Female Perception of Mating Status of Male is Important for Paternity Success of a Male: A Case Study in a Ladybird Beetle, Cheilomenes sexmaculata (Fabricius).
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Abstract
Multiple matings enable females to store sperm from multiple mates and select good-quality sperms for paternity. Hence, the quality of males and the pattern of sperm precedence shape mate choice and modulate female investment in mate assessment. Male ejaculate supply varies with age, mating status, and severity of sperm competition affecting the perception of females for good quality mates. In insects, cuticular hydrocarbons play an important role in identifying and assessing mates. Ladybirds exhibit last male sperm precedence but will the last male be able to win the competition if it is mated? Also, can females distinguish males when the males' elytra are washed or perfumed with CHCs from males of different mating statuses? This was tested in the ladybird beetle, Cheilomenes sexmaculata by subjecting females to double matings where the mating status of the last male was varied from unmated to once mated to twice mated. The experiment was performed at three levels (i) untreated, (ii) elytra of last males wiped using n-hexane, and (iii) males were perfumed with the CHCs of males of different mating status. Mated males were not able to outcompete the sperm of unmated males. Also, the effect of CHCs was evident in courtship behaviour and paternity share. Females showed preference for unmated males over mated males and this was prevalent in washed treatment also. Perfuming of males resulted in the exchange of CHCs, and the response of females to such “perfumed” males demonstrated that females’ perception of male status is CHC-driven.
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References
Agarwala BK, Yasuda H (2000) Competitive ability of ladybird predators of aphids: A review of Cheilomenes sexmaculata (Fabr.)(Coleoptera: Coccinellidae) with a worldwide checklist of pr eys. Journal of Aphidology 14:1-20.
Alavi Y, Elgar M, Jones TM (2016) Male Mating Success and the Effect of Mating History on Ejaculate Traits in a Facultatively Parthenogenic Insect (Extatosoma tiaratum). Ethol 122(7):523-530. https://doi.org/10.1111/eth.12497
Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60(2):145-164. https://doi.org/10.1006/anbe.2000.1446
Moore PJ (2014) Reproductive physiology and behaviour. In: Shuker DM, Simmons LW (eds) The Evolution of Insect Mating Systems, 1st edn. Oxford University Press, UK, pp. 78-91
Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56:21-40. https://doi.org/10.1146/annurev-ento-120709-144823
Bath E, Buzzoni D, Ralph T, Wigby S, Sepil I (2021) Male condition influences female post mating aggression and feeding in Drosophila. Func Ecol 35:1288–1298. https://doi.org/10.1111/1365-2435.13791
Beck CW, Promislow DE (2007) Evolution of female preference for younger males. PLoS One 2:939. https://doi.org/10.1371/journal.pone.0000939
Bind RB (2007). Reproductive behaviour of a generalist aphidophagous ladybird beetle Cheilomenes sexmaculata (Coleoptera: Coccinellidae). Int J Trop Insect Sci 27(2):78-84. https://doi.org/10.1017/S1742758407814688
Bonduriansky R, Brassil CE (2002). Rapid and costly ageing in wild male flies. Nature 420(6914):377-377. https://doi.org/10.1038/420377a
Bontonou G, Wicker-Thomas C (2014) Sexual communication in the Drosophila genus. Insects 5(2):439-458. https://doi.org/10.3390/insects5020439
Bro-Jørgensen J (2010) Dynamics of multiple signalling systems: animal communication in a world in flux. Trends ecol evol 25(5):292-300. https://doi.org/10.1016/j.tree.2009.11.003
Chaudhary DD, Mishra G, Omkar (2016) Last male wins the egg fertilization fight: A case study in ladybird, Menochilus sexmaculatus. Behav Processes 131:1-8. https://doi.org/10.1016/j.beproc.2016.07.015
Chen R, Xu T, Hao D, Teale SA (2019) Cuticular hydrocarbon recognition in the mating behavior of two pissodes species. Insects 10(7):217. https://doi.org/10.3390/insects10070217
Cook PA, Wedell N. (1996) Ejaculate dynamics in butterflies: a strategy for maximizing fertilization success? Proc. Royal Soc. B P ROY SOC B-BIOL SCI 263(1373):1047-1051. https://doi.org/10.1098/rspb.1996.0154
Cordero-Rivera A (2022) Sperm competition. In: Omkar and Mishra G (eds) Reproductive Strategies in Insects, 1st edn. Wiley, London, pp 205-24.
Cuvillier-Hot V, Cobb M, Malosse C, Peeters C (2001) Sex, age and ovarian activity affect cuticular hydrocarbons in Diacamma ceylonense, a queenless ant. J Insect Physiol 47(4-5):485-493. https://doi.org/10.1016/S0022-1910(00)00137-2
Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119(5):601-610.
Dowling DK, Simmons LW (2012) Ejaculate economics: testing the effects of male sexual history on the trade-off between sperm and immune function in Australian crickets. PLoS One 7(1):e30172. https://doi.org/10.1371/journal.pone.0030172
Dubey A, Omkar, Mishra G (2016a) Influence of temperature on reproductive biology and phenotype of a ladybird, Menochilus sexmaculata (Fabricius) (Coleoptera: Coccinellidae). J Therm Biol 58:35-42. https://doi.org/10.1016/j.jtherbio.2016.03.011
Dubey A, Omkar, Mishra G (2016b) Adult body size drives sexual selection mutually in the ladybirds, Menochilus sexmaculatus. Acta Entomol Sin 59(2):209-218.
Dubey A, Saxena S, Omkar, Mishra G (2018) Mating experience influences mate choice and reproductive output in an aphidophagous ladybird, Menochilus sexmaculatus. Anim Biol 68(3):247-263. https://doi.org/10.1163/15707563-17000128
Eliyahu D, Nojima S, Capracotta SS, Comins DL, Schal C (2008) Identification of cuticular lipids eliciting interspecific courtship in the German cockroach, Blattella germanica. Naturwissenschaften 95:403–412. https://doi.org/10.1007/s00114-007-0339-7
Durieux D, Verheggen F, Vandereycken A, Joie E, Haubruge É (2010) Bibliographic synthesis: the chemical ecology of ladybugs. Biotechnol Agron Soc Environ 14 (2): 351-367. https://hdl.handle.net/2268/3832
Lüpold S, Manier MK, Ala-Honkola O, Belote JM, Pitnick S (2011) Male Drosophila melanogaster adjust ejaculate size based on female mating status, fecundity, and age. Behav Ecol 22:184-191. https://doi.org/10.1093/beheco/arq193
Fassotte B, Francis F, and Verheggen FJ(2016). The scent of love: how important are semiochemicals in the sexual behavior of lady beetles? J Pest Sci 89(2):347-358. https://doi.org/10.1007/s10340-016-0735-x
Fassotte B, Fischer C, Durieux D, Lognay G, Haubruge E, Francis F, Verheggen FJ (2014) First evidence of a volatile sex pheromone in lady beetles. PLoS One 9(12):e115011. https://doi.org/10.1371/journal.pone.0115011
Legrand P, Vanderplanck M, Marko I, Gillard L, Lognay G, Lorge S, Maesen P, Vilcinskas A, Vogel H, Foucaud J, Estoup A (2019a) The taste of origin in a lady beetle: do males discriminate between females based on cuticular hydrocarbons? Physiol Entomol 44(2):160-168. https://doi.org/10.1111/phen.12286
Legrand P, Vanderplanck M, Lorge S, Maesen P, Lognay G, Vilcinskas A, Vogel H, Estoup A, Foucaud J, Francis F, Facon B (2019b) Cuticular hydrocarbon composition does not allow Harmonia axyridis males to identify the mating status of sexual partners. Entomol Gen 38(3):211-224. https://hdl.handle.net/21.11116/0000-0003-4239-3
Jones TM, Elgar MA (2004) The role of male age, sperm age and mating history on fecundity and fertilization success in the hide beetle. Proc. Royal Soc. B P ROY SOC B-BIOL SCI 271(1545):1311–1318. doi:10.1098/rspb.2004.2723
Francke W, Dettner K (2005) In: Schulz, S. (eds) The Chemistry of Pheromones and Other Semiochemicals II. Topics in Current Chemistry, vol 240. Springer, Berlin, Heidelberg. https://doi.org/10.1007/b98316
Friberg U (2006) Male perception of female mating status: its effect on copulation
duration, sperm defence and female fitness. Anim Behav 72(6):1259 –1268. https://doi.org/10.1016/j.anbehav.2006.03.021
Ginzel MD, Blomquist GJ (2016) Insect Hydrocarbons: Biochemistry and Chemical Ecology. In: Cohen E, Moussian B (eds) Extracellular Composite Matrices in Arthropods. Springer, Cham. pp. 221-252 https://doi.org/10.1007/978-3-319-40740-1_7
Guarino S, De Pasquale C, Peri E, Alonzo G, Colazza, S (2008) Role of volatile and contact pheromones in the mating behaviour of Bagrada hilaris (Heteroptera: Pentatomidae). Eur J Entomol 105(4):613. https://doi.org/10.14411/eje.2008.082
Haddrill PR, Shuker DM, Amos W, Majerus ME, Mayes S (2008) Female multiple mating in wild and laboratory populations of the two‐spot ladybird, Adalia bipunctata. Mol Ecol 17(13):3189-3197. https://doi.org/10.1111/j.1365-294X.2008.03812.x
Harris WE, Moore PJ (2005) Female mate preference and sexual conflict: females prefer males that have had fewer consorts. Am Nat, 165(S5):S64-S71. https://doi.org/10.1086/429352
Hemptinne JL, Dixon AF (2000) Defence, oviposition and sex: semiochemical parsimony in two species of ladybird beetles (Coleoptera: Coccinellidae)? A short review. Eur J Entomol 97(4):443-448. https://doi.org/10.14411/eje.2000.068
Hemptinne JL, Lognay G, Dixon AF (1998) Mate recognition in the two-spot ladybird beetle, Adalia bipunctata: role of chemical and behavioural cues. J Insect Physiol 44(12):1163-1171. https://doi.org/10.1016/S0022-1910(98)00081-X
Hopkins BR, Sepil I, Wigby S (2017) Seminal fluid. Curr Biol 27(11):R404-R405. doi: 10.1016/j.cub.2017.03.063.
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371-393. https://doi.org/10.1146/annurev.ento.50.071803.130359
Hughes L, Siew-Woon Chang B, Wagner D, Pierce NE (2000) Effects of mating history on ejaculate size, fecundity, longevity, and copulation duration in the ant-tended lycaenid butterfly, Jalmenus evagoras. Behav Ecol Sociobiol 47(3):119-128. https://doi.org/10.1007/s002650050002
Ingleby FC, Hosken DJ, Flowers K, Hawkes MF, Lane SM, Rapkin J, House CM, Sharma MD, Hunt J (2014) Environmental heterogeneity, multivariate sexual selection and genetic constraints on cuticular hydrocarbons in Drosophila simulans. J Evol Biol 27(4):700-713. https://doi.org/10.1111/jeb.12338
Ingleby FC (2015) Insect cuticular hydrocarbons as dynamic traits in sexual communication. Insects 6(3):732-742. https://doi.org/10.3390/insects6030732
Isa M, Kumano N, Tatsuta H (2019) When a male perceives a female: the effect of waxy components on the body surface on decision-making in the invasive pest weevil. R Soc Open Sci 6(2):181542. https://doi.org/10.1098/rsos.181542
Iwata Y, Sato N, Hirohashi N, Watanabe Y, Sauer WH, Shaw PW (2021). Sperm competition risk affects ejaculate strategy in terms of sperm number but not sperm size in squid. J Evol Biol 34(9):1352-1361. https://doi.org/10.1111/jeb.13894
Jiao X, Chen Z, Wu J, Du H, Liu F, Chen J, Li D (2011) Male remating and female fitness in the wolf spider Pardosa astrigera: the role of male mating history. Behav Ecol Sociobiol 65(2):325-332. https://doi.org/10.1007/s00265-010-1049-2
Jiménez-Pérez A, Wang Q (2004) Male remating behavior and its effect on female reproductive fitness in Cnephasia jactatana Walker (Lepidoptera: Tortricidae). J Insect Behav 17(5):685-694. https://doi.org/10.1023/B:JOIR.0000042549.59147.50
Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82(2):265-289. https://doi.org/10.1111/j.1469-185X.2007.00009.x
Jones TM, Balmford A, Quinnell RJ (2000) Adaptive female choice for middle–aged mates in a lekking sandfly Proc R Soc B: Biol Sci 267(1444):681-686. https://doi.org/10.1098/rspb.2000.1056
Jones TM, McNamara KB, Colvin PG, Featherston R, Elgar MA (2006) Mating frequency, fecundity and fertilization success in the hide beetle, Dermestes maculatus. J Insect Behav 19(3):357-371. https://doi.org/10.1007/s10905-006-9032-5
Kaitala A, Wiklund C (1994) Female mate choice and mating costs in the polyandrous butterfly Pieris napi (Lepidoptera: Pieridae). J Insect Behav 8(3), 355-363. https://doi.org/10.1007/BF01989364
King BH, Fischer CR (2010) Male mating history: effects on female sexual responsiveness and reproductive success in the parasitoid wasp Spalangia endius. Behav Ecol Sociobiol 64(4):607-615. https://doi.org/10.1007/s00265-009-0878-3
Klepetka B, Gould F (1996) Effects of age and size on mating in Heliothis virescens (Lepidoptera: Noctuidae): implications for resistance management. Environ Entomol 25(5):993-1001. https://doi.org/10.1093/ee/25.5.993
Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution of mate choice and mating biases. Proc R Soc B: Biol Sci 270 (1515):653–664. https://doi.org/10.1098/rspb.2002.2235
Lane S M, Solino JH, Mitchell C, Blount JD, Okada K, Hunt J, House CM (2015) Rival male chemical cues evoke changes in male pre-and post-copulatory investment in a flour beetle. Behav Ecol 26(4):1021-1029. https://doi.org/10.1093/beheco/arv047
Lane SM, Dickinson AW, Tregenza T, House CM (2016) Sexual Selection on male cuticular hydrocarbons via male–male competition and female choice. J Evol Biol 29(7):1346-1355. https://doi.org/10.1111/jeb.12875
Lauwers K, Van Dyck H (2006) The cost of mating with a non-virgin male in a monandrous butterfly: experimental evidence from the speckled wood, Pararge aegeria. Behav Ecol Sociobiol 60(1):69-76. https://doi.org/10.1007/s00265-005-0142-4
Jing LI, Yu WA, Chen YZ, Liu PC, Hu HY (2023) Effects of male age, body size and mating status on female mate preference and offspring sex ratio in Pachycrepoideus vindemmiae (Hymenoptera: Pteromalidae). Eur J Entomol 120:1-8. https://doi.org/10.14411/eje.2023.001
Redjdal A, Sahnoune M, Moali A, De Biseau JC (2023) High Divergence of Cuticular Hydrocarbons and Hybridization Success in Two Allopatric Seven-Spot Ladybugs. J Chem Ecol 49(3-4):103-115. https://doi.org/10.1007/s10886-023-01406-5
Singh P, Mishra G (2020) Impact of female mating status and female familiarity with remating interval on the reproductive success of Propylea dissecta (Mulsant)(Coleoptera: Coccinellidae). Anim Biol 70(3), 271-287. https://doi.org/10.1163/15707563-bja10002