Intraspecific Variation in the Alkaloids of Adalia decempunctata (Coleoptera, Coccinellidae): Sex, Reproduction and Colour Pattern Polymorphism
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ CESKE01
Erasmus+ Mobility
PubMed
39276200
PubMed Central
PMC11543752
DOI
10.1007/s10886-024-01544-4
PII: 10.1007/s10886-024-01544-4
Knihovny.cz E-zdroje
- Klíčová slova
- Aposematism, Chemical defence, Color morph, Polymorphism, Reproductive allocation, Sexual dimorphism,
- MeSH
- alkaloidy * analýza chemie metabolismus MeSH
- barva MeSH
- brouci * fyziologie chemie MeSH
- druhová specificita MeSH
- ovum chemie MeSH
- pigmentace MeSH
- pohlavní dimorfismus MeSH
- rozmnožování * MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- alkaloidy * MeSH
In this paper, we examine intraspecific variation in the quantity of alkaloid chemical defence in field collected individuals of the polymorphic ladybird beetle Adalia decempunctata (10-spot ladybird). Like its more widely studied relative Adalia bipunctata (2-spot ladybird), A. decempunctata possesses the alkaloids adaline and adalinine, which are, respectively, the major and minor alkaloids of A. bipunctata. We focused especially on alkaloid concentration in relation to colour pattern morph, sex, and the relationship between female and egg parameters. There was a marked sexual dimorphism in the balance of the two alkaloids, with adaline predominating in females and adalinine predominating in males: in males, on average, over 70% of total alkaloid was adalinine. Females had a lower proportion of adalinine (< 10%) than their eggs (> 15%) and relationships between egg alkaloid and female alkaloid or fecundity were weak or non-existent. Colour pattern morph had a borderline (although not) significant relationship with adaline concentration and total alkaloid concentration, which could be further explored with laboratory reared individuals. The sexual dimorphism in alkaloid content, which seems likely due to differences in synthesis, might be related to their relative costs to the two sexes and might provide insight into the evolution of alkaloid diversity in ladybirds.
Faculty of Science University of South Bohemia České Budějovice Czech Republic
Institute of Entomology Biology Centre of Czech Academy of Sciences České Budějovice Czech Republic
Maastricht Science Programme Maastricht University Maastricht the Netherlands
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Ahmad S (1992) Biochemical defence of pro-oxidant plant allelochemicals by herbivorous insects. Biochem Syst Ecol 20:269–296. 10.1016/0305-1978(92)90040-K
Arenas LM, Walter D, Stevens M (2015) Signal honesty and predation risk among a closely related group of aposematic species. Sci Rep 5:11021. 10.1038/srep11021 PubMed PMC
Aslam M, Nedvěd O (2024) Intraspecific and interspecific comparison of toxicity of ladybirds (Coleoptera: Coccinellidae) with contrasting colouration. Zoology 162:126144. 10.1016/j.zool.2024.126144 PubMed
Aslam M, Veselý P, Nedvěd O (2019) Response of passerine birds and chicks to larvae and pupae of ladybirds. Ecol Entomol 44:792–799. 10.1111/een.12756
Bezzerides AL, McGraw KJ, Parker RS, Husseini J (2007) Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmoniaaxyridis. Behav Ecol Sociobiol 61:1401–1408. 10.1007/s00265-007-0371-9
Blount JD, Speed MP, Ruxton GD, Stephens PA (2009) Warning displays may function as honest signals of toxicity. Proc R Soc Lond B 276:871–877. 10.1098/rspb.2008.1407 PubMed PMC
Blount JD, Rowland HM, Drijfhout FP, Endler JA, Inger R, Sloggett JJ, Hurst GDD, Hodgson DJ, Speed MP (2012) How the ladybird got its spots: effects of resource limitation on the honesty of aposematic signals. Funct Ecol 26:334–342. 10.1111/j.1365-2435.2012.01961.x
Braekman J-C, Charlier A, Daloze D, Heilporn S, Pasteels J, Plasman V, Wang S (1999) New piperidine alkaloids from two ladybird beetles of the genus Calvia (Coccinellidae). Eur J Org Chem 1999:1749–1755. 10.1002/(SICI)1099-0690(199907)1999:7%3c1749::AID-EJOC1749%3e3.0.CO;2-O
Brakefield PM (1985) Polymorphic Müllerian mimicry and interactions with thermal melanism in ladybirds and a soldier beetle: a hypothesis. Biol J Linn Soc 26:243–267. 10.1111/j.1095-8312.1985.tb01635.x
Briolat ES, Burdfield-Steel ER, Paul SC, Rönkä KH, Seymoure BM, Stankowich T, Stuckert AMM (2019) Diversity in warning coloration: selective paradox or the norm? Biol Rev 94:388–414. 10.1111/brv.12460 PubMed PMC
Brückner A, Raspotnig G, Wehner K, Meusinger R, Norton RA, Heethof M (2017) Storage and release of hydrogen cyanide in a chelicerate (Oribatulatibialis). Proc Natl Acad Sci USA 114:3469–3472. 10.1073/pnas.1618327114 PubMed PMC
Camarano S, González A, Rossini C (2009) Biparental endowment of endogenous defensive alkaloids in Epilachnapaenulata. J Chem Ecol 35:1–7. 10.1007/s10886-008-9570-8 PubMed
Daloze D, Braekman J-C, Pasteels JM (1994) Ladybird defence alkaloids: structural, chemotaxonomic and biosynthetic aspects (Col.: Coccinellidae). Chemoecology 5/6:173–183. 10.1007/BF01240602
Dixon AFG, Guo Y (1993) Egg and cluster size in ladybird beetles (Coleoptera: Coccinellidae): the direct and indirect effects of aphid abundance. Eur J Entomol 90:457–463
Eisner T, Eisner M, Siegler M (2007) Secret weapons: defenses of insects, spiders, scorpions, and other many-legged creatures. Belknap Press, Cambridge, Massachusetts. 10.2307/j.ctv1dp0twf
Griffith SC, Parker TH, Olson VA (2006) Melanin- versus carotenoid-based sexual signals: is the difference really so black and red? Anim Behav 71:749–763. 10.1016/j.anbehav.2005.07.016
Hartmann T (2004) Plant-derived secondary metabolites as defensive chemicals in herbivorous insects: a case study in chemical ecology. Planta 219:1–4. 10.1007/s00425-004-1249-y PubMed
Holloway GJ, de Jong PW, Brakefield PM, de Vos H (1991) Chemical defence in ladybird beetles (Coccinellidae). I. Distribution of coccinelline and individual variation in defence in 7-spot ladybirds (Coccinellaseptempunctata). Chemoecology 2:7–14. 10.1007/BF01240660
Holloway GJ, de Jong PW, Ottenheim M (1993) The genetics and cost of chemical defense in the two-spot ladybird (Adaliabipunctata L.). Evolution 47:1229–1239. 10.1111/j.1558-5646.1993.tb02149.x PubMed
Ireland H, Kearns P, Majerus M (1986) Interspecific hybridisation in the coccinellids: some observations on an old controversy. Entomol Rec J Var 98:181–185
de Jong PW, Holloway GJ, Brakefield PM, de Vos H (1991) Chemical defence in ladybird beetles (Coccinellidae). II. Amount of reflex fluid, the alkaloid adaline and individual variation in defence in 2-spot ladybirds (Adaliabipunctata). Chemoecology 2:15–19. 10.1007/bf01240661
King AG, Meinwald J (1996) Review of the defensive chemistry of coccinellids. Chem Rev 96:1105–1122. 10.1021/cr950242v PubMed
Laurent P, Lebrun B, Braekman J-C, Daloze D, Pasteels JM (2001) Biosynthetic studies on adaline and adalinine, two alkaloids from ladybird beetles (Coleoptera: Coccinellidae). Tetrahedron 57:3403–3412. 10.1016/S0040-4020(01)00207-1
Laurent P, Braekman J-C, Daloze D (2005) Insect chemical defense. Top Curr Chem 240:167–229. 10.1007/b98317
Lognay G, Hemptinne JL, Chan FY, Gaspar C, Marlier M, Braekman JC, Daloze D, Pasteels JM (1996) Adalinine, a new piperidine alkaloid from the ladybird beetles Adaliabipunctata and Adaliadecempunctata. J Nat Prod 59:510–511. 10.1021/np960129f
Majerus MEN (1994) Ladybirds. HarperCollins, London
Marples NM (1993) Is the alkaloid in 2spot ladybirds (Adaliabipunctata) a defence against ant predation? Chemoecology 4:29–32. 10.1007/BF01245893
Nedvěd O (2015) Brouci čeledi slunéčkovití (Coccinellidae) střední Evropy. Ladybird beetles (Coccinellidae) of Central Europe. Academia, Prague
Oudendijk Z, Sloggett JJ (2022) How diet leads to defensive dynamism: effect of the dietary quality on autogenous alkaloid recovery rate in a chemically defended beetle. J Chem Ecol 48:99–107. 10.1007/s10886-021-01326-2 PubMed
Pasteels JM, Deroe C, Tursch B, Braekman JC, Daloze D, Hootele C (1973) Distribution et activités des alcaloïdes défensifs des Coccinellidae. J Insect Physiol 19:1771–1784. 10.1016/0022-1910(73)90046-2
Paul SC, Pell JK, Blount JD (2015) Reproduction in risky environments: the role of invasive egg predators in ladybird laying strategies. PLoS One 10:e0139404. 10.1371/journal.pone.0139404 PubMed PMC
Paul SC, Stevens M, Burton J, Pell JK, Birkett MA, Blount JD (2018) Invasive egg predators and food availability interactively affect maternal investment in egg chemical defense. Front Ecol Evol 6:4. 10.3389/fevo.2018.00004
Randall K, Majerus M, Forge H (1992) Characteristics for sex determination in British ladybirds (Coleoptera: Coccinellidae). The Entomologist 111:109–122
Ruxton GD, Allen WL, Sherratt TN, Speed MP (2018) Avoiding attack: the evolutionary ecology of crypsis, aposematism, and mimicry, 2nd edn. Oxford University Press, Oxford. 10.1093/oso/9780199688678.001.0001
Sakaki S, Nedvěd O (2023) Root elongation test on seeds of Sinapisalba reveals toxicity of extracts from thirteen colour forms of the Asian multi-coloured ladybird, Harmoniaaxyridis. Entomol Exp Appl 171:186–195. 10.1111/eea.13271
Sherratt TN (2002) The coevolution of warning signals. Proc R Soc Lond B 269:741–746. 10.1098/rspb.2001.1944 PubMed PMC
Sloggett JJ (2005) Are we studying too few taxa? Insights from aphidophagous ladybird beetles (Coleoptera: Coccinellidae). Eur J Entomol 102:391–398. 10.14411/eje.2005.056
Sloggett JJ (2010) Colour pattern polymorphism and chemical defence in Harmoniaaxyridis. IOBC-WPRS Bull 58:115–123
Sloggett JJ (2022) Diet and chemical defence in ladybird beetles (Coleoptera: Coccinellidae). Eur J Entomol 119:362–367. 10.14411/eje.2022.037
Sloggett JJ, Lorenz MW (2008) Egg composition and reproductive investment in aphidophagous ladybird beetles (Coccinellidae: Coccinellini): egg development and interspecific variation. Physiol Entomol 33:200–208. 10.1111/j.1365-3032.2008.00622.x
Sloggett JJ, Honěk A (2012) Genetic studies. In: Hodek I, van Emden HF, Honěk A (eds) Ecology and behavior of the ladybird beetles (Coccinellidae). Wley-Blackwell, Chichester, pp 13–53. 10.1002/9781118223208.ch2
Speed MP (2000) Warning signals, receiver psychology and predator memory. Anim Behav 60:269–278. 10.1006/anbe.2000.1430 PubMed
Speed MP, Ruxton GD, Mappes J, Sherratt TN (2012) Why are defensive toxins so variable? An evolutionary perspective. Biol Rev 87:874–884. 10.1111/j.1469-185X.2012.00228.x PubMed
Steele T, Singer RD, Bjørnson S (2020) Effects of temperature on larval development, alkaloid production and microsporidiosis in the two-spotted lady beetle, Adalia bipunctata L. (Coleoptera: Coccinellidae). J Invert Pathol 172:107353. 10.1016/j.jip.2020.107353 PubMed
Steele T, Singer RD, Bjørnson S (2023) Alkaloid content in microsporidia-infected Adaliabipunctata (Coleoptera: Coccinellidae) life stages, and pathogen spore load in adults after exposure to physical stress. J Invert Pathol 200:107969. 10.1016/j.jip.2023.107969 PubMed
Summers K, Clough ME (2001) The evolution of coloration and toxicity in the poison frog family (Dendrobatidae). Proc Natl Acad Sci USA 98:6227–6232. 10.1073/pnas.101134898 PubMed PMC
Tursch B, Dalozc D, Dupont M, Pasteels JM, Tricot M-C (1971) A defense alkaloid in a carnivorous beetle. Experientia 27:1380–1381. 10.1007/BF02154239
Tursch B, Braekman JC, Dalozc D, Hootele C, Losman D, Karlsson R, Pasteels JM (1973) Chemical ecology of arthropods, VI. Adaline, a novel alkaloid from Adaliabipunctata L, (Coleoptera, Coccinellldae). Tetrahedron Lett 14:201–202. 10.1016/S0040-4039(01)95617-5
Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10. 10.1890/10-0340.1 PubMed
Wheeler CA, Millar JG, Cardé RT (2015) Multimodal signal interactions in the ladybeetle, Hippodamiaconvergens, aposematic system. Chemoecology 25:123–133. 10.1007/s00049-014-0181-2
Zvereva EL, Kozlov MV (2016) The costs and effectiveness of chemical defenses in herbivorous insects: a meta-analysis. Ecol Monogr 86:107–124. 10.1890/15-0911.1