptera) with an investigation into alignment parameter space and elision. J. Nat. Hist. 43:1305-1421.
50. R Development Core Team. 2009. R: A language and environment for statistical computing. Available at http://www.R-project.org.
51. Reshchikov, A. V., A. Soper, and R. G. van Driesche. 2010. Review and key to Nearctic Lathrolestes Förster (Hymenoptera: Ichneumonidae), with special reference to species attacking leaf mining tenthredinid sawflies in Betula Linnaeus (Betulaceae). Zootaxa 2614:1-17.
52. Rott, A. S., and H. C. J. Godfray. 2000. The structure of a leafminer-parasitoid community. J. Anim. Ecol. 69:274-289.
53. Segar, S. T., C. Lopez-Vaamonde, J.-Y. Rasplus, and J. M. Cook. 2012. The global phylogeny of the subfamily Sycoryctinae (Pteromalidae): parasites of an obligate mutualism. Mol. Phylogenet. Evol. 65:116-125.
54. Singer, M. S., and J. O. Stireman III. 2005. The tri-trophic niche concept and adaptive radiation of phytophagous insects. Ecol. Lett. 8:1247-1255.
55. Slove Davidson, J. 2012. The plasticity and geography of host use and the diversification of butterflies. Ph.D. thesis, Department of Zoology, Stockholm University, Sweden.
56. Smith, M. A., J. J. Rodriguez, J. B. Whitfield, A. R. Deans, D. H. Janzen, W. Hallwachs, and P. D. N. Hebert. 2008. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proc. Natl. Acad. Sci. USA 105:12359-12364.
57. Stireman, J. O. III. 2005. The evolution of generalization? Parasitoid flies and the perils of inferring host range evolution from phylogenies. J. Evol. Biol. 18:325-336.
58. Stireman, J. O. III., J. D. Nason, S. B. Heard, and J. M. Seehawer. 2006. Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Proc. R. Soc. B Biol. Sci. 273:523-530.
59. Stone, G. N., K. Lohse, J. A. Nicholls, P. Fuentes-Utrilla, F. Sinclair, K. Schönrogge, G. Csóka, G. Melika, J. L. Nieves-Aldrey, J. Pujade-Villar, et al. 2012. Reconstructing community assembly in time and space reveals enemy escape in a Western Palearctic insect community. Curr. Biol. 22:532-537.
60. Sugiura, S. 2007. Structure of a herbivore-parasitoid community: are parasitoids shared by different herbivore guilds? Basic Appl. Ecol. 8:544-551.
61. Taeger, A., S. M. Blank, and A. D. Liston. 2010. World catalog of Symphyta (Hymenoptera). Zootaxa 2580:1-1064.
62. Thompson, J. N. 2005. The geographic mosaic of coevolution. Univ. of Chicago Press, Chicago, IL.
63. Wilson, J. S., M. L. Forister, L. A. Dyer, J. M. O'Connor, K. Burls, C. R. Feldman, M. A. Jaramillo, J. S. Miller, G. Rodríguez-Castañeda, E. J. Tepe et al. 2012. Host conservatism, host shifts and diversification across three trophic levels in two Neotropical forests. J. Evol. Biol. 25:532-546.
64. Winkler, I. S., and C. Mitter. 2008. The phylogenetic dimension of insect-plant interactions: a review of recent evidence. Pp. 240-263 in K. J. Tilmon, ed. Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. Univ. of California Press, Berkeley, CA.
65. Zaldívar-Riverón, A., M. Mori, and D. J. L. Quicke. 2006. Systematics of the cyclostome subfamilies of braconid parasitic wasps (Hymenoptera: Ichneumonoidea): a simultaneous molecular and morphological Bayesian approach. Mol. Phylogenet. Evol. 38:130-145.
66. Zaldívar-Riverón, A., M. R. Shaw, A. G. Sáez, M. Mori, S. A. Belokoblylskij, S. R. Shaw, and D. L. J. Quicke. 2008. Evolution of the parasitic wasp subfamily Rogadinae (Braconidae): phylogeny and evolution of lepidopteran host ranges and mummy characteristics. BMC Evol. Biol. 8:329.