Sequential mate choice in the South American fruit fly: the role of male nutrition, female size and host availability on female remating behaviour

REFERENCES

• Abraham S, Cladera J, Goane L, Vera MT. 2012. Factors affecting Anastrepha fraterculus female receptivity modulation by accessory gland products. J Insect Physiol. 58:1–6.
   PubMed Web of Science ®Google Scholar
• Abraham S, Contreras-Navarro Y, Pérez-Staples D. 2016a. Female age determines remating behavior in wild Mexican fruit fly. J Insect Behav. 29:340–354.
   Web of Science ®Google Scholar
• Abraham S, Goane L, Cladera J, Vera MT. 2011b. Effects of male nutrition on sperm storage and remating behavior in wild and laboratory Anastrepha fraterculus (Diptera: Tephritidae) females. J Insect Physiol. 57:1501–1509.
   PubMed Web of Science ®Google Scholar
• Abraham S, Goane L, Rull J, Cladera J, Willink E, Vera MT. 2011a. Multiple mating in Anastrepha fraterculus females and its relationship with fecundity and fertility. Entomol Exp Appl. 141:15–24.
   Web of Science ®Google Scholar
• Abraham S, Lara-Pérez LA, Rodriguez C, Contreras-Navarro Y, Núñez-Beverido N, Ovruski S, Pérez-Staples D. 2016b. The male ejaculate as inhibitor of female remating in two tephritid flies. J Insect Physiol. 88:40–47.
   PubMed Web of Science ®Google Scholar
• Abraham S, Liendo MC, Devescovi F, Peralta PA, Yusef V, Ruiz J, Cladera J, Vera MT, Segura DF. 2013. Remating behaviour in Anastrepha fraterculus (Diptera: Tephritidae) females is affected by male juvenile hormone analogue treatment but not by male sterilization. Bull Entomol Res. 103:310–317.
   PubMed Web of Science ®Google Scholar
• Abraham S, Núñez-Beverido N, Contreras-Navarro Y, Pérez-Staples D. 2014. Female receptivity in Anastrepha ludens (Diptera: Tephritidae) is not modulated by accessory glands products. J Insect Physiol. 70:41–48.
   PubMed Web of Science ®Google Scholar
• Alonso-Pimentel H, Korel JB, Nufio C, Papaj DR. 1998. Role of colour and shape stimuli in host-enhanced oogenesis in the walnut fly, Rhagoletis juglandis. Physiol Entomol. 23:97–104.
   Web of Science ®Google Scholar
• Aluja M, Jácome I, Macías-Ordóñez R. 2001. Effects of adult nutrition on male sexual performance in four neotropical fruit fly species of the genus Anastrepha (Diptera: Tephritidae). J Insect Behav. 14:759–775.
   Web of Science ®Google Scholar
• Aluja M, Rull J, Sivinsky J, Trujillo G, Pérez-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.
   PubMed Web of Science ®Google Scholar
• Andersson M. 1994. Sexual selection. Princeton: Princeton University Press.
   Google Scholar
• Bakker TCM, Millinsky M. 1991. Sequential female choice and the previous male effect in sticklebacks. Behav Ecol Sociobiol. 29:205–210.
   Web of Science ®Google Scholar
• Blay S, Yuval B. 1997. Nutritional correlates of reproductive success of male Mediterranean fruit flies (Diptera: Tephritidae). Anim Behav. 54:59–66.
   PubMed Web of Science ®Google Scholar
• Blomquist GJ, Bagnères AG. 2010. Insect hydrocarbons biology, biochemistry, and chemical ecology. New York: University Press.
   Google Scholar
• Bradbury JW. 1981. The evolution of leks. In: Alexander RD, Tinkle DW, editors. Natural selection and social behavior. New York: Chiron Press; p. 138–169.
   Google Scholar
• Briceño RD, Eberhard WG. 2002. Decisions during courtship by male and female medflies (Diptera, Tephritidae): correlated changes in male behavior and female acceptance criteria in mass-reared flies. Fla Entomol. 85:14–31.
   Google Scholar
• Cáceres C, Segura DF, Vera MT, Wornoayporn V, Cladera J, Teal P, Sapountzis P, Bourtzis K, Zacharopoulou A, Robinson AS. 2009. Incipient speciation revealed in Anastrepha fraterculus (Diptera: Tephritidae) by studies on mating compatibility, sex pheromones, hybridization and cytology. Biol J Linn Soc. 97:152–165.
   Web of Science ®Google Scholar
• Candolin U. 2003. The use of multiple cues in mate choice. Biol Rev. 78:575–595.
   PubMed Web of Science ®Google Scholar
• Carsten LD, Papaj DR. 2005. Effects of reproductive state and host resource experience on mating decisions in a walnut fly. Behav Ecol. 16:528–533.
   Web of Science ®Google Scholar
• Costa AM, Anjos-Duarte CS, Roriz AKP, Dias VS, Joachim-Bravo IS. 2012. Male diet and age influence to inhibit female remating in Ceratitis capitata (Diptera: Tephritidae). J Appl Entomol. 136:456–463.
   Web of Science ®Google Scholar
• De Lima IS, Howse PE, Salles LAB. 1994. Reproductive behavior of the South American fruit fly Anastrepha fraterculus (Diptera: Tephritidae): laboratory and field studies. Physiol Entomol. 19:271–277.
   Web of Science ®Google Scholar
• Downhower JF, Lank DB. 1994. Effect of previous experience on mate choice by female mottled sculpins. Anim Behav. 47:369–372.
   Web of Science ®Google Scholar
• Droney DC. 1996. Environmental influences on male courtship and implications for female choice in a lekking Hawaiian Drosophila. Anim Behav. 51:821–830.
   Web of Science ®Google Scholar
• Fedina TY, Kuo T-H, Dreisewerd K, Dierick HA, Yew JY, Pletcher SD. 2012. Dietary effects on cuticular hydrocarbons and sexual attractiveness in Drosophila. PLoS ONE. 7:e49799.
   PubMed Web of Science ®Google Scholar
• Fox CW, Hickman DL. 1994. Influence of oviposition substrate on female receptivity to multiple mating in Callosobruchus maculatus (Coleoptera: Bruchidae). Ann Entomol Soc Am. 87:395–398.
   Web of Science ®Google Scholar
• Frike C, Bretman A, Chapman T. 2008. Adult male nutrition and reproductive success in Drosophila melanogaster. Evolution. 12:3170–3177.
   Google Scholar
• Gabor CR, Halliday TR. 1996. Sequential mate choice by multiply mating smooth newts: female become more choosy. Behav Ecol. 8:162–166.
   Web of Science ®Google Scholar
• Gavriel S, Gazit Y, Yuval B. 2009. Remating by female Mediterranean fruit flies (Ceratitis capitata, Diptera: Tephritidae): temporal patterns and modulation by male condition. J Insect Physiol. 55:637–642.
   PubMed Web of Science ®Google Scholar
• Gibson RM, Langen TA. 1996. How do animals choose their mates? Trends Ecol Evol. 11:468–470.
   PubMed Web of Science ®Google Scholar
• Gray DA. 1999. Intrinsic factors affecting female choice in house crickets: time cost, female age, nutritional condition, body size, and size-relative reproductive investment. J Insect Behav. 12:691–700.
   Web of Science ®Google Scholar
• Harris WE, Moore PJ. 2005. Female mate preference and sexual conflict: females prefer males that have had fewer consorts. Am Nat. 165:64–71.
   Web of Science ®Google Scholar
• Hernández-Ortiz V, Bartolucci AF, Morales-Valle P, Frias D, Selivon D. 2012. Cryptic species of the Anastrepha fraterculus complex (Diptera: Tephritidae): a multivariate approach for the recognition of South American morphotypes. Ann Entomol Soc Am. 105:305–318.
   Web of Science ®Google Scholar
• Ivy TM, Weddle CB, Sakaluk SK. 2005. Females use self-referent cues to avoid mating with previous mates. Proc R Soc Lond B. 272:2475–2478.
   PubMed Web of Science ®Google Scholar
• Jaldo HE, Gramajo MC, Willink E. 2001. Mass rearing of Anastrepha fraterculus (Diptera: Tephritidae): a preliminary strategy. Fla Entomol. 84:716–718.
   Web of Science ®Google Scholar
• Janetos AC. 1980. Strategies of female mate choice: a theoretical analysis. Behav Ecol Sociobiol. 7:107–112.
   Web of Science ®Google Scholar
• Jang EB. 2002. Physiology of mating behavior in Mediterranean fruit fly (Diptera: Tephritidae): chemoreception and male accessory gland fluids in female post-mating behavior. Fla Entomol. 85:89–93.
   Web of Science ®Google Scholar
• Jennions MD, Petrie M. 1997. Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev. 72:283–327.
   PubMed Web of Science ®Google Scholar
• Judge KA, Tran K-C, Gwynne TE. 2010. The relative effect of mating status and age on the mating behavior of female field crickets. Can J Zool. 88:219–223.
   Web of Science ®Google Scholar
• Karl I, Fischer K. 2013. Old male mating advantage results from sexual conflict in a butterfly. Anim Behav. 85:143–149.
   Web of Science ®Google Scholar
• Kaspi R, Taylor PW, Yuval B. 2000. Diet and size influence sexual advertisement and copulatory success of males in Mediterranean fruit fly leks. Ecol Entomol. 25:279–284.
   Web of Science ®Google Scholar
• Kokko H, Rankin DJ. 2006. Lonely hearts or sex in the city? Density-dependent effects in mating systems. Phil Trans R Soc B. 361:319–334.
   PubMed Web of Science ®Google Scholar
• Kotiaho JS. 2002. Sexual selection and condition dependence of courtship display in three species of horned dung beetles. Behav Ecol. 13:791–799.
   Web of Science ®Google Scholar
• Landeta-Escamilla A, Hernández E, Arredondo J, Díaz-Fleischer F, Pérez-Staples D. 2016. Male irradiation affects female remating behavior in Anastrepha serpentina (Diptera: Tephritidae). J Insect Physiol. 85:17–22.
   PubMed Web of Science ®Google Scholar
• Landolt PJ. 1994. Mating frequency of the papaya fruit fly (Diptera: Tephritidae) with and without host fruit. Fla Entomol. 77:305–312.
   Google Scholar
• Lewis Z, Lizé A, Wedell N. 2013. The interplay between different stages of reproduction in males of the moth Plodia interpunctella. Anim Behav. 86:917–922.
   Web of Science ®Google Scholar
• Liedo P, Orozco D, Cruz-Lopez L, Quinteros JL, Becerra-Perez C, Hernandez MR, Oropeza A, Toledo J. 2013. Effect of post-teneral diets on the performance of sterile Anastrepha ludens and Anastrepha obliqua fruit flies. J Appl Entomol. 137:49–60.
   Web of Science ®Google Scholar
• Malavasi A, Morgante JS, Prokopy RJ. 1983. Distribution and activities of Anastrepha fraterculus (Diptera: Tephritidae) flies on host and non host trees. Ann Entomol Soc Am. 76:286–292.
   Web of Science ®Google Scholar
• Pérez-Staples D, Aluja M. 2006. Sperm allocation and cost of mating in a tropical tephritid fruit fly. J Insect Physiol. 52:839–845.
   PubMed Web of Science ®Google Scholar
• Pérez-Staples D, Aluja M, Macías-Ordóñez R, Sivinski J. 2008a. Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua. Behav Ecol Sociobiol. 62:1333–1340.
   Web of Science ®Google Scholar
• Pérez-Staples D, Harmer AMT, Collins SR, Taylor PW. 2008b. Potential for pre-release diet supplements to increase the sexual performance and longevity of male Queensland fruit flies. Agric For Entomol. 10:255–262.
   Web of Science ®Google Scholar
• Pérez-Staples D, Martínez-Hernandez MG, Aluja M. 2010. Male age and experience increases mating success but not female fitness in the Mexican fruit fly. Ethology. 116:778–786.
   Web of Science ®Google Scholar
• Pérez-Staples D, Weldon CW, Smallridge C, Taylor PW. 2009. Pre-release feeding on yeast hydrolysate enhances sexual competitiveness of sterile male Queensland fruit flies in field cages. Entomol Exp App. 131:159–166.
   Web of Science ®Google Scholar
• Pérez-Staples D, Weldon CW, Taylor P. 2011. Sex differences in developmental response to yeast hydrolysate in adult Queensland fruit fly. Entomol Exp Appl. 141:103–113.
   Web of Science ®Google Scholar
• Pitnick S. 1991. Male size influences fecundity and remating internal in Drosophila melanogaster. Anim Behav. 41:735–745.
   Web of Science ®Google Scholar
• Prabhu V, Pérez-Staples D, Taylor PW. 2008. Protein: carbohydrate ratios promoting sexual activity and longevity of male Queensland fruit flies. J Appl Entomol. 132:575–582.
   Web of Science ®Google Scholar
• Prokopy R, Hendrichs J. 1979. Mating behavior of Ceratitis capitata on a field-cage host tree. Ann Entomol Soc Am. 72:642–648.
   Web of Science ®Google Scholar
• Radhakrishnan P, Pérez-Staples D, Weldon CW, Taylor PW. 2009. Multiple mating and sperm depletion in male Queensland fruit flies: effects on female remating behaviour. Anim Behav. 78:839–846.
   Web of Science ®Google Scholar
• Radhakrishnan P, Taylor PW. 2007. Seminal fluids mediate sexual receptivity and copula duration in Queensland fruit flies. J Insect Physiol. 53:741–745.
   PubMed Web of Science ®Google Scholar
• Radhakrishnan P, Taylor PW. 2008. Ability of male Queensland fruit flies to inhibit receptivity in multiple mates, and the associated recovery of accessory glands. J Insect Physiol. 54:421–428.
   PubMed Web of Science ®Google Scholar
• Rapkin J, Jensen K, House CM, Sakaluk SK, Sakaluk JK, Hunt J. 2017. The complex interplay between macronutrient intake, cuticular hydrocarbon expression and mating success in male decorated crickets. J Evol Biol. 30:711–727.
   PubMed Web of Science ®Google Scholar
• Real L. 1990. Search theory and mate choice. I. Models of single-sex discrimination. Am Nat. 136:376–404.
   Web of Science ®Google Scholar
• Rodriguero MS, Vilardi JC, Vera MT, Cayol JP, Rial E. 2002. Morphometric traits and sexual selection in medfly (Diptera: Tephritidae) under field cage conditions. Fla Entomol. 85:143–149.
   Web of Science ®Google Scholar
• Rull J, Abraham S, Kovaleski A, Segura DF, Mendoza M, Liendo MC, Vera MT. 2013. Evolution of prezygotic and postzygotic barriers to gene flow among three cryptic species within the Anastrepha fraterculus complex. Entomol Exp Appl. 148:213–222.
   Google Scholar
• Schafer MA, Uhl G. 2004. Sequential males encounters: female but not male body size influences female remating behavior. Behav Ecol. 16:461–466.
   Web of Science ®Google Scholar
• Schlaepfer MA, McNeil JN. 2000. Are virgin male lepidopterans more successful in mate acquisition than previously mated individuals? A study of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). Can J Zool. 78:2045–2050.
   Web of Science ®Google Scholar
• Sciurano R, Segura D, Rodriguero M, Gómez-Cendra P, Allinghi A, Cladera J, Vilardi JC. 2007. Sexual selection on multivariate phenotypes in Anastrepha fraterculus (Diptera: Tephritidae) from Argentina. Fla Entomol. 90:167–170.
   Google Scholar
• Segura DF, Petit-Marty N, Sciurano RB, Vera MT, Calcagno G, Allinghi A, Gómez-Cendra P, Cladera J, Vilardi JC. 2007. Lekking behavior of Anastrepha fraterculus (Diptera: Tephritidae). Fla Entomol. 90:154–162.
   Google Scholar
• Shelly TE, Kaneshiro KY. 1991. Lek behavior of the Oriental fruit fly, Dacus dorsalis, in Hawaii (Diptera: Tephritidae). J Insect Behav. 4:235–241.
   Web of Science ®Google Scholar
• Shelly TE, Kennelly S. 2002. Influence of male diet on male mating success and longevity and female remating in the Mediterranean fruit fly (Diptera: Tephritidae) under laboratory condition. Fla Entomol. 85:572–578.
   Google Scholar
• Shelly TE, Whittier TS. 1993. Effect of sexual experience on the mating success of males of the Mediterranean fruit fly, Ceratitis capitata Wiedemann (Diptera: Tephritidae). Proc Hawaii Entomol Soc. 32:91–94.
   Google Scholar
• Sivinski J. 1984. Effect of sexual experience on male mating success in a lek forming tephritid Anastrepha suspensa (Loew). Fla Entomol. 67:126–130.
   Google Scholar
• Sivinski J, Heath RR. 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.
   Web of Science ®Google Scholar
• South SH, House CM, Moore AJ, Simpson SJ, Hunt J. 2011. Male cockroaches prefer a high carbohydrates diet that makes them more attractive to females: implications for the study of condition dependence. Evolution. 6:1594–1606.
   Google Scholar
• Statsoft. 2007. STATISTICA 7.0. Tulsa (OK): StatSoft.
   Google Scholar
• Taylor PW, Pérez‐Staples D, Weldon CW, Collins SR, Fanson BG, Yap S, Smallridge C. 2013. Post‐teneral nutrition as an influence on reproductive development, sexual performance and longevity of Queensland fruit flies. J App Entomol. 137:113–125.
   Web of Science ®Google Scholar
• Taylor PW, Yuval B. 1999. Postcopulatory sexual selection in Mediterranean fruit flies, Ceratitis capitata: advantages for large and protein-fed males. Anim Behav. 58:247–254.
   PubMed Web of Science ®Google Scholar
• Teal PEA, Gómez-Simuta Y, Proveaux AT. 2000. Mating experience and juvenile hormone enhance sexual signaling and mating in male Caribbean fruit flies. Proc Natl Acad Sci. 97:3708–3712.
   PubMed Web of Science ®Google Scholar
• Vanicková L, Svatos A, Kroiss J, Kaltenpoth M, Do Nascimento RR, Hoskovec M, Brizová R, Kalinová B. 2012. Cuticular hydrocarbons of the South American fruit fly Anastrepha fraterculus: variability with sex and age. J Chem Ecol. 38:1133–1142.
   PubMed Web of Science ®Google Scholar
• Vera MT, Abraham S, Oviedo A, Willink E. 2007. Demographic and quality control parameters of Anastrepha fraterculus (Diptera: Tephritidae) artificial rearing. Fla Entomol. 90:53–57.
   Google Scholar
• Vijaysegaran S, Walter GH, Drew RAI. 2002. Influence of adult diet on the development of the reproductive system and mating ability of Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). J Trop Agric Food Sci. 30:119–136.
   Google Scholar
• Weddle CB, Steiger S, Hamaker CG, Ower GD, Mitchell C, Sakaluk SK, Hunt J. 2013. Cuticular hydrocarbons as a basis for chemosensory self-referencing in cricket: a potentially universal mechanism facilitating polyandry in insects. Ecol Lett. 16:346–353.
   PubMed Web of Science ®Google Scholar
• Wei D, Feng Y-C, Wei D-D, Yuan G-R, Dou W, Wang J-J. 2015. Female remating inhibition and fitness of Bactrocera dorsalis (Diptera: Tephritidae) associated with male accessory glands. Fla Entomol. 98:52–58.
   Google Scholar
• Weldon CW, Taylor PW. 2011. Sexual development of wild and mass-reared male Queensland fruit flies in response to natural food sources. Entomol Exp Appl. 139:17–24.
   Web of Science ®Google Scholar
• Wong BBM, Candolin U. 2005. How is female mate choice affected by male competition? Biol Rev. 80:559–571.
   PubMed Web of Science ®Google Scholar
• Yuval B, Kaspi R, Field SA, Blay S, Taylor P. 2002. Effects of post-teneral nutrition on reproductive success of male Mediterranean fruit flies (Diptera: Tephritidae). Fla Entomol. 85:165–170.
   Google Scholar