PHYLOGENY AND THE EVOLUTION OF HOST PLANT ASSOCIATIONS IN THE LEAF BEETLE GENUS OPHRAELLA (COLEOPTERA, CHRYSOMELIDAE)
Douglas J. Futuyma
Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, NY, 11794 USA
Search for more papers by this authorShawn S. McCafferty
Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, NY, 11794 USA
Search for more papers by this authorDouglas J. Futuyma
Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, NY, 11794 USA
Search for more papers by this authorShawn S. McCafferty
Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, NY, 11794 USA
Search for more papers by this authorAbstract
Species of Ophraella, a North American genus of leaf beetles (Chrysomelidae), feed variously on eight genera in four tribes of Asteraceae. A phylogenetic analysis, based on morphological features and allozymes, was undertaken to deduce the history of host affiliation within the genus. The two data sets are combined to arrive at a provisional phylogeny of the species, onto which host associations are parsimoniously mapped. Among and within the 12 species studied, at least two shifts are postulated to have occurred among congeneric plant species, five between genera in the same tribe, and four between different tribes of Asteraceae.
The phylogeny of Ophraella appears not to be congruent with that of its hosts. This and other evidence indicates that many host shifts in Ophraella postdate the divergence of the host plants, a conclusion that may apply commonly to phytophagous insects. A phenetic analysis of the plants' secondary compounds provides modest support for the hypothesis that host shifts are facilitated by commonalities in plant chemistry. A possible trend in host shifts is evident, from chemically simpler to chemically more forbidding plants. The chemical barriers to host shifts in Ophraella appear to require adaptation in both behavior and in physiological attributes. There is no evidence that the host associations of these insects or the divergence in secondary chemistry of their hosts can be attributed to coevolution.
Literature Cited
- Avise, J. C. 1989. Gene trees and organismal histories: A phylogenetic approach to population biology. Evolution 43: 1192–1208.
- Benson, W. W., K. S. Brown, Jr., andL. E. Gilbert. 1975. Coevolution of plants and herbivores: Passion flower butterflies. Evolution 29: 659–680.
- Blake, D. H. 1936. A redisposition of Monoxia puncticollis and allied species. J. Wash. Acad. Sci. 26: 423–430.
- Blake, D. H. 1939. A study of LeConte's types of the beetles in the genus Monoxia, with descriptions of new species. Proc. U.S. Nat. Mus. 87, no. 3072: 145–171.
10.5479/si.00963801.87-3072.145 Google Scholar
- Bohlmann, F., T. Burckhardt, andC. Zdero. 1973. Naturally Occurring Acetylenes. Academic Press, London and N.Y.
- Bolick, M. R. 1983. A cladistic analysis of the Ambrosiinae Less and Engelmanniinae Stuessy. Advances in Cladistics 2: 125–141. Columbia University Press, N.Y.
- Bövino, A. G. 1929. Beetle larvae of the subfamily Galerucinae. Proc. U.S. Nat. Mus. 75: 1–48.
10.5479/si.00963801.75-2773.1 Google Scholar
- Boyer, S. H., D. C. Fainer, andE. Watson-Williams. 1963. Lactate dehydrogenase variants from human blood: Evidence for molecular subunits. Science 141: 642–643.
- Bremer, K. 1987. Tribal interrelationships of the Asteraceae. Cladistics 3: 210–253.
- Brivio, C. 1977. L'apparato genitale femminile di alcune specie di Galerucella Crotch e generi vicini (Coleoptera Chrysomelidae Galerucinae). Mem. Soc. Ent. Ital. 56: 244–250.
- Brooks, D. R. 1988. Macroevolutionary comparisons of host and parasite phylogenies. Annu. Rev. Ecol. Syst. 19: 235–259.
- Brooks, D. R., T. B. Thorson, andM. A. Mayes. 1981. Freshwater stingrays (Potamotrygonidae) and their helminth parasites: Testing hypotheses of evolution and coevolution. Adv. in Cladistics 1: 147–176.
- Buth, D. G. 1984. The application of electrophoretic data in systematic studies. Annu. Rev. Ecol. Syst. 15: 501–522.
- Cavalli-Sforza, L. L., andA. W. F. Edwards. 1967. Phylogenetic analyses: Models and estimation procedures. Evolution 32: 550–570.
10.1111/j.1558-5646.1967.tb03411.x Google Scholar
- Crowson, R. A. 1967. The Natural Classification of the Families of Coleoptera. E. W. Classey, Hampton, England.
- Dethier, V. G. 1954. Evolution of feeding preferences in phytophagous insects. Evolution 833–854.
- Doyen, J. T. 1966. The skeletal anatomy of Tenebrio molitor (Coleoptera: Tenebrionidae). Misc. Publ. Entomol. Soc. Amer. 5(3): 103–150.
- Ehrlich, P. R., andP. H. Raven. 1964. Butterflies and plants: A study in coevolution. Evolution 18: 586–608.
- Eichler, W. 1948. Some rules in ectoparasitism. Ann. Mag. Nat. Hist. 12: 588–598.
10.1080/00222934808653932 Google Scholar
- Farrell, B., andC. Mitter. 1990. Phylogeny of host-affiliation: Have Phyllobrotica (Coleoptera: Chrysomelidae) and the Lamiales diversified in parallel? Evolution. In press.
- Farris, J. S. 1972. Estimating phylogenetic trees from distance matrices. Am. Nat. 106: 645–668.
- Farris, J. S. 1981. Distance data in phylogenetic analysis, pp. 3–23. In V. A. Funk and D. R. Brooks (eds.), Advances in Cladistics. New York Botanical Garden, N.Y.
- Felsenstein, J. 1981. Evolutionary trees from gene frequencies and quantitative characters: Finding maximum likelihood estimates. Evolution 35: 1229–1242.
- Felsenstein, J. 1984. Distance methods for inferring phylogenies: A justification. Evolution 38: 16–24.
- Felsenstein, J. 1985a. Phylogenies and the comparative method. Am. Nat. 125: 1–15.
- Felsenstein, J. 1985b. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791.
- Felsenstein, J. 1985c. Phylogenies from gene frequencies: A statistical problem. Syst. Zool. 34: 300–311.
- Fraenkel, G. 1959. The raison d'être of secondary plant substances. Science 129: 1466–1470.
- Futuyma, D. J. 1983. Evolutionary interactions among herbivorous insects and plants, pp. 207–231. In D. J. Futuyma and M. Slatkin (eds.), Co-evolution. Sinauer, Sunderland, MA.
- Futuyma, D. J. 1988. Sturm und Drang and the evolutionary synthesis. Evolution 42: 217–226.
- Futuyma, D. J. 1990. Observations on the taxonomy and natural history of Ophraella Wilcox (Coleoptera: Chrysomelidae), with a description of a new species. J. N.Y. Entomol. Soc. 98: 163–186.
- Futuyma, D. J. a. History and evolutionary processes. In M. Nitecki (ed.), History and Evolution. University of Chicago Press, Chicago. In press.
- Futuyma, D. J. b. The evolution of host specificity in herbivorous insects: Genetic, ecological, and phylogenetic aspects. In P. W. Price, W. Benson, T. Lewinsohn, and W. Fernandes (eds.), Herbivory: Tropical and Temperate Perspectives. Wiley, N.Y. In press.
- Goeden, R. D., andD. W. Ricker. 1985. The life history of Ophraella notulata (F.) on western ragweed Ambrosia psilostachya DeCandolle in southern California (Coleoptera: Chrysomelidae). Pan-Pacific Entomol. 6: 32–37.
- Gould, S. J., andR. C. Lewontin. 1979. The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proc. Roy. Soc. Lond. B 205: 581–598.
- Greger, H. 1977. Anthemideae—Chemical review, pp. 899–941. In V. H. Heywood, J. B. Harborne, and B. L. Turner (eds.), The Biology and Chemistry of the Compositae. Academic Press, London.
- Hafner, M. S., andS. A. Nadler. 1988. Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332: 258–259.
- Harris, H., andD. A. Hopkinson. 1976. Handbook of Enzyme Electrophoresis in Human Genetics. American Elsevier, N.Y.
- Hegnauer, R. 1964. Chemotaxonomie der Pflanzen. Band III. Birkhäuser, Basel, Switzerland.
10.1007/978-3-0348-9385-5 Google Scholar
- Herz, W. 1977. Astereae—Chemical review, pp. 567–576. In V. H. Heywood, J. B. Harborne, and B. L. Turner (eds.), The Biology and Chemistry of the Compositae. Academic Press, London.
- V. H. Heywood, J. B. Harborne, and B. L. Turner, eds. 1977. The Biology and Chemistry of the Compositae. Academic Press, London.
- Hillis, D. M. 1987. Molecular versus morphological approaches to systematics. Annu. Rev. Ecol. Syst. 18: 23–42.
- Humphries, C. J., J. M. Cox, andE. S. Nielsen. 1986. Nothofagus and its parasites: A cladistic approach to coevolution, pp. 55–76. In A. R. Stone and D. L. Hawksworth (eds.), Coevolution and Systematics. Clarendon, Oxford.
- Jansen, R. K., H. J. Michaels, andJ. D. Palmer. 1991. Phylogeny and character evolution in the Asteraceae based on chloroplast DNA restriction site mapping. Syst. Bot. In press.
- Jermy, T. 1976. Insect-host-plant relationship—Co-evolution or sequential evolution? Symp. Biol. Hung. 16: 109–113.
- Jermy, T. 1984. Evolution of insect/host-plant relationships. Am. Nat. 124: 609–630.
- Kelsey, R. G., andF. Shafizadeh. 1979. Sesquiterpene lactones and systematics of the genus Artemisia. Phytochemistry 18: 1591–1611.
- LeSage, L. 1986. A taxonomic monograph of the Nearctic galerucine genus Ophraella Wilcox (Coleoptera: Chrysomelidae). Mem. Entomol. Soc. Canada No. 133: 1–75. Ottawa, ON.
- Lyal, C. H. C. 1986. Coevolutionary relationships of lice and their hosts: A test of Fahrenholz's Rule, pp. 77–91. In A. R. Stone and D. L. Hawksworth (eds.), Coevolution and Systematics. Clarendon, Oxford.
- Mabry, T. J., andJ. E. Gill. 1979. Sesquiterpene lactones and other terpenoids, pp. 501–537. In G. A. Rosenthal and D. H. Jansen (eds.), Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, N.Y.
- Maddison, W. P., M. J. Donoghue, andD. R. Maddison. 1984. Outgroup analysis and parsimony. Syst. Zool. 33: 83–103.
10.2307/2413134 Google Scholar
- Margush, T., andF. R. McMorris. 1981. Consensus n-trees. Bull. Math. Biol. 43: 239–244.
- Maynard Smith, J., R. Burian, S. Kauffman, P. Alberch, J. Campbell, B. Goodwin, R. Lande, D. Raup, andL. Wolpert. 1985. Developmental constraints and evolution. Q. Rev. Biol. 60: 265–287.
- Menken, S. B. J. 1982. Biochemical genetics and systematics of small ermine moths. Z. Zool. Syst. Evolutionsforsch. 20: 131–143.
- Miller, J. S. 1987. Host-plant relationships in the Papilionidae (Lepidoptera): Parallel cladogenesis or colonization? Cladistics 3: 105–120.
10.1111/j.1096-0031.1987.tb00501.x Google Scholar
- Mitter, C., andD. L. Brooks. 1983. Phylogenetic aspects of coevolution, pp. 65–98. In D. J. Futuyma and M. Slatkin (eds.), Coevolution. Sinauer, Sunderland, MA.
- Mitter, C., andB. Farrell. 1990. Macroevolutionary aspects of insect/plant relationships. In E. A. Bernays (ed.), Insect-Plant Interactions, Vol. 2. CRC Press, Boca Raton, FL.
- Muller, J. 1981. Fossil pollen records of extant angiosperms. Bot. Rev. 47: 1–142.
- Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, N.Y.
10.1111/j.1365-294X.2006.02908.x Google Scholar
- Palmer, J. D., R. K. Jansen, H. J. Michaels, M. W. Chase, andJ. R. Manhart. 1988. Chloroplast DNA variation and plant phylogeny. Ann. Missouri Bot. Gard. 75: 1180–1206.
- Petitpierre, E., C. Juan, andD. J. Futuyma. A cytogenetic contribution to evolutionary interrelationships in the Nearctic genus Ophraella and allied species of leaf beetles (Coleoptera, Chrysomelidae). Ann. Ent. Soc. Am. 83: 689–693.
10.1093/aesa/83.4.689 Google Scholar
- Picman, A. C. 1986. Biological activities of sesquiterpene lactones. Biochem. Syst. Ecol. 14: 255–281.
- Raffauf, R. F. 1970. A Handbook of Alkaloids and Alkaloid-containing Plants. Wiley Interscience, N.Y.
- Ridley, M. 1983. The Explanation of Organic Diversity: The Comparative Method and Adaptations for Mating. Clarendon, Oxford.
- Robinson, T. 1979. The evolutionary ecology of alkaloids, pp. 413–448. In G. A. Rosenthal and D. H. Janzen (eds.), Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, N.Y.
- Rogers, J. S. 1972. Measures of genetic similarity and genetic distance. Studies in Genetics VII. Univ. Texas Publ. 7213: 145–153.
- Sanderson, M. J. 1989. Confidence limits on phylogenies: The bootstrap revisited. Cladistics 5: 113–129.
- Sarich, V. M. 1977. Rates, sample sizes, and the neutrality hypothesis for electrophoresis in evolutionary studies. Nature 265: 24–28.
- Seaman, F. C. 1982. Sesquiterpene lactones as taxonomic characters in the Asteraceae. Bot. Rev. 48: 121–595.
- Seaman, F.C., andV. A. Funk. 1983. Cladistic analysis of complex natural products: Developing transformation series from sesquiterpene lactone data. Taxon 32: 1–27.
- Seeno, T., andJ. A. Wilcox. 1982. Leaf beetle genera (Coleoptera: Chrysomelidae). Entomography 1: 1–221.
- Selander, R. K., M. H. Smith, S. Y. Yang, W. E. Johnson, andJ. B. Gentry. 1971. Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old-field mouse (Peromyscus polionotus). Studies Genet. Univ. Texas Publ. 7103: 49–90.
- Siciliano, M. R., andC. R. Shaw. 1976. Separation and visualization of enzymes on gels, pp. 185–209. In I. Smith (ed.), Chromatographic and Electrophoretic Techniques, Vol. 2. Heinemann, London.
- Silfverberg, H. 1974. The West Palaearctic species of Galerucella Crotch and related genera (Coleoptera, Chrysomelidae). Notulae Entomologicae 14: 1–11.
- Silfverberg, H. 1976. Studies on galerucine genitalia I (Coleoptera, Chrysomelidae). Notulae Entomologicae 16: 1–9.
- Smith, E. H. 1979. Techniques for the dissection and mounting of the male (aedeagus) and female (spermatheca) genitalia of the Chrysomelidae (Coleoptera). Coleop. Bull. 33: 93–103.
- Sneath, P. H. A., andR. R. Sokal. 1973. Numerical Taxonomy. Freeman, San Francisco.
- Spencer, K. C. 1988. Chemical mediation of coevolution in the Passiflora-Heliconius interaction, pp. 167–240. In K. C. Spencer (ed.), Chemical Mediation of Coevolution. Academic Press, San Diego.
10.1016/B978-0-12-656855-4.50011-5 Google Scholar
- A. R. Stone, and D. L. Hawksworth (eds.). 1986. Coevolution and Systematics. Clarendon, Oxford.
- Swain, T., andC.A. Williams. 1977. Heliantheae— Chemical review, pp. 673–697. In V. H. Heywood, J. B. Harborne, and B. L. Turner (eds.), The Biology and Chemistry of the Compositae. Academic Press, London.
- Swofford, D. L. 1985. PAUP: Phylogenetic Analysis Using Parsimony. User's Manual. Illinois Natural History Survey, Champaign, IL.
- Swofford, D. L., andS. H. Berlocher. 1987. Inferring evolutionary trees from gene frequency data under the principle of maximum parsimony. Syst. Zool. 36: 293–325.
- Swofford, D. L., andW. P. Maddison. 1987. Reconstructing ancestral character states under Wagner parsimony. Math. Biosci. 87: 199–229.
- Swofford, D. L., andR. B. Selander. 1981. BIOSYS-1: A FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. J. Hered. 72: 281–283.
- Tanner, V. M. 1927. A preliminary study of the genitalia of female Coleoptera. Trans. Am. Entomol. Soc. 53: 5–50.
- Templeton, A. R. 1983. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37: 221–244.
- Thompson, J. N. 1989. Concepts of coevolution. Trends Ecol. Evol. 4: 179–183.
- Thorpe, J. P. 1982. The molecular clock hypothesis: Biochemical evolution, genetic differentiation and systematics. Annu. Rev. Ecol. Syst. 13: 139–168.
- Timm, R. M. 1983. Fahrenholz's rule and resource tracking: A study of host-parasite coevolution, pp. 225–265. In M. H. Nitecki (ed.), Coevolution. University of Chicago Press, Chicago.
- Turner, B. L. 1977. Fossil history and geography, pp. 21–39. In V. H. Heywood, J. B. Harborne, and B. L. Turner (eds.), The Biology and Chemistry of the Compositae. Academic Press, London.
- Wagner, G. P. 1989. The origin of morphological characters and the biological basis of homology. Evolution 43: 1157–1171.
- Welch, K. A. 1978. Biology of Ophraella notulata (Coleoptera: Chrysomelidae). Ann. Entomol. Soc. Am. 72: 269–270.
- Wiebes, J. T. 1979. Co-evolution of figs and their insect pollinators. Annu. Rev. Ecol. Syst. 10: 1–12.
- Wilcox, J. A. 1965. A synopsis of North American Galerucinae (Coleoptera:Chrysomelidae). Bull. N.Y. State Mus. Sci. Serv. 400: 1–226. Albany, NY.
- Woods, C. W. 1924. The blueberry leaf beetle and some of its relatives. II. Ecological and biological. Bull. Maine Agric. Exp. Sta. 319: 92–141.
- Zwölfer, H., andJ. Herbst. 1988. Präadaptation, Wirtskreiserweiterung und Parallele-Cladogenese in der Evolution von phytophagen Insekten. Z. Zool. Syst. Evolutionsforsch. 26: 320–340.
10.1111/j.1439-0469.1988.tb00321.x Google Scholar