No evidence that gut microbiota impose a net cost on their butterfly host

Abstract

Gut microbes are believed to play a critical role in most animal life, yet fitness effects and cost–benefit trade‐offs incurred by the host are poorly understood. Unlike most hosts studied to date, butterflies largely acquire their nutrients from larval feeding, leaving relatively little opportunity for nutritive contributions by the adult's microbiota. This provides an opportunity to measure whether hosting gut microbiota comes at a net nutritional price. Because host and bacteria may compete for sugars, we hypothesized that gut flora would be nutritionally neutral to adult butterflies with plentiful food, but detrimental to semistarved hosts, especially when at high density. We held field‐caught adult Speyeria mormonia under abundant or restricted food conditions. Because antibiotic treatments did not generate consistent variation in their gut microbiota, we used interindividual variability in bacterial loads and operational taxonomic unit abundances to examine correlations between host fitness and the abdominal microbiota present upon natural death. We detected strikingly few relationships between microbial flora and host fitness. Neither total bacterial load nor the abundances of dominant bacterial taxa were related to butterfly fecundity, egg mass or egg chemical content. Increased abundance of a Commensalibacter species did correlate with longer host life span, while increased abundance of a Rhodococcus species correlated with shorter life span. Contrary to our expectations, these relationships were unchanged by food availability to the host and were unrelated to reproductive output. Our results suggest the butterfly microbiota comprises parasitic, commensal and beneficial taxa that together do not impose a net reproductive cost, even under caloric stress.

Cabbage looper (Trichoplusia ni Hübner) labial glands contain unique bacterial flora in contrast with their alimentary canal, mandibular glands, and Malpighian tubules

“…The two most abundant ASVs from the midgut and other organs, apparently belong to the genera Cloacibacterium and Diaphorobacter, members of which have been previously reported from insect gut microbiomes (Montagna et al, 2016;Ravenscraft, Kish, Peay, & Boggs, 2019). Interestingly, a Diaphorobacter isolate closely related to the ASV from our study was able to utilize the organophosphate insecticide Triazophos as its sole carbon source (Yang et al, 2011), suggesting the possibility that it could contribute to insecticide resistance.…”

“…In terms of the distribution of ASVs among phyla and families of bacteria, the alimentary canal bacteria of T. ni larvae feeding on collards appeared similar to other lepidopteran species (Jones et al, ; Paniagua Voirol, Frago, Kaltenpoth, Hilker, & Fatouros, ). The two most abundant ASVs from the midgut and other organs, apparently belong to the genera Cloacibacterium and Diaphorobacter , members of which have been previously reported from insect gut microbiomes (Montagna et al, ; Ravenscraft, Kish, Peay, & Boggs, ). Interestingly, a Diaphorobacter isolate closely related to the ASV from our study was able to utilize the organophosphate insecticide Triazophos as its sole carbon source (Yang et al, ), suggesting the possibility that it could contribute to insecticide resistance.…”

Heliconiusbutterflies host characteristic and phylogenetically structured adult-stage microbiomes

“…Other microbial roles in host nutrition are possible, although a recent experiment on the butterfly Speyeria mormonia did not find evidence for nutrition-related functions (79). We suggest that colonization resistance (i.e., protection from pathogens and parasites), which is a feature common to many symbioses (63,80), could be a primary ecological function of adult butterfly gut microbiomes.…”

Disrupting butterfly caterpillar microbiomes does not impact their survival and development

“…In many insects, gut microbes strongly influence adult foraging [47], fecundity [7], behaviour [48,49] and lifespan [6]. Butterfly adults may derive similar benefits from their microbiomes, although prior work on the microbiomes of wildcaught adult butterflies did not suggest strong host-microbial associations [16,20]. Overall, our results pose an interesting open question: have butterfly caterpillars occupied vastly different dietary niches without recourse to strong gut-bacterial associations, in contrast to the predominant dependence observed in other insects with similarly diverse diets?…”

“…These studies indicate that caterpillars may not depend on specific gut bacteria to derive critical nutrition from different dietary resources. Finally, butterfly adults do not bear a reproductive cost of disturbance in gut microbes, even when food is limited [20]. Together, these studies suggest that gut microbiomes of butterflies could be largely transient and may not have functional associations with their hosts.…”