Maternally inherited sex ratio distortion as a result of a male-killing agent in spilostethus hospes (hemiptera: lygaeidae)

ABSTRACT A family composed solely of daughters was produced by a pair of milkweed bugs, _Spilostethus hospes_ (Hemiptera: Lygaeidae). The sex ratio among the offspring of the daughters was

significantly female-biased, indicating that sex ratio distortion is heritable. The following results suggest that sex ratio distortion is caused by a maternally inherited, male-killing

bacterium: females transmitted sex ratio distortion but males did not, egg hatch among pairs expressing sex ratio distortion was half that observed in pairs with unbiased offspring sex

ratio, and pairs expressing sex ratio distortion converted to unbiased offspring sex ratio following tetracycline treatment. Successful selection for a highly female-biased sex ratio

suggests that there is resistance to sex ratio distortion. Vertical transmission was incomplete and considerably reduced among females that underwent a forced delay in reproduction at cool

temperatures analogous to an overwintering phase of the life cycle. An attempt to transfer bacteria horizontally by forcing early instars from a nonhost line to cannibalize host eggs was

unsuccessful. With incomplete vertical transmission and no horizontal transmission, the bacterium presumably promotes its existence by boosting the reproductive success of host females, a

possibility which remains to be investigated. SIMILAR CONTENT BEING VIEWED BY OTHERS INTRACELLULAR SYMBIONTS DRIVE SEX RATIO IN THE WHITEFLY BY FACILITATING FERTILIZATION AND PROVISIONING OF

B VITAMINS Article 20 July 2020 BIAS IN SEX RATIOS AND POLYANDRY RATE IN REPRODUCTION OF _LEPTINOTARSA DECEMLINEATA_ Article Open access 14 December 2022 MUTUAL MATE CHOICE AND ITS BENEFITS

FOR BOTH SEXES Article Open access 10 November 2020 ARTICLE PDF REFERENCES * Bull, J J. 1983. _Evolution of Sex Determining Mechanisms_. Benjamin/Cummings, Menlo Park CA. Google Scholar  *

Cosmides, L M, and Tooby, J. 1981. Cytoplasmic inheritance and intragenomic conflict. _J Theor Biol_, 89, 83–129. Article  CAS  PubMed  Google Scholar  * Dingle, H. 1968. Life history and

population consequences of density, photoperiod, and temperature in a migrant insect, the milkweed bug, _Oncopeltus_. _Am Nat_, 102, 149–163. Article  Google Scholar  * Dingle, H. 1978.

Migration and diapause in tropical, temperate and island milkweed bugs. In: Dingle, H (ed.) _The Evolution of Insect Migration and Diapause_, pp. 254–276. Springer, New York. Chapter  Google

Scholar  * Ebbert, M A. 1991. The interaction phenotype in the Drosophila willistoni-spiroplasma symbiosis. _Evolution_, 45, 971–988. PubMed  Google Scholar  * Ebbert, M A. 1992.

Endosymbiotic sex ratio distorters in insects and mites. In: Wrensch, D. L. and Ebbert, M. A (eds) _Evolution and Diversity of Sex Ratio in Haplodip-loid Insects and Mites_, pp. 150–191.

Chapman and Hall, New York. Google Scholar  * Ebbert, M A. 1995. Variable effects of crowding on _Drosophila_ hosts of male-lethal and non-male-lethal spiroplasmas in laboratory populations.

_Heredity_, 74, 227–240. Article  PubMed  Google Scholar  * Eberhard, W G. 1980. Evolutionary consequences of intracellular organelle competition. _Q Rev Biol_, 55, 231–249. Article  CAS 

PubMed  Google Scholar  * Gherna, R L, Werren, J H, Weisburg, W, Cote, R, Woese, C R, Mandelco, L, and Brenner, D J. 1991. _Arsenophus 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  * Hoffmann, A A, Turelli, M, and Simmons, G M. 1986. Unidirectional

incompatibility between populations of _Drosophila simulans_. _Evolution_, 40, 692–701. Article  PubMed  Google Scholar  * Holloway, G J. 1984. An analysis of inherited factors affecting

the sex ratio in the rice weevil, _Sitophilus oryzae_ L. _Heredity_, 55, 145–150. Article  Google Scholar  * Hurst, G D D, and Majerus, M E N. 1992. Why do maternally inherited

microorganisms kill males? _Heredity_, 71, 81–95. 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. 1992. Intragenomic conflict as an evolutionary force. _Proc R Soc B_, 248, 135–140. 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  * Hurst, L D, and Vollrath, F. 1992. Sex-ratio adjustment in solitary and social

spiders. _Trends Ecol Evol_, 7, 326–327. Article  CAS  PubMed  Google Scholar  * Lamb, R Y, and Willey, R B. 1987. Cytological mechanisms of thelytokous parthenogenesis in insects. _Genome_,

29, 367–369. Article  Google Scholar  * Legrand, J J, Legrand-Hamelin, E, and Juchault, P. 1987. Sex determination in Crustacea. _Biol Rev_, 62, 439–470. Article  Google Scholar  * Leslie,

J F. 1984. A “sex-ratio” condition in _Oncopeltus fasciatus_. _J Hered_, 75, 260–264. Article  Google Scholar  * Lyttle, T W. 1991. Segregation distorters. _Ann Rev Genet_, 25, 511–557.

Article  CAS  PubMed  Google Scholar  * Ralph, C P. 1977. Effect of host plant density on populations of a specialized, seed sucking bug, _Oncopeltus fasciatus_. _Ecology_, 58, 799–809.

Article  Google Scholar  * Rigaud, T, and Juchault, P. 1992. Genetic control of the vertical transmission of a cytoplasmic sex factor in _Armadillidium vulgare_(Latr.) (Crustacea,

Oniscidea). _Heredity_, 68, 47–52. Article  Google Scholar  * Sauer, D, and Feir, D. 1973. Studies on natural populations of _Oncopeltus fasciatus_ (Dallas), the large milk weed bug. _Am

Midl Nat_, 90, 13–37. Article  Google Scholar  * Skinner, S W. 1985. _Son-killer:_ a third extrachromosomal factor affecting the sex ratio in the parasitoid wasp, _Nasonia_ (= _Mormoniella_)

_vitripennis_. _Genetics_, 109, 745–759. CAS  PubMed  PubMed Central  Google Scholar  * Stouthamer, R, Luck, R F, and Hamilton, W S. 1990. Antibiotics cause parthenogenetic _Trichogramma_

(Hymenoptera/Trichogrammatidae) to revert to sex. _Proc Natl Acad Sci USA_, 87, 2424–2427. Article  CAS  PubMed  PubMed Central  Google Scholar  * Thangavelu, K. 1978. Some notes on the

ecology of three milkweed bugs in India (Heteroptera: Lygaeidae). _J Nat Hist_, 12, 641–647. Article  Google Scholar  * Uyenoyama, M K, and Feldman, M W. 1978. The genetics of sex ratio

distortion by cytoplasmic infection under maternal and contagious transmission: an epidemiological study. _Theor Pop Biol_, 14, 471–497. Article  CAS  Google Scholar  * Vulinec, K. 1990.

Aggregation by insects as a defense. In: Evans, D. L. and Schmidt, J. O (eds) _Insect Defenses: Adaptive Mechanisms and Strategies of Prey and Predators_, pp. 251–277. State University of

New York Press, Albany, NY. Google Scholar  * Werren, J H. 1987. The coevolution of autosomal and cytoplasmic sex ratio factors. _Theor Biol_, 124, 317–334. Article  Google Scholar  *

Willamson, D L, and Poulson, D F. 1979. Sex ratio organisms (spiroplasmas) of _Drosophila_. In: Whitcomb, R. F. and Tully, J. G (eds) _The Mycoplasmas_, vol. 3, pp. 175–208. Academic Press,

New York. Chapter  Google Scholar  * Wrensch, D L, and Ebbert, M A. (eds) 1992. _Evolution and Diversity of Sex Ratio in Haplodiploid Insects and Mites_. Chapman and Hall, New York. Google

Scholar  * Zchori-Fein, E, Rousch, R T, and Hunter, M S. 1992. Male production by antibiotic treatment in _Encarsia formosa_ (Hymenoptera: Aphelinidae), an asexual species. _Experientia_,

48, 102–105. Article  Google Scholar  Download references AUTHOR INFORMATION Author notes * Francis R Groeters Present address: Department of Biological Sciences, University of South

Carolina, Columbia, SC, 29208, U.S.A. AUTHORS AND AFFILIATIONS * Molecular Evolution and Systematics Group, Research School of Biological Sciences, Australian National University, PO Box

475, Canberra, A.C.T., 2601, Australia Francis R Groeters Authors * Francis R Groeters 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 Groeters, F. Maternally inherited sex ratio distortion as a result of a male-killing agent in _Spilostethus hospes_

(Hemiptera: Lygaeidae). _Heredity_ 77, 201–208 (1996). https://doi.org/10.1038/hdy.1996.125 Download citation * Received: 09 November 1995 * Issue Date: 01 August 1996 * DOI:

https://doi.org/10.1038/hdy.1996.125 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 * horizontal transmission * male-killing bacteria *

maternal inheritance * sex ratio distortion * _Spilostethus hospes_