Michael E. N. Majerus

Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid

Native to Asia, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is considered an invasive alien ladybird in Europe and North America, where it was widely introduced as a biological control agent of aphids and coccids. In Europe, H. axyridis was sold by various biological control companies from 1995 in France, Belgium and the Netherlands, and was also intentionally released in at least nine other countries. It has spread very rapidly, particularly since 2002, and is now regarded as established in thirteen European countries. The established range extends from Denmark in the north to southern France in the south, and from Czech Republic in the east to Great Britain in the west. In this paper we map the spread and distribution of H. axyridis in Europe, and examine the situation on a country-by-country basis. We report first records of the species in five countries; Spain, Sweden, Denmark, Czech Republic and Italy; and first evidence of H. axyridis establishment in the latter three countries. Despite releases of H. axyridis in Portugal, Spain and Greece, there is little evidence of establishment in southern Europe. It is predicted that the spread and increase within Europe will continue and that H. axyridis will become one of the most widely distributed coccinellids in the continent.

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.

Tri-trophic interactions involving pest aphids, predatory 2-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance

Transgenic crops genetically engineered for enhanced insect resistance should be compatible with other components of IPM for the pest resistance to be durable and effective. An experimental potato line was genetically engineered to express an anti-aphid plant protein (snowdrop lectin, GNA), and assessed for possible interactions of the insect resistance gene with a beneficial pest predator. These extended laboratory studies are the first to demonstrate adverse tri-trophic interactions involving a lectin- expressing transgenic crop, a target pest aphid and a beneficial aphidophagous predator. When adult 2-spot ladybirds (Adalia bipunctata[L.]) were fed for 12 days on peach-potato aphids (Myzus persicae Sulzer) colonising transgenic potatoes expressing GNA in leaves, ladybird fecundity, egg viability and longevity significantly decreased over the following 2–3 weeks. No acute toxicity due to the transgenic plants was observed, although female ladybird longevity was reduced by up to 51%. Adverse effects on ladybird reproduction, caused by eating peach-potato aphids from transgenic potatoes, were reversed after switching ladybirds to feeding on pea aphids from non-transgenic bean plants. These results demonstrate that expression of a lectin gene for insect resistance in a transgenic potato line can cause adverse effects to a predatory ladybird via aphids in its food chain. The significance of these potential ecological risks under field conditions need to be further evaluated.

Why do maternally inherited microorganisms kill males

Maternally-inherited male killing microorganisms are known in a number of insect species. We here discuss the evolutionary reasons for such behaviour through examining the ongoing dynamics of these elements. In cases where death occurs late in the life cycle, horizontal transmission associated with male death occurs but in others no such direct advantage to killing the individual appears to exist. The evidence that early male killing is analogous to primary sex ratio distortion through increasing the fitness with respect to producing females from increases in resources to surviving (female) offspring and through the prevention of inbreeding is discussed. The early life history of many of these species suggests an early resource advantage may accrue from male killing. Inbreeding avoidance appears to be an important factor in at least two cases. The potential for horizontal transmission to maintain these elements is also discussed. It is concluded that male killing appears to be an adaptive strategy for the microorganism in most cases.

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.

Sex ratio distortion in Acraea encedon (Lepidoptera: Nymphalidae) is caused by a male-killing bacterium

Females of the butterfly Acraea encedon produce either entirely female offspring or males and females in an almost 1:1 sex ratio. The sex ratio produced is maternally inherited and was previously attributed to sex chromosome meiotic drive. We report that all-female lineages are associated with low egg-hatching rates and that the trait is cured by antibiotic treatment. We thus reject the hypothesis that this sex ratio bias is caused by a meiotically driven sex chromosome and, instead, propose that it is associated with a maternally inherited bacterium that kills males.

Cytoplasmic male killing elements in Adalia bipunctata (Linnaeus) (Coleoptera: Coccinellidae)

A wild sample of Adalia bipunctata larvae and pupae were collected from Surrey, and F1 virgin adults mated. The sex ratio produced by these pairs was found be be variable, 22 pairs produced a sex ratio consistent with a 1:1 sex ratio, but four produced a strong female bias. Daughters and males from biased broods were mated to adults from non-biased broods of different parentage. Males and females from unrelated families were crossed. Where the female was taken from a biased clutch, the biased sex ratio trait recurred in a high proportion of cases. Where males from such broods were crossed, or females from broods with no history of bias were mated, sex ratios consistent with 1:1 were obtained. Pairs producing a strong female bias showed hatch rates which were approximately half that of crosses producing non-biased sex ratios. Treatment with tetracycline in golden syrup cured females who showed the biased sex ratio trait. Daughters conceived after this treatment produced normal sex ratios. Females fed purely on golden syrup, as a control, continued to produce female biased sex ratios until treated with tetracycline. We therefore suggest that an unknown bacterium, transmitted through egg cytoplasm but not sperm, is responsible for the early mortality of male embryos and thus a bias in the secondary sex ratio. The contribution that the study of the Coccinellidae can make to theories concerning the incidences and evolution of male killing elements is discussed in relation to egg cannibalism.

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

ABSTRACT 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 thatA. decempunctata harbors male-killingRickettsia (α-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 genusRickettsia. 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.

Extreme variation in the prevalence of inherited male-killing microorganisms between three populations of Harmonia axyridis (Coleoptera: Coccinellidae)

Females from three populations of Harmonia axyridis (Pallas) were assayed for two phenotypical indicators of the presence of male-killing endosymbionts: low egg hatch-rates and strongly female-biased progenic sex ratios. Samples from Sapporo City, Japan, and the Altai Mountains, Mongolia, but not from Novosibirsk, Russia, were found to contain some females displaying both of these traits. Furthermore, there was a profound difference in the prevalence of infection between the Japanese and Mongolian populations. The proportion of females infected from the Japanese sample was approximately 0.49, whereas that from Altai was only 0.02. The trait was inherited by more than 99% of the progeny of infected females. The trait was inherited maternally with the same high efficiency over five generations. Treatment with antibiotics produced a small increase in the production of males from the male-killing lines, suggesting that the male-killer is bacterial in nature. Causes of variation in prevalence are discussed, and the consequences of high levels of infection with an efficiently transmitted male-killing microorganism on host population demography are considered.

Evidence for preferential mating in Adalia bipunctata

SummaryNon-random mating may be involved in the maintenance of colour polymorphism in Adalia bipunctata. Mating choice experiments have been carried out on a stock of A. bipunctata from Keele. Specific frequencies of the melanic quadrimaculata form and the non-melanic typica form were placed in population cages or mating chambers and allowed to mate. The frequencies of the forms amongst mating pairs were scored. The results gave a good fit to a model of mixed sexual selection and assortative mating showing a strongly frequency dependent, non-assorting preference for quadrimaculata males in the matings. Data from the wild Keele population showed a similar preference for quadrimaculata males, and an excess of males of a second melanic phenotype, sexpustulata. Observation of courting pairs indicated that female choice determined frequency of mating. Field data from Keele also gave evidence of assortative mating between typica and another non-melanic form, annulata.