Phylogenetic evidence that aphids, rather than plants, determine gall morphology
1995; Royal Society; Volume: 260; Issue: 1357 Linguagem: Inglês
10.1098/rspb.1995.0063
ISSN1471-2954
Autores Tópico(s)Plant and animal studies
ResumoRestricted accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Stern David L. 1995Phylogenetic evidence that aphids, rather than plants, determine gall morphologyProc. R. Soc. Lond. B.26085–89http://doi.org/10.1098/rspb.1995.0063SectionRestricted accessArticlePhylogenetic evidence that aphids, rather than plants, determine gall morphology David L. Stern Google Scholar Find this author on PubMed Search for more papers by this author David L. Stern Google Scholar Find this author on PubMed Published:22 April 1995https://doi.org/10.1098/rspb.1995.0063AbstractMany diverse taxa have evolved independently the habit of living in plant galls. For all but some viral galls, it is unknown whether plants produce galls as a specialized plant reaction to certain types of herbivory, or whether herbivores direct gall development. Here I present a phylogenetic analysis of gall-forming cerataphidine aphids which demonstrates that gall morphology is extremely conservative with respect to aphid phylogeny, but variable with respect to plant taxonomy. In addition, the phylogeny reveals at least three host plant switches where the aphids produce galls most similar to the galls of their closest relatives, rather than galls similar to the galls of aphids already present on the host plant. These results suggest that aphids determine the details of gall morphology essentially extending their phenotype to include plant material. Based on this and other evidence, I suggest that the aphids and other galling insects manipulate latent plant developmental programmes to produce modified atavistic plant morphologies rather than create new forms de novo.FootnotesThis text was harvested from a scanned image of the original document using optical character recognition (OCR) software. As such, it may contain errors. Please contact the Royal Society if you find an error you would like to see corrected. Mathematical notations produced through Infty OCR. Previous ArticleNext Article VIEW FULL TEXT DOWNLOAD PDF FiguresRelatedReferencesDetailsCited by Maderspacher F (2021) Cecidology: Anatomy of a biohack, Current Biology, 10.1016/j.cub.2021.03.095, 31:9, (R430-R433), Online publication date: 1-May-2021. Yukawa J, Tokuda M, Sato S, Ganaha-Kikumura T and Uechi N (2021) Speciation Biology of Gall Midges, 10.1007/978-981-33-6534-6_2, (11-52), . Korgaonkar A, Han C, Lemire A, Siwanowicz I, Bennouna D, Kopec R, Andolfatto P, Shigenobu S and Stern D (2021) A novel family of secreted insect proteins linked to plant gall development, Current Biology, 10.1016/j.cub.2021.01.104, 31:9, (1836-1849.e12), Online publication date: 1-May-2021. Sato S, Harris K, Collet D, Kim W and Yukawa J (2020) Genetic variation in intraspecific populations of Rabdophaga rosaria (Diptera: Cecidomyiidae) indicating possible diversification scenarios into sibling species along with host range expansion on willows (Salicaceae: Salix), Zoological Journal of the Linnean Society, 10.1093/zoolinnean/zlz179, 189:4, (1426-1437), Online publication date: 3-Aug-2020. Álvarez R, Moreno-González V, Martinez J, Ferreira B and Hidalgo N (2020) Microscopic study of nine galls induced in Populus nigra by aphids of the Iberian Peninsula, Arthropod-Plant Interactions, 10.1007/s11829-020-09778-1, 14:6, (799-809), Online publication date: 1-Dec-2020. Lin S, Tokuda M and Yang M (2019) Leaf gall polymorphism and molecular phylogeny of a new Bruggmanniella species (Diptera: Cecidomyiidae: Asphondyliini) associated with Litsea acuminata (Lauraceae) in Taiwan, with ecological comparisons and a species description , Entomological Science, 10.1111/ens.12391, 23:1, (10-22), Online publication date: 1-Mar-2020. Qi Y, Duan C, Ren L and Wu H (2020) Growth dynamics of galls and chemical defence response of Pinus thunbergii Parl. to the pine needle gall midge, Thecodiplosis japonensis Uchida & Inouye (Diptera: Cecidomyiidae), Scientific Reports, 10.1038/s41598-020-69231-4, 10:1, Online publication date: 1-Dec-2020. Guiguet A, Ohshima I, Takeda S, Laurans F, Lopez-Vaamonde C and Giron D (2019) Origin of gall-inducing from leaf-mining in Caloptilia micromoths (Lepidoptera, Gracillariidae), Scientific Reports, 10.1038/s41598-019-43213-7, 9:1, Online publication date: 1-Dec-2019. Schultz J, Edger P, Body M and Appel H (2019) A galling insect activates plant reproductive programs during gall development, Scientific Reports, 10.1038/s41598-018-38475-6, 9:1, Online publication date: 1-Dec-2019. Uematsu K, Kutsukake M and Fukatsu T (2018) Water-repellent plant surface structure induced by gall-forming insects for waste management, Biology Letters, 14:10, Online publication date: 1-Oct-2018. Martinez J, Moreno-González V, Jonas-Levi A, Álvarez R and Leiss K (2018) Quantitative differences detected in the histology of galls induced by the same aphid species in different varieties of the same host, Plant Biology, 10.1111/plb.12705, 20:3, (516-524), Online publication date: 1-May-2018. Xu T, Chen J, Jiang L and Qiao G (2017) Historical and cospeciating associations between Cerataphidini aphids (Hemiptera: Aphididae: Hormaphidinae) and their primary endosymbiont Buchnera aphidicola, Zoological Journal of the Linnean Society, 10.1093/zoolinnean/zlx048, 182:3, (604-613), Online publication date: 17-Mar-2018. Uechi N, Yukawa J, Tokuda M, Maryana N, Ganaha-Kikumura T and Kim W (2016) Description of the Asian chili pod gall midge, Asphondylia capsicicola sp. n., with comparative notes on Asphondylia gennadii (Diptera: Cecidomyiidae) that induces the same sort of pod gall on the same host plant species in the Mediterranean region, Applied Entomology and Zoology, 10.1007/s13355-016-0461-0, 52:1, (113-123), Online publication date: 1-Feb-2017. Guedes L, Aguilera N, Becerra J, Hernández V and Isaias R (2016) Leaf and stem galls of Schinus polygamus (Cav.) Cabr (Anacardiaceae): Anatomical and chemical implications, Biochemical Systematics and Ecology, 10.1016/j.bse.2016.10.012, 69, (266-273), Online publication date: 1-Dec-2016. Álvarez R, Martinez J, Muñoz-Viveros A, Molist P, Abad-González J, Nieto Nafría J and Arroyo J (2016) Contribution of gall microscopic structure to taxonomy of gallicolous aphids on Pistacia , Plant Biology, 10.1111/plb.12475, 18:5, (868-875), Online publication date: 1-Sep-2016. Yamazaki K (2016) Caterpillar mimicry by plant galls as a visual defense against herbivores, Journal of Theoretical Biology, 10.1016/j.jtbi.2016.05.028, 404, (10-14), Online publication date: 1-Sep-2016. Kurzfeld-Zexer L, Lev-Yadun S and Inbar M (2015) One aphid species induces three gall types on a single plant: Comparative histology of one genotype and multiple extended phenotypes, Flora - Morphology, Distribution, Functional Ecology of Plants, 10.1016/j.flora.2014.10.007, 210, (19-30), Online publication date: 1-Jan-2015. Chen J, Jiang L and Qiao G (2013) A total-evidence phylogenetic analysis of Hormaphidinae (Hemiptera: Aphididae), with comments on the evolution of galls, Cladistics, 10.1111/cla.12024, 30:1, (26-66), Online publication date: 1-Feb-2014. Muñoz-Viveros A, Martinez J, Molist P, González-Sierra S, Julián P and Álvarez R (2014) Microscopic study of galls induced by three species of Geopemphigus (Hemiptera: Aphididae: Eriosomatinae) on Pistacia mexicana, Arthropod-Plant Interactions, 10.1007/s11829-014-9333-0, 8:6, (531-538), Online publication date: 1-Dec-2014. Liu L, Li X, Huang X and Qiao G (2014) Evolutionary relationships of Pemphigus and allied genera (Hemiptera: Aphididae: Eriosomatinae) and their primary endosymbiont, Buchnera aphidicola , Insect Science, 10.1111/1744-7917.12113, 21:3, (301-312), Online publication date: 1-Jun-2014. Rui-ling Z, Xiao-lei H, Li-yun J and Ge-xia Q (2013) Molecular phylogenetic evidence for paraphyly of Ceratovacuna and Pseudoregma (Hemiptera, Hormaphidinae) reveals late Tertiary radiation , Bulletin of Entomological Research, 10.1017/S0007485313000321, 103:6, (644-655), Online publication date: 1-Dec-2013. Álvarez R, González-Sierra S, Candelas A and Martinez J (2013) Histological study of galls induced by aphids on leaves of Ulmus minor: Tetraneura ulmi induces globose galls and Eriosoma ulmi induces pseudogalls, Arthropod-Plant Interactions, 10.1007/s11829-013-9278-8, 7:6, (643-650), Online publication date: 1-Dec-2013. Chen J and Qiao G (2012) Galling Aphids (Hemiptera: Aphidoidea) in China: Diversity and Host Specificity, Psyche: A Journal of Entomology, 10.1155/2012/621934, 2012, (1-11), . Isaias R and de Oliveira D (2012) Gall Phenotypes – Product of Plant Cells Defensive Responses to the Inducers Attack Plant Defence: Biological Control, 10.1007/978-94-007-1933-0_11, (273-290), . HUANG X, XIANG-YU J, REN S, ZHANG R, ZHANG Y and QIAO G (2012) Molecular phylogeny and divergence times of Hormaphidinae (Hemiptera: Aphididae) indicate Late Cretaceous tribal diversification, Zoological Journal of the Linnean Society, 10.1111/j.1096-3642.2011.00795.x, 165:1, (73-87), Online publication date: 1-May-2012. SANO M and AKIMOTO S (2011) Morphological phylogeny of gall-forming aphids of the tribe Eriosomatini (Aphididae: Eriosomatinae), Systematic Entomology, 10.1111/j.1365-3113.2011.00589.x, 36:4, (607-627), Online publication date: 1-Oct-2011. YANG Z, CHEN X, HAVILL N, FENG Y and CHEN H (2010) Phylogeny of Rhus gall aphids (Hemiptera : Pemphigidae) based on combined molecular analysis of nuclear EF1α and mitochondrial COII genes, Entomological Science, 10.1111/j.1479-8298.2010.00391.x, 13:3, (351-357) Aoki S and Kurosu U (2010) A Review of the Biology of Cerataphidini (Hemiptera, Aphididae, Hormaphidinae), Focusing Mainly on Their Life Cycles, Gall Formation, and Soldiers, Psyche: A Journal of Entomology, 10.1155/2010/380351, 2010, (1-34), . DORCHIN N, HOFFMANN J, STIRK W, NOVÃfiK O, STRNAD M and VAN STADEN J (2009) Sexually dimorphic gall structures correspond to differential phytohormone contents in male and female wasp larvae, Physiological Entomology, 10.1111/j.1365-3032.2009.00702.x, 34:4, (359-369), Online publication date: 1-Dec-2009. ORTIZ-RIVAS B, MARTÍNEZ-TORRES D and PÉREZ HIDALGO N (2009) Molecular phylogeny of Iberian Fordini (Aphididae: Eriosomatinae): implications for the taxonomy of genera Forda and Paracletus , Systematic Entomology, 10.1111/j.1365-3113.2008.00464.x, 34:2, (293-306), Online publication date: 1-Apr-2009. Tokuda M, Yang M and Yukawa J (2008) Taxonomy and Molecular Phylogeny of Daphnephila Gall Midges (Diptera: Cecidomyiidae) Inducing Complex Leaf Galls on Lauraceae, with Descriptions of Five New Species Associated with Machilus thunbergii in Taiwan, Zoological Science, 10.2108/zsj.25.533, 25:5, (533-545), Online publication date: 1-May-2008. Moura M, Soares G and Isaias R (2008) Species-specific changes in tissue morphogenesis induced by two arthropod leaf gallers in Lantana camara L. (Verbenaceae), Australian Journal of Botany, 10.1071/BT07131, 56:2, (153), . Cook L and Gullan P (2008) Insect, not plant, determines gall morphology in the Apiomorpha pharetrata species-group (Hemiptera: Coccoidea), Australian Journal of Entomology, 10.1111/j.1440-6055.2007.00605.x, 47:1, (51-57), Online publication date: 1-Feb-2008. Coeur d'acier A, Jousselin E, Martin J and Rasplus J (2007) Phylogeny of the Genus Aphis Linnaeus, 1758 (Homoptera: Aphididae) inferred from mitochondrial DNA sequences, Molecular Phylogenetics and Evolution, 10.1016/j.ympev.2006.10.006, 42:3, (598-611), Online publication date: 1-Mar-2007. GANAHA T, NOHARA M, SATO S, UECHI N, YAMAGISHI K, YAMAUCHI S and YUKAWA J (2007) Polymorphism of axillary bud galls induced by Rhopalomyia longitubifex (Diptera: Cecidomyiidae) on Artemisia princeps and A. montana (Asteraceae) in Japan and Korea, with designation of new synonyms , Entomological Science, 10.1111/j.1479-8298.2007.00210.x, 10:2, (157-169), Online publication date: 1-Jun-2007. Zhang H and Qiao G (2007) Molecular phylogeny of Fordini (Hemiptera: Aphididae: Pemphiginae) inferred from nuclear gene EF-1 α and mitochondrial gene COI, Bulletin of Entomological Research, 10.1017/S0007485307005020, 97:4, (379-386), Online publication date: 1-Aug-2007. McLeish M, Crespi B, Chapman T and Schwarz M (2007) Parallel diversification of Australian gall-thrips on Acacia, Molecular Phylogenetics and Evolution, 10.1016/j.ympev.2007.03.007, 43:3, (714-725), Online publication date: 1-Jun-2007. Inbar M The Evolution of Gall Traits in the Fordinae (Homoptera) Galling Arthropods and Their Associates, 10.1007/4-431-32185-3_23, (265-273) MCLEISH M, CHAPMAN T and MOUND L (2006) Gall morpho-type corresponds to separate species of gall-inducing thrips (Thysanoptera: Phlaeothripidae), Biological Journal of the Linnean Society, 10.1111/j.1095-8312.2006.00641.x, 88:4, (555-563) Shorthouse J, Leggo J, Sliva M and Lalonde R (2005) Has egg location influenced the radiation of Diplolepis (Hymenoptera: Cynipidae) gall wasps on wild roses?, Basic and Applied Ecology, 10.1016/j.baae.2005.07.006, 6:5, (423-434), Online publication date: 1-Oct-2005. Wool D (2004) G ALLING A PHIDS : Specialization, Biological Complexity, and Variation , Annual Review of Entomology, 10.1146/annurev.ento.49.061802.123236, 49:1, (175-192), Online publication date: 7-Jan-2004. Pike N and Foster W (2004) Fortress repair in the social aphid species Pemphigus spyrothecae, Animal Behaviour, 10.1016/j.anbehav.2003.08.020, 67:5, (909-914), Online publication date: 1-May-2004. Dorchin N, Freidberg A and Mokady O (2004) Phylogeny of the Baldratiina (Diptera: Cecidomyiidae) inferred from morphological, ecological and molecular data sources, and evolutionary patterns in plant–galler relationships, Molecular Phylogenetics and Evolution, 10.1016/S1055-7903(03)00232-X, 30:3, (503-515), Online publication date: 1-Mar-2004. Inbar M, Wink M and Wool D (2004) The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia, Molecular Phylogenetics and Evolution, 10.1016/j.ympev.2004.01.006, 32:2, (504-511), Online publication date: 1-Aug-2004. Stone G and Schönrogge K (2003) The adaptive significance of insect gall morphology, Trends in Ecology & Evolution, 10.1016/S0169-5347(03)00247-7, 18:10, (512-522), Online publication date: 1-Oct-2003. Cook J, Rokas A, Pagel M and Stone G (2002) EVOLUTIONARY SHIFTS BETWEEN HOST OAK SECTIONS AND HOST-PLANT ORGANS IN ANDRICUS GALLWASPS, Evolution, 10.1554/0014-3820(2002)056[1821:ESBHOS]2.0.CO;2, 56:9, (1821), . Cook J, Rokas A, Pagel M and Stone G (2002) EVOLUTIONARY SHIFTS BETWEEN HOST OAK SECTIONS AND HOST-PLANT ORGANS IN ANDRICUS GALLWASPS, Evolution, 10.1111/j.0014-3820.2002.tb00196.x, 56:9, (1821-1830), Online publication date: 1-Sep-2002. COOK L (2008) Extensive chromosomal variation associated with taxon divergence and host specificity in the gall-inducing scale insect Apiomorpha munita (Schrader) (Hemiptera: Sternorrhyncha: Coccoidea: Eriococcidae), Biological Journal of the Linnean Society, 10.1111/j.1095-8312.2001.tb01316.x, 72:2, (265-278), Online publication date: 1-Feb-2001. Nyman T, Widmer A and Roininen H (2000) EVOLUTION OF GALL MORPHOLOGY AND HOST-PLANT RELATIONSHIPS IN WILLOW-FEEDING SAWFLIES (HYMENOPTERA: TENTHREDINIDAE), Evolution, 10.1554/0014-3820(2000)054[0526:EOGMAH]2.0.CO;2, 54:2, (526), . Nyman T and Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies, Proceedings of the National Academy of Sciences, 10.1073/pnas.230294097, 97:24, (13184-13187), Online publication date: 21-Nov-2000. Caterino M, Cho S and Sperling F (2000) The Current State Of Insect Molecular Systematics: A Thriving Tower of Babel, Annual Review of Entomology, 10.1146/annurev.ento.45.1.1, 45:1, (1-54), Online publication date: 1-Jan-2000. Nyman T, Widmer A and Roininen H (2000) EVOLUTION OF GALL MORPHOLOGY AND HOST-PLANT RELATIONSHIPS IN WILLOW-FEEDING SAWFLIES (HYMENOPTERA: TENTHREDINIDAE), Evolution, 10.1111/j.0014-3820.2000.tb00055.x, 54:2, (526-533), Online publication date: 1-Apr-2000. Stone G and Cook J (1998) The structure of cynipid oak galls: patterns in the evolution of an extended phenotype, Proceedings of the Royal Society of London. Series B: Biological Sciences, 265:1400, (979-988), Online publication date: 7-Jun-1998. Nyman T, Roininen H and Vuorinen J (2017) EVOLUTION OF DIFFERENT GALL TYPES IN WILLOW-FEEDING SAWFLIES (HYMENOPTERA: TENTHREDINIDAE), Evolution, 10.1111/j.1558-5646.1998.tb01646.x, 52:2, (465-474), Online publication date: 1-Apr-1998. Stern D (2017) PHYLOGENY OF THE TRIBE CERATAPHIDINI (HOMOPTERA) AND THE EVOLUTION OF THE HORNED SOLDIER APHIDS, Evolution, 10.1111/j.1558-5646.1998.tb05148.x, 52:1, (155-165), Online publication date: 1-Feb-1998. Crespi B and Worobey M (2017) COMPARATIVE ANALYSIS OF GALL MORPHOLOGY IN AUSTRALIAN GALL THRIPS: THE EVOLUTION OF EXTENDED PHENOTYPES, Evolution, 10.1111/j.1558-5646.1998.tb02248.x, 52:6, (1686-1696), Online publication date: 1-Dec-1998. Gullan P and Kosztarab M (1997) ADAPTATIONS IN SCALE INSECTS, Annual Review of Entomology, 10.1146/annurev.ento.42.1.23, 42:1, (23-50), Online publication date: 1-Jan-1997. Crespi B, Carmean, and D and Chapman T (1997) ECOLOGY AND EVOLUTION OF GALLING THRIPS AND THEIR ALLIES, Annual Review of Entomology, 10.1146/annurev.ento.42.1.51, 42:1, (51-71), Online publication date: 1-Jan-1997. STERN D and FOSTER W (1996) THE EVOLUTION OF SOLDIERS IN APHIDS, Biological Reviews, 10.1111/j.1469-185X.1996.tb00741.x, 71:1, (27-79), Online publication date: 1-Feb-1996. Wang W, Cui Y, Chen X, Bashir N and Chen H (2021) A new species of aphid of the genus Nipponaphis (Hemiptera: Aphididae: Hormaphidinae) from China, inducing galls on the trunk of a witch-hazel (Hamamelidaceae), Zoologia, 10.3897/zoologia.38.e60598, 38, (1-9) Hearn J, Blaxter M, Schönrogge K, Nieves-Aldrey J, Pujade-Villar J, Huguet E, Drezen J, Shorthouse J, Stone G and Copenhaver G (2019) Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp, PLOS Genetics, 10.1371/journal.pgen.1008398, 15:11, (e1008398) López-Núñez F, Marchante H and Marchante E (2018) Primeros registros para Portugal del inductor de agallas foliares Cystiphora sonchi (Vallot, 1827) (Diptera: Cecidomyiidae) y algunas notas sobre su distribución en la Península Ibérica, Graellsia, 10.3989/graellsia.2017.v74.192, 74:1, (068) Kutsukake M, Uematsu K and Fukatsu T (2019) Plant Manipulation by Gall-Forming Social Aphids for Waste Management, Frontiers in Plant Science, 10.3389/fpls.2019.00933, 10 Carneiro R, Pacheco P, Isaias R and Ayele B (2015) Could the Extended Phenotype Extend to the Cellular and Subcellular Levels in Insect-Induced Galls?, PLOS ONE, 10.1371/journal.pone.0129331, 10:6, (e0129331) This Issue22 April 1995Volume 260Issue 1357 Article InformationDOI:https://doi.org/10.1098/rspb.1995.0063Published by:Royal SocietyPrint ISSN:0962-8452Online ISSN:1471-2954History: Manuscript received03/01/1995Manuscript accepted26/01/1995Published online01/01/1997Published in print22/04/1995 License:Scanned images copyright © 2017, Royal Society Citations and impact Large datasets are available through Proceedings B's partnership with Dryad
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