Male-killing bacteria are widespread in arthropods, and can profoundly alter the reproductive biology of their host species. Here we detail the first case of complete suppression of a male killer. ...The nymphalid butterfly Hypolimnas bolina is infected with a strain of the bacterium Wolbachia, wBol1, which kills male host embryos in Polynesian populations, but does not do so in many areas of Southeast Asia, where both males and female adults are naturally infected, and wBol1-infected females produce a 1:1 sex ratio. We demonstrate that absence of male killing by wBol1 is associated with dominant zygotic suppression of the action of the male killer. Simulations demonstrate host suppressors of male-killer action can spread very rapidly, and historical data indicating the presence of male killing in Southeast Asia in the very recent past suggests suppressor spread has been a very recent occurrence. Thus, male killer/host interactions are much more dynamic than previously recognised, with rapid and dramatic loss of the phenotype. Our results also indicate that suppression can render male killers completely quiescent, leading to the conclusion that some species that do not currently express a male killer may have done so in the past, and thus that more species have had their biology affected by these parasites than previously believed.
Models estimate that up to 80% of all butterfly and moth species host vertically transmitted endosymbiotic microorganisms, which can affect the host fitness, metabolism, reproduction, population ...dynamics, and genetic diversity, among others. The supporting empirical data are however currently highly biased towards the generally more colourful butterflies, and include less information about moths. Additionally, studies of symbiotic partners of Lepidoptera predominantly focus on the common bacterium Wolbachia pipientis, while infections by other inherited microbial partners have more rarely been investigated. Here, we mine the whole genome sequence data of 47 species of Erebidae moths, with the aims to both inform on the diversity of symbionts potentially associated with this Lepidoptera group, and discuss the potential of metagenomic approaches to inform on host associated microbiome diversity. Based on the result of Kraken2 and MetaPhlAn2 analyses, we found clear evidence of the presence of Wolbachia in four species. Our result also suggests the presence of three other bacterial symbionts (Burkholderia spp., Sodalis spp. and Arsenophonus spp.) in three other moth species. Additionally, we recovered genomic material from bracovirus in about half of our samples. The detection of the latter, usually found in mutualistic association to braconid parasitoid wasps, may inform on host-parasite interactions that take place in the natural habitat of the Erebidae moths, suggesting either contamination with material from species of the host community network, or horizontal transfer of members of the microbiome between interacting species.
Maternally inherited bacterial symbionts are extremely widespread in insects. They owe their success to their ability to promote their own transmission through various manipulations of their hosts' ...life-histories. Many symbionts however very often go undetected. Consequently, we have only a restricted idea of the true symbiont diversity in insects, which may hinder our understanding of even bigger questions in the field such as the evolution or establishment of symbiosis. In this study, we screened publicly available Lepidoptera genomic material for two of the most common insect endosymbionts, namely Wolbachia and Spiroplasma, in 1904 entries, encompassing 106 distinct species. We compared the performance of two screening software, Kraken2 and MetaPhlAn2, to identify the bacterial infections and using a baiting approach we reconstruct endosymbiont genome assemblies. Of the 106 species screened, 20 (19%) and nine (8.5%) were found to be infected with either Wolbachia or Spiroplasma, respectively. Construction of partial symbiotic genomes and phylogenetic analyses suggested the Wolbachia strains from the supergroup B were the most prevalent type of symbionts, while Spiroplasma infections were scarce in the Lepidoptera species screened here. Our results indicate that many of the host-symbiont associations remain largely unexplored, with the majority of associations we identify never being recorded before. This highlights the usefulness of public databases to explore the hidden diversity of symbiotic entities, allowing the development of hypotheses regarding host-symbiont associations. The ever-expanding genomic databases provide a diverse databank from which one can characterize and explore the true diversity of symbiotic entities.
Success and impact metrics in science are based on a system that perpetuates sexist and racist “rewards” by prioritizing citations and impact factors. These metrics are flawed and biased against ...already marginalized groups and fail to accurately capture the breadth of individuals’ meaningful scientific impacts. We advocate shifting this outdated value system to advance science through principles of justice, equity, diversity, and inclusion. We outline pathways for a paradigm shift in scientific values based on multidimensional mentorship and promoting mentee well-being. These actions will require collective efforts supported by academic leaders and administrators to drive essential systemic change.
The Lepidoptera is one of the most widespread and recognisable insect orders. Due to their remarkable diversity, economic and ecological importance, moths and butterflies have been studied ...extensively over the last 200 years. More recently, the relationship between Lepidoptera and their heritable microbial endosymbionts has received increasing attention. Heritable endosymbionts reside within the host's body and are often, but not exclusively, inherited through the female line. Advancements in molecular genetics have revealed that host-associated microbes are both extremely prevalent among arthropods and highly diverse. Furthermore, heritable endosymbionts have been repeatedly demonstrated to play an integral role in many aspects of host biology, particularly host reproduction. Here, we review the major findings of research of heritable microbial endosymbionts of butterflies and moths. We promote the Lepidoptera as important models in the study of reproductive manipulations employed by heritable endosymbionts, with the mechanisms underlying male-killing and feminisation currently being elucidated in moths and butterflies. We also reveal that the vast majority of research undertaken of Lepidopteran endosymbionts concerns
. While this highly prevalent bacterium is undoubtedly important, studies should move towards investigating the presence of other, and interacting endosymbionts, and we discuss the merits of examining the microbiome of Lepidoptera to this end. We finally consider the importance of understanding the influence of endosymbionts under global environmental change and when planning conservation management of endangered Lepidoptera species.
Maternally inherited parasites are known to impose a wide variety of reproductive manipulations upon their host. These often produce strong selection on the host to suppress the parasite, resulting ...in a reduction in the frequency of the parasite. However, in the butterfly Hypolimnas bolina, infected with a Wolbachia bacterium, field data demonstrate that suppression of the male-killing phenotype does not depress parasite frequency. Here we test and verify one hypothesis to explain this apparent paradox—Wolbachia induces a second phenotype, Cytoplasmic Incompatibility (CI), in populations where host suppression has evolved. We further demonstrate that the capacity to induce CI has not evolved de novo, but instead is instantaneously expressed upon the survival of infected males. The significance of these results is threefold: (1) multiple phenotypes can provide Wolbachia with the means to maintain itself in a host following suppression of a single manipulative phenotype; (2) the ability to induce CI can remain hidden in systems in which male-killing is observed, just as the ability to induce male-killing may be obscured in strains exhibiting CI; (3) the evolutionary maintenance of CI in a system in which it is not expressed suggests a functional link with male-killing or other traits under selection.
Plant tissues often lack essential nutritive elements and may contain a range of secondary toxic compounds. As nutritional imbalance in food intake may affect the performances of herbivores, the ...latter have evolved a variety of physiological mechanisms to cope with the challenges of digesting their plant‐based diet. Some of these strategies involve living in association with symbiotic microbes that promote the digestion and detoxification of plant compounds or supply their host with essential nutrients missing from the plant diet. In Lepidoptera, a growing body of evidence has, however, recently challenged the idea that herbivores are nutritionally dependent on their gut microbial community. It is suggested that many of the herbivorous Lepidopteran species may not host a resident microbial community, but rather a transient one, acquired from their environment and diet. Studies directly testing these hypotheses are however scarce and come from an even more limited number of species.
By coupling comparative metabarcoding, immune gene expression, and metabolomics analyses with experimental manipulation of the gut microbial community of prediapause larvae of the Glanville fritillary butterfly (Melitaea cinxia, L.), we tested whether the gut microbial community supports early larval growth and survival, or modulates metabolism or immunity during early stages of development.
We successfully altered this microbiota through antibiotic treatments and consecutively restored it through fecal transplants from conspecifics. Our study suggests that although the microbiota is involved in the up‐regulation of an antimicrobial peptide, it did not affect the life history traits or the metabolism of early instars larvae.
This study confirms the poor impact of the microbiota on diverse life history traits of yet another Lepidoptera species. However, it also suggests that potential eco‐evolutionary host‐symbiont strategies that take place in the gut of herbivorous butterfly hosts might have been disregarded, particularly how the microbiota may affect the host immune system homeostasis.
Our study showed that the microbiota within the gut of Lepidoptera could efficiently be altered by antibiotic treatment and restored either by fecal transplants or self‐resilience after antibiotic relaxation. The dominant species of the gut bacterial community of the larvae did not impact larval performances and metabolism, but rather significantly impacted the host immunity by up‐regulating the expression of a gene involved in the response against pathogens.
Phylogenetically closely related strains of maternally inherited endosymbiotic bacteria are often found in phylogenetically divergent, and geographically distant insect host species. The interspecies ...transfer of the symbiont Wolbachia has been thought to have occurred repeatedly, facilitating its observed global pandemic. Few ecological interactions have been proposed as potential routes for the horizontal transfer of Wolbachia within natural insect communities. These routes are however likely to act only at the local scale, but how they may support the global distribution of some Wolbachia strains remains unclear.
Here, we characterize the Wolbachia diversity in butterflies from the tropical forest regions of central Africa to discuss transfer at both local and global scales. We show that numerous species from both the Mylothris (family Pieridae) and Bicyclus (family Nymphalidae) butterfly genera are infected with similar Wolbachia strains, despite only minor interclade contacts across the life cycles of the species within their partially overlapping ecological niches. The phylogenetic distance and differences in resource use between these genera rule out the role of ancestry, hybridization, and shared host-plants in the interspecies transfer of the symbiont. Furthermore, we could not identify any shared ecological factors to explain the presence of the strains in other arthropod species from other habitats, or even ecoregions.
Only the systematic surveys of the Wolbachia strains from entire species communities may offer the material currently lacking for understanding how Wolbachia may transfer between highly different and unrelated hosts, as well as across environmental scales.
Previous studies have reported that chromosome synteny in Lepidoptera has been well conserved, yet the number of haploid chromosomes varies widely from 5 to 223. Here we report the genome (393 Mb) of ...the Glanville fritillary butterfly (Melitaea cinxia; Nymphalidae), a widely recognized model species in metapopulation biology and eco-evolutionary research, which has the putative ancestral karyotype of n=31. Using a phylogenetic analyses of Nymphalidae and of other Lepidoptera, combined with orthologue-level comparisons of chromosomes, we conclude that the ancestral lepidopteran karyotype has been n=31 for at least 140 My. We show that fusion chromosomes have retained the ancestral chromosome segments and very few rearrangements have occurred across the fusion sites. The same, shortest ancestral chromosomes have independently participated in fusion events in species with smaller karyotypes. The short chromosomes have higher rearrangement rate than long ones. These characteristics highlight distinctive features of the evolutionary dynamics of butterflies and moths.
The maternally transmitted bacterium Wolbachia pipientis is well known for spreading and persisting in insect populations through manipulation of the fitness of its host. Here, we identify three new ...Wolbachia pipientis strains, wHho, wHho2 and wHho3, infecting Hyposoter horticola, a specialist wasp parasitoid of the Glanville fritillary butterfly. The wHho strain (ST435) infects about 50% of the individuals in the Åland islands in Finland, with a different infection rate in the two mitochondrial (COI) haplotypes of the wasp. The vertical transmission rate of Wolbachia is imperfect, and lower in the haplotype with lower infection rate, suggesting a fitness trade-off. We found no association of the wHho infection with fecundity, longevity or dispersal ability of the parasitoid host. However, preliminary results convey spatial associations between Wolbachia infection, host mitochondrial haplotype and parasitism of H. horticola by its hyperparasitoid, Mesochorus cf. stigmaticus. We discuss the possibility that Wolbachia infection protects H. horticola against hyperparasitism.
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