Skip to main content
Log in

The Role of Males in Host-Fruit Selection by Females of a Walnut Infesting Tephritid (Diptera) Rhagoletis zoqui

  • Published:
Journal of Insect Behavior Aims and scope Submit manuscript

Abstract

Rhagoletis zoqui Bush flies have a mating system in which males guard and defend walnut fruit-hosts from other males and mate, apparently without courtship, with females as they arrive to oviposit. Hypothetically, female selection of a particular fruit may be due to the quality of fruit for larval development (previously determined by guarding males), the quality of the male upon the fruit as a mate, or both, but this is not clear. We performed an experiment to determine if R. zoqui females or males select the fruit to oviposit or guard based on its quality for larval development (i.e., size, sugar-content [brix] or hardness), or following male-mediated cues such as chemical residues, related to prior fruit occupation by the male during guarding. Fruit choice by R. zoqui females and males were examined under semi-natural conditions on caged branches of English walnut trees, Juglans regia L., growing in the highlands of south-central Mexico. A single male or female was allowed to select a fruit and was then removed. An individual of the opposite sex was then introduced to the same branch and presented with the opportunity to choose among the same array of hosts. The pattern of fruit choice was consistent, with female choice on the basis of male presence, suggesting that males left a chemical cue that persisted in their absence. No fruit quality differences were detected between selected and non-selected fruit. Fruit features selected by females and males matched almost exactly, although males rarely select the same fruit as females. We conclude that females preferentially selected fruit previously occupied by males although additional studies are required to determine the cues used by R. zoqui for oviposition resource selection by both females and resource guarding males.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alcock J, Thornhill R (2014) The evolution of insect mating systems. In: DM Shuker, LW Simmons (eds) The Evolution of Insect Mating Systems. Oxford University Press, USA, pp 275–278

  • Alonso-Pimentel H, Korer J, Nufio C, Papaj D (1998) Role of colour and shape stimuli in host-enhanced oogenesis in the walnut fly, Rhagoletis juglandis. Physiol Entomol 23:97–104

    Article  Google Scholar 

  • Aluja M, Mangan RL (2008) Fruit fly (Diptera: Tephritidae) host status determination: critical conceptual, methodological, and regulatory considerations. Annu Rev Entomol 53:473–502

  • Aluja M, Piñero J, López M, Ruíz C, Zúñiga A, Piedra E, Díaz-Fleischer F, Sivinski J (2000) New host plant and distribution records in Mexico for Anastrepha spp., Toxotrypana curvicauda Gerstacker, Rhagoletis zoqui Bush, Rhagoletis sp., and Hexachaeta sp. (Diptera: Tephritidae). P Entomol Soc Wash 102:802–815

  • Aluja M, Lozada N, Piñero J, Birke A, Hernández- Ortíz V, Díaz-Fleischer F (2001) Basic behavior of Rhagoletis turpiniae (Diptera: Tephritidae) with comparative notes on the sexual behavior of Rhagoletis pomonella and Rhagoletis zoqui. Annals Entomol Soc Am 94: 268–274

  • Aluja M, Rull J, Sivinski J, Trujillo G, Perez-Staples D (2009) Male and female condition influence mating performance and sexual receptivity in two tropical fruit flies (Diptera: Tephritidae) with contrasting life histories. J Insect Physiol 55:1091–1098

    Article  CAS  PubMed  Google Scholar 

  • Andersson MB (1994) Sexual selection. Princeton, New Jersey. Princeton University Press

    Google Scholar 

  • Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Animal Behav 60:145–164

    Article  Google Scholar 

  • Balagawi S, Vijaysegaran S, Drew RAI, Raghu S (2005) Influence of fruit traits on oviposition preference and offspring performance of Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) on three tomato (Lycopersicon lycopersicum) cultivars. Aust J Entomol 44:97–103

    Article  Google Scholar 

  • Balagawi S, Drew RAI, Clarke AR (2013) Simultaneous test of the preference-performance and phylogenetic conservatism hypotheses: is either theory useful? Arth-Plant Int 7:299–313

    Article  Google Scholar 

  • Bierbaum T, Bush GL (1990) Host fruit chemical stimuli eliciting distinct ovipositional responses from sibling species of Rhagoletis fruit flies. Entomol Exp Appl 56:165–177

    Article  Google Scholar 

  • Burk T (1981) Signaling and sex in acalyptrate flies. Fla Entomol 64:30–43

    Article  Google Scholar 

  • Cha DH, Yee W, Goughnour R, Sim S, Powell T, Feder J, Linn CE (2012) Identification of host fruit volatiles from domestic apple (Malus domestica), native black hawthorn (Crataegus douglasii) and introduced ornamental hawthorn (C. monogyna) attractive to Rhagoletis pomonella flies from the western United States. J Chem Ecol 38:319–329

    Article  CAS  PubMed  Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    Article  CAS  PubMed  Google Scholar 

  • Guillén L (2008) Rhagoletis zoqui Bush (Diptera: Tephritidae) Como un posible modelo de especiación simpátrica. Instituto de Neuroetología, Universidad Veracruzana, Tesis de Maestría

  • Guillén L, Aluja M, Rull J, Höhn H, Schwitzer T, Samietz J (2011) Influence of walnut cultivar on infestation by Rhagoletis completa (Diptera: Tephritidae): behavioural and management implications. Entomol Exp Appl 140:207–217

    Article  Google Scholar 

  • Henneman ML, Papaj DR (1999) Role of host fruit color in the behavior of the walnut fly Rhagoletis juglandis. Entomol Exp Appl 93:249–258

    Article  Google Scholar 

  • Jaenike J (1990) Host specialization in phytophagous insects. Ann Rev Ecol Syst 21:243–273

  • Jaenike J (1978) Optimal oviposition behavior in phytophagous insects. Theor Popul Biol 14:350–356

    Article  CAS  PubMed  Google Scholar 

  • Katsoyannos BI (1975) Oviposition-deterring, male-arresting, fruit marking pheromone in Rhagoletis cerasi. Env Entomol 4:801–807

    Article  Google Scholar 

  • Katsoyannos BI (1976) Female attraction to males in Rhagoletis cerasi. Env Entomol 5:474–476

    Article  Google Scholar 

  • Katsoyannos BI (1989) Response to shape, size and color. In: Robinson A, Hooper G (eds) World crop pests, Fruit Flies Their Biology, vol 3ª. Natural Enemies and Control. Elsevier, Amsterdam, pp. 307–324

    Google Scholar 

  • Katsoyannos B, Boller E, Remund U (1980) A simple olfactometer for the investigation of sex pheromones and other olfactory attractants in fruit flies and moths. Zeit für Ange Entomol 90:105–112

    Article  Google Scholar 

  • Lalonde RG, Mangel M (1994) Seasonal effects on superparasitism by Rhagoletis completa. J Anim Ecol 63:583–588

    Article  Google Scholar 

  • Linn Jr CE, Yee WL, Sim SB, Cha DH, Powell THQ, Goughnour RB, Feder JL (2012) Behavioral evidence for fruit odor discrimination and sympatric host races of Rhagoletis pomonella flies in the western United States. Evolution 66:3632–3641

    Article  PubMed  Google Scholar 

  • Mayhew PJ (1997) Adaptative patterns of host-plant selection by phytophagous insects. Oikos 79:417–428

    Article  Google Scholar 

  • Messina FJ (1990) Components of host choice by two Rhagoletis species (Diptera: Tephritidae) in Utah. J Kans Entomol Soc 3:80–87

  • Messina FJ, Alston DG, Jones VP (1991) Oviposition by the western cherry fruit fly (Diptera: Tephritidae) in relation to host development. J Kans Entomol Soc 64:197–208

    Google Scholar 

  • Nufio CR, Papaj DR (2004) Superparasitism of larval hosts by the walnut fly, Rhagoletis juglandis, and its implications for female and offspring performance. Oecologia 141:460–467

    Article  PubMed  Google Scholar 

  • Nufio CR, Papaj DR, Alonso-Pimentel H (2000) Host utilization by the walnut fly, Rhagoletis juglandis (Diptera: Tephritidae). Environ Entomol 29:994–1001

    Article  Google Scholar 

  • Opp S, Prokopy R (2000) Multiple mating and reproductive success of male and female apple maggot flies, Rhagoletis pomonella (Diptera: Tephritidae). J Insect Behav 13:901–914

    Article  Google Scholar 

  • Papaj DR (1993) Use and avoidance of occupied hosts as a dynamic process in tephritid flies. In: Bernays EA (ed) Insect-plant interactions, CRC Press, vol 5. Boca Raton, FL, pp. 25–46

    Google Scholar 

  • Papaj DR (1994) Oviposition site guarding by male walnut flies and its possible consequences for mating success. Behav Ecol Sociobiol 34:187–195

    Article  Google Scholar 

  • Papaj DR, Alonso-Pimentel H (1997) Why walnut flies superparasitize: time savings as a possible explanation. Oecologia 109:166–174

    Article  Google Scholar 

  • Papaj DR, García JM, Alonso-Pimentel H (1996) Marking of host fruit by male Rhagoletis boycei Cresson flies (Diptera: Tephritidae) and its effect on egg-laying. J Insect Behav 9:585–597

    Article  Google Scholar 

  • Parker GA (1979) Sexual selection and sexual conflict. In: Blum M, Blum N (eds) Sexual selection and reproductive competition in insects. Academic Press, NY, pp. 123–166

    Google Scholar 

  • Perez-Staples D, Aluja M, Macias-Ordóñez R, Sivinski J (2008) Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua. Behav Ecol Sociobiol 62:1333–1340

  • Pizzari T, Wedell N (2013) The polyandry revolution. Phil Trans Roy Soc B 368:20120041

    Article  Google Scholar 

  • Prokopy RJ (1975) Mating behavior in Rhagoletis pomonella. V. Virgin female attraction to male odor. Can Entomol 107:905–908

    Article  Google Scholar 

  • Prokopy RJ (1980) Mating behavior of frugivorous Tephritidae in nature. In: Proceedings, symposioum on fruit fly problems, XVI international congress of entomology, Kyoto. Japan. National Institute of Agricultural Science, Yatabe, Ibaraki, Japan, pp. 37–37

    Google Scholar 

  • Prokopy RJ, Bush GL (1972) Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). III. Male aggregation in response to an arrestant. Can Entomol 104:275–283

    Article  Google Scholar 

  • Prokopy RJ, Papaj DR (2000) Behavior of flies of the genera Rhagoletis, Zonosemata, and Carpomya. In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press Boca Raton, Florida, USA, pp. 219–252

  • Prokopy RJ, Moericke V, Bush GL (1973) Attraction of apple maggot flies to odor of apples. Env Entomol 2:743–749

    Article  Google Scholar 

  • Ridley M (1990) The control and frequency of mating in insects. Funct Ecol 4:75–84

    Article  Google Scholar 

  • Roitberg BD, Mangel M (1998) On the evolutionary ecology of marking pheromones. Evol Ecol 2:289–315

    Article  Google Scholar 

  • Rull J, Aluja M, Tadeo E, Guillén L, Egan S, Glover M, Feder JL (2013) Distribution, host plant affiliation, phenology, and phylogeny of walnut-infesting Rhagoletis flies (Diptera: Tephritidae) in Mexico. Biol J Linn Soc 110:765–779

  • Simmons L (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Ann Rev Ecol Evol Syst 36:125–146

    Article  Google Scholar 

  • Sivinski J, Heath R (1988) Effects of oviposition on remating, response to pheromones, and longevity in the female Caribbean fruit-fly, Anastrepha suspensa (Diptera, Tephritidae). Ann Entomol Soc Am 81:1021–1024

    Article  Google Scholar 

  • Sivinski J, Burk T, Webb JC (1984) Acoustic courtship signals in the Caribbean fruit fly, Anastrepha suspensa (Loew). Animal Behav 32:1011–1016

    Article  Google Scholar 

  • Sivinski J, Klug H, Shapiro J, Lane J, Mankin R (2004) Ultra violet reflectance on the heads and wings of Anastrepha suspensa (Loew) and Ceratitis capitata (Weidemann). Stud Dipterol 11:313–322

    Google Scholar 

  • Slayter R, Mautz B, Backwell P, Jennions M (2011) Estimating genetic benefits of polyandry from experimental studies: a meta-analysis. Biol Rev 87:1–33

    Article  Google Scholar 

  • StatSoft Inc. (2004) STATISTICA (data analysis software system), version 7., OK, USA. www.statsoft.com

  • Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14

    Article  Google Scholar 

Download references

Acknowledgments

We are very grateful to Emilio Acosta Hernández for technical support in the field and to the Jinéz, Cervantes, Flores-García, Cerón-Cortés, López and Montes-Piña families for permission to use their trees during this study. Abdo Zaid (USDA-ARS. Office of the Director RBRRC, 950 College Station Rd., Athens, GA, 30605) provided useful statistical advice. We thank to four anonymous reviewers and Trevor Williams for constructive comments. Financial support was provided by the Mexican National Council for Science and Technology (CONACYT) (Reference No. CB 2005-25889-50008Q), Campaña Nacional contra Moscas de la Fruta (DGSV-SAGARPA), by the Instituto de Ecología, A.C., and by the Center for Medical, Agricultural and Veterinary Entomology (ARS-USDA). This study formed part of the PhD dissertation of LG (Universidad Veracruzana, Instituto de Neuroetología).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Larissa Guillén.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guillén, L., Sivinski, J. & Rull, J. The Role of Males in Host-Fruit Selection by Females of a Walnut Infesting Tephritid (Diptera) Rhagoletis zoqui . J Insect Behav 29, 69–79 (2016). https://doi.org/10.1007/s10905-015-9541-1

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10905-015-9541-1

Keywords

Navigation