Fifty Shades of the Harlequin Ladybird and a Sexually Transmitted Fungus
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články
PubMed
31765476
PubMed Central
PMC6876665
DOI
10.1093/jisesa/iez107
PII: 5641434
Knihovny.cz E-zdroje
- Klíčová slova
- Harmonia axyridis, Hesperomyces virescens, carotenoids, color pattern, melanism,
- MeSH
- Ascomycota fyziologie MeSH
- biologické modely MeSH
- brouci metabolismus mikrobiologie MeSH
- interakce hostitele a patogenu * MeSH
- karotenoidy metabolismus MeSH
- melaniny metabolismus MeSH
- pigmentace * MeSH
- sexuální chování zvířat * MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- karotenoidy MeSH
- melaniny MeSH
The ectoparasitic fungus Hesperomyces virescens was studied on its invasive host, the harlequin ladybird Harmonia axyridis, in the Czech Republic. A primary aim was to examine the relationship between fungal infection and elytral coloration of the ladybird. Furthermore, the role of host sex and mating status of females were analyzed. Beetles (n = 1,102) were sampled during autumn migration, and then sexed, weighed, and screened for infection. Females were dissected for detection of sperm in their spermathecae. Ladybirds were sorted according to color form and absorbance spectrophotometry was used to quantify carotenoid contents in their elytra. In individuals of the nonmelanic succinea form, the degree of melanization was measured using digital photographs and putative age groups were estimated based on background color of elytra. Sexual differences in infection patterns indicated transmission during copulation: males were infected mostly on elytra and venter, and females had infection almost exclusively on elytra. Mated females had higher infection rate than virgins. There was no influence of genetic color form on the fungal infection. Putative age groups (visual sorting to yellow, orange, and red) correlated with fungal infection. Infected individuals had elevated elytral carotenoid levels in comparison to uninfected individuals, which could be explained by host age. Infection-free succinea beetles were extensively melanized because they emerged later in the season at lower temperatures which induced melanization. Overall, we highlight that H. axyridis is a multivoltine species whose age, if not taken into account in ecophysiological studies, might present a considerable confounding factor.
Faculty of Science University of South Bohemia Branišovská České Budějovice Czech Republic
Institute of Entomology Biology Centre AS CR Branišovská České Budějovice Czech Republic
Zobrazit více v PubMed
Altincicek B., Kovacs J. L., and Gerardo N. M.. 2012. Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biol. Lett. 8: 253–257. PubMed PMC
Ando T., and Niimi T.. 2019. Development and evolution of color patterns in ladybird beetles: a case study in Harmonia axyridis. Dev. Growth Differ. 61: 73–84. PubMed
Awad M., Kalushkov P., Karabüyük F., and Nedvěd O.. 2015. Non-random mating activity of colour morphs of ladybird Harmonia axyridis (Coleoptera : –Coccinellidae). Acta Soc. Zool. Bohem. 79: 11–17.
Babin A., Biard C., and Moret Y.. 2010. Dietary supplementation with carotenoids improves immunity without increasing its cost in a crustacean. Am. Nat. 176: 234–241. PubMed
Báthori F., Pfliegler W. P., Rádai Z., and Tartally A.. 2018. Host age determines parasite load of Laboulbeniales fungi infecting ants: implications for host-parasite relationship and fungal life history. Mycoscience. 59: 99–104.
Bezzerides A. L., McGraw K. J., Parker R. S., and Husseini J.. 2007. Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behav. Ecol. Sociobiol. 61: 1401–1408.
Brakefield P. M. 1984. Ecological studies on the polymorphic ladybird Adalia bipunctata in the Netherlands. I. Population biology and geographical variation of melanism. J. Anim. Ecol. 53: 761–774.
Brown P. M. J., and Roy H. E.. 2017. Native ladybird decline caused by the invasive harlequin ladybird Harmonia axyridis: evidence from a long-term field study. Insect Conserv. Divers. 11: 230–239.
Brown P. M. J., Adriaens T., Bathon H., Cuppen J., Goldarazena A., Hägg T., Kenis M., Klausnitzer B. E. M., Kovář I., Loomans A. J. M.. et al. 2008. Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl. 53: 5–21.
Camacho-Cervantes M., Ortega-Iturriaga A., and Del-Val E.. 2017. From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. Peerj. 5: e3296. PubMed PMC
Ceryngier P., and Romanowski J.. 2017. Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) and its parasite in south-western Bulgaria and northern Greece. BioInvasions Rec. 6: 307–310.
Ceryngier P., and Twardowska K.. 2013. Harmonia axyridis (Coleoptera: Coccinellidae) as a host of the parasitic fungus Hesperomyces virescens (Ascomycota: Laboulbeniales, Laboulbeniaceae): a case report and short review. Eur. J. Entomol. 110: 549–557.
Ceryngier P., Nedvěd O., Grez A. A., Riddick E. W., Roy H. E., San Martin G., Steenberg T., Veselý P., Zaviezo T., Zúñiga-Reinoso Á.. et al. 2018. Predators and parasitoids of the harlequin ladybird, Harmonia axyridis, in its native range and invaded areas. Biol. Invasions. 20: 1009–1031.
Cornet S., Biard C., and Moret Y.. 2007. Is there a role for antioxidant carotenoids in limiting self-harming immune response in invertebrates? Biol. Lett. 3: 284–288. PubMed PMC
De Kesel A. 2011. Hesperomyces (Laboulbeniales) and coccinellid hosts. Sterbeeckia. 30: 32–37.
Felton G. W., and Summers C. B.. 1995. Antioxidant systems in insects. Arch. Insect Biochem. Physiol. 29: 187–197. PubMed
Fox J. 2003. Effect displays in R for generalised linear models. J. Stat. Softw. 8: 1–27.
Garcés S., and Williams R.. 2004. First record of Hesperomyces virescens Thaxter (Laboulbeniales: Ascomycetes) on Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). J. Kansas Entomol. Soc. 77: 156–158.
Goetz D. W. 2008. Harmonia axyridis ladybug invasion and allergy. Allergy Asthma Proc. 29: 123–129. PubMed
Haelewaters D., Van Wielink P., and Van Zuijlen J. W.. 2012. New records of Laboulbeniales (Fungi, Ascomycota) for The Netherlands. Entomolog. Ber. 72: 175–183.
Haelewaters D., Zhao S. Y., Clusella-Trullas S., Cottrell T. E., De Kesel A., Fiedler L., Herz A., Hesketh H., Hui C., Kleespies R. G., . et al. 2017. Parasites of Harmonia axyridis: current research and perspectives. BioControl. 62: 355–371.
Haelewaters D., Hiller T., Gorczak M., and Pfister D. H.. 2018a. Influence of elytral color pattern, size, and sex of Harmonia axyridis (Coleoptera, Coccinellidae) on parasite prevalence and intensity of Hesperomyces virescens (Ascomycota, Laboulbeniales). Insects. 9: 1–9. PubMed PMC
Haelewaters D., De Kesel A., and Pfister D. H.. 2018b. Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds. Sci. Rep. 8: 15966. PubMed PMC
Haelewaters D., Shapiro-Ilan D. I., and Cottrell T. E.. 2018c. Will dual fungal infections increase mortality of Harmonia axyridis in natural populations? IOBC-WPRS Bull. 137: 12–16.
Honek A., Martinkova Z., Dixon A. F. G., Skuhrovec J., Roy H. E., Brabec M., and Pekar S.. 2018. Life cycle of Harmonia axyridis in central Europe. BioControl. 63: 241–252. PubMed
Knapp M., and Nedvěd O.. 2013. Gender and timing during ontogeny matter: effects of a temporary high temperature on survival, body size and colouration in Harmonia axyridis. PLoS One. 8: e74984. PubMed PMC
Koch R. L., and Galvan T. L.. 2008. Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl. 53: 23–35.
Komai T., Chino M., and Hosino Y.. 1950. Contributions to the evolutionary genetics of the lady-beetle, Harmonia. I. Geographic and temporal variations in the relative frequencies of the elytral pattern types and in the frequency of elytral ridge. Genetics. 35: 589–601. PubMed PMC
Konrad M., Grasse A. V., Tragust S., and Cremer S.. 2015. Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. Proc. Biol. Sci. 282: 20141976. PubMed PMC
LaMana M. L., and Miller J. C.. 1996. Field observations on Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in Oregon. Biological Control. 6: 232–237.
Lombaert E., Guillemaud T., Cornuet J. M., Malausa T., Facon B., and Estoup A.. 2010. Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. Plos One. 5: e9743. PubMed PMC
McGraw K. J. 2005. The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Anim. Behav. 69: 757–764.
Michie L. J., Mallard F., Majerus M. E., and Jiggins F. M.. 2010. Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis. J. Evol. Biol. 23: 1699–1707. PubMed
Moran N. A., and Jarvik T.. 2010. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science. 328: 624–627. PubMed
Nalepa C. A., and Weir A.. 2007. Infection of Harmonia axyridis (Coleoptera: Coccinellidae) by Hesperomyces virescens (Ascomycetes: Laboulbeniales): role of mating status and aggregation behavior. J. Invertebr. Pathol. 94: 196–203. PubMed
Nedvěd O., Muhammad A., Abdolahi R., Sakaki S., and Onofre Soares A.. 2019. Age and temperature effects on accumulation of carotenoids in ladybirds. IOBC-WPRS Bull. 145: 33–36
Obata S. 1987. Mating behavior and sperm transfer in the Ladybird Beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Appl. Entomol. Zool. 22: 434–442.
Obata S. 1988. Mating refusal and its significance in females of the ladybird beetle, Harmonia axyridis. Physiol. Entomol. 13: 193–199.
Orlova-Bienkowskaja M. J., Spiridonov S. E., Butorina N. N., and Bieńkowski A. O.. 2018. Coinvasion by the ladybird Harmonia axyridis (Coleoptera: Coccinellidae) and its parasites, Hesperomyces virescens (Ascomycota: Laboulbeniales) and Parasitylenchus bifurcatus (Nematoda: Tylenchida, Allantonematidae), in the Caucasus. PLoS One. 13: e0202841. PubMed PMC
Osawa N., and Nishida T.. 1992. Seasonal variation in elytral color polymorphism in Harmonia axyridis (the ladybird beetle) – the role of nonrandom mating. Heredity. 69: 297–307.
Pickering G., Lin J., Riesen R., Reynolds A., Brindle I., and Soleas G.. 2004. Influence of Harmonia axyridis on the sensory properties of white and red wine. Am. J. Enol. Viticult. 55: 153–159.
Purse B. V., Comont R., Butler A., Brown P. M. J., Kessel C., and Roy H. E.. 2015. Landscape and climate determine patterns of spread for all colour morphs of the alien ladybird Harmonia axyridis. J. Biogeogr. 42: 575–588.
R Core Team 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: http://www.R-project.org/
Riddick E. W. 2006. Influence of host gender on infection rate, density and distribution of the parasitic fungus, Hesperomyces virescens, on the multicolored Asian lady beetle, Harmonia axyridis. J. Insect Sci. 6: 1–15. PubMed PMC
Riddick E. W., and Schaefer P. W.. 2005. Occurrence, density, and distribution of parasitic fungus Hesperomyces virescens (Laboulbeniales: Laboulbeniaceae) on multicolored asian lady beetle (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 98: 615–624.
Roy H. E., Brown P. M. J., Adriaens T., Berkvens N., Borges I., Clusella-Trullas S., Comont R. F., De Clercq P., Eschen R., Estoup A., . et al. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biolog. Invasions. 18: 997–1044.
Sloan D. B., and Moran N. A.. 2012. Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol. Lett. 8: 986–989. PubMed PMC
Stocks I. C., and Lindsey D. E.. 2008. Acute corrosion of the oral mucosa in a dog due to ingestion of multicolored Asian lady beetles (Harmonia axyridis: Coccinellidae). Toxicon. 52: 389–391. PubMed
Su W., Michaud J. P., Runzhi Z., Fan Z., and Shuang L.. 2009. Seasonal cycles of assortative mating and reproductive behaviour in polymorphic populations of Harmonia axyridis in China. Ecol. Entomol. 34: 483–494.
Sun Y. X., Hao Y. N., and Liu T. X.. 2018. A β-carotene-amended artificial diet increases larval survival and be applicable in mass rearing of Harmonia axyridis. Biol. Control. 123: 105–110.
Svensson P. A., and Wong B. B. M.. 2011. Carotenoid-based signals in behavioural ecology: a review. Behaviour. 148: 131–189.
Tan C. C. 1946. Mosaic dominance in the inheritance of color patterns in the ladybird beetle, Harmonia axyridis. Genetics. 31: 195–210. PubMed
Tan C. C., and Li J. C.. 1934. Inheritance of the elytral color patterns of the ladybird beetle, Harmonia axyridis Pallas. Am. Nat. 68: 252–265.
Weir A., and Beakes G. W.. 1996. Correlative light- and scanning electron microscope studies on the developmental morphology of Hesperomyces virescens. Mycologia. 88: 677–693.
Welch V. L., Sloggett J. J., Webberley K. M., and Hurst G. D. D.. 2001. Short-range clinal variation in the prevalence of a sexually transmitted fungus associated with urbanisation. Ecol. Entomol. 26: 547–550.
Wormington J. D., and Luttbeg B.. 2018. Red clypeal membrane color predicts immune function in a burying beetle (Coleoptera: Silphidae). J. Zool. 304: 284–292.