Silence of the killers: discovery of male-killing suppression in a rearing strain of the small brown planthopper, Laodelphax striatellus

According to evolutionary theory, sex ratio distortions caused by reproductive parasites such as Wolbachia and Spiroplasma are predicted to be rapidly normalized by the emergence of host nuclear suppressors. However, such processes in the evolutionary arms race are difficult to observe because sex ratio biases will be promptly hidden and become superficially unrecognizable. The evolution of genetic suppressors has been reported in just two insect species so far. In the small brown planthopper, Laodelphax striatellus , female-biases caused by Spiroplasma , which is a ‘late’ male-killer, have been found in some populations. During the continuous rearing of L. striatellus , we noted that a rearing strain had a 1 : 1 sex ratio even though it harboured Spiroplasma . Through introgression crossing experiments with a strain lacking suppressors, we revealed that the L. striatellus strain had the zygotic male-killing suppressor acting as a dominant trait. The male-killing phenotype was hidden by the suppressor even though Spiroplasma retained its male-killing ability. This is the first study to demonstrate the existence of a late male-killing suppressor and its mode of inheritance. Our results, together with those of previous studies, suggest that the inheritance modes of male-killing suppressors are similar regardless of insect order or early or late male killing.

Circulating inhibin and testosterone during sexual maturation and reproductive seasonality of captive male killer whales (Orcinus orca)

The present study aimed to investigate the reproductive biology of male killer whales. Changes in the concentrations of two circulating testicular hormones, inhibin and testosterone, were monitored during sexual maturation of two male Type 1 Eastern Northern Atlantic killer whales over a period of 20 years. The two killer whales grew rapidly at the pubertal stage and reached a plateau at the age of 23 and 20 years, respectively, after which growth slowed down. In the younger male, circulating inhibin was higher in the juvenile than in the pubertal and mature stages; whereas circulating testosterone exhibited the opposite trend. The pubertal period was estimated to last approximately 5 years, from 12 to 17 years of age. In the elder male, circulating testosterone was high from the onset of this study (12 years of age), when the animal also sired successfully for the first time. This finding shows that the male killer whale is possible to sire even if it is not socially matured, if there is opportunity for copulation. During the mature stage, both animals exhibited significantly higher circulating testosterone concentrations in spring compared to autumn and winter; whereas no seasonal change was observed for circulating inhibin. These results clearly demonstrate that the male killer whale is a seasonal breeder, even though it is fertile throughout the year. This is the first study to elucidate the inhibin concentration and secretory source in the male killer whale.

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

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.

Maternally transmitted non-bacterial male killer in Drosophila biauraria

A maternally inherited, all-female trait is widely found among arthropods, which is caused by bacterial endosymbionts such as Wolbachia , Rickettsia , Spiroplasma and Cardinium . We discovered a single female of Drosophila biauraria, collected from Tomakomai, Hokkaido, Japan, that produced all-female offspring. This all-female trait was maternally inherited in the iso-female line (SP12F) by backcrossing with males of a normal line (SP11-20) with a 1 : 1 sex ratio derived from the same population. The all-female trait was not affected by tetracycline treatment performed for two consecutive generations. However, the microinjection of filter-sterilized homogenate of SP12F females into SP11-20 females established all-female matrilines. Our data suggest the role of transmissible agents, most likely viruses, but not bacteria or protists, as the possible cause of the all-female phenotype, which is likely to be achieved by killing of male embryos because egg hatch rates of SP12F were nearly half those of SP11-20. This is the first report in Diptera to demonstrate a maternally inherited virus-like element as the cause of the male-killing phenotype in D. biauraria .

A neo-W chromosome in a tropical butterfly links colour pattern, male-killing, and speciation

Sexually antagonistic selection can drive both the evolution of sex chromosomes and speciation itself. The tropical butterfly the African Queen, Danaus chrysippus , shows two such sexually antagonistic phenotypes, the first being sex-linked colour pattern, the second, susceptibility to a male-killing, maternally inherited mollicute, Spiroplasma ixodeti , which causes approximately 100% mortality in male eggs and first instar larvae. Importantly, this mortality is not affected by the infection status of the male parent and the horizontal transmission of Spiroplasma is unknown. In East Africa, male-killing of the Queen is prevalent in a narrow hybrid zone centred on Nairobi. This hybrid zone separates otherwise allopatric subspecies with different colour patterns. Here we show that a neo-W chromosome, a fusion between the W (female) chromosome and an autosome that controls both colour pattern and male-killing, links the two phenotypes thereby driving speciation across the hybrid zone. Studies of the population genetics of the neo-W around Nairobi show that the interaction between colour pattern and male-killer susceptibility restricts gene flow between two subspecies of D. chrysippus . Our results demonstrate how a complex interplay between sex, colour pattern, male-killing, and a neo-W chromosome, has set up a genetic ‘sink' that keeps the two subspecies apart. The association between the neo-W and male-killing thus provides a ‘smoking gun' for an ongoing speciation process.