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More eggs are not more sires: long-term monogamy reduces fertility in a predatory ladybird

Published online by Cambridge University Press:  08 January 2025

Gabriela Streppel Steindorff*
Affiliation:
Laboratório de Entomologia Aplicada, Departamento de Zoologia, Centro de Biociências, Universidade Federal de Pernambuco, Recife, PE, Brasil Programa de Pós-Graduação em Biologia Animal, Centro de Biociências, Universidade Federal de Pernambuco, Recife, PE, Brasil
Wendel José Teles Pontes
Affiliation:
Laboratório de Entomologia Aplicada, Departamento de Zoologia, Centro de Biociências, Universidade Federal de Pernambuco, Recife, PE, Brasil
*
Corresponding author: Gabriela Streppel Steindorff; Email: gabriela.steindorff@ufpe.br

Abstract

Multiple mating is a behaviour observed across various polyandrous insect species. It is suggested that, in ladybirds, this strategy of multiple copulations is used to enhance fecundity and fertility through sperm replenishment. Studies on sperm depletion need to correlate fertility with the presence of spermatozoa in the spermatheca. This study investigates the role of sperm replenishment in the ladybird Cryptolaemus montrouzieri. We hypothesised that females of this species exhibit fecundity and fertility rates proportional to the number of sperm replenishment opportunities (constant, periodic or absent). We observed oviposition behaviour and hatching rates over 30 days, and simultaneously tested for sperm depletion in females that copulated once. We dissected the spermathecae at four post-copulation moments to count spermatozoa under a microscope. Our results indicate that a single copulation suffices to maintain fertility for at least 30 days. Females with constant replenishment opportunities exhibited higher fecundity but lower fertility and increased mortality, suggesting a reproductive cost associated with frequent mating. Females with no replenishment during the experiment, exhibited the highest hatchability rate and lowest oviposition. Periodic copulation resulted in optimal female mating rate, with average fertility and fecundity. A plausible hypothesis would be that paired females choose to fertilise fewer eggs from a single male but are unable to control the effects of the oviposition stimulus induced by the male's presence. These findings have implications for the management and rearing of C. montrouzieri in biological control programmes, optimizing mating strategies for mass production.

Type
Research Paper
Copyright
Copyright © The Author(s), 2025. Published by Cambridge University Press

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References

Arnqvist, G and Nilsson, T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour 60, 145164.CrossRefGoogle ScholarPubMed
Awad, M, Kalushkov, P, Nedvedovaá, T and Nedved, O (2013) Fecundity and fertility of ladybird beetle Harmonia axyridis after a prolonged cold storage. BioControl 58, 657666.CrossRefGoogle Scholar
Awad, M, Piálek, L, Krejčí, A, Laugier, G and Nedved, O (2017) Paternity following multiple mating in ladybird Harmonia axyridis. BioControl 62, 297307.CrossRefGoogle Scholar
Bayoumy, MH and Michaud, JP (2014) Female fertility in Hippodamia convergens (Coleoptera: Coccinellidae) is maximized by polyandry, but reduced by continued male presence. European Journal of Entomology 111, 513520.CrossRefGoogle Scholar
Bloch Qazi, MC, Herbeck, JT and Lewis, SM (1996) Mechanisms of sperm transfer and storage in the red flour beetle (Coleoptera: Tenebrionidae). Annals of the Entomological Society of America 89, 892897.CrossRefGoogle Scholar
De Lima, CHM, Nóbrega, RL, Ferraz, ML and Pontes, WJT (2022) Mating duration and spermatophore transfer in Cryptolaemus montrouzieri (Coccinellidae). Biologia 77, 149155.CrossRefGoogle Scholar
Fedina, TY (2007) Cryptic female choice during spermatophore transfer in Tribolium castaneum (Coleoptera: Tenebrionidae). Journal of Insect Physiology 53, 9398.CrossRefGoogle ScholarPubMed
Felix, KES, De Lima, CHM, De Lima, MS and Pontes, WJT (2022) No sex, no job: sexual abstinence reduces feeding rates of Cryptolaemus montrouzieri. Bulletin of Insectology 75, 293298.Google Scholar
Gillott, C (1988) Arthropoda – Insecta. In Adiyodi, KG and Adiyodi, RG (eds), Reproductive Biology of Invertebrates. III. Accessory Sex Glands. Chichester: Wiley and Sons, pp. 319471.Google Scholar
Gunawardana, DUM and Hemachandra, KS (2020) Mass rearing of mealybug predator, Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) on two mealybug species, Planococcus minor and Pseudococcus viburni. Tropical Agricultural Research 31, 3141.CrossRefGoogle Scholar
Haddrill, PR, Shuker, DM, Amos, W, Majerus, MEN and Mayes, S (2008) Female multiple mating in wild and laboratory populations of the two-spot ladybird, Adalia bipunctata. Molecular Ecology 17, 31893197.CrossRefGoogle ScholarPubMed
Hodek, I, van Emden, HF and Honek, A (2012) Ecology and Behavior of the Ladybird Beetles (Coccinellidae). West Sussex: Wiley-Blackwell U.K.CrossRefGoogle Scholar
Jayanthi, PK, Sangeetha, P and Verghese, A (2013) Influence of polyandry on clutch size of the predatory coccinellid, Cryptolaemus montrouzieri (Coleoptera: Coccinellidae). Florida Entomologist 96, 10731076.CrossRefGoogle Scholar
Junior, LLF, Silva, LAN, Santos, ICL and Santos, A (2019) Desenvolvimento e multiplicação da joaninha Cryptolaemus montrouzieri no controle biológico da cochonilha rosada. In de Francisco, ALO (ed.), Sustentabilidade de Recursos Florestais. Ponta Grossa: Atena Editora, pp. 2539.CrossRefGoogle Scholar
Kairo, MTK, Paraiso, O, Gautam, RD and Peterkin, DD (2013) Cryptolaemus montrouzieri (Mulsant) (Coccinellidae: Scymninae): a review of biology, ecology, and use in biological control with particular reference to potential impact on non-target organisms. CAB Reviews 8, 120.CrossRefGoogle Scholar
Katakura, H (1986) Evidence for the incapacitation of heterospecific sperm in the female genital tract in a pair of closely related ladybirds (Insecta, Coleoptera, Coccinellidae). Zoological science 3, 115121.Google Scholar
Kaufmann, T (1996) Dynamics of sperm transfer, mixing, and fertilization in Cryptolaemus montrouzieri (Coleoptera: Coccinellidae) in Kenya. Annals of the Entomological Society of America 89, 238242.CrossRefGoogle Scholar
Lange, AB and Loughton, BG (1985) An oviposition-stimulating factor in the male accessory reproductive gland of the locust, Locusta migratoria. General and Comparative Endocrinology 57, 208215.CrossRefGoogle ScholarPubMed
Mishra, G and Omkar, O (2006) Ageing trajectory and longevity trade-off in an aphidophagous ladybird, Propylea dissecta (Coleoptera: Coccinellidae). European Journal of Entomology 103, 3340.CrossRefGoogle Scholar
Monalisa, , Pervez, A and Jahan, M (2020) Mating behavior of the predaceous ladybird, Harmonia dimidiata. European Journal of Environmental Sciences 10, 58.Google Scholar
Nielson, MW and Toles, SL (1968) Observations on the biology of Acinopterus angulatus and Aceratagallia curvata in Arizona (Homoptera: Cicadellidae). Annals of the Entomological Society of America 61, 5456.CrossRefGoogle Scholar
Omkar, O and Mishra, G (2005) Mating in aphidophagous ladybirds: costs and benefits. Journal of Applied Entomology 129, 432436.CrossRefGoogle Scholar
Omkar, O and Sahu, J (2012) Costs and benefits of reproduction in predaceous ladybird: effect of multiple matings on reproduction and offspring development. Journal of Asia-Pacific Entomology 15, 219224.CrossRefGoogle Scholar
Orsetti, DM and Rutowski, RL (2003) No material benefits, and a fertilization cost, for multiple mating by female leaf beetles. Animal Behaviour 66, 477484.CrossRefGoogle Scholar
Osawa, N (2005) The effect of prey availability on ovarian development and oosorption in the ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology 102, 503511.CrossRefGoogle Scholar
Pang, X and Gordon, RD (1986) The Scymnini (Coleoptera: Coccinellidae) of China. The Coleopterists Bulletin 40, 157199.Google Scholar
Parker, GA (1984) Sperm competition and the evolution of animal mating strategies. In Smith, RL (ed.), Sperm Competition and the Evolution of Animal Mating Systems. London: Academic Press, pp. 260.Google Scholar
Parker, GA, Simmons, LW and Kirk, H (1990) Analysing sperm competition data: simple models for predicting mechanisms. Behavioral Ecology and Sociobiology 27, 5565.CrossRefGoogle Scholar
Pervez, A and Maurice, N (2011) Mate choice and polyandry benefit reproduction and progeny fitness in the ladybird, Hippodamia variegata (Goeze). European Journal of Environmental Sciences 1, 1923.CrossRefGoogle Scholar
Pervez, A, Omkar, and Richmond, A (2004) The influence of age on the reproductive performance of a predatory ladybird, Propylea dissecta. Journal of Insect Science 4, 18.CrossRefGoogle ScholarPubMed
Pyle, DW and Gromko, MH (1981) Genetic basis for repeated mating in Drosophila melanogaster. American Naturalist 117, 133146.CrossRefGoogle Scholar
Rodriguez, V (1995) Relation of flagellum length to reproductive success in male Chelymorpha alternans Boheman (Coleoptera: Chrysomelidae: Cassidinae). The Coleopterists Bulletin 49, 201205.Google Scholar
Rodriguez, V (1999) Spermatophore transfer and ejection in the beetle Pseudoxychila tarsalis (Coleoptera: Cicindelidae). Journal of Kansas Entomological Society 72, 19.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, 165172.CrossRefGoogle Scholar
Sakurai, T (1998) Variation in time to sperm depletion and oviposition patterns in females of Riptortus clavatus (Heteroptera: Alydidae). Annals of the Entomological Society of America 91, 737740.CrossRefGoogle Scholar
Sanches, NF and Carvalho, RS (2010) Procedimentos para manejo da criação e multiplicação do predador exótico Cryptolaemus montrouzieri. Cruz das Almas: Brasil, Embrapa Mandioca e Fruticultura (Circular Técnica, 99).Google Scholar
Santos, MLF, Rodrigues-Pedrosa, J and Pontes, WJT (2023) The pre-oviposition period is associated with ovary maturation in Cryptolaemus montrouzieri Mulsant, 1850 (Coleoptera: Coccinellidae). Invertebrate Reproduction and Development 67, 129134.CrossRefGoogle Scholar
Shahid, M, Siddiqui, A, Omkar, O and Mishra, G (2016) Mating alters the rate of development of ovarioles in the ladybird, Propylea dissecta (Coleoptera: Coccinellidae). European Journal of Entomology 113, 4450.CrossRefGoogle Scholar
Simmons, LW (2001) Sperm Competition and its Evolutionary Consequences in the Insects. Princeton: Princeton University Press.Google Scholar
Simmons, LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annual Review of Ecology, Evolution, and Systematics 36, 125146.CrossRefGoogle Scholar
Sivinski, J (1980) Sexual selection and insect sperm. Florida Entomologist 63, 99111.CrossRefGoogle Scholar
Smith, RL (1979) Repeated copulation and sperm precedence: paternity assurance for a male brooding water bug. Science 205, 10291031.CrossRefGoogle ScholarPubMed
Susset, EC, Hemptinne, JL, Danchin, E and Magro, A (2018) Overwintering aggregations are part of Hippodamia undecimnotata's (Coleoptera: Coccinellidae) mating system. PLoS ONE 13, e0197108.CrossRefGoogle ScholarPubMed
Thornhill, R and Alcock, J (1983) The Evolution of Insect Mating Systems. Massachusetts: Harvard University Press.CrossRefGoogle Scholar
Tregenza, T and Wedell, N (1998) Benefits of multiple mates in the cricket Gryllus bimaculatus. Evolution 52, 17261730.CrossRefGoogle Scholar
Tyler, F and Tregenza, T (2012) Why do so many flour beetle copulations fail? Entomologia Experimentalis et Applicata 146, 199206.CrossRefGoogle Scholar
Wedell, N (2006) Male genotype affects female fitness in a paternally investing species. Evolution 60, 16381645.Google Scholar
Wedell, N, Gage, MJG and Parker, GA (2002) Sperm competition, male prudence and sperm-limited females. TRENDS in Ecology & Evolution 17, 313320.CrossRefGoogle Scholar
Worthington, AM and Kelly, CD (2016) Direct costs and benefits of multiple mating: are high female mating rates due to ejaculate replenishment? Behavioural Processes 124, 115122.CrossRefGoogle ScholarPubMed
Xie, J, Zhang, Y, Wu, H, Liu, P, Deng, C and Pang, H (2014) Effects of mating patterns on reproductive performance and offspring fitness in Cryptolaemus montrouzieri. Entomologia Experimentalis Et Applicata 153, 2023.Google Scholar
Xu, J and Wang, Q (2011) Seminal fluid reduces female longevity and stimulates egg production and sperm trigger oviposition in a moth. Journal of Insect Physiology 57, 385390.CrossRefGoogle Scholar
Yadav, M and Pervez, A (2022) Reproductive behaviour of predaceous ladybirds (Coleoptera: Coccinellidae): a review. International Journal of Tropical Insect Science 42, 30833095.CrossRefGoogle Scholar
Yadav, P, Mishra, G and Omka, O (2023) Socio-sexual environment manipulates sperm allocation strategies in ladybird beetle, Cheilomenes sexmaculata (Fabricius). Research Square [Preprint] (Version 1).CrossRefGoogle Scholar