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Host fidelity over geologic time: restricted use of oaks by oak gallwasps

Published online by Cambridge University Press:  24 April 2015

Erin H. Leckey  and
Dena M. Smith
Erin H. Leckey
Affiliation:
399 UCB, University of Colorado Department of Geological Sciences, University of Colorado, Boulder Colorado 80309, USA, 〈[email protected]〉
Dena M. Smith
Affiliation:
265 UCB, University of Colorado Museum of Natural History, University of Colorado, Boulder Colorado 80309, USA, 〈[email protected]〉
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Abstract

Oaks and their associated gallwasps are often cited as a classic example of coevolution in a plant-insect system. Therefore, it is expected that these gallwasps should demonstrate a high degree of host fidelity over their evolutionary history. To test this, we studied 25 fossil floras from the Oligocene through Pliocene of the western United States. Galls were found on the leaves of Quercus simulata-type Knowlton, 1898 and Q. pollardiana-type (Knowlton) Axelrod, 1940, and match previously reported galls of the form genus Antronoides Waggoner and Poteet, 1996. These fossil leaf-galls are similar to those made on oaks by modern Cynipini wasps, and were restricted to two oak species. Galls are present on these oaks in western floras for a span of 30 million years, indicative of remarkable host fidelity through time. The distribution of galled leaves from across the western United States indicates that the radiation of this group of gallwasps occurred more or less simultaneously across a wide geographic area.

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Articles
Information
Journal of Paleontology , Volume 89 , Issue 2 , March 2015 , pp. 236 - 244
Copyright
Copyright © 2015, The Paleontological Society 

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References

Abe, Y., Melika, G., and Stone, G.N., 2007, The diversity and phylogeography of cynipid gallwasps (Hymenoptera: Cynipidae) of the oriental and eastern Palearctic regions, and their associated communities: Oriental Insects, v. 41, p. 169–212, doi: 10.1080/00305316.2007.10417504.Google Scholar
Abrahamson, W.G., Hunter, M.D., Melika, G., and Price, P.W., 2003, Cynipid gall-wasp communities correlate with oak chemistry: Journal of Chemical Ecology, v. 29, p. 209–223, doi: 10.1023/A:1021993017237.Google Scholar
Ashmead, W.H., 1897, Description of five new genera in the family Cynipidae: Canadian Entomologist, v. 29, p. 260–263.Google Scholar
Axelrod, D.I., 1983, Biogeography of oaks in the Arcto–Tertiary Province: Annals of the Missouri Botanical Garden, v. 70, p. 629–657.Google Scholar
Axelrod, D. I., 1995, The Miocene Purple Mountain Flora of western Nevada: University of California Publiactions Geological Sciences, v. 139, p. 1–62.Google Scholar
Berenbaum, M., 2001, Chemical mediation of coevolution: phylogenetic evidence for Apiaceae and associates: Annals of the Missouri Botanical Garden, v. 88, p. 45–59.Google Scholar
Berenbaum, M., and Feeny, P., 1981, Toxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race?: Science, v. 212, p. 927–929, doi: 10.1126/science.212.4497.927.Google Scholar
Bernays, E., 1998, Evolution of feeding behavior in insect herbivores: success seen as different ways to eat without being eaten: Bioscience, v. 48, p. 35–44.Google Scholar
Bortgard, S.J., and Pigg, K.B., 1999. Anatomical and developmental study of petrified Quercus (Fagaceae) fruits from the middle Miocene: Yakima Canyon, Washington, USA, American Journal of Botany v. 86, p. 307–325.Google Scholar
Buechler, W. K., Dunn, M.T., and Rember, W.C., 2007. Late Miocene Pickett Creek Flora of Owyhee County: Idaho, Contributions from the Museum of Paleontology, the University of Michigan v. 31, p. 305–362.Google Scholar
Camus, A., 1934–1954. Les chénes. Monographie du genre Quercus (et Lithocarpus) Académiedes Sciences Paris, France v. 6–8.Google Scholar
Condit, C., 1944, The Remington Hill Flora, in R. W. Chaney (ed.), Pliocene Floras of California and Oregon Carnegie Institution of Washington Publication v. 2, p. 21–55.Google Scholar
Cornell, H.V., 1983, The secondary chemistry and complex morphology of galls formed by the Cynipinae (Hymenoptera): why and how?: American Midland Naturalist, v. 110, p. 225–234.Google Scholar
Cornell, H.V., 1985, Local and regional richness of cynipine gall wasps on California oaks: Ecology, v. 66, p. 1247–1260.Google Scholar
Ehrlich, P., and Raven, P., 1964, Butterflies and plants: a study in coevolution: Evolution, v. 18, p. 586–608.Google Scholar
Erwin, D. M., and Schick, K.N., 2007, New Miocene oak galls (Cynipini) and their bearing on the history of cynipid wasps in western North America: Journal of Paleontology, v. 81, p. 568–580.Google Scholar
Estiatre, M., 2007, Effects of resource availability on condensed tannins and nitrogen in two Quercus species differing in leaf life span: Annals of Forest Science, v. 64, p. 439–445, doi: 10.1051/forest:2007021.Google Scholar
Farrell, B., and Mitter, C., 1998, The timing of insect/plant diversification: might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co–evolved?: Biological Journal of the Linnean Society, v. 63, p. 553–577, doi: 10.1111/j.1095-8312.1998.tb00329.x.Google Scholar
Fields, P.F., 1996, The Succor Creek Flora of the middle Miocene Sucker Creek Formation, southwestern Idaho and eastern Oregon: systematics and paleoecology [Ph.D. thesis]: Michigan State University, 674 p.Google Scholar
Floate, K.D., and Whitham, T.G., 1995, Insects as traits in plant systematics: their use in discriminating between hybrid cottonwoods: Canadian Journal of Botany, v. 73, p. 1–13, doi: 10.1139/b95-001.Google Scholar
Futuyma, D., and Moreno, G., 1988, The evolution of ecological specialization: Annual Review of Ecology and Systematics, v. 19, p. 207–233.Google Scholar
Gagné, R.J., 1989. The plant-feeding gall midges of North America: New York, Cornell University Press, Ithaca, 355 p.Google Scholar
Gagné, R.J., and Riley, E.G., 1999, A new gall midge (Diptera: Cecidomyiidae) pest of live oak in Texas: Southwestern Entomologist, v. 24, p. 159–165.Google Scholar
Hardy, N. B., and Cook, L.G., 2010, Gall-induction in insects: evolutionary dead-end or speciation driver?: BMC Evolutionary Biology, v. 10, p. 257, doi:10.1186/1471-2148-10-257.Google Scholar
Hartig, T., 1840, Ueber die familie der gallwespen, III: Zeitschrift Für Entomologie, v. 2, p. 176–209.Google Scholar
Jaenike, J., 1990, Host specialization in phytophagous insects: Annual Review of Ecology and Systematics, v. 21, p. 243–273.Google Scholar
Jones, J.H., 1986, Evolution of the Fagaceae: the implications of foliar features: Annals of the Missouri Botanical Garden, v. 73, p. 228–275.CrossRefGoogle Scholar
Kampichler, C., and Teschner, M., 2002, The spatial distribution of leaf galls of Mikiola fage (Diptera: Cecidomyiidae) and Neuroterus quercusbaccarum (Hymenoptera: Cynipidae) in the canopy of a Central European mixed forest: European Journal of Entomology, v. 99, p. 79–84.Google Scholar
Karban, R., 2007, Deciduous leaf drop reduces insect herbivory: Oecologia, v. 153, p. 81–88, doi: 10.1007/s00442-007-0709-z.Google Scholar
Kinsey, A.C., 1922, Studies of some new and described Cynipidae (Hymenoptera): Indiana University Studies, v. 9, p. 3–141.Google Scholar
Kinsey, A.C., 1930, The gall wasp genus Cynips: a study in the origin of the species: Indiana University Studies, v. 16, p. 1–577.Google Scholar
Kinsey, A.C., 1936, The origin of higher categories in Cynips: Indiana University Publications in Science Series, v. 4, p. 1–334.Google Scholar
Knor, S., Skuhravá, M., Wappler, T., and Prokop, J., 2013, Galls and gall makers on plant leaves from the lower Miocene (Burdigalian) of the Czech Republic: systematic and palaeoecological implications: Review of Palaeobotany and Palynology, v. 188, p. 38–51, doi:10.1016/j.revpalbo.2012.10.001.Google Scholar
Knowlton, F.H., 1898, The fossil plants of the Payette Formation, in Lindgren, W., ed., The Mining Districts of the Idaho Basin and the Boise Ridge, Idaho: U. S. Geological Survey Annual Report, v. 18, p. 721–744.Google Scholar
Krassilov, V., 2008. Mine and gall predation as top down regulation in the plant-insect systems from the Cretaceous of Negev: Israel, Palaeogeography Palaeoclimatology Palaeoecology v. 261, p. 261–269, doi:10.1016/j.palaeo.2008.01.017.Google Scholar
Labandeira, C.C., Dilcher, D., Davis, D., and Wagner, D., 1994, Ninety-seven million years of angiosperm-insect association—paleobiological insights into the meaning of coevolution: Proceedings of the National Academy of Sciences of the United States of America, v. 91, p. 12278–12282.Google Scholar
Labandeira, C.C., and Phillips, T.L., 2002, Stem borings and petiole galls from Pennsylvanian tree ferns of Illinois, USA: implications for the origin of the borer and galler functional-feeding-groups and holometabolous insects: Palaeontographica Abteilung A: Paläozoologie–Stratigraphie, v. 264, p. 1–84.Google Scholar
Larew, H.G., 1992, Fossil galls, in Shorthouse, J.D., and Rohfritsch, O., eds., The Biology of Insect-Induced Galls: New York, Oxford University Press, p. 50–59.Google Scholar
Liebmann, F., 1854, Oversigt over det Kongelige Danske Videnskabernes Selskabs Forhandlinger og dets Midlemmers Arbeider: Copenhagen173 p.Google Scholar
Liljeblad, J., Ronquist, F., Nieves–Aldrey, J., Fontal–Cazalla, F., Ros–Farre, P., Gaitros, D., and Pujade–Villar, J., 2008, A fully web–illustrated morphological phylogenetic study of relationships among oak gall wasps and their closest relatives (Hymenoptera: Cynipidae): Zootaxa, v. 1796, p. 1–73.Google Scholar
Linnaeus, C., 1753, Species Plantarum, 997 p.Google Scholar
Linnaeus, C., 1758, Systema Naturae Laurentii Salvii, Holmiae, 824 p.Google Scholar
Liu, Z., Engel, M.S., and Grimaldi, D.A., 2007, Phylogeny and geological history of the cynipoid wasps (Hymenoptera: Cynipoidea): American Museum Novitates, v. 3583, p. 1–48, doi: 10.1206/0003-0082(2007)3583[1:PAGHOT]2.0.CO;2.Google Scholar
Lopez-Vaamonde, C., Wikström, N., Labandeira, C., Godfray, H.C.J., Goodman, S.J., and Cook, J.M., 2006, Fossil-calibrated molecular phylogenies reveal that leaf-mining moths radiated millions of years after their host plants: Journal of Evolutionary Biology, v. 19, p. 1314–1326, doi: 10.1111/j.1420-9101.2005.01070.x.Google Scholar
Louden, J.C., 1830, Hortus Britanicus (Loudon) a Catalogue, p. 385.Google Scholar
Manos, P., Doyle, J., and Nixon, K., 1999, Phylogeny, biogeography, and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae): Molecular Phylogenetics and Evolution, v. 12, p. 333–349, doi:10.1006/mpev.1999.0614.Google Scholar
MacGinitie, H.D., 1933, The Trout Creek flora of southeastern Oregon: Carnegie Institute of Washington Publications, v. 416, p. 21–68.Google Scholar
Miller, P., 1754. Gardeners Dictionary, The Abridged, 4th Edition: London615 p.Google Scholar
Mitter, C., Farrell, B., and Futuyma, D., 1991, Phylogenetic studies of insect plant interactions—insights into the genesis of diversity: Trends in Ecology & Evolution, v. 6, p. 290–293, doi:10.1016/0169-5347(91)90007-K.Google Scholar
Moran, N.A., 1989, A 48-million-year-old aphid host plant-association and complex life-cycle—biogeographic evidence: Science, v. 245, p. 173–175, doi: 10.1126/science.245.4914.173.Google Scholar
Newberry, J.S., 1883, Brief descriptions of fossil plants, chiefly Tertiary, from western North America: Proceedings of the United States National Museum, v. 1883, p. 502–514.Google Scholar
Pascual–Alvarado, E., Cuevas–Reyes, P., Quesada, M., and Oyama, K., 2008, Interactions between galling insects and leaf–feeding insects: the role of plant phenolic compounds and their possible interference with herbivores: Journal of Tropical Ecology, v. 24, p. 329–336, doi: 10.1017/S0266467408005038.Google Scholar
Pearse, I.S., 2011, The role of leaf defensive traits in oaks on the preference and performance of a polyphagous herbivore, Orgyia vetusta: Ecological Entomology, v. 36, p. 635–642, doi: 10.1111/j.1365-2311.2011.01308.x.Google Scholar
Pearse, I.S., and Baty, J.H., 2012, The predictability of traits and ecological interactions on 17 different crosses of hybrid oaks: Oecologia, v. 169, p. 489–497, doi: 10.1007/s00442-011-2216-5.Google Scholar
Ramamurthy, V.V., 2007, Faunistic, ecological, biogeographical and phylogenetic aspects of Coleoptera as gall–inducers and associates in plant galls in the orient and eastern Palearctic: Oriental Insects, v. 41, p. 93–119, doi: 10.1080/00305316.2007.10417501.Google Scholar
Retallack, G.J., 2004, Late Miocene climate and life on land in Oregon within a context of Neogene global change: Palaeogeography, Palaeoclimatology, Palaeoecology, v. 214, p. 97–123, doi: 10.1016/j.palaeo.2004.07.024.Google Scholar
Retallack, G., Orr, W., Prothero, D., Duncan, R., Kester, P., and Ambers, C., 2004, Eocene–Oligocene extinction and paleoclimatic change near Eugene, Oregon: Geological Society of America Bulletin, v. 116, p. 817–839, doi: 10.1130/B25281.1.Google Scholar
Ronquist, F., 1999, Phylogeny, classification and evolution of the Cynipoidea: Zoologica Scripta, v. 28, p. 139–164, doi: 10.1046/j.1463-6409.1999.00022.x.Google Scholar
Ronquist, F., and Liljeblad, J., 2001, Evolution of the gall wasp–host plant association: Evolution, v. 55, p. 2503–2522, doi: 10.1111/j.0014-3820.2001.tb00765.x.Google Scholar
Schorn, H.E., Meyers, J.A., and Erwin, D.M., 2007, Navigating the Neogene: An updated chronology of Neogene paleofloras from the western United States: Courier Forschung-Institut Senckenberg, v. 258, p. 139–146.Google Scholar
Scott, A.C., Stephenson, J., and Collinson, M.E., 1994, The fossil record of leaves with galls, in Willimas, M.A.J., ed., Plant Galls. Systematics Association Special Volume: Oxford, Clarendon Press 49, p. 44–70.Google Scholar
Smith, D.M., 2008, A comparison of plant-insect associations in the middle Eocene Green River Formation and the Upper Eocene Florissant Formation and their climatic implications, in Smith, D.M., and Meyer, H.W., eds., Paleontology of the Upper Eocene Florissant Formation: Colorado, Geological Society of America Special Papers v. 435, p. 89–104, doi: 10.1130/2008.2435(06).Google Scholar
Stone, G.N., Atkinson, R., Rokas, A., Csóka, G., and Nieves-Aldrey, J.L., 2001, Differential success in northwards range expansion between ecotypes of the marble gallwasp Andricus kollari: a tale of two lifecycles: Molecular Ecology, v. 10, p. 761–778, doi: 10.1046/j.1365-294x.2001.01211.x.Google Scholar
Stone, G.N., 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, v. 265, p. 979–988, doi: 10.1098/rspb.1998.0387.Google Scholar
Stone, G.N., Hernandez–Lopez, A., Nicholls, J.A., Di Pierro, E., Pujade–Villar, J., Melika, G., and Cook, J.M., 2009, Extreme host plant conservatism during at least 20 million years of host plant pursuit by oak gallwasps: Evolution, v. 63, p. 854–869. doi: 10.1111/j.1558-5646.2008.00604.x.Google Scholar
Stone, G.N., and Schönrogge, K., 2003, The adaptive significance of insect gall morphology: Trends in Ecology & Evolution, v. 18, p. 512–522, doi:10.1016/S0169-5347(03)00247-7.Google Scholar
Stone, G.N., Van Der Ham, R.W.J.M., and Brewer, J.G., 2008, Fossil oak galls preserve ancient multitrophic interactions: Proceedings of the Royal Society of London, Series B, 275, p. 2213–2219, doi: 10.1098/rspb.2008.0494.Google Scholar
Waggoner, B.M., 1999, Fossil oak leaf galls from the Stinking Water paleoflora of Oregon (middle Miocene): PaleoBios, v. 19, p. 8–14.Google Scholar
Waggoner, B.M., and Poteet, M., 1996, Unusual oak leaf galls from the middle Miocene of northwestern Nevada: Journal of Paleontology, v. 70, p. 1080–1084.Google Scholar
Wappler, T., 2010, Insect herbivory close to the Oligocene–Miocene transition—A quantitative analysis: Palaeogeography Palaeoclimatology Palaeoecology, v. 292, p. 540–550, doi:10.1016/j.palaeo.2010.04.029.Google Scholar
Ward, L., Hackshaw, A., and Clarke, R., 2003, Do food-plant preferences of modern families of phytophagous insects and mites reflect past evolution with plants?: Biological Journal of the Linnean Society, v. 78, p. 51–83, doi: 10.1046/j.1095-8312.2003.00128.x.Google Scholar
Westphal, E., 1992, Cecidogenesis and resistance phenomena in mite-induced galls, in Shorthouse, J.D., and Rohfritsch, O., eds., The Biology of Insect-Induced Galls: New York, Oxford University Press, p. 141–156.Google Scholar
Wilf, P., Labandeira, C.C., Johnson, K.R., and Cúneo, N. R., 2005, Richness of plant–insect associations in Eocene Patagonia: A legacy for South American biodiversity: Proceedings of the National Academy of Sciences of the United States of America, v. 102, p. 8944–8948, doi: 10.1073/pnas.0500516102.Google Scholar
Wolfe, J.A., 1964, Miocene floras from Fingerrock Wash, southwestern Nevada: U.S. Geological Survey Professional Paper 454N, p. 1–36.Google Scholar