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Title: Conserved microbiota among young Heliconius butterfly species
Background Insects are the most diverse group of animals which have established intricate evolutionary interactions with bacteria. However, the importance of these interactions is still poorly understood. Few studies have focused on a closely related group of insect species, to test the similarities and differences between their microbiota. Heliconius butterflies are a charismatic recent insect radiation that evolved the unique ability to use pollen as a protein source, which affected life history traits and resulted in an elevated speciation rates. We hypothesize that different Heliconius butterflies sharing a similar trophic pollen niche, harbor a similar gut flora within species, population and sexes. Methods To test our hypothesis, we characterized the microbiota of 38 adult male and female butterflies representing six species of Heliconius butterflies and 2 populations of the same species. We sequenced the V4 region of the 16S rRNA gene with the Roche 454 system and analyzed the data with standard tools for microbiome analysis. Results Overall, we found a low microbial diversity with only 10 OTUs dominating across all individuals, mostly Proteobacteria and Firmicutes, which accounted for 99.5% of the bacterial reads. When rare reads were considered, we identified a total of 406 OTUs across our samples. We identified reads within Phyla Chlamydiae , found in 5 butterflies of four species. Interestingly, only three OTUs were shared among all 38 individuals ( Bacillus, Enterococcus and Enterobacteriaceae ). Altogether, the high individual variation overshadowed species and sex differences. Thus, bacterial communities were not structured randomly with 13% of beta-diversity explained by species, and 40 rare OTUs being significantly different across species. Finally, 13 OTUs, including the intercellular symbiont Spiroplasma, varied significantly in relative abundance between males and females. Discussion The Heliconius microbial communities in these 38 individuals show a low diversity with few differences in the rare microbes between females, males, species or populations. Indeed, Heliconius butterflies, similarly to other insects, are dominated by few OTUs, mainly from Proteobacteria and Firmicutes. The overall low microbial diversity observed contrasts with the high intra-species variation in microbiome composition. This could indicate that much of the microbiome maybe acquired from their surroundings. The significant differences between species and sexes were restricted to rare taxa, which could be important for microbial community stability under changing conditions as seen in other host-microbiome systems. The presence of symbionts like Spiroplasma or Chlamydiae , identified in this study for the first time in Heliconius , could play a vital role in their behavior and evolution by vertical transmission. Altogether, our study represents a step forward into the description of the microbial diversity in a charismatic group of closely related butterflies. more »« less
Briscoe, Adriana
(, Peer Community in Evolutionary Biology)
Growth, development and reproduction in animals are all limited by dietary nutrients. Expansion of an organism’s diet to sources not accessible to closely related species reduces food competition, and eases the constraints of nutrient limited diets. Adult butterflies are herbivorous insects known to feed primarily on nectar from flowers, which is rich in sugars but poor in amino acids. Only certain species in the genus Heliconius are known to also feed on pollen, which is especially rich in amino acids, and is known to prolong their lives by several months. The ability to digest pollen in Heliconius has been linked to specialized feeding behaviors (Krenn et al. 2009) and extra-oral digestion using enzymes, possibly including duplicated copies of cocoonase (Harpel et al. 2016; Smith et al. 2016 and 2018), a protease used by some moths to digest silk upon eclosion from their cocoons. In this reprint, Pinheiro de Castro and colleagues investigated the impact of artificial and natural diets on egg-laying ability, body weight, and cyanogenic glucoside abundance in adult Heliconius erato butterflies of both sexes.
Abstract Diet profoundly influences the composition of an animal’s microbiome, especially in holometabolous insects, offering a valuable model to explore the impact of diet on gut microbiome dynamics throughout metamorphosis. Here, we use monarch butterflies (Danaus plexippus), specialist herbivores that feed as larvae on many species of chemically well-defined milkweed plants (Asclepias sp.), to investigate the impacts of development and diet on the composition of the gut microbial community. While a few microbial taxa are conserved across life stages of monarchs, the microbiome appears to be highly dynamic throughout the life cycle. Microbial diversity gradually diminishes throughout the larval instars, ultimately reaching its lowest point during the pupal stage and then recovering again in the adult stage. The microbial composition then undergoes a substantial shift upon the transition from pupa to adult, with female adults having significantly different microbial communities than the eggs that they lay, indicating limited evidence for vertical transmission of gut microbiota. While diet did not significantly impact overall microbial composition, our results suggest that fourth instar larvae exhibit higher microbial diversity when consuming milkweed with high concentrations of toxic cardenolide phytochemicals. This study underscores how diet and developmental stage collectively shape the monarch’s gut microbiota.
Pagalilauan, Alison; Pavloudi, Christina; Ospina, Santiago Meneses; Smith, Adam; Saw, Jimmy H
(, Access Microbiology)
Comparing the diversity of gut microbiota between and within social insect colonies can illustrate interactions between bacterial community composition and host behaviour. In many eusocial insect species, different workers exhibit different task behaviours. Evidence of compositional differences between core microbiota in different worker types could suggest a microbial association with the division of labour among workers. Here, we present the core microbiota ofAphaenogaster piceaant workers with different task behaviours. The genusAphaenogasteris abundant worldwide, yet the associated microbiota of this group is unstudied. Bacterial communities fromAphaenogaster piceagut samples in this study consist of 19 phyla, dominated by Proteobacteria, Cyanobacteria and Firmicutes. Analysis of 16S rRNA gene sequences reveals distinct similarity clustering ofAphaenogaster piceagut bacterial communities in workers that have more interactions with the refuse piles. Though gut bacterial communities of nurse and foraging ants are similar in overall composition and structure, the worker groups differ in relative abundances of dominant taxa. Gut bacterial communities from ants that have more interactions with refuse piles are dominated by amplicon sequence variants associated with Entomoplasmataceae. Interaction with faecal matter via refuse piles seems to have the greatest impact on microbial taxa distribution, and this effect appears to be independent of worker type. This is the first report surveying the gut microbiome community composition ofAphaenogasterants.
Vera-Ponce de León, Arturo; Jahnes, Benjamin C.; Otero-Bravo, Alejandro; Sabree, Zakee L.
(, mSystems)
Klassen, Jonathan L.
(Ed.)
ABSTRACT Omnivorous animals, including humans, harbor diverse, species-rich gut communities that impact their growth, development, and homeostasis. Model invertebrates are broadly accessible experimental platforms that enable linking specific species or species groups to host phenotypes, yet often their specialized diets and distinct gut microbiota make them less comparable to human and other mammalian and gut communities. The omnivorous cockroach Periplaneta americana harbors ∼4 × 10 2 bacterial genera within its digestive tract and is enriched with taxa commonly found in omnivorous mammals (i.e., Proteobacteria, Bacteroidetes , and Firmicutes ). These features make P. americana a valuable platform for identifying microbe-mediated host phenotypes with potential translations to mammals. Rearing P. americana insects under germfree conditions resulted in prolonging development time by ∼30% and an up to ∼8% reduction in body size along three dimensions. Germfree rearing resulted in downregulation of gene networks involved in growth, energy homeostasis, and nutrient availability. Reintroduction of a defined microbiota comprised of a subset of P. americana commensals to germfree insects did not recover normal growth and developmental phenotypes or transcriptional profiles observed in conventionally reared insects. These results are in contrast with specialist-feeding model insects (e.g., Drosophila ), where introduction of a single endemic bacterial species to germfree condition-reared specimens recovered normal host phenotypes. These data suggest that understanding microbe-mediated host outcomes in animals with species-rich communities should include models that typically maintain similarly diverse microbiomes. The dramatic transcriptional, developmental, and morphological phenotypes linked to gut microbiome status in this study illustrates how microbes are key players in animal growth and evolution. IMPORTANCE Broadly accessible model organisms are essential for illustrating how microbes are engaged in the growth, development, and evolution of animals. We report that germfree rearing of omnivorous Periplaneta americana cockroaches resulted in growth defects and severely disrupted gene networks that regulate development, which highlights the importance of gut microbiota in these host processes. Absence of gut microbiota elicited a starvation-like transcriptional response in which growth and development were inhibited while nutrient scavenging was enhanced. Additionally, reintroduction of a subset of cockroach gut bacterial commensals did not broadly recover normal expression patterns, illustrating that a particular microbiome composition may be necessary for normal host development. Invertebrate microbiota model systems that enable disentangling complex, species-rich communities are essential for linking microbial taxa to specific host phenotypes.
Massardo, Darli; VanKuren, Nicholas W.; Nallu, Sumitha; Ramos, Renato R.; Ribeiro, Pedro G.; Silva-Brandão, Karina L.; Brandão, Marcelo M.; Lion, Marília B.; Freitas, André V.; Cardoso, Márcio Z.; et al
(, BMC Biology)
null
(Ed.)
Abstract Background Heliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Müllerian mimicry and mating behavior. Their rapid radiation has been strongly influenced by hybridization, which has created new species and allowed sharing of color patterning alleles between mimetic species pairs. While these processes have frequently been observed in widespread species with contiguous distributions, many Heliconius species inhabit patchy or rare habitats that may strongly influence the origin and spread of species and color patterns. Here, we assess the effects of historical population fragmentation and unique biology on the origins, genetic health, and color pattern evolution of two rare and sparsely distributed Brazilian butterflies, Heliconius hermathena and Heliconius nattereri . Results We assembled genomes and re-sequenced whole genomes of eight H. nattereri and 71 H. hermathena individuals. These species harbor little genetic diversity, skewed site frequency spectra, and high deleterious mutation loads consistent with recent population bottlenecks. Heliconius hermathena consists of discrete, strongly isolated populations that likely arose from a single population that dispersed after the last glacial maximum. Despite having a unique color pattern combination that suggested a hybrid origin, we found no genome-wide evidence that H. hermathena is a hybrid species. However, H. hermathena mimicry evolved via introgression, from co-mimetic Heliconius erato , of a small genomic region upstream of the color patterning gene cortex . Conclusions Heliconius hermathena and H. nattereri population fragmentation, potentially driven by historical climate change and recent deforestation, has significantly reduced the genetic health of these rare species. Our results contribute to a growing body of evidence that introgression of color patterning alleles between co-mimetic species appears to be a general feature of Heliconius evolution.
van Schooten, Bas, Godoy-Vitorino, Filipa, McMillan, W. Owen, and Papa, Riccardo. Conserved microbiota among young Heliconius butterfly species. Retrieved from https://par.nsf.gov/biblio/10094450. PeerJ 6. Web. doi:10.7717/peerj.5502.
van Schooten, Bas, Godoy-Vitorino, Filipa, McMillan, W. Owen, & Papa, Riccardo. Conserved microbiota among young Heliconius butterfly species. PeerJ, 6 (). Retrieved from https://par.nsf.gov/biblio/10094450. https://doi.org/10.7717/peerj.5502
@article{osti_10094450,
place = {Country unknown/Code not available},
title = {Conserved microbiota among young Heliconius butterfly species},
url = {https://par.nsf.gov/biblio/10094450},
DOI = {10.7717/peerj.5502},
abstractNote = {Background Insects are the most diverse group of animals which have established intricate evolutionary interactions with bacteria. However, the importance of these interactions is still poorly understood. Few studies have focused on a closely related group of insect species, to test the similarities and differences between their microbiota. Heliconius butterflies are a charismatic recent insect radiation that evolved the unique ability to use pollen as a protein source, which affected life history traits and resulted in an elevated speciation rates. We hypothesize that different Heliconius butterflies sharing a similar trophic pollen niche, harbor a similar gut flora within species, population and sexes. Methods To test our hypothesis, we characterized the microbiota of 38 adult male and female butterflies representing six species of Heliconius butterflies and 2 populations of the same species. We sequenced the V4 region of the 16S rRNA gene with the Roche 454 system and analyzed the data with standard tools for microbiome analysis. Results Overall, we found a low microbial diversity with only 10 OTUs dominating across all individuals, mostly Proteobacteria and Firmicutes, which accounted for 99.5% of the bacterial reads. When rare reads were considered, we identified a total of 406 OTUs across our samples. We identified reads within Phyla Chlamydiae , found in 5 butterflies of four species. Interestingly, only three OTUs were shared among all 38 individuals ( Bacillus, Enterococcus and Enterobacteriaceae ). Altogether, the high individual variation overshadowed species and sex differences. Thus, bacterial communities were not structured randomly with 13% of beta-diversity explained by species, and 40 rare OTUs being significantly different across species. Finally, 13 OTUs, including the intercellular symbiont Spiroplasma, varied significantly in relative abundance between males and females. Discussion The Heliconius microbial communities in these 38 individuals show a low diversity with few differences in the rare microbes between females, males, species or populations. Indeed, Heliconius butterflies, similarly to other insects, are dominated by few OTUs, mainly from Proteobacteria and Firmicutes. The overall low microbial diversity observed contrasts with the high intra-species variation in microbiome composition. This could indicate that much of the microbiome maybe acquired from their surroundings. The significant differences between species and sexes were restricted to rare taxa, which could be important for microbial community stability under changing conditions as seen in other host-microbiome systems. The presence of symbionts like Spiroplasma or Chlamydiae , identified in this study for the first time in Heliconius , could play a vital role in their behavior and evolution by vertical transmission. Altogether, our study represents a step forward into the description of the microbial diversity in a charismatic group of closely related butterflies.},
journal = {PeerJ},
volume = {6},
author = {van Schooten, Bas and Godoy-Vitorino, Filipa and McMillan, W. Owen and Papa, Riccardo},
}
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