Natural selection in the tropical treehopper Alchisme grossa (Hemiptera: Membracidae) on two sympatric host-plants

Abstract

The pronotum is the most distinctive and representative structure in treehoppers. Although several functions have been proposed for this structure, its involvement in fitness has not been formally evaluated. Given the high degree of maternal investment exhibited by the subsocial membracid Alchisme grossa (Hoplophorionini), the pronotum has been suggested as a shield for offspring protection. We performed selection gradient analyses on A. grossa in order to evaluate how natural selection is acting upon two traits associated with this structure considering three different fitness proxies: (1) number of eggs, (2) the ratio between the number of first-stage nymphs and the number of eggs (early survival), and (3) the number of third-stage nymphs (late survival). Since A. grossa feeds, oviposits and mates on two alternative host-plants (Brugmansia suaveolens and Solanum ursinum, both Solanaceae), we also evaluated and compared selection gradients between these host-plants. We found positive linear selection acting upon pronotum length considering the number of eggs and the late survival fitness proxies and positive linear selection acting on the distance between the suprahumeral horns considering the early survival proxy on females ovipositing on both host-plants. These results highlight the importance of the pronotum in treehoppers females’ fitness and suggest that maternal care appears to have a greater importance in the way that natural selection is operating than the host-plant where oviposition occurs.

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References

  1. Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361

    Article  Google Scholar 

  2. Boulard M (1983) Sur deux Anchistrotus et la mutilation naturelle du pronotum chez les Membracides de ce genre. Bull Soc Entomol Fr 88:274–283

    Google Scholar 

  3. Bristow CM (1983) Treehoppers transfer maternal care to ants: a new benefit of mutualism. Science 220:532–533

    CAS  Article  PubMed  Google Scholar 

  4. Camacho L, Keil C, Dangles O (2014) Factors influencing egg parasitism in sub-social insects: insights from the treehopper Alchisme grossa (Hemiptera, Auchenorrhyncha, Membracidae). Ecol Entomol 39(1):58–65

    Article  Google Scholar 

  5. Caruso CM, Peterson SB, Ridley CE (2003) Natural selection on floral traits of Lobelia (Lobelliaceae): spatial and temporal variation. Am J Bot 90(9):1333–1340

    Article  PubMed  Google Scholar 

  6. Choe JC, Crespi BJ (1997) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge

    Book  Google Scholar 

  7. Cocroft RB (1996) Insect vibrational defense signals. Nature 382:679–680

    Article  Google Scholar 

  8. Cocroft RB (1999a) Offspring-parent communication in a subsocial treehopper (Hemiptera: Membracidae: Umbonia crassicornis). Behaviour 136(1):1–21

    Article  Google Scholar 

  9. Cocroft RB (1999b) Parent-offspring communication in response to predators in a subsocial treehopper (Hemiptera: Membracidae: Umbonia crassicornis). Ethology 105:553–568

    Google Scholar 

  10. Cocroft RB (2002) Antipredator defense as a limited resource: unequal predation risk in broods of an insect with maternal care. Behav Ecol 13(1):125–133

    Article  Google Scholar 

  11. Cocroft RB, Rodríguez RL, Hunt RE (2008) Host shifts, the evolution of communication and speciation in the Enchenopa binotata species complex of treehoppers. In: Tilmon KJ (ed) Speciation, specialization and radiation: the evolutionary biology of insect and plant interactions. University of California Press, California, pp 88–100

    Google Scholar 

  12. Cocroft RB, Rodríguez RL, Hunt RE (2010) Host shifts and signal divergence: mating signals covary with host plant use in a complex of specialized plant-feeding insects. Biol J Linn Soc 99:60–72

    Article  Google Scholar 

  13. Creão-Duarte AJ, Sakakibara AM (1997) Revisao de Alchisme Kirkaldy (Hemiptera, Membracidae, Membracinae, Hoplophorionini). Rev Bras Zool 14(2):425–472

    Article  Google Scholar 

  14. Cuartas-Domínguez M, Medel R (2010) Pollinator-mediated selection and experimental manipulation of the flower phenotype in Chloraea bletioides (Orchidaceae). Funct Ecol 24:1219–1227

    Article  Google Scholar 

  15. Del-Claro K, Oliveira PS (1996) Honeydew flicking by treehoppers provides cues to potential tending ants. Anim Behav 51:1071–1075

    Article  Google Scholar 

  16. Del-Claro K, Oliveira PS (1999) Ant-Homoptera interactions in a Neotropical savanna: the honeydew-producing treehopper, Guayaquila xiphias (Membracidae), and its associated ant fauna on Didymopanax vinosum (Araliaceae). Biotropica 31(1):135–144

    Google Scholar 

  17. Flores-Prado L, Pinto CF, Rojas A, Fontúrbel FE (2014) Strong selection on mandible and nest features in a carpenter bee that nests in two sympatric host plants. Ecol Evol 4(10):1820–1827

    Article  PubMed  PubMed Central  Google Scholar 

  18. Godoy C, Miranda X, Nishida K (2006) Treehoppers of Tropical America. Instituto Nacional de Biodiversidad, San José

    Google Scholar 

  19. Hodgins KA, Barrett SCH (2008) Natural selection on floral traits through male and female function in wild populations of the heterostylous daffodil Narcissus triandrus. Evolution 62(7):1751–1763

    Article  PubMed  Google Scholar 

  20. Honek A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66(3):483–492

    Article  Google Scholar 

  21. Jordano P (1995) Frugivore-mediated selection on fruit and seed size: birds and St. Lucie’s cherry, Prunus mahaleb. Ecology 76(8):2627–2639

    Article  Google Scholar 

  22. Keese MC, Wood TK (1991) Host-plant mediated geographic variation in the life history of Platycottis vittata (Homoptera: Membracidae). Ecol Entomol 16:63–72

    Article  Google Scholar 

  23. Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three rules. Evol Ecol Res 10:251–268

    Google Scholar 

  24. Kingsolver JG, Pfennig DW (2004) Individual-level selection as a cause of Cope’s rule of phyletic size increase. Evolution 58(7):1608–1612

    Article  PubMed  Google Scholar 

  25. Kudo S (2002) Phenotypic selection and function of reproductive behavior in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae). Behav Ecol 13(6):742–749

    Article  Google Scholar 

  26. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37(6):1210–1226

    Article  Google Scholar 

  27. Lin CP (2006) Social behaviour and life history of membracine treehoppers. J Nat Hist 40(32):1887–1907

    Article  Google Scholar 

  28. Lin CP (2007) Observations of a subsocial treehopper, Stalotypa fairmairii from Cuba (Hemiptera: Membracidae). Fla Entomol 90(2):398–400

    Article  Google Scholar 

  29. Lin CP, Danforth BN, Wood TK (2004) Molecular phylogenetics and evolution of maternal care in membracine treehoppers. Syst Biol 53(3):400–421

    Article  PubMed  Google Scholar 

  30. McKamey SH, Deitz LL (1996) Generic revision of the New World tribe Hoplophorionini (Hemiptera: Membracidae: Membracinae). Syst Entomol 21:295–342

    Article  Google Scholar 

  31. Medel R (2000) Assessment of parasite-mediated selection in a host-parasite system in plants. Ecology 81(6):1554–1564

    Google Scholar 

  32. Murúa M, Espinoza C, Bustamante R, Marín VH, Medel R (2010) Does human-induced hábitat transformation modify pollinator-mediated selection? A case study in Viola portalesia (Violaceae). Oecologia 163:153–162

    Article  PubMed  Google Scholar 

  33. Nault LR, Wood TK, Goff AM (1974) Treehopper (Membracidae) alarm pheromones. Nature 249:387–388

    CAS  Article  PubMed  Google Scholar 

  34. Poulton EB (1903) Suggestions as to the meaning of the shapes and colours of the Membracidae, in the struggle for existence. In: Buckton GB (ed) A monograph of the Membracidae. Lovell Reeve, London, pp 273–285

    Google Scholar 

  35. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria www.R-project.org

  36. Ramaswamy K, Cocroft RB (2009) Collective signals in treehoppers provide predator location cues to the defending mother. Anim Behav 78:697–704

    Article  Google Scholar 

  37. Ruiz-Montoya L, Núñez-Farfán J (2009) Natural selection and maternal effects in life history traits of Brevicoryne brassicae (Homoptera: Aphididae) on two sympatric closely related hosts. Fla Entomol 92(4):635–644

    Article  Google Scholar 

  38. Stegmann UE (1998) An exaggerated trait in insects: the prothoracic skeleton of Stictocephala bisonia (Homoptera: Membracidae). J Morphol 238:157–178

    Article  Google Scholar 

  39. Tallamy DW, Wood TK (1986) Convergence patterns in subsocial insects. Annu Rev Entomol 31:369–390

    Article  Google Scholar 

  40. Torrico-Bazoberry D (2014) Selección natural en el membrácido subsocial Alchisme grossa (Hemiptera: Membracidae) en el contexto de uso de plantas hospederas alternativas. B.Sc. thesis, Universidad Mayor de San Simón, Cochabamba, Bolivia

  41. Torrico-Bazoberry D, Caceres-Sanchez L, Saavedra-Ulloa D, Flores-Prado L, Niemeyer H, Pinto CF (2014) Biology and ecology of the treehopper Alchisme grossa in a cloud forest of the Bolivian Yungas. J Insect Sci 14(169):1–4

    Google Scholar 

  42. Trumbo ST (2012) Patterns of parental care in invertebrates. In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 81–100

    Chapter  Google Scholar 

  43. Visser ME (1994) The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). J Anim Ecol 63:963–978

    Article  Google Scholar 

  44. Wade MJ, Kalisz S (1990) The causes of natural selection. Evolution 44(8):1947–1955

    Article  Google Scholar 

  45. Weber A, Kolb A (2013) Population size, pollination and phenotypic trait selection in Phyteuma spicatum. Acta Oecol 47:46–51

    Article  Google Scholar 

  46. Wood TK (1974) Aggregation behavior of Umbonia crassicornis (Homoptera: Membracidae). Can Entomol 106:169–173

    Article  Google Scholar 

  47. Wood TK (1975) Studies on the function of the Membracid pronotum (Homoptera) II: histology. Proc Entomol Soc Wash 77(1):78–82

    Google Scholar 

  48. Wood TK (1976) Biology and presocial behavior of Platycotis vittata (Homoptera: Membracidae). Ann Entomol Soc Am 69:807–811

    Article  Google Scholar 

  49. Wood TK (1977) Defense in Umbonia crassicornis: role of pronotum and adult aggregations (Homoptera: Membracidae). Ann Entomol Soc Am 70:524–528

    Article  Google Scholar 

  50. Wood TK (1984) Life history patterns of tropical membracids (Homoptera: Membracidae). Sociobiology 8:299–344

    Google Scholar 

  51. Wood TK (1993) Diversity in the new world Membracidae. Ann Rev Entomol 38:409–435

    Article  Google Scholar 

  52. Wood TK, Morris GK (1974) Studies on the function of the membracid pronotum (Homoptera) I: occurrence and distribution of articulated hairs. Can Entomol 106(2):143–148

    Article  Google Scholar 

  53. Wood TK, Tilmon KJ, Shantz AB, Harris CK, Pesek J (1999) The role of host-plant fidelity in initiating insect race formation. Evol Ecol Res 1:317–332

    Google Scholar 

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Acknowledgments

Liliana Caceres and Alejandro Coca provided field support. Comments of Mariano Ordano, Santiago Benitez and two anonymous reviewers improved an earlier version of the manuscript. LANBIO (Latin American Network for Research on Bioactive Natural Compounds) and International Foundation for Science (IFS), who supported and funded this work, and INTEGRA S.A. authorized the work at Incachaca and provided housing facilities.

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Correspondence to Carlos F. Pinto.

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Torrico-Bazoberry, D., Pinto, C.F., Flores-Prado, L. et al. Natural selection in the tropical treehopper Alchisme grossa (Hemiptera: Membracidae) on two sympatric host-plants. Arthropod-Plant Interactions 10, 229–235 (2016). https://doi.org/10.1007/s11829-016-9427-y

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Keywords

  • Bolivia
  • Phenotypic selection
  • Pronotum
  • Selection gradients
  • Yungas