Microbial Communities of Lycaenid Butterflies Do Not Correlate with Larval Diet

Whitaker, Melissa R. L.; Salzman, Shayla; Sanders, Jon G.; Kaltenpoth, Martin; Pierce, Naomi E.

doi:10.3389/fmicb.2016.01920

Cited by 72 publications

(80 citation statements)

References 98 publications

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“…On the other hand, we cannot exclude the hypothesis that the excretion of the microbiota has happened during the moulting right before the individuals enter into diapause. Furthermore, a recent study on several Lycaenid butterfly species showed that starved carnivorous or herbivorous caterpillars did not present any differences in their intestinal communities in comparison to each other (Whitaker et al ., ). In our study, we did not consider the soil below the host plant.…”

Section: Discussionmentioning

confidence: 97%

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

Minard

Tikhonov

Ovaskainen

et al. 2019

Environmental Microbiology

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Summary Understanding of the ecological factors that shape intraspecific variation of insect microbiota in natural populations is relatively poor. In Lepidopteran caterpillars, microbiota is assumed to be mainly composed of transient bacterial symbionts acquired from the host plant. We sampled Glanville fritillary (Melitaea cinxia) caterpillars from natural populations to describe their gut microbiome and to identify potential ecological factors that determine its structure. Our results demonstrate high variability of microbiota composition even among caterpillars that shared the same host plant individual and most likely the same genetic background. We observed that the caterpillars harboured microbial classes that varied among individuals and alternated between two distinct communities (one composed of mainly Enterobacteriaceae and another with more variable microbiota community). Even though the general structure of the microbiota was not attributed to the measured ecological factors, we found that phylogenetically similar microbiota showed corresponding responses to the sex and the parasitoid infection of the caterpillar and to those of the host plant's microbial and chemical composition. Our results indicate high among‐individual variability in the microbiota of the M. cinxia caterpillar and contradict previous findings that the host plant is the major driver of the microbiota communities of insect herbivores.

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Section: Discussionmentioning

confidence: 97%

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

Minard

Tikhonov

Ovaskainen

et al. 2019

Environmental Microbiology

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“…While some P. alcon caterpillars on plants hosted diverse bacterial communities, many were dominated by Pseudomonadaceae, which include both plant‐growth promoting and pathogenic species (Preston, ) and Enterobacteriaceae, which include many common, harmless symbionts, but also pathogenic species. Enterobacteriaceae appear to be a common bacterial symbiont in Lycaenid larvae (Phalnikar et al, ; Whitaker et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Building on recent broad molecular surveys of microbial diversity within caterpillars (Hammer et al, 2017;Phalnikar et al, 2018;Whitaker et al, 2016), we characterized and compared bacterial communities within Phengaris alcon caterpillars before and after their trophic shift and social association with M. schencki ants.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, Whitaker, Salzman, Sanders, Kaltenpoth, and Pierce (2016) found no clear link between trophic regime and gut bacterial composition, despite sampling a wide range of feeding strategies across 31 species of Lycaenid caterpillars. Hammer, Janzen, Hallwachs, Jaffe, and Fierer (2017) similarly found low densities of microbes in the guts of caterpillars spanning 124 species and 15 families.…”

Section: Introductionmentioning

confidence: 99%

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Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies

Szenteczki

Pitteloud

Casacci

et al. 2019

Ecology and Evolution

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Bacterial symbionts are known to facilitate a wide range of physiological processes and ecological interactions for their hosts. In spite of this, caterpillars with highly diverse life histories appear to lack resident microbiota. Gut physiology, endogenous digestive enzymes, and limited social interactions may contribute to this pattern, but the consequences of shifts in social activity and diet on caterpillar microbiota are largely unknown. Phengaris alcon caterpillars undergo particularly dramatic social and dietary shifts when they parasitize Myrmica ant colonies, rapidly transitioning from solitary herbivory to ant tending (i.e., receiving protein‐rich regurgitations through trophallaxis). This unique life history provides a model for studying interactions between social living, diet, and caterpillar microbiota. Here, we characterized and compared bacterial communities within P . alcon caterpillars before and after their association with ants, using 16S rRNA amplicon sequencing and quantitative PCR. After being adopted by ants, bacterial communities within P. alcon caterpillars shifted substantially, with a significant increase in alpha diversity and greater consistency in bacterial community composition in terms of beta dissimilarity. We also characterized the bacterial communities within their host ants ( Myrmica schencki ), food plant ( Gentiana cruciata ), and soil from ant nest chambers. These data indicated that the aforementioned patterns were influenced by bacteria derived from caterpillars’ surrounding environments, rather than through transfers from ants. Thus, while bacterial communities are substantially reorganized over the life cycle of P. alcon caterpillars, it appears that they do not rely on transfers of bacteria from host ants to complete their development.

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“…Some studies report a highly abundant and consistent bacterial community (23)(24)(25), characteristics that may indicate a functional association with the host. Others report high intraspecific variability in composition and similarity between diet-and gut-associated microbes (26)(27)(28)(29). Inconsistencies could arise from methodological factors such as contamination of low-biomass samples (30), starvation before sampling, sequencing of extracellular DNA, and the use of laboratory-raised insects or artificial diets (27,31,32).…”

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confidence: 99%

Caterpillars lack a resident gut microbiome

Hammer

Janzen

Hallwachs

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

377

347

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Many animals are inhabited by microbial symbionts that influence their hosts’ development, physiology, ecological interactions, and evolutionary diversification. However, firm evidence for the existence and functional importance of resident microbiomes in larval Lepidoptera (caterpillars) is lacking, despite the fact that these insects are enormously diverse, major agricultural pests, and dominant herbivores in many ecosystems. Using 16S rRNA gene sequencing and quantitative PCR, we characterized the gut microbiomes of wild leaf-feeding caterpillars in the United States and Costa Rica, representing 124 species from 15 families. Compared with other insects and vertebrates assayed using the same methods, the microbes that we detected in caterpillar guts were unusually low-density and variable among individuals. Furthermore, the abundance and composition of leaf-associated microbes were reflected in the feces of caterpillars consuming the same plants. Thus, microbes ingested with food are present (although possibly dead or dormant) in the caterpillar gut, but host-specific, resident symbionts are largely absent. To test whether transient microbes might still contribute to feeding and development, we conducted an experiment on field-collected caterpillars of the model species Manduca sexta. Antibiotic suppression of gut bacterial activity did not significantly affect caterpillar weight gain, development, or survival. The high pH, simple gut structure, and fast transit times that typify caterpillar digestive physiology may prevent microbial colonization. Moreover, host-encoded digestive and detoxification mechanisms likely render microbes unnecessary for caterpillar herbivory. Caterpillars illustrate the potential ecological and evolutionary benefits of independence from symbionts, a lifestyle that may be widespread among animals.

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Microbial Communities of Lycaenid Butterflies Do Not Correlate with Larval Diet

Cited by 72 publications

References 98 publications

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

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

Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies

Caterpillars lack a resident gut microbiome

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