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Biomedical subjects

M E Majerus

Publications and source records attributed to M E Majerus.

At least 19 recordsLinked to original sources
PubMed2001

Recombination confounds interpretations of Wolbachia evolution.

Wolbachia are vertically transmitted bacteria known from arthropods and nematode worms, which are maintained in host populations because they either physiologically benefit infected individuals or parasitically manipulate their reproduction. The different manipulation phenotypes are scattered across the Wolbachia phylogeny, suggesting that there have been multiple evolutions of similar phenotypes. This conclusion relies on the assumption of an absence of recombination between bacterial strains, so that the gene used to reconstruct the phylogeny reflects the evolutionary history of the genes involved in the trait. We tested for recombination by reconstructing the phylogeny of two Wolbachia genes from seven B-subdivision strains. The two genes produced mutually incompatible topologies, indicating that these lineages are subject to genetic recombination. This means that many evolutionary patterns inferred from Wolbachia phylogenies must be re-evaluated. Furthermore, recombination may be an important feature both in the evolution of the manipulation phenotypes and avoidance of Müller's ratchet. Finally, we discuss the implications of recombination for attempts to genetically engineer Wolbachia for use in the control of crop pests and human pathogens.

Biological Evolution↗
PubMed2001

How many species are infected with Wolbachia? Cryptic sex ratio distorters revealed to be common by intensive sampling.

Inherited bacterial symbionts from the genus Wolbachia have attracted much attention by virtue of their ability to manipulate the reproduction of their arthropod hosts. The potential importance of these bacteria has been underlined by surveys, which have estimated that 17% of insect species are infected. We examined whether these surveys have systematically underestimated the proportion of infected species through failing to detect the low-prevalence infections that are expected when Wolbachia distorts the sex ratio. We estimated the proportion of species infected with Wolbachia within Acraea butterflies by testing large collections of each species for infection. Seven out of 24 species of Acraea were infected with Wolbachia. Four of these were infected with Wolbachia at high prevalence, a figure compatible with previous broad-scale surveys, whilst three carried low-prevalence infections that would have had a very low likelihood of being detected by previous sampling methods. This led us to conclude that sex-ratio-distorting Wolbachia may be common in insects that have an ecology and/or genetics that permit the invasion of these parasites and that previous surveys may have seriously underestimated the proportion of species that are infected.

Animals↗
PubMed2001

Two male-killing Wolbachia strains coexist within a population of the butterfly Acraea encedon.

Inherited bacteria that kill male hosts early in their development are known from five insect orders. We ask to what extent the incidence of male-killers might be restricted by the rate at which new host-parasite interactions arise, by testing whether multiple male-killers have invaded a single host species. In Uganda, the butterflies Acraea encedon and A. encedana are both infected by the same strain of male-killing Wolbachia and there was no evidence of variation within the population. In Tanzanian A. encedon however, two phylogenetically distinct strains of male-killing Wolbachia were found within the same population. If this pattern of male-killer polymorphism is found to be general across infected species, it suggests that new male-killing infections arise frequently on an evolutionary time scale. Whether this polymorphism is stable, and what forces may be maintaining it, are unknown.

Animals↗
PubMed2001

Extreme length and length variation in the first ribosomal internal transcribed spacer of ladybird beetles (Coleoptera: Coccinellidae).

DNA sequences of the first ribosomal internal transcribed spacer (ITS1) were isolated from 10 ladybird beetle species (Coleoptera: Coccinellidae) representing four subfamilies (Coccinellinae, Chilocorinae, Scymninae, and Coccidulinae). The spacers ranged in length from 791 to 2,572 bp, thereby including one of the longest ITS1s and exhibiting one of the most extreme cases of ITS1 size variation in eukaryotes recorded to date. The causes of length variation were therefore analyzed. Almost no putatively homologous sequence similarities were identified for the taxa included. The only exception was for the subfamily Coccinellinae, which yielded sequence similarities in six regions of approximately 550 nucleotide positions, primarily at the 5' and 3' ends of ITS1. The majority of differences in ITS1 length between taxa could be attributed to the presence of repetitive elements with comparatively long repeat units. Repetition arose several times independently and was confined to the middle of the spacer which, in contrast to the 5' and 3' ends, had not been inferred in previous studies to be subject to functional constraints. These elements were characterized by high rates of evolutionary change, most likely as a result of high substitution rates in combination with inefficient homogenization across repeats. The repeated origin and subsequent divergence of "long" repetitive elements should thus be assumed to be an important factor in the evolution of coccinellid ITS1.

Amino Acid Sequence↗
PubMed2001

Incidence of male-killing Rickettsia spp. (alpha-proteobacteria) in the ten-spot ladybird beetle Adalia decempunctata L. (Coleoptera: Coccinellidae).

The diversity of endosymbiotic bacteria that kill male host offspring during embryogenesis and their frequencies in certain groups of host taxa suggest that the evolution of male killing and the subsequent spread of male-killing symbionts are primarily determined by host life history characteristics. We studied the 10-spot ladybird beetle, Adalia decempunctata L. (Coleoptera: Coccinellidae), in which male killing has not been recorded previously, to test this hypothesis, and we also assessed the evolution of the male killer identified by DNA sequence analysis. Our results show that A. decempunctata harbors male-killing Rickettsia (alpha-proteobacteria). Male-killing bacteria belonging to the genus Rickettsia have previously been reported only for the congeneric two-spot ladybird beetle, Adalia bipunctata L. Phylogenetic analysis of Rickettsia DNA sequences isolated from different populations of the two host species revealed a single origin of male killing in the genus Rickettsia. The data also indicated possible horizontal transfer of symbionts between host species. In addition, A. bipunctata is known to bear at least four different male-killing symbionts in its geographic range two of which coexist in the two locations from which A. decempunctata specimens were obtained for the present study. Since only a single male-killing taxon was found in A. decempunctata, we assume that the two closely related ladybird beetle species must differ in the number and/or geographic distribution of male killers. We discuss the importance of these findings to our understanding of the evolution and dynamics of symbiotic associations between male-killing bacteria and their insect hosts.

Animals↗
PubMed2000

Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host.

Sex-role-reversed mating systems in which females compete for males and males may be choosy are usually associated with males investing more than females in offspring. We report that sex-role reversal may also be caused by selfish genetic elements which distort the sex ratio towards females. Some populations of the butterflies Acraea encedon and Acraea encedana are extremely female biased because over 90% of females are infected with a Wolbachia bacterium that is maternally inherited and kills male embryos. Many females in these populations are virgins suggesting that their reproductive success may be limited by access to males. These females form lekking swarms at landmarks in which females exhibit behaviours which we interpret as functioning to solicit matings from males. The hypothesis that female A. encedon swarm in order to mate is supported by the finding that, in release recapture experiments, mated females tend to leave the swarm while unmated females remained. This behaviour is a sex-role-reversed form of a common mating system in insects in which males form lekking swarms at landmarks and compete for females. Female lekking swarms are absent from less female-biased populations and here the butterflies are instead associated with resources in the form of the larval food plant.

Animals↗
PubMed2000

The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium.

Many insects carry maternally inherited bacteria which kill male offspring. Such bacteria will spread if male death benefits the female siblings who transmit the bacterium, and they are therefore expected in insects with antagonistic sibling interactions. We report that the butterfly Danaus chrysippus is host to a maternally inherited male-killing bacterium. Using diagnostic PCR and rDNA sequence, the bacterium was identified as a Spiroplasma closely related to 2 ladybird beetle male-killers and the tick symbiont Spiroplasma ixodetis. The male-killer was found to have a geographically restricted distribution, with up to 40% of females being infected in East Africa, but no detectable infection in small samples from other populations. Danaus chrysippus is a surprising host for a male-killer as its eggs are laid singly. This suggests that the ecological conditions permitting male-killers to invade may be more widespread than previously realized.

Animals↗
PubMed2000

Multiple causes of male-killing in a single sample of the two-spot ladybird, Adalia bipunctata (Coleoptera: coccinellidae) from Moscow.

Thirty-six matrilines from a single Muscovite sample of Adalia bipunctata were assayed, using appropriate primers, for presence of the four male-killing symbionts known to infect this species of ladybird. All four, a Rickettsia, a Spiroplasma and two different strains of Wolbachia, were found to be present. Vertical transmission efficiencies were assessed from F1 and F2 families from each of the matrilines, and were found to differ significantly between symbionts. Potential explanations of the presence of four different male-killing symbionts within a single population, are considered.

Animals↗
PubMed2000

Molecular evolution and phylogenetic utility of Wolbachia ftsZ and wsp gene sequences with special reference to the origin of male-killing.

A detailed assessment of the evolution and phylogenetic utility of two genes, ftsZ and wsp, was used to investigate the origin of male-killing Wolbachia, previously isolated from the ladybird Adalia bipunctata and the butterfly Acraea encedon. The analysis included almost all available sequences of B-group Wolbachia and two outgroup taxa and showed that (1) the two gene regions differ in phylogenetic utility, (2) sequence variation is here correlated with phylogenetic information content, (3) both genes show significant rate heterogeneity between lineages, (4) increased substitution rates are associated with homoplasy in the data, (5) wsp sequences of some taxa appear to be subject to positive selection, and (6) only a limited number of clades can be inferred with confidence due to either lack of phylogenetic information or the presence of homoplasy. With respect to the evolution of male-killing, the two genes nevertheless seemed to provide unbiased information. However, they consistently produce contradictory results. Current data therefore do not permit clarification of the origin of this behavior. In addition, A. bipunctata was found to be a host to two recently diverged strains of male-killing Wolbachia that showed increased substitution rates for both genes. Moreover, the wsp gene, which codes for an outer membrane protein, was found to be subject to positive selection in these taxa. These findings were postulated to be the product of high selection pressures due to antagonistic host-symbiont interactions in this ladybird species. In conclusion, our study demonstrates that the results of a detailed phylogenetic analysis, including characterization of the limitations of such an approach, can serve as a valuable basis for an understanding of the evolution of Wolbachia bacteria. Moreover, particular features of gene evolution, such as elevated substitution rates or the presence of positive selection, may provide information about the dynamics of Wolbachia-host associations.

Bacterial Outer Membrane Proteins↗
PubMed1999

Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited flavobacteria that kill males only.

Inherited bacteria that parasitically distort the pattern of sex allocation of their host, biasing allocation towards female progeny, are found in many arthropods. One such manipulation is male-killing, where male progeny of infected females die during embryogenesis. We here provide evidence for a male-killing bacterium in the coccinellid beetle, Adonia variegata. We then address 3 questions. First, is this male-killing bacterium one that is found in other hosts, or does it represent a new transition to male-killing within the eubacteria? Using the sequence of the 16S rDNA of the bacterium, we found that the male-killing bacterium is a member of the Flavobacteria--Bacteroides group, most closely related to the male-killing bacterium in another ladybird beetle, Coleomegilla maculata. Secondly, is there any evidence that this bacterium affects female host physiology? In a paired test under nutritional stress, we found no evidence for a physiological benefit to infection, and weak evidence of a physiological cost, in terms of reduced fecundity. Thirdly, is there any evidence of host involvement in the transmission of the bacterium to the germ line? We found no evidence of host involvement. Rather, bacteria migrated to the ovariole independently of host cells. We conclude that the bacterium is a parasite, and discuss how 2 different species of ladybird come to be infected with 1 lineage of bacterium, and why case studies of male-killing bacteria have generally found little evidence of any symbiont contribution to host physiological functioning.

Animals↗
PubMed1999

Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria.

Male-killing bacteria, which are inherited through the female line and kill male progeny only, are known from five different orders of insect. Our knowledge of the incidence of these elements has stemmed from discovery of their phenotype in different species. Our estimate of the frequency with which insects have been invaded by these elements therefore depends on each observation of the male-killing phenotype within a species being associated with a single microorganism. We here record an example of a single insect species being infected with two taxonomically distinct male-killing bacteria. Western European populations of the two-spot ladybird, Adalia bipunctata, have previously been shown to bear a male-killing Rickettsia. However, we here show that the majority of the male-killing lines tested from Central and Eastern Europe do not bear this bacterium. Rather, 16S rDNA sequence analysis suggests male-killing is associated with a member of the genus Spiroplasma. We discuss this conclusion in relation to the evolutionary genetics of male-killing bacteria, and the evolution of male-killing behaviour in the eubacteria.

Animals↗
PubMed1999

[Sex ratio and male killing in Siberian populations of Harmonia axyridis (Pass.)].

In populations of Harmonia axyridis Pall. from Novosibirsk and Kyzyl, females (three out of 34 studied) that produce exclusively female progeny were found. In one of the families studied, the inheritance of the male-killing trait was monitored over five generations. The male-killing trait was maternally inherited. The beetles of this family were infected with the bacteria that, according to the sequence analysis of the gene fragment for 16S rRNA, belong to the genus Spiroplasma (VI group).

Animals↗
PubMed1996

Male-killing bacterium in a fifth ladybird beetle, Coleomegilla maculata (Coleoptera:Coccinellidae).

Inherited symbionts which selectively cause the death of male hosts are found widely across the Insecta. Previous studies have shown a single, but different micro-organism to be responsible for male-killing in each taxonomic group studied. We here produce evidence that within a group of insects, the Coccinellidae, there is more than one causal agent of male lethality. We report a novel observation of a male-killing trait in the species Coleomegilla maculata. Six of 26 crosses were found to produce a female-biased sex ratio associated with a low egg hatch-rate. The trait was matrilinearly inherited and was observed to be tetracycline-sensitive. However, tests which indicate the presence of a Rickettsia, previously found to cause male-killing in another member of the Coccinellidae, Adalia bipunctata, proved negative. We therefore conclude that the phenomenon of male-killing is multicausal, within, as well as between, taxonomic groups of the Insecta.

Animals↗
PubMed1994

Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata).

A cytoplasmically inherited microorganism associated with male killing in the two-spot ladybird beetle, Adalia bipunctata, is shown to be closely related to bacteria in the genus Rickettsia. Sequencing of a PCR-amplified product of the 16S genes coding for rRNA (16S rDNA) shows the organism associated with male killing in ladybirds to share a common ancestry with the Rickettsias relative to other genera (e.g., Anaplasma, Ehrlichia, and Cowdria). The rickettsial 16S rDNA product is found in four strains of ladybird beetle showing male embryo lethality and is absent from two uninfected strains and an antibiotic-cured strain. In addition, a revertant strain that had naturally lost the male-killing trait failed to amplify the rickettsial 16S rDNA product. Use of PCR primers for a 17-kDa protein antigen which is found only in rickettsias also resulted in an amplified product from infected strains. Uninfected, cured, and revertant strains and insect species infected with related bacteria (cytoplasmic-incompatibility bacteria from Nasonia wasps) failed to amplify the product. Discovery of a close relative of rickettsias associated with sex ratio distortion in insects has implications for the evolution and population dynamics of this bacterial genus.

Animals↗
PubMed1988

Frequency-dependent sexual selection.

Sexual selection by female choice is expected to give rise to a frequency-dependent sexual advantage in favour of preferred male phenotypes: the rarer the preferred phenotypes, the more often they are chosen as mates. This 'rare-male advantage' can maintain a polymorphism when two or more phenotypes are mated preferentially: each phenotype gains an advantage when it is rarer than the others; no preferred phenotype can then be lost from the population. Expression of preference may be complete or partial. In models of complete preference, females with a preference always mate preferentially. Models of partial preference are more realistic: in these models, the probability that a female mates preferentially depends on the frequency with which she encounters the males she prefers. Two different 'encounter models' of partial preference have been derived: the O'Donald model and the Charlesworth model. The encounter models contain the complete preference model as a limiting case. In this paper, the Charlesworth model is generalized to allow for female preference of more than one male phenotype. Levels of frequency dependence can then be compared in the O'Donald and Charlesworth models. The complete preference model and both encounter models are formulated in the same genetical terms of preferences for dominant and recessive male phenotypes. Polymorphic equilibria and conditions for stability are derived for each of the three models. The models are then fitted to data of frequencies of matings observed in experiments with the two-spot ladybird. The complete preference model gives as good a fit as the encounter models to the data of these and other experiments. The O'Donald and Charlesworth encounter models are shown to produce a very similar frequency-dependent relation. Generally, as females become less choosy, they express their preference with more dependence on male frequency, whereas the resulting selection of the males becomes less frequency dependent. More choosy females are more constant in expressing their preference, producing greater frequency dependence in the selection of the males.

Animals↗