Whole-chromosome hitchhiking driven by a male-killing endosymbiont

Whilst most animals invest equally in males and females when they reproduce, a variety of vertically transmitted parasites has evolved the ability to distort the offspring sex ratios of their hosts. One such group of parasites are male-killing bacteria. Here we report the discovery of females of the ladybirdAnisosticta novemdecimpunctatathat produced highly female-biased offspring sex ratios associated with a 50% reduction in egg hatch rate. This trait was maternally transmitted with high efficiency, was antibiotic sensitive and was infectious following experimental haemolymph injection. We identified the cause as a male-killingSpiroplasmabacterium and phylogenetic analysis of rDNA revealed that it belongs to theSpiroplasma ixodetisclade in which other sex ratio distorters lie. We tested the potential for interspecific horizontal transfer by injection from an infectedA. novemdecimpunctataline into uninfected individuals of the two-spot ladybirdAdalia bipunctata. In this novel host, the bacterium was able to establish infection, transmit vertically and kill male embryos.

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The importance of cytoplasmic male killing elements in natural populations of the two spot ladybird, Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae)

Biological Journal of the Linnean Society ◽

10.1111/j.1095-8312.1993.tb00898.x ◽

1993 ◽

Vol 49 (2) ◽

pp. 195-202 ◽

Cited By ~ 23

Author(s):

GREGORY D. D. HURST ◽

MICHAEL E. N. MAJERUS ◽

LINDA E. WALKER

Keyword(s):

Natural Populations ◽

Adalia Bipunctata ◽

Male Killing

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Wolbachia infection in Argentinean populations of Anastrepha fraterculus sp1: preliminary evidence of sex ratio distortion by one of two strains

10.1101/738500 ◽

2019 ◽

Cited By ~ 1

Author(s):

CA Conte ◽

DF Segura ◽

FH Milla ◽

AA Augustinos ◽

JL Cladera ◽

...

Keyword(s):

Sex Ratio ◽

Insect Pests ◽

Wolbachia Infection ◽

Larval Survival ◽

Preliminary Evidence ◽

Wild Populations ◽

Crossing Experiments ◽

Anastrepha Fraterculus ◽

Male Killing ◽

Filarial Nematodes

ABSTRACTBackgroundWolbachia, one of the most abundant taxa of intracellular Alphaproteobacteria, is widespread among arthropods and filarial nematodes. The presence of these maternally inherited bacteria is associated with modifications of host fitness, including a variety of reproductive abnormalities, such as cytoplasmic incompatibility, thelytokous parthenogenesis, host feminization and male-killing. Wolbachia has attracted much interest for its role in biological, ecological and evolutionary processes as well as for its potential use in novel and environmentally-friendly strategies for the control of insect pests and disease vectors including a major agricultural pest, the South American fruit fly, Anastrepha fraterculus Wiedemann (Diptera: Tephritidae).ResultsWe used wsp, 16S rRNA and a multilocus sequence typing (MLST) scheme including gatB, coxA, hcpA, fbpA, and ftsZ genes to detect and characterize the Wolbachia infection in laboratory strains and wild populations of A. fraterculus from Argentina. Wolbachia was found in all A. fraterculus individuals studied. Nucleotide sequences analysis of wsp gene allowed the identification of two Wolbachia nucleotide variants (named wAfraCast1_A and wAfraCast2_A). After the analysis of 76 individuals, a high prevalence of the wAfraCast2_A variant was found both, in laboratory (82%) and wild populations (95%). MLST analysis identified both Wolbachia genetic variants as sequence type 13. Phylogenetic analysis of concatenated MLST datasets clustered wAfraCast1/2_A in the supergroup A. Paired-crossing experiments among single infected laboratory strains showed a phenotype specifically associated to wAfraCast1_A that includes slight detrimental effects on larval survival, a female-biased sex ratio; suggesting the induction of male-killing phenomena, and a decreased proportion of females producing descendants that appears attributable to the lack of sperm in their spermathecae.ConclusionsWe detected and characterized at the molecular level two wsp gene sequence variants of Wolbachia both in laboratory and wild populations of A. fraterculus sp.1 from Argentina. Crossing experiments on singly-infected A. fraterculus strains showed evidence of a male killing-like mechanism potentially associated to the wAfraCast1_A - A. fraterculus interactions. Further mating experiments including antibiotic treatments and the analysis of early and late immature stages of descendants will contribute to our understanding of the phenotypes elicited by the Wolbachia variant wAfraCast1_A in A. fraterculus sp.1.

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Male-killing and aposematic polymorphism in African butterflies: Is there a connection?

Ideas in Ecology and Evolution ◽

10.4033/iee.2013.6.4.c ◽

2013 ◽

Vol 6 ◽

Cited By ~ 2

Author(s):

Ian Gordon

Keyword(s):

Male Killing

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Rapid comeback of males: evolution of male-killer suppression in a green lacewing population

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.0369 ◽

2018 ◽

Vol 285 (1877) ◽

pp. 20180369 ◽

Cited By ~ 8

Author(s):

Masayuki Hayashi ◽

Masashi Nomura ◽

Daisuke Kageyama

Keyword(s):

Sex Ratio ◽

Female Offspring ◽

Mitochondrial Haplotype ◽

Green Lacewing ◽

Haplotype Variation ◽

Male Killing ◽

Significant Difference ◽

High Prevalence ◽

Laboratory Line ◽

Male Killer

Evolutionary theory predicts that the spread of cytoplasmic sex ratio distorters leads to the evolution of host nuclear suppressors, although there are extremely few empirical observations of this phenomenon. Here, we demonstrate that a nuclear suppressor of a cytoplasmic male killer has spread rapidly in a population of the green lacewing Mallada desjardinsi . An M. desjardinsi population, which was strongly female-biased in 2011 because of a high prevalence of the male-killing Spiroplasma endosymbiont, had a sex ratio near parity in 2016, despite a consistent Spiroplasma prevalence. Most of the offspring derived from individuals collected in 2016 had 1 : 1 sex ratios in subsequent generations. Contrastingly, all-female or female-biased broods appeared frequently from crossings of these female offspring with males derived from a laboratory line founded by individuals collected in 2011. These results suggest near-fixation of a nuclear suppressor against male killing in 2016 and reject the notion that a non-male-killing Spiroplasma variant has spread in the population. Consistently, no significant difference was detected in mitochondrial haplotype variation between 2011 and 2016. These findings, and earlier findings in the butterfly Hypolimnas bolina in Samoa, suggest that these quick events of male recovery occur more commonly than is generally appreciated.

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