Abstract
Male-killing endosymbionts have been widely reported in the invertebrates and are highly prevalent in the Coccinellidae. The presence of male-killers can lead to extreme bias in host population sex ratios and may have important and far-reaching consequences for the life-history and evolution of their hosts. Male-killers may have direct and indirect effects on host fitness and reproductive behaviour, as well as affecting the host genome, either via strong selection pressure imposed by highly female-biased population sex ratios or by selective sweeps caused as a male-killer conferring an advantage to infected individuals spreads through a population. Criteria used to predict which species are liable to male-killer invasion, based on a variety of ecological factors, have been produced. In summary male-killers are predicted to occur in aphidophageous species, that lay eggs in clutches, show sibling egg consumption and are liable to neonatal larval mortality due to starvation. We assayed 30 species of Coccinellid for the presence of such male-killers to assess the predictive accuracy of the criteria. Male-killers were identified in 8 species in which they were predicted to occur and were absent from all 10 species predicted not to harbor them. Analysis of the remaining 12 species, where male-killers were predicted by the original criteria, but where they were not found, allowed us to identify areas where the criteria can be refined and improved. We conclude that whilst the original criteria give a reasonably accurate prediction, there are refinements and improvements, concerning details of host diet and life-history, which make them more robust, especially in the light of discoveries of male-killing suppressors and when incorporated give a better fit to our findings from field samples.
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References
Brakefield PM (1984) Ecological studies on the polymorphic ladybird Adalia bipunctata in the Netherlands. II Population dynamics, differential timing of reproduction and thermal melanism. J Anim Ecol 53:775–790
Ebbert MA (1991) The interaction phenotype in the Drosophila willistoni-spiroplasma symbiosis. Evolution 45:971–988
Engelstädter J, Hurst GDD (2009) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40:127–149
Hodek I (1973) Biology of Coccinellidae. Academia, Prague and Dr W Junk, The Hague
Hodek I, Honek A (1996) Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, The Netherlands
Hoffmann AA, Turelli M (1997) Cytoplasmic incompatibility in insects. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers. Oxford University Press, Oxford, pp 42–80
Hornett EA, Charlat S, Duplouy AM, Davies N, Roderick GK, Wedell N, Hurst GD (2006) Evolution of male-killer suppression in a natural population. PLOS Biol e283
Hornett EA, Engelstädter J, Hurst GD (2010) Hidden cytoplasmic incompatibility alters the dynamics of male-killer/host interactions. J Evolution Biol 23:479–487
Hu K (1979) Maternally inherited ‘sonless’ abnormal sex ratio condition in the ladybeetle Harmonia axyridis. Acta Genet Sin 6:296–304
Hurst LD (1991) The incidences and evolution of cytoplasmic male killers. Proc Roy Soc Lond B 244:91–99
Hurst GDD, Majerus MEN, Walker LE (1992) Cytoplasmic male killing elements in Adalia bipunctata (Linnaeus) (Coleoptera:Coccinellidae). Heredity 69:84–91
Hurst GDD, Hammarton T, Obrycki JJ, Majerus TMO, Walker LE, Bertrand D, Majerus MEN (1996) Male-killing in a fifth coccinellid beetle, Coleomegilla maculata. Heredity 77:177–185
Hurst GDD, Hammarton TM, Bandi C, Majerus TMO, Bertrand D, Majerus MEN (1997a) The diversity of inherited parasites of insects: the male-killing agent of the ladybird beetle Coleomegilla maculata is a member of the Flavobacteria. Genet Res 70:1–6
Hurst GDD, Hurst LD, Majerus MEN (1997b) Cytoplasmic sex-ratio distorters. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers. Oxford University Press, Oxford, pp 125–154
Hurst GDD, Schulenburg JHGvd, Majerus TMO, Bertrand D, Zakharov IA, Baungaard J, Völkl W, Stouthamer R, Majerus MEN (1999a) Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Ins Mol Biol 8:133–139
Hurst GDD, Jiggins FM, Schulenburg JHGvd, Bertrand D, West SA, Goriacheva II, Zakharov IA, Werren JH, Stouthamer R, Majerus MEN (1999b) Male-killing Wolbachia in two species of insect. Proc Roy Soc Lond B 266:735–740
Hurst GDD, Bandi C, Sacchi L, Cochrane AG, Bertrand D, Karaca I, Majerus MEN (1999c) Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited flavobacteria that kill males only. Parasitology 118:125–134
Jaenike J (2009) Coupled population dynamics of endosymbionts within and between hosts. Oikos 118:353–362
Jiggins FM, Hurst GD, Majerus ME (2000) Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc Roy Soc Lond B 267:69–73
Jiggins FM, Bentley JK, Majerus MEN, Hurst GDD (2002) Recent changes in phenotypes and patterns of host specialization in Wolbachia bacteria. Mol Ecol 11:1275–1283
Lus JJ (1947) Some aspects of the population increase in Adalia bipunctata 2. The strains without males. Dokl Akad Nauk SSSR 57:951–954
Majerus MEN (1993) Notes on the inheritance of a scarce form of the striped ladybird, Myzia oblongoguttata (Coleoptera: Coccinellidae). Ent Rec J Var 105:271–277
Majerus MEN (1994) Ladybirds. New naturalist series no 81, HarperCollins, London
Majerus MEN (1999) Simbiontes hereditarios causantes de efectos deletéreos en los artrópodos/Deleterious endosymbionts of Arthropods. In: Melic A, De Haro JJ, Méndez M, Ribera I (eds) The evolution and ecology of arthropods. (In Spanish and English). Sociedad Entomologica Aragonera, Zaragosa, Spain, pp 777–806
Majerus TMO (2001) The evolutionary genetics of male-killing in the Coccinellidae. PhD thesis, University of Cambridge
Majerus MEN, Hurst GDD (1997) Ladybirds as a model system for the study of male-killing symbionts. Entomophaga 42:13–20
Majerus MEN, Kearns PWE (1989) Ladybirds (Naturalists’ Handbooks no 10). Richmond Publishing, Slough
Majerus MEN, Majerus TMO (2000) Female-biased sex ratio due to male-killing in the Japanese ladybird Coccinula sinensis. Ecol Entomol 25:234–238
Majerus TMO, Majerus MEN (2010a) Discovery and identification of a male-killing agent in the Japanese ladybird Propylea japonica (Coleoptera: Coccinellidae). BMC Evol Biol 10:37
Majerus TMO, Majerus MEN (2010b) Intergenomic arms races: detection of a nuclear rescue gene of male-killing in a ladybird. PLoS Pathog 6(7):e1000987
Majerus TMO, Majerus MEN, Knowles B, Wheeler J, Betrand D, Kuznetzov VN, Ueno H, Hurst GDD (1998) Extreme variation in the prevalence of male-killing microorganisms between three populations of the ladybird Harmonia axyridis (Coleoptera: Coccinellidae). Heredity 81:683–691
Majerus TMO, Schulenburg JHGvd, Majerus MEN, Hurst GDD (1999) Molecular identification of a male-killing agent in the ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Ins Mol Biol 8:551–555
Malogolowkin-Cohen C, Rodriguez-Pereira MAQ (1975) Sexual drive of normal and SR flies of Drosophila nebulosa. Evolution 29:579–580
Matsuka M, Hashi H, Okada I (1975) Abnormal sex ratio found in the lady beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Appl Entomol Zool 10:84–89
Michie LJ, Mallard F, Majerus ME, Jiggins FM (2010) Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis. J Evol Biol 23:1699–1707
Niijima K, Nakajima K (1981) Abnormal sex ratio in Menochilus sexmaculatus (Fabricius). Bull Fac Agric Tamagawa Univ 21:59–67
Randall K, Majerus MEN, Forge H (1992) Characteristics for sex determination in British ladybirds, Coleoptera: Coccinellidae. Entomologist 111:109–122
Randerson JP, Smith GC, Hurst LD (2000) The evolutionary dynamics of male-killers and their hosts. Heredity 84:152–160
Schulenburg JHGvd, Habig M, Sloggett JJ, Webberley M, Bertrand D, Hurst GDD, Majerus MEN (2001) The incidence of male-killing Rickettsia (alpha proteobacteria) in the 10-spot ladybird, Adalia decempunctata L. (Coleoptera: Coccinellidae). Appl Env Microbiol 67:270–277
Shull HF (1948) An all-female strain of lady beetles with reversions to normal sex ratio. Am Nat 82:241–251
Tinsley M (2003) The ecology and evolution of male-killing bacteria in ladybirds. PhD Thesis, Department of Genetics, University of Cambridge
Tinsley MC, Majerus MEN (2006) A new male-killing parasitism: spiroplasma bacteria infect the ladybird beetle Anisosticta novemdecimpunctata (Coleoptera: Coccinellidae). Parasitology 132:757–765
Werren JH, O’Neill SL (1997) The evolution of heritable symbionts. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers. Oxford University Press, Oxford, pp 1–41
Werren JH, Hurst GDD, Zhang W, Breeuwer JAJ, Stouthamer R, Majerus MEN (1994) Rickettsial related male-killing in the ladybird beetle (Adalia bipunctata). J Bacteriol 176:388–394
Williamson DL, Poulson DF (1979) Sex ratio organisms (spiroplasmas) of Drosophila. In: Whitcomb RF, Tully JG (eds) The Mycoplasmas Vol 3. Academic Press, New York, pp 175–208
Acknowledgments
We thank Professor Yoshiaki Obara, Professor Ilia Zakharov, Dr Toshiyuki Satoh, Dr John Acorn and the Tropical Research Station, Atherton, Australia for aid during collection of samples and Professor John Armour, Dr Francis Gilbert and Dr Markus Eichhorn for comments on the manuscript. TMOM was funded by an NERC research studentship, otherwise this work was funded privately by the authors.
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Michael E. N. Majerus—deceased.
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Majerus, T.M.O., Majerus, M.E.N. Male-killing in the Coccinellidae: testing the predictions. Evol Ecol 26, 207–225 (2012). https://doi.org/10.1007/s10682-011-9490-x
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DOI: https://doi.org/10.1007/s10682-011-9490-x