Eur. J. Entomol. 111 (2): 307-311, 2014 | DOI: 10.14411/eje.2014.029
Prevalence of male-killer in a sympatric population of two sibling ladybird species, Harmonia yedoensis and Harmonia axyridis (Coleoptera: Coccinellidae)
- 1 Laboratory of Conservation Biology, Center for Northeast Asian Studies, Tohoku University, 41 Kawauchi, Aoba, Sendai, Miyagi 980-8576, Japan; e-mails: fvgnoriyuki@gmail.com; yuichi.c.kameda@gmail.com
- 2 Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University, Kyoto, Japan; e-mail: osawa@kais.kyoto-u.ac.jp
In predatory ladybirds male embryos in clutches of eggs infected with male-killing bacterial endosymbionts do not hatch and are consumed by female hatchlings. Moreover, it is predicted that infection with male-killing bacteria should be prevalent in a ladybird population if the fitness advantage to female ladybirds due to the resulting reallocation of resources is high. We compared male-killer bacterial prevalence in two sibling species of the ladybird genus Harmonia that use different host ranges. Harmonia yedoensis feeds mostly on the highly elusive pine aphid and its hatchlings can greatly enhance their ability to capture prey and thus their survival by consuming un-hatched eggs in the clutch. In contrast, Harmonia axyridis feeds on a wide range of prey and consumption of un-hatched eggs by the hatchlings does not necessarily increase their foraging success. In the study area where these two species of ladybird occur sympatrically 14 of the 22 females of H. yedoensis (64%) laid clutches of eggs of which approximately only a half hatched and did not produce male offspring, whereas only one of 12 of the females of H. axyridis (8%) exhibited symptoms indicating infection with male-killing bacteria. In the H. yedoensis that exhibited symptoms of being infected with male-killing bacteria, the total allocation of resources to each hatchling, which was provided by laying larger eggs and eating the un-hatched eggs in the clutch, was considerable. These results suggest that the difference in the prevalence of infection with male-killing bacteria in these two species of ladybird may reflect differences in the quality of their prey and their foraging behaviour.
Keywords: Coleoptera, Coccinellidae, Harmonia axyridis, H. yedoensis, aphidophagous ladybird, early male-killing, maternal investment, maternally inherited bacteria, sex ratio, sibling cannibalism, sibling species
Received: November 5, 2013; Revised: January 2, 2014; Accepted: January 2, 2014; Prepublished online: March 14, 2014; Published: May 5, 2014 Show citation
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References
- Agarwala B.K., Yasuda H. & Kajita Y. 2003: Effect of conspecific and heterospecific feces on foraging and oviposition of two predatory ladybirds: role of fecal cues in predator avoidance. - J. Chem. Ecol. 29: 357-376
Go to original source... - Ceryngier P. & 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
Go to original source... - Dyer K.A. & Jaenike J. 2004: Evolutionary stable infection by a male-killing endosymbiont in Drosophila innubila: molecular evidence from the host and parasite genomes. - Genetics 168: 1443-1455
Go to original source... - Elnagdy S., Majerus M.E.N., Gardener M. & Lawson Handley L.-J. 2013: The direct effects of male killer infection on fitness of ladybird hosts (Coleoptera: Coccinellidae). - J. Evol. Biol. 26: 1816-1825
Go to original source... - Graham R.I. & Wilson K. 2012: Male-killing Wolbachia and mitochondrial selective sweep in a migratory African insect. - BMC Evol. Biol. 12: 204
Go to original source... - Hurst L.D. 1991: The incidences and evolution of cytoplasmic male killers. - Proc. R. Soc. (B) 244: 91-99
Go to original source... - Hurst G.D.D. & Jiggins F.M. 2000: Male-killing bacteria in insects: mechanism, incidence, and implications. - Emerg. Infect. Dis. 6: 329-336
Go to original source... - Hurst G.D.D. & Majerus M.E.N. 1993: Why do maternally inherited microorganisms kill males? - Heredity 71: 81-95
Go to original source... - Hurst G.D.D., Majerus M.E.N. & Walker L.E. 1992: Cytoplasmic male killing elements in Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae). - Heredity 69: 84-91
Go to original source... - Hurst G.D.D., Purvis E.L., Sloggett J.J. & Majerus M.E.N. 1994: The effect of infection with male-killing Rockettsia on the demography of female Adalia bipunctata L. (two spot ladybird). - Heredity 73: 309-316
Go to original source... - Hurst G.D.D., Hurst L.D. & Majerus M.E.N. 1997: Cytoplasmic sex-ratio distorters. In O'Neill S.L., Hoffmann A.A. & Werren J.H. (eds): Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press, Oxford, pp. 125-154
Go to original source... - Hurst G.D.D., von der Schulenburg J.H.G., Majerus T.M.O., Bertrand D., Zakharov I.A., Baungaard J., Voelkl W., Stouthamer R. & Majerus M.E.N. 1999: Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. - Insect Mol. Biol. 8: 133-139
Go to original source... - Jaenike J. 2009: Coupled population dynamics of endosymbionts within and between hosts. - Oikos 118: 353-362
Go to original source... - Jaenike J., Dyer K.A. & Reed L.K. 2003: Within-population structure of competition and the dynamics of male-killing Wolbachia. - Evol. Ecol. Res. 5: 1023-1036
- Jiggins F.M. 2003: Male-killing Wolbachia and mitochondrial DNA: selective sweeps, hybrid introgression and parasite population dynamics. - Genetics 164: 5-12
Go to original source... - Kenis M., Roy H.E., Zindel R. & Majerus M.E.N. 2008: Current and potential management strategies against Harmonia axyridis. - BioControl 53: 235-252
Go to original source... - Majerus M.E.N. 2006: The impact of male-killing bacteria on the evolution of aphidophagous coccinellids. - Eur. J. Entomol. 103: 1-7
Go to original source... - Majerus M.E.N. & Hurst G.D.D. 1997: Ladybirds as a model system for the study of male-killing symbionts. - Entomophaga 42: 13-20
Go to original source... - Majerus T.M.O. & Majerus M.E.N. 2012: Male-killing in the Coccinellidae: testing the predictions. - Evol. Ecol. 26: 207-225
Go to original source... - Majerus T.M.O., Majerus M.E.N., Knowles B., Wheeler J., Bertrand D., Kuznetzov V.N., Ueno H. & Hurst G.D.D. 1998: Extreme variation in the prevalence of inherited male-killing microorganisms between three populations of Harmonia axyridis (Coleoptera: Coccinellidae). - Heredity 81: 683-691
Go to original source... - Martins A.B., Ventura I.M. & Klaczko L.B. 2010: Spiroplasma infection in Drosophila melanogaster: What is the advantage of killing males? - J. Invertebr. Pathol. 105: 145-150
Go to original source... - Matsuka M., Hashi H. & Okada I. 1975: Abnormal sex-ratio found in the lady beetle, Harmonia axyridis Pallas. - Appl. Entomol. Zool. 10: 84-89
Go to original source... - Nakamura K., Ueno H. & Miura K. 2005: Prevalence of inherited male-killing microorganisms in Japanese population of ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). - Ann. Entomol. Soc. Am. 98: 96-99
Go to original source... - Niijima K., Tobita M. & Matsuka M. 2000: Development of low-cost and laborsaving technique for group rearing of a ladybird, Harmonia axyridis. - Tamagawa Univ. Res. Rev. 6: 23-33 [in Japanese, English abstr.]
- Noriyuki S., Osawa N. & Nishida T. 2011: Prey capture performance in hatchlings of two sibling Harmonia ladybird species in relation to maternal investment through sibling cannibalism. - Ecol. Entomol. 36: 282-289
Go to original source... - Noriyuki S., Osawa N. & Nishida T. 2012: Asymmetric reproductive interference between specialist and generalist predatory ladybirds. - J. Anim. Ecol. 81: 1077-1085
Go to original source... - Okada I., Nijima K. & Toriumi Y. 1978: Comparative studies on sibling species of lady beetles, Harmonia yedoensis and H. axyridis (Coleoptera: Coccinellidae). - Bull. Fac. Agric. Tamagawa Univ. 18: 60-68 [in Japanese, English abstr.]
- O'Neill S.L., Hoffmann A.A. & Werren J.H. 1997: Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press, Oxford, 214 pp
Go to original source... - Osawa N. 1992: Sibling cannibalism in the ladybird beetle Harmonia axyridis Pallas: fitness consequences for mothers and offspring. - Res. Popul. Ecol. 34: 45-55
Go to original source... - Osawa N. 2000: Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. - Popul. Ecol. 42: 115-127
Go to original source... - Osawa N. & Ohashi K. 2008: Sympatric coexistence of sibling species Harmonia yedoensis and H. axyridis (Coleoptera: Coccinellidae) and the roles of maternal investment through egg and sibling cannibalism. - Eur. J. Entomol. 105: 445-454
Go to original source... - Roy H.E., Rhule E., Harding S., Lawson Handley L.-J., Poland R.L., Riddick E.W. & Steenberg T. 2011: Living with the enemy: parasites and pathogens of the ladybird Harmonia axyridis. - BioControl 56: 663-679
Go to original source... - Sasaji H. 1977: How to distinguish the sexes in ladybirds. - Insectarium 14: 13 [in Japanese]
- Sasaji H. 1998: Natural History of the Ladybirds. University of Tokyo Press, Tokyo, 251 pp. [in Japanese]
- Schall R. 1991: Estimation in generalized linear models with random effects. - Biometrika 78: 719-727
Go to original source... - Takakura K. 2004: Variation in egg size within and among generations of the bean weevil, Bruchidius dorsalis (Coleoptera, Bruchidae): effects of host plant quality and paternal nutritional investment. - Ann. Entomol. Soc. Am. 97: 346-352
Go to original source... - Unckless R.L. & Jaenike J. 2011: Maintenance of a male-killing Wolbachia in Drosophila innubila by male-killing dependent and male-killing independent mechanisms. - Evolution 66: 678-689
Go to original source... - van Kuppeveld F.J., van der Logt J.T., Angulo A.F., van Zoest M.J., Quint W.G., Niesters H.G., Galama J.M. & Melchers W.J. 1992: Genus- and species-specific identification of mycoplasmas by 16S rRNA amplification. - Appl. Environ. Microbiol. 58: 2606-2615
Go to original source... - Weinert L.A., Tinsley M.C., Temperley M. & Jiggins F.M. 2007: Are we underestimating the diversity and incidence of insect bacterial symbionts? A case study in ladybird beetles. - Biol. Lett. 3: 678-671
Go to original source... - Werren J.H. 1987: The coevolution of autosomal and cytoplasmic sex-ratio factors. - J. Theor. Biol. 124: 317-334
Go to original source...
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