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

Hurst, Gregory D. D.; Majerus, Michael E. N.; Walker, Linda E.

doi:10.1111/j.1095-8312.1993.tb00898.x

Cited by 38 publications

(15 citation statements)

References 9 publications

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“…The vertical transmission efficiency of the SR trait from mother to adult daughter, calculated as 1 - (the number of males produced divided by the number of females produced) [24], assessed from PF12, PF12.2-4, PF12.7, PF12.8, PF12.10 and the ten additional PF12 F 1 pairs was 0.998 (2 males in 878 progeny).…”

Section: Resultsmentioning

confidence: 99%

Discovery and identification of a male-killing agent in the Japanese ladybird Propylea japonica (Coleoptera: Coccinellidae)

Majerus

2010

BMC Evol Biol

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BackgroundEndosymbionts that manipulate the reproduction of their hosts have been reported widely in invertebrates. One such group of endosymbionts is the male-killers. To date all male-killers reported are bacterial in nature, but comprise a diverse group. Ladybirds have been described as a model system for the study of male-killing, which has been reported in multiple species from widespread geographic locations. Whilst criteria of low egg hatch-rate and female-biased progenic sex ratio have been used to identify female hosts of male-killers, variation in vertical transmission efficiency and host genetic factors may result in variation in these phenotypic indicators of male-killer presence. Molecular identification of bacteria and screening for bacterial presence provide us with a more accurate method than breeding data alone to link the presence of the bacteria to the male-killing phenotype. In addition, by identifying the bacteria responsible we may find evidence for horizontal transfer between endosymbiont hosts and can gain insight into the evolutionary origins of male-killing. Phylogenetic placement of male-killing bacteria will allow us to address the question of whether male-killing is a potential strategy for only some, or all, maternally inherited bacteria. Together, phenotypic and molecular characterisation of male-killers will allow a deeper insight into the interactions between host and endosymbiont, which ultimately may lead to an understanding of how male-killers identify and kill male-hosts.ResultsA male-killer was detected in the Japanese coccinellid, Propylea japonica (Thunberg) a species not previously known to harbour male-killers. Families produced by female P. japonica showed significantly female-biased sex ratios. One female produced only daughters. This male-killer trait was maternally inherited and antibiotic treatment produced a full, heritable cure. Molecular analysis identified Rickettsia to be associated with the trait in this species of ladybird.ConclusionWe conclude that P. japonica is host to a bacterial male-killer that is vertically inherited with variable transmission efficiency. Rickettsia presence correlates with the male-killing trait, but there is some variation in the phenotypic expression of the trait due to interaction with host factors. Phylogenetic analysis using the 16S rRNA and 17 kDa antigen genes suggests there may have been horizontal transfer of Rickettsial male-killers between different ladybird hosts.

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Section: Resultsmentioning

confidence: 99%

Discovery and identification of a male-killing agent in the Japanese ladybird Propylea japonica (Coleoptera: Coccinellidae)

Majerus

2010

BMC Evol Biol

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“…The two host taxa show similarly low levels of infection with male-killing Rickettsia spp. (18,20,28). Such low levels seem to be required for long-term persistence of associations between male killers and hosts (13).…”

Section: Discussionmentioning

confidence: 99%

Incidence of Male-KillingRickettsiaspp. (α-Proteobacteria) in the Ten-Spot Ladybird BeetleAdalia decempunctataL. (Coleoptera: Coccinellidae)

Schulenburg

Habig

Sloggett

et al. 2001

Appl Environ Microbiol

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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 (␣-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.

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“…Although male killers with perfect maternal inheritance do obtain very high prevalence (.80% of females infected) (Jiggins et al 2002;Dyson and Hurst 2004), imperfect maternal inheritance combined with modest benefits of male killing (and a lack of other benefits to female hosts) is associated with low prevalence. In many cases, male killers exist in ,20% of female hosts (Williamson and Poulson 1979;Hurst et al 1993Hurst et al , 2000. At this prevalence, they may still create strong selection against their action, but ecological impacts are more limited.…”

Section: Embryonic Male Killingmentioning

confidence: 99%

Reproductive Parasitism: Maternally Inherited Symbionts in a Biparental World

Hurst

Frost

2015

Cold Spring Harb Perspect Biol

133

159

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Most species of insect, and many other plants and animals, carry maternally heritable microorganisms-viruses, bacteria, unicellular eukaryotes, and fungi that pass from a female host to her progeny. Maternal inheritance establishes a correlation between the fitness of symbiont and host female, which can select for the symbiont to contribute to host fitness. Nevertheless, its lack of transmission through male hosts places the symbiont in conflict with biparentally inherited nuclear genes. In this review, we first examine how this conflict is manifest in selection to promote the production and survival of infected female hosts and gametes. We then examine how the distorted population sex ratios that they produce may affect host reproductive ecology, and thus the intensity of other conflicts associated with sexual reproduction. Finally, we examine evolved host responses to symbiont manipulation. We argue that the unusual intensity of symbiont-host conflict generates extreme selection pressures that can drive changes in sex-determination systems, the basic pathway through which males and females are constructed.

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

Cited by 38 publications

References 9 publications

Discovery and identification of a male-killing agent in the Japanese ladybird Propylea japonica (Coleoptera: Coccinellidae)

Discovery and identification of a male-killing agent in the Japanese ladybird Propylea japonica (Coleoptera: Coccinellidae)

Incidence of Male-KillingRickettsiaspp. (α-Proteobacteria) in the Ten-Spot Ladybird BeetleAdalia decempunctataL. (Coleoptera: Coccinellidae)

Reproductive Parasitism: Maternally Inherited Symbionts in a Biparental World

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