ABSTRACT Inherited symbionts which selectively cause the death of male hosts are found widely across the Insecta. Previous studies have shown a single, but different micro-organism to be

responsible for male-killing in each taxonomic group studied. We here produce evidence that within a group of insects, the Coccinellidae, there is more than one causal agent of male

lethality. We report a novel observation of a male-killing trait in the species _Coleomegilla maculata_. Six of 26 crosses were found to produce a female-biased sex ratio associated with a

low egg hatch-rate. The trait was matrilinearly inherited and was observed to be tetracycline-sensitive. However, tests which indicate the presence of a _Rickettsia_, previously found to

_CARDINIUM_ SYMBIONTS Article 05 February 2022 A MALE-KILLING GENE ENCODED BY A SYMBIOTIC VIRUS OF _DROSOPHILA_ Article Open access 13 March 2023 INTRACELLULAR SYMBIONTS DRIVE SEX RATIO IN

THE WHITEFLY BY FACILITATING FERTILIZATION AND PROVISIONING OF B VITAMINS Article 20 July 2020 ARTICLE PDF REFERENCES * Balayeva, N M, Eremeeva, M E, Tissot-Dupont, H, Zakharov, I A, and

Raoult, D. 1995. Genotype characterization of the bacterium expressing the male-killing trait in the ladybird beetle _Adalia bipunctata_ with specific Rickettsial molecular tools. _Appl Env

Microbiol_, 61, 1431–1437. CAS  Google Scholar  * Breeuwer, J A J, and Werren, J H. 1990. Microorganisms associated with chromosome destruction and reproductive isolation between two insect

species. _Nature_, 346, 558–560. Article  CAS  PubMed  Google Scholar  * Breeuwer, J A J, and Werren, J H. 1993. Effect Of genotype on cytoplasmic incompatibility between two species of

_Nasonia_. _Heredity_, 70, 428–436. Article  Google Scholar  * Gherna, R L, Werren, J H, Weisburg, W, Cote, R, Woese, C R, Mandelco, L, and Brenner, D J. 1991. _Arsenophonus nasoniae_

gen.-nov., sp.-nov., the causative agent of the son killer trait in the parasitic wasp _Nasonia vitripennis_. _Int J Syst Bact_, 41, 563–565. Article  Google Scholar  * Hu, K. 1979.

Maternally inherited ‘sonless’ abnormal SR condition in the ladybeetle _Harmonia axyridis_. _Acta Genet Sinica_, 6, 296–304. Google Scholar  * Hurst, G D D, and Majerus, M E N. 1993. Why do

maternally inherited microorganisms kill males? _Heredity_, 71, 81–95. Article  Google Scholar  * Hurst, G D D, Majerus, M E N, and Walker, L E. 1992. Cytoplasmic male killing elements in

_Adalia bipunctata_ (Linnaeus) (Coleoptera: Coccinellidae). _Heredity_, 69, 84–91. Article  Google Scholar  * Hurst, L D. 1991. The incidences and evolution of cytoplasmic male killers.

_Proc R Soc B_, 244, 91–99. Article  Google Scholar  * Hurst, L D. 1993. The incidences, mechanisms and evolution of cytoplasmic sex ratio distorters in animals. _Biol Rev_, 68, 121–193.

Article  Google Scholar  * Matsuka, M, Hashi, H, and Okada, I. 1975. Abnormal sex-ratio found in the lady beetle, _Harmonia axyridis_ Pallas (Coleoptera: Coccinellidae). _Appl Ent Zool_, 10,

84–89. Article  Google Scholar  * Moran, N A, Munson, M A, Baumann, P, and Ishikawa, H. 1993. A molecular clock in endosymbiotic bacteria is callibrated using the insect hosts. _Proc R Soc

B_, 253, 167–171. Article  Google Scholar  * Niuima, K, and Nakajima, K. 1981. Abnormal sex ratio in _Menochilius sexmaculatus_ (Fabricius). _Bull Fac Agric Tamagawa Univ_, 21, 59–67. Google

Scholar  * O'Neill, S L, Giordano, R, Colbert, A M E, Karr, T L, and Robertson, H M. 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic

incompatibility in insects. _Proc Natl Acad Sci USA_, 89, 2699–2702. Article  CAS  PubMed  PubMed Central  Google Scholar  * Pienkowski, R L. 1965. The incidence and effect of egg

cannibalism in first instar _Coleomegilla maculata lengi_ (Coccinellidae). _Ann Entomol Soc Am_, 58, 150–153. Article  Google Scholar  * Rigaud, T, and Juchault, P. 1992. Genetic control of

the vertical transmission of a cytoplasmic sex factor in _Armadillidium vulgare_. _Heredity_, 68, 47–52. Article  Google Scholar  * Rousset, F, Bouchon, D, Pintureau, B, Juchault, P, and

Solignac, M. 1992. _Wolbachia_ endosymbionts responsible for various alterations of sexuality in arthropods. _Proc R Soc B_, 250, 91–98. Article  CAS  PubMed  Google Scholar  * Shull, H F.

1948. An all-female strain of lady beetles with reversion to normal sex ratios. _Am Nat_, 82, 241–251. Article  Google Scholar  * Skinner, S W. 1985. Son-killer: a third extrachromosomal

factor affecting sex ratios in the parasitoid wasp _Nasonia vitripennis_. _Genetics_, 109, 745–754. CAS  PubMed  PubMed Central  Google Scholar  * Smith, B C. 1961. Influence of water and

previous food on the longevity of unfed larvae of _Coleomegilla maculata lengi_. _J Econ Entomol_, 54, 194–195. Article  Google Scholar  * Stouthamer, R, Breeuwer, J A J, Luck, R F, and

Werren, J H. 1993. Molecular identification of organisms associated with parthenogenesis. _Nature_, 361, 66–68. Article  CAS  PubMed  Google Scholar  * Werren, J H. 1987. The coevolution of

autosomal and cytoplasmic sex ratio factors. _J Theor Biol_, 124, 317–334. Article  Google Scholar  * Werren, J H, Skinner, S W, and Huger, A M. 1986. Male-killing bacteria in a parasitic

wasp. _Science_, 231, 990–992. Article  CAS  PubMed  Google Scholar  * Werren, J H, Hurst, G D D, Zhang, W, Breeuwer, J A J, Stouthamer, R, and Majerus, M E N. 1994. Rickettsial relative

associated with male killing in the ladybird beetle (_Adalia bipunctata_). _J Bacteriol_, 176, 388–394. Article  CAS  PubMed  PubMed Central  Google Scholar  * Werren, J H, Zhang, W, and

Guo, L R. 1995. Evolution and phylogeny of _Wolbachia_: reproductive parasites of arthropods. _Proc R Soc B_, 261, 55–71. Article  CAS  PubMed  Google Scholar  * Williams, S G, Sacci, J B J,

Schriefer, M E, Andersen, E M, Fujioka, K K, Sorvillo, F J, Barr, A R, and Azad, A F. 1992. Typhus and typhuslike rickettsiae associated with opposums and their fleas in Los Angeles. _J

Clin Microbiol_, 30, 1758–1762. CAS  PubMed  PubMed Central  Google Scholar  * Williamson, D L, and Poulson, D F. 1979. Sex ratio organisms (Spiroplasmas) of _Drosophila_. In: Whitcomb, R.

F. and Tully, J. G. (eds) _The Mycoplasmas_, pp. 175–208. Academic Press, New York. Chapter  Google Scholar  Download references AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of

Genetics, Downing Street, Cambridge, CB2 3EH, UK Gregory D D Hurst, Tansy C Hammarton, Tamsin M O Majerus, Linda E Walker, Dominique Bertrand & Michael E N Majerus * Department of

Entomology, Iowa State University, Ames, IA 50011, USA John J Obrycki Authors * Gregory D D Hurst View author publications You can also search for this author inPubMed Google Scholar * Tansy

C Hammarton View author publications You can also search for this author inPubMed Google Scholar * John J Obrycki View author publications You can also search for this author inPubMed 

Google Scholar * Tamsin M O Majerus View author publications You can also search for this author inPubMed Google Scholar * Linda E Walker View author publications You can also search for

this author inPubMed Google Scholar * Dominique Bertrand View author publications You can also search for this author inPubMed Google Scholar * Michael E N Majerus View author publications

You can also search for this author inPubMed Google Scholar RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Hurst, G., Hammarton, T., Obrycki, J. _et

al._ Male-killing bacterium in a fifth ladybird beetle, _Coleomegilla maculata_ (Coleoptera: Coccinellidae). _Heredity_ 77, 177–185 (1996). https://doi.org/10.1038/hdy.1996.122 Download

citation * Received: 30 October 1995 * Issue Date: 01 August 1996 * DOI: https://doi.org/10.1038/hdy.1996.122 SHARE THIS ARTICLE Anyone you share the following link with will be able to read

this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative

KEYWORDS * _Coleomegilla maculata_ * female-biased sex ratio * inherited symbiont * male-killing