Uncovering the hidden players in Lepidoptera biology: the heritable microbial endosymbionts

Abstract

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 both moths and butterflies. We also reveal that the vast majority of research undertaken of Lepidopteran endosymbionts concerns Wolbachia. While this highly prevalent bacteria 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.

Gut microbiota metabolic potential correlates with body size between mulberry‐feeding lepidopteran pest species

“…44 Moreover, the existence of endosymbionts indicates strict vertical transmission of certain bacteria within host lineages. 46 Despite the strong taxonomic variability, we found that the metabolic potential of gut prokaryotic communities, in terms of the relative abundances of proxy genes, was similar among caterpillars and was possibly dependent on body size. Currently, there are only three shotgun sequencing-based gut metagenomes for Lepidopteran insects.…”

“…Species differences in host physiology and local gut environment, such as pH, oxygen levels and redox conditions, can contribute to variation in microbiotas . Moreover, the existence of endosymbionts indicates strict vertical transmission of certain bacteria within host lineages …”

The microbiome of theMelitaea cinxiabutterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant

“…As recently reported, only 16.3% of the Lepidopteran caterpillars are infected by Wolbachia with different impacts of the endosymbiotic bacteria on the reproduction and the sex ratio of their host e.g. male killing, feminization and cytoplasmic incompatibility (Duplouy and Hornett, ).…”

Variation inMelitaea cinxiagut microbiota is phylogenetically highly structured but only mildly driven by host plant microbiota, sex or parasitism

“…As recently reported only 16.3% of the Lepidopteran 333 caterpillars are infected by Wolbachia with different impacts of the endosymbiotic bacteria 334on the reproduction and the sex ratio of their host e.g. male killing, feminization, and 335 cytoplasmic incompatibility(Duplouy and Hornett, 2018). 336 337Effects of host plant's microbiota and metabolite composition 338The microbiome of plant phyllosphere is partially conserved across species with presence 339 of recurrent taxa such as Methylobacterium, Pseudomonas and Sphyngobium(Delmotte et 340 al., 2009).…”