HOST‐PLANT SWITCHES AND THE EVOLUTION OF CHEMICAL DEFENSE AND LIFE HISTORY IN THE LEAF BEETLE GENUS OREINA

Insect‐plant interactions have played a prominent role in investigating phylogenetic constraints in the evolution of ecological traits. The patterns of host association among specialized insects have often been described as highly conservative, yet not all specialized herbivorous insect lineages display the same degree of fidelity to their host plants. In this paper, we present an estimate of the evolutionary history of the leaf beetle genus Oreina. This genus displays an amazing flexibility in several aspects of its ecology and life history: (1) host plant switches in Oreina occurred between plant families or distantly related tribes within families and thereby to more distantly related plants than in several model systems that have contributed to the idea of parallel cladogenesis; (2) all species of the genus are chemically defended, but within the genus a transition between autogenous production of defensive toxins and sequestration of secondary plant compounds has occurred; and (3) reproductive strategies in the genus range from oviparity to viviparity including all intermediates that could allow the gradual evolution of viviparity. Cladistic analysis of 18 allozyme loci found two most parsimonious trees that differ only in the branching of one species. According to this phylogeny estimate, Oreina species were originally associated with Asteraceae, with an inclusion of Apiaceae in the diet of one oligophagous species and an independent switch to Apiaceae in a derived clade. The original mode of defense appears to be the autogenous production of cardenolides as previously postulated; the additional sequestration of pyrrolizidine alkaloids could have either originated at the base of the genus or have arisen three times independently in all species that switched to plants containing these compounds. Viviparity apparently evolved twice in the genus, once without matrotrophy, through a retention of the eggs inside the female's oviducts, and once in combination with matrotrophy. We hypothesize that the combination of autogenous defense and a life history that involves mobile externally feeding larvae allowed these beetles to switch host plants more readily than has been reported for highly conservative systems.

[1]  M. Rowell‐Rahier,et al.  Reproductive biology of viviparous and oviparous species of the leaf beetle genus Oreina , 1996 .

[2]  A. Meyer,et al.  A HISTORY OF HOST ASSOCIATIONS AND EVOLUTIONARY DIVERSIFICATION FOR OPHRAELLA (COLEOPTERA: CHRYSOMELIDAE): NEW EVIDENCE FROM MITOCHONDRIAL DNA , 1995, Evolution; international journal of organic evolution.

[3]  D. Futuyma,et al.  GENETIC CONSTRAINTS ON MACROEVOLUTION: THE EVOLUTION OF HOST AFFILIATION IN THE LEAF BEETLE GENUS OPHRAELLA , 1995, Evolution; international journal of organic evolution.

[4]  L. Dyer Tasty Generalists and Nasty Specialists? Antipredator Mechanisms in Tropical Lepidopteran Larvae , 1995 .

[5]  J. Pasteels,et al.  Relative unpalatability of leaf beetles with either biosynthesized or sequestered chemical defence , 1995, Animal Behaviour.

[6]  J. Pasteels,et al.  Coding Allozyme Data Using Step Matrices: Defining New Original States for the Ancestral Taxa , 1994 .

[7]  K. Bremer,et al.  Asteraceae: Cladistics and Classification , 1994 .

[8]  A. Meyer,et al.  The evolution of copulatory organs, internal fertilization, placentae and viviparity in killifishes (Cyprinodontiformes) inferred from a DNA phylogeny of the tyrosine kinase gene X-src , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  D. Futuyma,et al.  GENETIC CONSTRAINTS AND THE PHYLOGENY OF INSECT‐PLANT ASSOCIATIONS: RESPONSES OF OPHRAELLA COMMUNA (COLEOPTERA: CHRYSOMELIDAE) TO HOST PLANTS OF ITS CONGENERS , 1993, Evolution; international journal of organic evolution.

[10]  J. Bull,et al.  An Empirical Test of Bootstrapping as a Method for Assessing Confidence in Phylogenetic Analysis , 1993 .

[11]  Paula M. Mabee,et al.  Coding Polymorphic Data: Examples from Allozymes and Ontogeny , 1993 .

[12]  G. Fernandes,et al.  Plant--Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions , 1992 .

[13]  Julian Lombardi,et al.  Reflections on the Evolution of Piscine Viviparity , 1992 .

[14]  Daniel G. Blackburn,et al.  Convergent Evolution of Viviparity, Matrotrophy, and Specializations for Fetal Nutrition in Reptiles and Other Vertebrates , 1992 .

[15]  Jean-Claude Bourdonné,et al.  Données sur La Biosystématique des Chrysolina L. S. (Coleoptera: Chrysomelidae: Chrysomelinae) , 1991, Annales de la Société entomologique de France (N.S.).

[16]  D. Futuyma,et al.  PHYLOGENY AND THE EVOLUTION OF HOST PLANT ASSOCIATIONS IN THE LEAF BEETLE GENUS OPHRAELLA (COLEOPTERA, CHRYSOMELIDAE) , 1990, Evolution; international journal of organic evolution.

[17]  Brian D. Farrell,et al.  PHYLOGENESIS OF INSECT/PLANT INTERACTIONS: HAVE PHYLLOBROTICA LEAF BEETLES (CHRYSOMELIDAE) AND THE LAMIALES DIVERSIFIED IN PARALLEL? , 1990, Evolution; international journal of organic evolution.

[18]  N. Moran A 48-Million-Year-Old Aphid—Host Plant Association and Complex Life Cycle: Biogeographic Evidence , 1989, Science.

[19]  E. Bernays Host specificity in phytophagous insects: selection pressure from generalist predators , 1988 .

[20]  E. Bernays,et al.  On the Evolution of Host Specificity in Phytophagous Arthropods , 1988 .

[21]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[22]  Tibor Jermy,et al.  Evolution of Insect/Host Plant Relationships , 1984, The American Naturalist.

[23]  D. Janzen,et al.  Herbivores: Their Interaction With Secondary Plant Metabolites , 1982 .

[24]  R. B. Selander,et al.  BIOSYS-1: a FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics , 1981 .

[25]  Bruce A. McPheron,et al.  Interactions Among Three Trophic Levels: Influence of Plants on Interactions Between Insect Herbivores and Natural Enemies , 1980 .

[26]  W. Fitch,et al.  Construction of phylogenetic trees. , 1967, Science.

[27]  P. Raven,et al.  BUTTERFLIES AND PLANTS: A STUDY IN COEVOLUTION , 1964 .

[28]  W. Brown FOOD-PLANTS AND DISTRIBUTION OF THE SPECIES OF CALLIGRAPHA IN CANADA, WITH DESCRIPTIONS OF NEW SPECIES (COLEOPTERA, CHRYSOMELIDAE) , 1945, The Canadian Entomologist.

[29]  J. Braekman,et al.  Chemical defence of adult leaf beetles updated , 1994 .

[30]  R. Murphy The phylogenetic analysis of allozyme data: Invalidity of coding alleles by presence/absence and recommended procedures , 1993 .

[31]  J. Pasteels The value of defensive compounds as taxonomic characters in the classification of leaf beetles , 1993 .

[32]  J. Pasteels,et al.  Proximate and Ultimate Causes for Host plant Influence on Chemical Defense of Leaf beetles (Coleoptera: Chrysomelidae) , 1991 .

[33]  H. Zwölfer EVOLUTIONARY AND ECOLOGICAL RELATIONSHIPS OF THE INSECT FAUNA OF THISTLES , 1988 .

[34]  T. Hsiao Host specificity, seasonality and bionomics of Leptinotarsa beetles , 1988 .

[35]  C. Bontems Localization of spermatozoa inside viviparous and oviparous females of Chrysomelinae , 1988 .

[36]  D. Buth The Application of Electrophoretic Data in Systematic Studies , 1984 .

[37]  C. Bontemps La viviparité chez les Chrysomelinae [Col.] , 1984, Bulletin de la Société entomologique de France.

[38]  J. Lawton,et al.  Insects on Plants , 1984 .

[39]  J. Powell,et al.  Enzyme variability in the Drosophila willistoni group. IV. Genic variation in natural populations of Drosophila willistoni. , 1972, Genetics.

[40]  Jan Bechyné Achter Beitrag zur Kenntnis der Gattung Chrysolina Motsch. (Col. Phytoph. Chrysomelidae) , 1952 .