title: Host niches and defensive extended phenotypes structure parasitoid wasp communities.
abstract: Oak galls are spectacular extended phenotypes of gallwasp genes in host oak tissues and have evolved complex morphologies that serve, in part, to exclude parasitoid natural enemies.Parasitoids and their insect herbivore hosts have coevolved to produce diverse communities comprising about a third of all animal species. The factors structuring these communities, however, remain poorly understood. An emerging theme in community ecology is the need to consider the effects of host traits, shaped by both natural selection and phylogenetic history, on associated communities of natural enemies. Here we examine the impact of host traits and phylogenetic relatedness on 48 ecologically closed and species-rich communities of parasitoids attacking gall-inducing wasps on oaks. Gallwasps induce the development of spectacular and structurally complex galls whose species- and generation-specific morphologies are the extended phenotypes of gallwasp genes. All the associated natural enemies attack their concealed hosts through gall tissues, and several structural gall traits have been shown to enhance defence against parasitoid attack. Here we explore the significance of these and other host traits in predicting variation in parasitoid community structure across gallwasp species. In particular, we test the "Enemy Hypothesis," which predicts that galls with similar morphology will exclude similar sets of parasitoids and therefore have similar parasitoid communities. Having controlled for phylogenetic patterning in host traits and communities, we found significant correlations between parasitoid community structure and several gall structural traits (toughness, hairiness, stickiness), supporting the Enemy Hypothesis. Parasitoid community structure was also consistently predicted by components of the hosts' spatiotemporal niche, particularly host oak taxonomy and gall location (e.g., leaf versus bud versus seed). The combined explanatory power of structural and spatiotemporal traits on community structure can be high, reaching 62% in one analysis. The observed patterns derive mainly from partial niche specialisation of highly generalist parasitoids with broad host ranges (>20 hosts), rather than strict separation of enemies with narrower host ranges, and so may contribute to maintenance of the richness of generalist parasitoids in gallwasp communities. Though evolutionary escape from parasitoids might most effectively be achieved via changes in host oak taxon, extreme conservatism in this trait for gallwasps suggests that selection is more likely to have acted on gall morphology and location. Any escape from parasitoids associated with evolutionary shifts in these traits has probably only been transient, however, due to subsequent recruitment of parasitoid species already attacking other host galls with similar trait combinations.
authors.affiliation: Institute of Evolutionary Biology, School of Biology, University of Edinburgh, Edinburgh, United Kingdom.
authors.forename: Richard
authors.initials: R
authors.lastname: Bailey
authors.forename: Karsten
authors.initials: K
authors.lastname: Schönrogge
authors.forename: James M
authors.initials: JM
authors.lastname: Cook
authors.forename: George
authors.initials: G
authors.lastname: Melika
authors.forename: György
authors.initials: G
authors.lastname: Csóka
authors.forename: Csaba
authors.initials: C
authors.lastname: Thuróczy
authors.forename: Graham N
authors.initials: GN
authors.lastname: Stone
mesh_terms: D000818:Animals; D006790:Host-Parasite Interactions; D010641:Phenotype; D010802:Phylogeny; D029963:Quercus / Q000469:parasitology*; D014863:Wasps / Q000145:classification / Q000469:parasitology* / Q000502:physiology*
references.citation: Am Nat. 1993 Apr;141(4):634-41
references.pmid: 19426002
references.citation: Mol Ecol. 2007 May;16(10):2103-14
references.pmid: 17498235
references.citation: Bioinformatics. 2001 Aug;17(8):754-5
references.pmid: 11524383
references.citation: Nature. 2007 Jan 11;445(7124):202-5
references.pmid: 17215842
references.citation: Oecologia. 1989 May;79(3):293-9
references.pmid: 23921393
references.citation: Science. 2001 Aug 17;293(5533):1314-6
references.pmid: 11509730
references.citation: Mol Ecol. 2007 Jul;16(13):2768-81
references.pmid: 17594446
references.citation: Philos Trans R Soc Lond B Biol Sci. 1989 Dec 21;326(1233):119-57
references.pmid: 2575770
references.citation: J Anim Ecol. 2000 Sep;69(5):841-868
references.pmid: 29313993
references.citation: Nature. 2002 Jun 13;417(6890):735-8
references.pmid: 12066183
references.citation: Proc Biol Sci. 2006 Mar 7;273(1586):523-30
references.pmid: 16537122
references.citation: Annu Rev Entomol. 2002;47:633-68
references.pmid: 11729087
references.citation: Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15694-9
references.pmid: 14673114
references.citation: Nature. 2004 Mar 18;428(6980):310-3
references.pmid: 15029194
references.citation: Proc Biol Sci. 2007 Jul 7;274(1618):1617-24
references.pmid: 17456452
references.citation: Evolution. 2009 Apr;63(4):854-69
references.pmid: 19292826
references.citation: Annu Rev Entomol. 2006;51:187-208
references.pmid: 16332209
references.citation: Nature. 2000 Jun 29;405(6790):1016
references.pmid: 10890434
references.citation: Science. 2001 Oct 12;294(5541):321-6
references.pmid: 11598291
references.citation: Mol Ecol. 2008 Jan;17(2):652-65
references.pmid: 18086197
references.citation: Genetics. 1997 Aug;146(4):1475-87
references.pmid: 9258689
references.citation: Oecologia. 1995 Oct;104(2):207-217
references.pmid: 28307357
references.citation: Evolution. 2002 Sep;56(9):1821-30
references.pmid: 12389727
references.citation: Oecologia. 1989 Oct;81(1):75-88
references.pmid: 28312160
references.citation: Phys Rev Lett. 2004 Oct 8;93(15):158701
references.pmid: 15524949
references.citation: Science. 2008 Feb 15;319(5865):952-4
references.pmid: 18276890
references.citation: Science. 2003 Feb 28;299(5611):1388-91
references.pmid: 12610303
references.citation: Science. 2004 Jan 16;303(5656):356-9
references.pmid: 14726588
references.citation: BMC Biol. 2007 Nov 01;5:49
references.pmid: 17976232
references.citation: Nature. 2002 May 9;417(6885):170-3
references.pmid: 12000959
references.citation: Nature. 2003 Jul 31;424(6948):542-5
references.pmid: 12891355
references.citation: Science. 2008 Feb 8;319(5864):804-7
references.pmid: 18258913
references.citation: Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):8013-6
references.pmid: 10393939
references.citation: Evolution. 2007 Apr;61(4):784-95
references.pmid: 17439611