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 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 Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

mSystems ◽  
2020 ◽  
Vol 5 (1) ◽  
Author(s):  
Jessamyn I. Perlmutter ◽  
Jane E. Meyers ◽  
Seth R. Bordenstein
Keyword(s):  
Drosophila Melanogaster ◽  
Copy Number ◽  
Cytoplasmic Incompatibility ◽  
Functional Study ◽  
Content Type ◽  
Transgenic Expression ◽  
Additional Gene ◽  
Reproductive Parasitism ◽  
Transcript Length ◽  
Male Killing

ABSTRACT Endosymbiotic bacteria in the genus Wolbachia remarkably infect nearly half of all arthropod species. They spread in part because of manipulations of host sexual reproduction that enhance the maternal transmission of the bacteria, including male killing (death of infected males) and unidirectional cytoplasmic incompatibility (CI; death of offspring from infected fathers and uninfected mothers). Recent discoveries identified several genes in prophage WO of Wolbachia (wmk, cifA, and cifB) that fully or partially recapitulate male killing or CI when transgenically expressed in Drosophila melanogaster. However, it is not yet fully resolved if other gene candidates contribute to these phenotypes. Here, we transgenically tested 10 additional gene candidates for their involvement in male killing and/or CI. The results show that despite sequence and protein architecture similarities or comparative associations with reproductive parasitism, transgenic expression of the candidates does not recapitulate male killing or CI. Sequence analysis across Wmk and its closest relatives reveals amino acids that may be important to its function. In addition, evidence is presented to propose new hypotheses regarding the relationship between wmk transcript length and its ability to kill a given host, as well as copy number of wmk homologs within a bacterial strain, which may be predictive of host resistance. Together, these analyses continue to build the evidence for identification of wmk, cifA, and cifB as the major genes that have thus far been shown to cause reproductive parasitism in Wolbachia, and the transgenic resources provide a basis for further functional study of phage WO genes. IMPORTANCE Wolbachia are widespread bacterial endosymbionts that manipulate the reproduction of diverse arthropods to spread through a population and can substantially shape host evolution. Recently, reports identified three prophage WO genes (wmk, cifA, and cifB) that transgenically recapitulate many aspects of reproductive manipulation in Drosophila melanogaster. Here, we transgenically tested 10 additional gene candidates for CI and/or male killing in flies. The results yield no evidence for the involvement of these gene candidates in reproductive parasitism, bolstering the evidence for identification of the cif and wmk genes as the major factors involved in their phenotypes. In addition, evidence supports new hypotheses for prediction of male-killing phenotypes or lack thereof based on wmk transcript length and copy number. These experiments inform efforts to understand the full basis of reproductive parasitism for basic and applied purposes and lay the foundation for future work on the function of an interesting group of Wolbachia and phage WO genes.

scholarly journals Rapid evolution and horizontal gene transfer in the genome of a male-killing Wolbachia

2020 ◽  
Author(s):  
Tom Hill ◽  
Robert L. Unckless ◽  
Jessamyn I. Perlmutter
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Host Species ◽  
Evolutionary Dynamics ◽  
Population Genomics ◽  
Rapid Evolution ◽  
Male Killing ◽  
Show Evidence ◽  
Bacterial Endosymbionts ◽  
Unique Genes

AbstractWolbachia are widespread bacterial endosymbionts that infect a large proportion of insect species. While some strains of this bacteria do not cause observable host phenotypes, many strains of Wolbachia have some striking effects on their hosts. In some cases, these symbionts manipulate host reproduction to increase the fitness of infected, transmitting females. Here we examine the genome and population genomics of a male-killing Wolbachia strain, wInn, that infects Drosophila innubila mushroom-feeding flies. We compared wInn to other closely-related Wolbachia genomes to understand the evolutionary dynamics of specific genes. The wInn genome is similar in overall gene content to wMel, but also contains many unique genes and repetitive elements that indicate distinct gene transfers between wInn and non-Drosophila hosts. We also find that genes in the Wolbachia prophage and Octomom regions are particularly rapidly evolving, including those putatively or empirically confirmed to be involved in host pathogenicity. Of the genes that rapidly evolve, many also show evidence of recent horizontal transfer among Wolbachia symbiont genomes, suggesting frequent movement of rapidly evolving regions among individuals. These dynamics of rapid evolution and horizontal gene transfer across the genomes of several Wolbachia strains and divergent host species may be important underlying factors in Wolbachia’s global success as a symbiont.

scholarly journals The Temporal Dynamics of Three Bacterial Endosymbionts, Wolbachia, Arsenophonus, And Rhizobiales, of the Invasive Yellow Crazy Ant (Anoplolepisgracilipes) in Taiwan are associated with Climate Extremes

2021 ◽  
Author(s):  
Yi-Ting Hsiao ◽  
Ching-Ting Lai ◽  
Li-Hsin Wu
Keyword(s):  
Temporal Dynamics ◽  
Climate Extremes ◽  
Sampling Period ◽  
Temperature Treatment ◽  
High Temperature Treatment ◽  
Evolutionary Transitions ◽  
Symbiotic Interactions ◽  
Bacterial Endosymbionts ◽  
Southern Taiwan ◽  
Symbiotic Organisms

Abstract Symbiotic interactions have facilitated major evolutionary transitions, making them a key component of the success of life. By altering the host’s life-history traits or potential to respond to natural stresses, symbiotic organisms could either exacerbate or ameliorate the effects of environmental pressure on their hosts. These variations are in turn likely to alter the population dynamics of the host species. We examined the temporal dynamics of three bacterial symbionts, Wolbachia, Arsenophonus, and Rhizobiales, in two neighboring yellow crazy ant (Anoplolepis gracilipes (Smith)) colonies for three consecutive months (July - September 2019) in southern Taiwan. Coinfections of Wolbachia and Rhizobiales were consistently detected in all colonies. While the symbiont compositions remained consistent throughout the sampling period at both sites, the coinfection rate of Wolbachia and Rhizobiales showed a negative tendency with increases in the daily mean temperature and its standard deviation, the diurnal temperature difference, and especially precipitation over time. These relationships might be the key to understanding the temporal effects of coinfection dynamics on possible adaptations and physiological responses in A. gracilipes. We then empirically demonstrated the best Wolbachia removal efficiency (40%-27%) under high-temperature treatment, and that the spatial prevalence of Wolbachia increased with latitude in the Southern Hemisphere. Our work highlights the potential protection against climate extremes provided by symbiont coinfection and how climate affects the microbial ecological community at a fine scale.

scholarly journals Symbiont-Mediated Cytoplasmic Incompatibility: What have we Learned in 50 Years?

2020 ◽  
Author(s):  
J. Dylan Shropshire ◽  
Brittany Leigh ◽  
Seth R. Bordenstein
Keyword(s):  
Cytoplasmic Incompatibility ◽  
Life Sciences ◽  
Relative Fitness ◽  
Incipient Speciation ◽  
High Frequencies ◽  
The Past ◽  
Arthropod Species ◽  
Reproductive Processes

Cytoplasmic incompatibility (CI) is the most common symbiont-induced reproductive manipulation. Specifically, symbiont-induced sperm modifications cause catastrophic mitotic defects in the fertilized embryo and ensuing lethality in crosses between symbiotic males and either aposymbiotic females or females harboring a different symbiont strain. However, if the female carries the same symbiont strain, then embryos develop properly, which imparts a relative fitness benefit to symbiont-transmitting mothers. Thus, CI drives maternally transmitted bacteria to high frequencies in arthropod species worldwide. In the past two decades, CI has experienced a boom in interest due in part to its (i) deployment in successful, worldwide efforts to reduce the spread of mosquito-borne diseases, (ii) causation by bacteriophage genes, cifA and cifB, that modify animal reproductive processes, and (iii) important impacts on incipient speciation. This review serves as a gateway to experimental, conceptual, and quantitative themes of CI and outlines significant gaps in our understanding of CI’s mechanism that are ripe for investigation from a diversity of subdisciplines in the life sciences.

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.

scholarly journals Symbiont-mediated Cytoplasmic Incompatibility:What Have We Learned in 50 years?

2020 ◽  
Author(s):  
J. Dylan Shropshire ◽  
Brittany Leigh ◽  
Seth R. Bordenstein
Keyword(s):  
Cytoplasmic Incompatibility ◽  
Life Sciences ◽  
Relative Fitness ◽  
Incipient Speciation ◽  
High Frequencies ◽  
The Past ◽  
Arthropod Species ◽  
Reproductive Processes

Cytoplasmic incompatibility (CI) is the most common symbiont-induced reproductive manipulation. Specifically, symbiont-induced sperm modifications cause catastrophic mitotic defects in the fertilized embryo and ensuing lethality in crosses between symbiotic males and either aposymbiotic females or females harboring a different symbiont strain. However, if the female carries the same symbiont strain, then embryos develop properly, which imparts a relative fitness benefit to symbiont-transmitting mothers. Thus, CI drives maternally transmitted bacteria to high frequencies in arthropod species worldwide. In the past two decades, CI has experienced a boom in interest due in part to its (i) deployment in successful, worldwide efforts to reduce the spread of mosquito-borne diseases, (ii) causation by bacteriophage genes, cifA and cifB, that modify animal reproductive processes, and (iii) important impacts on incipient speciation. This review serves as a gateway to experimental, conceptual, and quantitative themes of CI and outlines significant gaps in our understanding of CI’s mechanism that are ripe for investigation from a diversity of subdisciplines in the life sciences.

SPECIAL PROBLEMS IN TOXICITY TESTING OF LONG ACTING DEPOT CONTRACEPTIVES

1974 ◽  
Vol 77 (1_Suppla) ◽  
pp. S315-S354 ◽  
Author(s):  
F. Neumann ◽  
R. von Berswordt-Wallrabe ◽  
W. Elger ◽  
K.-J. Gräf ◽  
S. H. Hasan ◽  
...  
Keyword(s):  
Biological Effects ◽  
Histological Finding ◽  
Toxicity Testing ◽  
Prolactin Secretion ◽  
List Type ◽  
Human Species ◽  
Prolactin Plasma Level ◽  
Human Use ◽  
Long Acting ◽  
Reproductive Processes

ABSTRACT Two types of so-called "depot contraceptives", long-acting steroids which are of interest for human use, were studied in animals. Norethisterone oenanthate, mainly gestagenic in the human and other species, turned out to be predominantly oestrogenic in rats. This oestrogenicity caused indirectly, via an enhanced hypophysial prolactin secretion, the well-known hypophysial and mammary tumours in rats. Another synthetic gestagen, 4,6-dichloro- 17- acetoxy- 16α-methyl-4,6-pregnadiene-3,20-dione, which might be considered in its biological actions similar to preparations containing chlormadinone acetate or medroxy-progesterone acetate, induced no signs of oestrogenicity in dogs. It is surmised that its gestagenic influence indirectly, and probaby, via an enhanced hypophysial prolactin secretion caused "mammary nodules" in this "non-rodent" species. These studies have born out mainly two facts: A synthetic steroid, norethisterone oenanthate, exerted different biological effects in different species: it was a gestagen in the rabbit, whereas in rats, its predominant influence was oestrogenic. The hypophysial prolactin secretion was enhanced in various species by different mechanisms: in rats, the oestrogenicity caused an increased prolactin plasma level, whereas in dogs, a gestagen with obviously no inherent oestrogenicity, 4,6-dichloro-17-acetoxy-16α-methyl-4,6-pregnadiene-3,20-dione, converted the histological appearance of the anterior pituitary into a condition with a greatly increased number of eosinophils. This histological finding was interpreted as an indicator for a hypersecretion of prolactin. Hence, animal work with "gestagens" has only limited predictive value with respect to their possible effects in the human species. Therefore, inflexible recommendations are not helpful in solving the safety problem of long-acting steroids which affect primarily reproductive processes.

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