Biology subjects

Kageyama, D.

Publications and source records attributed to Kageyama, D..

10 recordsLinked to original sources

bioRxiv2026

The rise and fall of feminizing Wolbachia in a butterfly

In sexually reproducing animals, sex ratios generally evolve toward parity1 but can be distorted by selfish genetic elements, including sex chromosome-linked meiotic drivers and cytoplasmically inherited symbionts such as Wolbachia2. We previously documented the rapid spread of the feminizing Wolbachia strain wFem in an island population of the butterfly Eurema hecabe3. Within just four years, the proportion of females increased from approximately 50% in 2015-2018 to 93.1% in 2022. Here, continued monitoring of the same population revealed an equally striking reversal: the sex ratio returned to near parity in 2024-2025, accompanied by a sharp decline in the frequency of wFem. These observations suggest that host-symbiont conflict can drive major shifts in population sex ratio over remarkably short timescales.

evolutionary biology↗

bioRxiv2025

Concerted genome expansion of heritable symbionts in an insect host

Maternally transmitted symbionts represent important components of arthropod biology, acting as both beneficial partners and as reproductive parasites. Their strict vertical transmission greatly reduces their effective population size, making selection less efficient and driving a pattern of molecular evolution where genome size reduces. Contrastingly, there are sporadic observations of genome expansion in symbionts from clades where the genome has previously reduced in size. It is currently unclear whether these events are an idiosyncratic consequence of exposure to novel active mobile elements, or are driven by the host context. In this paper, we report the concerted genome expansion of two co-infecting heritable symbionts that supports a host-related driver of expansion. We assembled the genomes of Spiroplasma and Rickettsia bacteria that co-infect the lacewing Mallada desjardinsi. Both symbionts had the largest genome reported to date in their clade, approximately twice the median size for their respective genus. Genome expansion was driven by proliferation of mobile elements in both cases, but the underpinning elements were distinct. The observation that the proximate causes of expansion differed between symbionts led us to reject the hypothesis that concerted expansion was driven by a common mobile element invasion. We hypothesize these processes are driven either by bottleneck events impacting host population size, by the host environment causing stress-induced activation of mobile genetic elements, or by both symbionts having undergone a recent and coincident transition to vertical transmission.

genomics↗

bioRxiv2025

Evolution of Wolbachia male-killing mechanism within a host species

Male-killing bacterial symbionts, prevalent in arthropods, skew population sex ratios by selectively killing male progeny, profoundly impacting ecology and evolution of their hosts. Male-killing is a convergently evolved trait, with microbes evolving diverse male-killing mechanisms across host species with widely divergent sex determination pathways. A common evolutionary response to MK presence is the spread of suppressor mutations that restore male survival. In this study, we demonstrate evolution of a novel male-killing mechanism that is insensitive to an existing male-killing suppressor. Hypolimnas bolina butterflies from Yogyakarta, Indonesia, showed extreme female biased population sex ratio associated with high prevalence of a male-killing Wolbachia. This strain, wBol1Y, shared a very recent common ancestor with the previously characterized suppressed male-killing strain in the species, wBol1, but retained its male-killing ability in the presence of the male-killing suppressor. The genome of wBol1Y differed from the suppressed wBol1 in carrying an additional prophage that included strong candidate genes for male-killing. In vitro and in vivo data demonstrated that wBol1Y feminized splicing and expression of lepidopteran sex determination pathway genes, and that the gene Hb-oscar - present on wBol1Ys unique prophage insert - was sufficient to disrupt the male sex determination pathway. Our study demonstrates the diversity of male-killing mechanisms is a product both of interaction with varying insect sex determination systems and evolution of male-killing within a host species. Our data indicate male-killer and host may be involved in escalating arms races, where spread male-killing suppression drives evolution of additional systems that reestablish male killing by the symbiont.

evolutionary biology↗

bioRxiv2024

Variable prevalence of protective Spiroplasma infection over time in two natural populations of Drosophila hydei

The temporal dynamics of protective symbionts have rarely been characterized outside of aphid hosts. Here, we determine the prevalence of Spiroplasma in two populations of D. hydei where Spiroplasma infection had been previously recorded (UK and Japan). We observe that infection in both populations is variable over time and confirm the persistence of Spiroplasma in the UK population for 9 years. Thus, variable prevalence over time appears to be a common feature of these symbioses.

ecology↗

bioRxiv2024

Prophage-encoded Hm-oscar gene recapitulates Wolbachia-induced male killing in the tea tortrix moth Homona magnanima

Wolbachia are maternally transmitted bacterial symbionts that are ubiquitous among arthropods. They can hijack host reproduction in various ways, including male killing (MK), where the sons of infected mothers are killed during development. The recent discovery of MK-associated Wolbachia genes, i.e., oscar in Ostrinia moths and wmk in Drosophila flies, stimulates our interest in the diversity and commonality of MK mechanisms, which remain largely unclear. We recently discovered that a Wolbachia symbiont of the moth Homona magnanima carries an MK-associated prophage region encoding homologs of oscar (Hm-oscar) and wmk (wmk-1-4). Here, we investigated the effects of these genes in the native host. Upon transient overexpression, Hm-oscar, but not wmk, induced male lethality in H. magnanima, in contrast to our observations in Drosophila, where the wmk homologs, but not Hm-oscar, killed the males. Hm-oscar disrupted sex determination in male embryos by inducing a female-type doublesex splicing and impaired dosage compensation, recapitulating the Wolbachia phenotype. Cell-based transfection assays confirmed that Hm-oscar suppressed the function of masculinizer, the primary male sex determinant involved in lepidopteran dosage compensation. Our study highlights the conserved roles of oscar homologs in Wolbachia-induced lepidopteran MK and argues that Wolbachia have evolved multiple MK mechanisms in insects.

evolutionary biology↗

bioRxiv2024

Rapid spread of a vertically transmitted symbiont induces drastic shifts in butterfly sex ratio

BRIEF SUMMARYSex ratio dynamics constitutes a pivotal subject in evolutionary biology1. Under conditions of evolutionary equilibrium, the male-to-female ratio tends to be approximately 1:1; however, this equilibrium is susceptible to distortion by selfish genetic elements exemplified by driving sex chromosomes and cytoplasmic elements2,3. While previous studies have substantiated instances of these genetic elements distorting the sex ratio, studies specifically tracking the process with which these distorters spread within populations, leading to a transition from balanced parity to a skewed, female-biased state, are notably lacking. Herein, we present compelling substantiation regarding the rapid spread of the cytoplasmic endosymbiont Wolbachia within a localized population of the pierid butterfly Eurema hecabe (Figure 1A). This resulted in a shift in the sex ratio from near parity to an exceedingly skewed state overwhelmingly biased toward females, reaching 94.4% within a remarkably brief period of 4 years.

evolutionary biology↗

bioRxiv2024

Cell-based assays and comparative genomics revealed the conserved and hidden effects of Wolbachia on insect sex determination

It is advantageous for maternally transmitted endosymbionts to skew the sex ratio of their hosts toward females. Some endosymbiotic bacteria such as Wolbachia cause their insect hosts to exclusively produce female offspring through male killing or feminization. In some lepidopteran insects, male killing is achieved by affecting the sex-determining process in males, and a unique mechanism of male killing and its functional link with feminization have been implicated. However, comparative analysis of these phenotypes is often difficult because they have been analyzed in different host-symbiont systems and transinfection of Wolbachia across different hosts is often challenging. In this study, we demonstrated the effects of nine Wolbachia strains on the splicing of sex-determining genes in Lepidoptera by fixing the host genetic background using a cell culture system. Cell transinfection assays confirmed that three male killing-inducing Wolbachia strains and one feminization-inducing Wolbachia strain increased the female-type splicing products of the core sex-determining genes doublesex, masculinizer, and zinc finger protein 2. Regarding Wolbachia strains that do not induce male killing/feminization, three had no effect on these sex-determining genes, whereas two strains induced female-type splicing of masculinizer and doublesex but not zinc finger protein 2. Comparative genomics confirmed that homologs of oscar, the Wolbachia gene responsible for male killing in Ostrinia, were encoded by male killing/feminizing Wolbachia strains, but not by non-male killing/non-feminizing strains. These results demonstrated the conserved effects underlying male killing and feminization induced by oscar-bearing Wolbachia, and suggested other potential mechanisms that Wolbachia might employ to manipulate host sex. IMPORTANCEArthropods commonly carry maternally transmitted microbial symbionts such as Wolbachia. The lack of paternal transmission frequently led to the evolution of reproductive parasitism traits, namely the manipulation of host reproduction in favor of female hosts, substantiated by male killing and feminization. Although Wolbachia induces these phenotypes in a wide range of insects, the underlying mechanisms, diversity, and commonality remain largely unclear. In this study, we used a combination of transinfection assays and comparative genomics to reveal the conserved effects of male killing and feminizing Wolbachia strains on lepidopteran sex determination. Furthermore, we demonstrated that some non-male killing/non-feminizing Wolbachia strains also have an inherent ability to influence sex determination, albeit in a different manner, suggesting the potential for multiple mechanisms to manipulate host sex. This study also implied the frequent evolution of host suppressors against Wolbachia-induced reproductive manipulation.

microbiology↗

bioRxiv2022

Male-killing-associated bacteriophage WO identified from comparisons of Wolbachia endosymbionts of Homona magnanima

The origin and mechanism of male-killing, an advantageous strategy employed by maternally transmitted symbionts such as Wolbachia, remain unclear. We compared genomes of four Wolbachia strains derived from Homona magnanima, a male-killing strain wHm-t (1.5 Mb), and three non-male-killing strains, wHm-a (1.1 Mb), wHm-b (1.3 Mb), and wHm-c (1.4 Mb). A wHm-t-specific 76-kbp prophage region harboured two tandemly arrayed WO-mediated killing (wmk) gene homologs (wmk-1/wmk-2 and wmk-3/wmk-4). Of these, wmk-1 or wmk-3 killed almost all Drosophila melanogaster individuals when transgenically overexpressed. Dual expression of wmk-3 and wmk-4 killed all males and rescued females. We propose a novel hypothesis wherein horizontally transmitted proto-Wolbachia with a single wmk killed both sexes, and tandem duplication of wmk allowed an evolutionary transition to a vertically transmitted symbiont, causing male-killing. Our study highlights the bacteriophage as a critical driver of the evolution of male-killing and argues for a conserved male-killing mechanism in diverse insects.

evolutionary biology↗

bioRxiv2020

Persistence of a Wolbachia-driven sex ratio bias in an island population of Eurema butterflies

It is generally believed that when maternally inherited sex ratio distorters become predominant, either the host population goes extinct or nuclear suppressors evolve in the host. Here, we show an empirical case where all-female-producing Wolbachia is likely to be stably maintained at a high frequency. On an island population of the butterfly Eurema mandarina, a Wolbachia strain wFem, which makes female hosts produce all-female offspring without sibling lethality (female drive), is highly prevalent. We found that, with some fluctuations, wFem appeared to be stably maintained for at least 12 years at a high frequency, resulting in the existence of an abnormally high number of virgin females. Interestingly, comparison between sex ratios of captive individuals and sex ratios deduced from wFem frequencies suggested a plastic behavioral change of males and females in response to the shift of sex ratios. wFem presence does not affect brood size but has a slightly negative effect on body size. Stable coexistence of wFem-positive and -negative females in the population may be explained via mate choice by males, which keeps wFem in check. Taken together, this butterfly population is an attractive model for future studies on the population dynamics of sex ratios and mating behavior.

evolutionary biology↗

bioRxiv2017

Master manipulation continued: feminizing Wolbachia endosymbiont distorts sex chromosome inheritance

Genomes are vulnerable to selfish genetic elements that enhance their own transmission often at the expense of host fitness. Examples are cytoplasmic elements such as maternally inherited bacteria that cause feminization, male-killing, parthenogenesis and cytoplasmic incompatibility. We demonstrate, for the first time, that segregation distortion, a phenomenon so far seen only for nuclear genetic elements, can also be caused by a cytoplasmic element, the ubiquitous endosymbiotic bacterium Wolbachia. For Eurema mandarina butterfly lineages with a Z0 sex chromosome constitution, we provide direct and conclusive evidence that Wolbachia induces production of all-female progeny by a dual role: the compensation for the female-determining function that is absent in Z0 lineages (feminization) and the prevention of maternal sex chromosome inheritance to offspring as a specific type of segregation distortion. Therefore, our findings highlight that both sex determination and chromosome inheritance -- crucially important developmental processes of higher eukaryotes -- can be manipulated by cytoplasmic parasites.

evolutionary biology↗