scholarly journals A single synonymous nucleotide change impacts the male-killing phenotype of prophage WO gene wmk

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Jessamyn I Perlmutter ◽  
Jane E Meyers ◽  
Seth R Bordenstein
Keyword(s):  
Sex Ratio ◽  
Relative Fitness ◽  
Nucleotide Change ◽  
Transgenic Expression ◽  
Synonymous Codons ◽  
Sex Ratio Bias ◽  
Complex Phenotypes ◽  
Male Killing ◽  
Bacterial Endosymbionts ◽  
Reproductive Processes

Wolbachia are the most widespread bacterial endosymbionts in animals. Within arthropods, these maternally-transmitted bacteria can selfishly hijack host reproductive processes to increase the relative fitness of their transmitting females. One such form of reproductive parasitism called male killing, or the selective killing of infected males, is recapitulated to degrees by transgenic expression of the WO-mediated killing (wmk) gene. Here, we characterize the genotype-phenotype landscape of wmk-induced male killing in D. melanogaster using transgenic expression. While phylogenetically distant wmk homologs induce no sex-ratio bias, closely-related homologs exhibit complex phenotypes spanning no death, male death, or death of all hosts. We demonstrate that alternative start codons, synonymous codons, and notably a single synonymous nucleotide in wmk can ablate killing. These findings reveal previously unrecognized features of transgenic wmk-induced killing and establish new hypotheses for the impacts of post-transcriptional processes in male killing variation. We conclude that synonymous sequence changes are not necessarily silent in nested endosymbiotic interactions with life-or-death consequences.

scholarly journals A single synonymous nucleotide change impacts the male-killing phenotype of prophage WO gene wmk

2021 ◽  
Author(s):  
Jessamyn I. Perlmutter ◽  
Jane E. Meyers ◽  
Seth R. Bordenstein
Keyword(s):  
Relative Fitness ◽  
Synonymous Mutation ◽  
Nucleotide Change ◽  
Transgenic Expression ◽  
Sex Ratio Bias ◽  
Symbiotic Interactions ◽  
Complex Phenotypes ◽  
Male Killing ◽  
Bacterial Endosymbionts ◽  
Reproductive Processes

AbstractWolbachia are the most widespread bacterial endosymbionts in animals. Within arthropods, these maternally-transmitted bacteria can selfishly hijack host reproductive processes to increase the relative fitness of their transmitting females. One such form of reproductive parasitism called male killing, or the selective killing of infected males, is recapitulated to degrees by transgenic expression of the WO-mediated killing gene wmk. Here, we characterize the genotype-phenotype landscape of wmk-induced male killing in D. melanogaster. While phylogenetically distant wmk homologs induce no sex-ratio bias, closely-related homologs exhibit complex phenotypes spanning no death, male death, or death of all hosts. We demonstrate that alternative start codons and, notably, one synonymous mutation in wmk can ablate killing. These findings reveal previously unrecognized relationships of wmk-induced killing and establish new hypotheses for the impacts of post-transcriptional processes in wmk-induced male killing. We conclude that single synonymous sequence changes are not necessarily silent in important nested symbiotic interactions.

scholarly journals Wolbachia, sex ratio bias and apparent male killing in the harlequin beetle riding pseudoscorpion

Heredity ◽  
2005 ◽  
Vol 95 (1) ◽  
pp. 41-49 ◽  
Author(s):  
D W Zeh ◽  
J A Zeh ◽  
M M Bonilla
Keyword(s):  
Sex Ratio ◽  
Ratio Bias ◽  
Sex Ratio Bias ◽  
Male Killing

scholarly journals Suppression of Wolbachia-mediated male-killing in the butterfly Hypolimnas bolina involves a single genomic region

PeerJ ◽  
2019 ◽  
Vol 7 ◽  
pp. e7677 ◽  
Author(s):  
Louise A. Reynolds ◽  
Emily A. Hornett ◽  
Chris D. Jiggins ◽  
Gregory D.D. Hurst
Keyword(s):  
Sex Ratio ◽  
Selection Pressure ◽  
Rare Event ◽  
Genomic Region ◽  
High Frequencies ◽  
Sex Ratio Bias ◽  
Male Killing ◽  
Mapping Family ◽  
Evolutionary Lag ◽  
Genomic Locations

Background Sex ratio distorting agents (maternally inherited symbionts and meiotically-driving sex chromosomes) are common in insects. When these agents rise to high frequencies they create strong population sex ratio bias and selection then favours mutations that act to restore the rare sex. Despite this strong selection pressure, the evolution of mutations that suppress sex ratio distorting elements appears to be constrained in many cases, where sex-biased populations persist for many generations. This scenario has been observed in the butterfly Hypolimnas bolina, where Wolbachia-mediated male killing endured for 800–1,000 generations across multiple populations before the evolution of suppression. Here we test the hypothesis that this evolutionary lag is the result of suppression being a multilocus trait requiring multiple mutations. Methods We developed genetic markers, based on conservation of synteny, for each H. bolina chromosome and verified coverage using recombinational mapping. We then used a Wolbachia-infected mapping family to assess each chromosome for the presence of loci required for male survival, as determined by the presence of markers in all surviving sons. Results Informative markers were obtained for each of the 31 chromosomes in H. bolina. The only marker that cosegregated with suppression was located on chromosome 25. A genomic region necessary for suppression has previously been located on this chromosome. We therefore conclude that a single genomic region of the H. bolina genome is necessary for male-killing suppression. Discussion The evolutionary lag observed in our system is not caused by a need for changes at multiple genomic locations. The findings favour hypotheses in which either multiple mutations are required within a single genomic region, or the suppressor mutation is a singularly rare event.

CULTURAL INHERITANCE AS A MECHANISM FOR POPULATION SEX-RATIO BIAS IN REPTILES

Evolution ◽  
2007 ◽  
Vol 55 (5) ◽  
pp. 1049-1055 ◽  
Author(s):  
Steven Freedberg ◽  
Michael J. Wade
Keyword(s):  
Sex Ratio ◽  
Cultural Inheritance ◽  
Ratio Bias ◽  
Sex Ratio Bias

A new male-killing parasitism:Spiroplasmabacteria infect the ladybird beetleAnisosticta novemdecimpunctata(Coleoptera: Coccinellidae)

Parasitology ◽  
2006 ◽  
Vol 132 (6) ◽  
pp. 757-765 ◽  
Author(s):  
M. C. TINSLEY ◽  
M. E. N. MAJERUS
Keyword(s):  
Phylogenetic Analysis ◽  
Sex Ratio ◽  
High Efficiency ◽  
Sex Ratios ◽  
Egg Hatch ◽  
Hatch Rate ◽  
Male Killing ◽  
Offspring Sex ◽  
Novel Host ◽  
Males And Females

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.

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

2019 ◽  
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.

Behavioral variation in nesting phenology may offset sex-ratio bias in tuatara

2018 ◽  
Vol 329 (6-7) ◽  
pp. 373-381 ◽  
Author(s):  
Nicola J. Nelson ◽  
Susan N. Keall ◽  
Jeanine M. Refsnider ◽  
Anna L. Carter
Keyword(s):  
Sex Ratio ◽  
Behavioral Variation ◽  
Ratio Bias ◽  
Sex Ratio Bias

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

2018 ◽  
Vol 285 (1877) ◽  
pp. 20180369 ◽  
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.

Translocation reverses birth sex ratio bias depending on its timing during gestation: evidence for the action of two sex-allocation mechanisms

2007 ◽  
Vol 19 (7) ◽  
pp. 831 ◽  
Author(s):  
W. L. Linklater
Keyword(s):  
Glucose Metabolism ◽  
Sex Ratio ◽  
Sex Allocation ◽  
Preimplantation Embryo ◽  
Sex Ratio Bias ◽  
In Captivity ◽  
Developmental Asynchrony ◽  
Adjustment Mechanisms ◽  
Excess Glucose

Many sex allocation mechanisms are proposed but rarely have researchers considered and tested more than one at a time. Four facultative birth sex ratio (BSR) adjustment mechanisms are considered: (1) hormone-induced conception bias; (2) sex-differential embryo death from excess glucose metabolism; (3) sex-differential embryo death from embryo–uterine developmental asynchrony; and (4) pregnancy hormone suppression and resource deprivation. All mechanisms could be switched on by the corticoadrenal stress response. A total of 104 female rhinoceroses (Rhinocerotidae), translocated from 1961 to 2004 at different stages of gestation or conceived soon after arrival in captivity, were used to test for a reversal in BSR bias as evidence for the action of multiple sex-allocation mechanisms. Translocation induced a statistically significant BSR reversal between early gestation (86% male births from 0 to 0.19 gestation) and mid-gestation (38% male from 0.2 to 0.79 gestation). Captivity also induced a strongly male-biased (67% male) BSR for conceptions after arrival in captivity. The results indicate the action of at least two sex-allocation mechanisms operating in sequence, confirm the important role of sex-differential embryo death around implantation and of stress in sex allocation, and lend support to suggestions that sex-differential glucose metabolism by the preimplantation embryo likely plays a role in facultative BSR adjustment.

scholarly journals Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects

2011 ◽  
Vol 279 (1729) ◽  
pp. 787-793 ◽  
Author(s):  
Rufus A. Johnstone ◽  
Michael A. Cant ◽  
Jeremy Field
Keyword(s):  
Sex Ratio ◽  
Social Insects ◽  
Family Relationships ◽  
Nest Building ◽  
Kin Discrimination ◽  
Sterile Female ◽  
Sex Ratio Bias ◽  
Non Local ◽  
Reproductive Altruism ◽  
Existing Data

In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister–sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that ‘family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism’.

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