Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-27T07:16:51.746Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of operational sex ratio, mating age, and male mating history on mating and reproductive behavior in Grapholita molesta

Published online by Cambridge University Press:  17 May 2021

Weina Kong Open the ORCID record for Weina Kong [Opens in a new window] ,
Yi Wang ,
Yongfu Guo ,
Xiaohan Chai ,
Jie Li  and
Ruiyan Ma
Weina Kong
Affiliation:
College of Plant Protection, Shanxi Agricultural University, Taigu, Shanxi, China Shanxi Key Laboratory of Integrated Pest Management in Agriculture, Taiyuan, Shanxi, China
Yi Wang
Affiliation:
College of Plant Protection, Shanxi Agricultural University, Taigu, Shanxi, China College of Horticulture, Shanxi Agricultural University, Taigu, Shanxi, China
Yongfu Guo
Affiliation:
College of Plant Protection, Shanxi Agricultural University, Taigu, Shanxi, China
Xiaohan Chai
Affiliation:
College of Plant Protection, Shanxi Agricultural University, Taigu, Shanxi, China
Jie Li
Affiliation:
College of Horticulture, Shanxi Agricultural University, Taigu, Shanxi, China
Ruiyan Ma*
Affiliation:
College of Plant Protection, Shanxi Agricultural University, Taigu, Shanxi, China
*
Author for correspondence: Ruiyan Ma, Email: maruiyan2019@163.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The short-lived polygamous moth Grapholita molesta (Busck) is an important fruit pest worldwide. Trapping males by synthetic female sex pheromones is not an effective reproductive control strategy. It is important to improve this technology by understanding the mating system of G. molesta. This study investigated mating opportunities and fertile egg production by altering the operational sex ratio, mating age, and male mating history in repeated single mating and multiple mating in the two sexes. Our results showed that the mating and reproductive parameters of virgin males were affected by the number and age of virgin females. Males preferred a female number ≤three-fifths of the male number or ≤2-day-old females, while they discriminated against a female number ≥three times of the male number or ≥5-day-old females. On the other hand, the mating and reproductive parameters of virgin females were affected by repeated single mating and especially multiple mating under different male mating histories. Females preferred once-mated males and discriminated against virgin males. These results indicated that mating systems including more and older virgin females for virgin males and different virgin males for virgin females may be suitable for suppressing G. molesta populations. Hence, these results revealed that preventing mating of virgin adults by synthetic female sex pheromones should be most effective in controlling G. molesta.

Keywords

male mating historiesmating agemating propensitymating systemoperational sex ratiooriental fruit moth
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 5 , October 2021 , pp. 616 - 627
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adler, MI and Bonduriansky, R (2011) The dissimilar costs of love and war: age-specific mortality as a function of the operational sex ratio. Journal of Evolutionary Biology 24, 1169–1177.CrossRefGoogle ScholarPubMed
Allou, K, Morin, JP, Kouassi, P, Hala N'klo, FH and Rochat, D (2008) Sex ratio and female sexual status of the coconut pest, Oryctes monoceros (Coleoptera: Dynastidae), differ in feeding galleries and pheromone-baited traps. Bulletin of Entomological Research 98, 581–586.CrossRefGoogle Scholar
Andrade, MC and Kasumovic, MM (2005) Terminal investment strategies and male mate choice: extreme tests of Bateman. Integrative and Comparative Biology 45, 838–847.CrossRefGoogle ScholarPubMed
Avila, GA, Withers, TM and Holwell, GI (2017) Courtship and mating behaviour in the parasitoid wasp Cotesia urabae (Hymenoptera: Braconidae): mate location and the influence of competition and body size on male mating success. Bulletin of Entomological Research 107, 439–447.CrossRefGoogle ScholarPubMed
Baker, TC, Nishida, R and Roelofs, WL (1981) Close-range attraction of female oriental fruit moths to herbal scent of male hairpencils. Science (New York, N.Y.) 214, 1359–1361.CrossRefGoogle ScholarPubMed
Blyth, JE and Gilburn, AS (2006) Extreme promiscuity in a mating system dominated by sexual conflict. Journal of Insect Behavior 19, 447–455.CrossRefGoogle Scholar
Bolboacă, SD and Jäntschi, L (2006) Pearson versus Spearman, Kendall's tau correlation analysis on structure-activity relationships of biologic active compounds. Leonardo Journal of Sciences 9, 179–200.Google Scholar
Brown, GR, Laland, KN and Mulder, MB (2009) Bateman's principles and human sex roles. Trends in Ecology & Evolution 24, 297–304.CrossRefGoogle ScholarPubMed
Candolin, U (1998) Reproduction under predation risk and the trade-off between current and future reproduction in the three spine stickleback. Proceedings of the Royal Society of London B 265, 1171–1175.CrossRefGoogle Scholar
Cardé, RT and Minks, AK (1995) Control of moth pests by mating disruption: successes and constraints. Annual Review of Entomology 40, 559–585.CrossRefGoogle Scholar
Chinajariyawong, A, Drew, RAI, Meats, A, Balagawi, S and Vijaysegaran, S (2010) Multiple mating by females of two Bactrocera species (Diptera: Tephritidae: Dacinae). Bulletin of Entomological Research 100, 325–330.CrossRefGoogle Scholar
Clutton-Brock, HT (1983) Selection in relation to sex. In Bendall, DS (ed.), Evolution From Molecules to man. Cambridge: Cambridge University Press, pp. 457–482.Google Scholar
Cook, PA (1999) Sperm numbers and female fertility in the moth Plodia interpunctella (hübner) (Lepidoptera; Pyralidae). Journal of Insect Behavior 12, 767–779.CrossRefGoogle Scholar
de Jong, K, Forsgren, E, Sandvik, H and Amundsen, T (2012) Measuring mating competition correctly: available evidence supports operational sex ratio theory. Behavioral Ecology 23, 1170–1177.CrossRefGoogle Scholar
de Morais, M, Sant'Ana, J, Redaelli, LR and Lorscheiter, R (2011) Effects of aging and polygamy on the reproductive performance of Grapholita molesta (Lepidoptera: Tortricidae). Revista Colombiana de Entomologia 37, 67–70.Google Scholar
de Morais, RM, Redaelli, LR and Sant'Ana, J (2012) Age and multiple mating effects on reproductive success of Grapholita molesta (Busck) (Lepidoptera, Tortricidae). Revista Brasileira de Entomologia 56, 319–324.CrossRefGoogle Scholar
Du, J, Wang, YR and Wu, JX (2010) Effect of four different artificial diets on development and reproduction of Grapholita molesta (Lepidoptera: Tortricidae). Journal of Shanxi Agricultural University 30, 229–231.Google Scholar
El-Shafie, HAF and Faleiro, JR (2017) Semiochemicals and their potential use in pest management. In Shields, V (ed.), Biological Control of Pest and Vector Insects. London: IntechOpen, pp. 3–22.Google Scholar
Emlen, ST and Oring, LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science (New York, N.Y.) 197, 215–223.CrossRefGoogle ScholarPubMed
Fiumera, AC, DeWoody, YD, DeWoody, JA, Asmussen, MA and Avise, JC (2001) Accuracy and precision of methods to estimate the number of parents contributing to a half-sib progeny array. Journal of Heredity 92, 120–126.CrossRefGoogle ScholarPubMed
Fraser, HW and Trimble, RM (2001) Effect of delayed mating on reproductive biology of the oriental fruit moth (Lepidoptera: Tortricidae). Canadian Entomologist 133, 219–227.CrossRefGoogle Scholar
Fritzsche, K, Booksmythe, I and Arnqvist, G (2016) Sex ratio bias leads to the evolution of sex role reversal in honey locust beetles. Current Biology 26, 2522–2526.CrossRefGoogle ScholarPubMed
Gress, BE, Waltzer, RJ, Lüpold, S, Droge-Young, EM, Manier, MK and Pitnick, S (2014) Alternative mating tactics in the yellow dung fly: resolving mechanisms of small-male advantage off pasture. Proceedings of the Royal Society B 281, e20132164.CrossRefGoogle ScholarPubMed
Huang, F and Subramanyam, BH (2003) Effects of delayed mating on reproductive performance of Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae). Journal of Stored Products Research 39, 53–63.CrossRefGoogle Scholar
Jiménez-Pérez, A and Wang, Q (2003) Effect of mating delay on the reproductive performance of Cnephasia jactatana (Lepidoptera: Tortricidae). Journal of Economic Entomology 96, 592–598.CrossRefGoogle Scholar
Jones, TM and Elgar, MA (2004) The role of male age, sperm age and mating history on fecundity and fertilization success in the hide beetle. Proceedings of the Royal Society B 271, 1311–1318.CrossRefGoogle ScholarPubMed
Kawazu, K, Shintani, Y and Tatsuki, S (2014) Effect of increased male and female age at mating on the reproductive performance of Cnaphalocrocis medinalis (Crambidae: Lepidoptera). Journal of Economic Entomology 107, 1434–1439.CrossRefGoogle Scholar
Knight, AL (2007) Multiple mating of male and female codling moth (Lepidoptera: Tortricidae) in apple orchards treated with sex pheromone. Environmental Entomology 36, 157–164.CrossRefGoogle ScholarPubMed
Knight, AL (2009) Multiple mating of male and female codling moth (Lepidoptera: Tortricidae) in apple orchards treated with sex pheromone. Environmental Entomology 36, 157–164.CrossRefGoogle Scholar
Kong, WN, Hu, RS, Zhao, ZG, Li, J, Zhang, ZW, Li, SC and Ma, RY (2014a) Effects of trap height, location and spacing on pheromone-baited trap catch efficacy for oriental fruit moths in a peach orchard. Canadian Entomologist 146, 684–692.CrossRefGoogle Scholar
Kong, WN, Li, J, Fan, RJ, Li, SC and Ma, RY (2014b) Sex-pheromone-mediated mating disruption technology for the oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae): overview and prospects. Psyche: A Journal of Entomology 2014, 1–8.CrossRefGoogle Scholar
Kong, WN, Wang, Y, Liu, ZF, Guo, YF, Zhao, F and Fan, RJ (2018) The effect of different hosts on the oviposition preferences of Grapholita molesta (Busck) (Lepidoptera: Tortricidae). Chinese Journal of Applied Entomology 55, 104–111.Google Scholar
Kong, WN, Wang, Y, Jia, XT, Gao, Y, Fan, RJ, Li, J and Ma, RY (2019) Emergence and mating behavior of the oriental fruit moth Cydia molesta (Lepidoptera: Tortricidae) and its potential for reproduction. Annales de la Société entomologique de France (N.S.) 55, 446–453.CrossRefGoogle Scholar
Kong, WN, Wang, Y, Guo, YF, Chai, XH, Li, J and Ma, RY (2020a) Behavioral effects of different attractants on adult male and female oriental fruit moths, Grapholita molesta. Pest Management Science 76, 3225–3235.CrossRefGoogle Scholar
Kong, WN, Wang, Y, Guo, YF, Chai, XH, Li, J and Ma, RY (2020b) Importance of preovipositional period of an oligophagous moth in predicting host suitability. Journal of Economic Entomology 113, 222–229.Google Scholar
Kong, WN, Wang, Y, Guo, YF, Chai, XH, Niu, GF, Li, Y, Li, J and Ma, RY (2020c) Effects of disruption of Grapholita molesta (Lepidoptera: Tortricidae) using sex pheromone on moth pests and insect communities in orchards. Applied Entomology and Zoology 55, 367–377.CrossRefGoogle Scholar
Koppik, M, Ruhmanna, H and Fricke, C (2018) The effect of mating history on male reproductive ageing in Drosophila melanogaster. Journal of Insect Physiology 111, 16–24.CrossRefGoogle ScholarPubMed
Kvarnemo, C and Ahnesjo, I (1996) The dynamics of operational sex ratios and competition for mates. Trends in Ecology & Evolution 11, 404–408.CrossRefGoogle ScholarPubMed
Lai, M, Zhang, S, Zhang, Y and Liu, X (2020) Male age affects female mating preference but not fitness in the monandrous moth Dendrolimus punctatus Walker (Lepidoptera: Lasiocampidae). Physiological Entomology 45, 22–29.CrossRefGoogle Scholar
Li, GY and Zhang, ZQ (2020) Sex-specific response to delayed and repeated mating in spider mite Tetranychus urticae. Bulletin of Entomological Research 111, 49–56.CrossRefGoogle ScholarPubMed
Li, XW, Jia, XT, Xiang, HM, Diao, HL, Yan, Y, Wang, Y and Ma, RY (2019) The effect of photoperiods and light intensity on mating behavior and reproduction of Grapholita molesta (Lepidoptera: Tortricidae). Environmental Entomology 48, 1035–1041.CrossRefGoogle Scholar
Marcotte, M, Delisle, J and McNeil, JN (2005) Impact of male mating history on the temporal sperm dynamics of Choristoneura rosaceana and C. fumiferana females. Journal of Insect Physiology 51, 537–544.CrossRefGoogle ScholarPubMed
Marieorleach, L, Janicke, T and Scharer, L (2013) Effects of mating status on copulatory and postcopulatory behaviour in a simultaneous hermaphrodite. Animal Behaviour 85, 453–461.CrossRefGoogle Scholar
Matthews, RW and Matthews, JR (2010) Insect Behavior. London: Springer.CrossRefGoogle Scholar
Mori, BA and Evenden, ML (2013) When mating disruption does not disrupt mating: fitness consequences of delayed mating in moths. Entomologia Experimentalis et Applicata 146, 50–65.CrossRefGoogle Scholar
Moura, RR and Peixoto, PEC (2013) The effect of operational sex ratio on the opportunity for sexual selection: a meta-analysis. Animal Behaviour 86, 675–683.CrossRefGoogle Scholar
Nilsson, JÅ and Svensson, E (1996) The cost of reproduction: a new link between current reproduction effort and future reproductive success. Proceedings of the Royal Society of London B 263, 711–714.Google Scholar
Ono, T, Hayakawa, F, Matsuura, Y, Shiraishi, M, Yasui, H, Nakamura, T and Arakawa, M (1995) Reproductive biology and function of multiple mating in the mating system of a tree cricket, Truljalia hibinonis (Orthoptera: Podoscritinae). Journal of Insect Behavior 8, 813–824.CrossRefGoogle Scholar
Opp, SB and Prokopy, RJ (2000) Multiple mating and reproductive success of male and female apple maggot flies, Rhagoletis pomonella (Diptera: Tephritidae). Journal of Insect Behavior 13, 901–914.CrossRefGoogle Scholar
Parker, GA (2006) Sexual conflict over mating and fertilization: an overview. Philosophical Transactions of the Royal Society B 361, 235–259.CrossRefGoogle ScholarPubMed
Parker, PG and Tang-Martinez, Z (2005) Bateman gradients in field and laboratory studies: a cautionary tale. Integrative and Comparative Biology 45, 895–902.CrossRefGoogle ScholarPubMed
Pinto, AP, Sant'Ana, J and Botton, M (2005) Influência da idade da fêmea na performance reprodutiva e longevidade de Argyrotaenia sphaleropa (Lepidoptera: Tortricidae). Iheringia 95, 435–440.CrossRefGoogle Scholar
Rothschild, G and Vickers, R (1991) Biology, ecology and control of the oriental fruit moth. In van der Geest, LPS and Evenhuis, HH (eds.), Tortricid Pests: Their Biology, Natural Enemies and Control. Amsterdam: Elsevier, pp. 389–412.Google Scholar
Sadek, MM (2001) Polyandry in field-collected Spodoptera littoralis moths and laboratory assessment of the effects of male mating history. Entomologia Experimentalis et Applicata 98, 165–172.CrossRefGoogle Scholar
Safonkin, AF (2011) The monogamous reproductive strategy in lepidoptera. Biological Bulletin 38, 361–368.CrossRefGoogle Scholar
Siva-Jothy, MT (2000) The young sperm gambit. Ecology Letters 3, 172–174.CrossRefGoogle Scholar
Snedecor, GW and Cochran, WG (1967) Statistical Methods. Ames: Iowa State University Press Iowa.Google Scholar
Soffan, A, Yousif, NA and Aldawood, SA (2012) Effects of sex ratio and pairing duration on the biological performance of adult almond moth, Ephestia cautella (Walker) (Lepidoptera: Pyralidae). Journal of Agricultural and Urban Entomology 28, 25–33.CrossRefGoogle Scholar
Stelinski, LL and Gut, LJ (2009) Delayed mating in tortricid leafroller species: simultaneously aging both sexes prior to mating is more detrimental to female reproductive potential than aging either sex alone. Bulletin of Entomological Research 99, 245–251.CrossRefGoogle ScholarPubMed
Thornhill, R and Alcock, J (1983) The Evolution of Insect Mating Systems. Cambridge: Harvard University Press.CrossRefGoogle Scholar
Thornhill, R and Gwynne, DT (1986) The evolution of sexual differences in insects. American Scientist 74, 382–389.Google Scholar
Torresvila, LM and Jennions, MD (2005) Male mating history and female fecundity in the lepidoptera: do male virgins make better partners? Behavioral Ecology and Sociobiology 57, 318–326.CrossRefGoogle Scholar
Trivers, RL (1972) Parental investment and sexual selection. In Campbell, B (ed.), Sexual Selection and the Descent of man. Chicago: University of California Los Angeles Aldine Publishing Company, pp. 136–179.Google Scholar
Túler, A, Silva-Torres, C, Torres, J, Moraes, R and Rodrigues, A (2018) Mating system, age, and reproductive performance in Tenuisvalvae notata, a long-lived ladybird beetle. Bulletin of Entomological Research 108, 616–624.CrossRefGoogle ScholarPubMed
Unnithan, GC and Paye, SO (1991) Mating, longevity, fecundity, and egg fertility of Chilo partellus (Lepidoptera: Pyralidae): effects of delayed or successive matings and their relevance to pheromonal control methods. Environmental Entomology 20, 150–155.CrossRefGoogle Scholar
Vargas, C, Shannon, PJ, Taveras, R, Soto, F and Hilje, L (2001) Un nuevo mé todo para la cri ́a masiva de Hypsipyla grandella. Manejo Integrado de Plagas 39, 1–4.Google Scholar
Wang, Q, He, XZ, Yang, L, Duncan, H and Lorraine, KD (2009) Biased sex ratio and low population density increase male mating success in the bug Nysius huttoni (Heteroptera: Lygaeidae). Naturwissenschaften 96, 87–91.CrossRefGoogle Scholar
Wang, XP, Fang, YL and Zhang, ZN (2011) Effects of delayed mating on the fecundity, fertility and longevity of females of diamondback moth, Plutella xylostella. Insect Science 18, 305–310.CrossRefGoogle Scholar
Wang, Y, Kong, WN, Zhao, LL, Xiang, HM, Zhang, LJ, Li, J, Ridsdill-Smith, J and Ma, RY (2018) Methods to measure performance of Grapholita molesta on apples of five varieties. Entomologia Experimentalis et Applicata 166, 162–170.CrossRefGoogle Scholar
Waqas, M, Shoaib, A, Elabasy, A, Cheng, XL, Zhang, QQ and Shi, ZH (2020) Effects of delayed mating on male mating success and female reproductive performance of Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae). Crop Protection 132, 105–135.CrossRefGoogle Scholar
Wedell, N, Gage, MJG and Parker, GA (2002) Sperm competition, male prudence and sperm-limited females. Trends in Ecology & Evolution 17, 313–320.CrossRefGoogle Scholar
Weir, LK, Grant, JWA and Hutchings, JA (2011) The influence of operational sex ratio on the intensity of competition for mates. American Naturalist 177, 167–176.CrossRefGoogle ScholarPubMed
Yang, YQ, Zhang, LZ, Zhang, YZ, Zhang, LW and Long, YH (2017) Delayed mating impacts on the reproductive performance of Ectropis obliqua (Lepidoptera: Geometridae). Journal of Entomological Science 52, 52–59.CrossRefGoogle Scholar
Zhan, YD, Liu, JH and Liu, Y (2020) The mating strategy and reproductive performance of Agriphila aeneociliella (Lepidoptera: Crambidae), a new insect pest of wheat in China. Agricultural and Forest Entomology 22, 203–211.CrossRefGoogle Scholar
Zhang, SY, Zeng, JP, Wu, XF, Peng, LH and Liu, XP (2015) The effect of multiple mating on female reproductive fitness in moths: a meta-analysis. Journal of Environmental Entomology 37, 1272–1279.Google Scholar
Zhang, SY, Li, D, Zeng, JP, Wu, XF and Liu, XP (2016) Effect of male mating history on female reproductive fitness in moths: a meta-analysis. Chinese Journal of Ecology 35, 551–558.Google Scholar
Zhang, ZW, Men, LN, Peng, YF, Li, J, Deng, A, Chen, Y, Liu, XQ and Ma, RY (2017) Morphological differences of the reproductive system could be used to predict the optimum Grapholita molesta (Busck) control period. Scientific Reports 7, e8198.CrossRefGoogle ScholarPubMed