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1. Reciprocal microbiome transplants differentially rescue fitness in two syntopic dung beetle sister species (Scarabaeidae: Onthophagus )

   https://doi.org/10.1111/een.13031  

   Parker, Erik S. ; Moczek, Armin P. ; Macagno, Anna L. M. ( March 2021 , Ecological Entomology)

   1. Microbial symbionts play a crucial role in the development, health, and homeostasis of their hosts. However, the eco‐evolutionary conditions shaping these relationships and the evolutionary scale at which host–microbiome interactions may diverge warrant further investigation, especially in non‐model systems. This study examines the impact of reciprocal gut microbiome transplants between two ecologically very similar, sympatric, and syntopic dung beetle sister species.

   2.Onthophagus vaccaandOnthophagus mediuswere specifically used to compare the growth, development, and fitness outcomes of individuals that were either (i) reared in the presence of a microbiome provided by a mother of the same species (“self‐inoculated”), (ii) forced to develop with a microbiome derived from a heterospecific mother (“cross‐inoculated”), or (iii) reared without a maternally transmitted microbiome.

   3. This study found that individuals reared in the absence of a maternally derived gut microbiome incur detrimental changes in survival, as well as in several metrics signalling normative development. Furthermore, such negative effects are only partly rescued through inoculation with a heterologous microbiome.

   4. Collectively, this study's results suggest that inoculation with a species‐specific, maternally transmitted microbiome is critical for normative development, that the significance of maternally derived microbiota for host survival differs across species, and that the phenotypic outcomes resulting from host–microbiome interactions may diverge even between closely related, ecologically similar host species.

    

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2. Fidelity varies in the symbiosis between a gutless marine worm and its microbial consortium

   https://doi.org/10.1186/s40168-022-01372-2  

   Sato, Yui ; Wippler, Juliane ; Wentrup, Cecilia ; Ansorge, Rebecca ; Sadowski, Miriam ; Gruber-Vodicka, Harald ; Dubilier, Nicole ; Kleiner, Manuel ( October 2022 , Microbiome)

   Many animals live in intimate associations with a species-rich microbiome. A key factor in maintaining these beneficial associations is fidelity, defined as the stability of associations between hosts and their microbiota over multiple host generations. Fidelity has been well studied in terrestrial hosts, particularly insects, over longer macroevolutionary time. In contrast, little is known about fidelity in marine animals with species-rich microbiomes at short microevolutionary time scales, that is at the level of a single host population. Given that natural selection acts most directly on local populations, studies of microevolutionary partner fidelity are important for revealing the ecological and evolutionary processes that drive intimate beneficial associations within animal species.

   In this study on the obligate symbiosis between the gutless marine annelidOlavius algarvensisand its consortium of seven co-occurring bacterial symbionts, we show that partner fidelity varies across symbiont species from strict to absent over short microevolutionary time. Using a low-coverage sequencing approach that has not yet been applied to microbial community analyses, we analysed the metagenomes of 80O. algarvensisindividuals from the Mediterranean and compared host mitochondrial and symbiont phylogenies based on single-nucleotide polymorphisms across genomes. Fidelity was highest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium of allO. algarvensisindividuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts with lower abundance. These differences in fidelity are likely driven by both selective and stochastic forces acting on the consistency with which symbionts are vertically transmitted.

   We hypothesize that variable degrees of fidelity are advantageous forO. algarvensisby allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources.

    

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3. Gut microbiota of dung beetles correspond to dietary specializations of adults and larvae

   https://doi.org/10.1111/mec.13901  

   Shukla, Shantanu P. ; Sanders, Jon G. ; Byrne, Marcus J. ; Pierce, Naomi E. ( November 2016 , Molecular Ecology)

   Vertebrate dung is central to the dung beetle life cycle, constituting food for adults and a protective and nutritive refuge for their offspring. Adult dung beetles have soft mandibles and feed primarily on nutritionally rich dung particles, while larvae have sclerotized mandibles and consume coarser dung particles with a higher C/N ratio. Here, using the dung beetlesEuoniticellus intermediusandE. triangulatus, we show that these morphological adaptations in mandibular structure are also correlated with differences in basic gut structure and gut bacterial communities between dung beetle life stages. Metagenome functional predictions based on 16SrDNAcharacterization further indicated that larval gut communities are enriched in genes involved in cellulose degradation and nitrogen fixation compared to adult guts. Larval gut communities are more similar to female gut communities than they are to those of males, and bacteria present in maternally provisioned brood balls and maternal ‘gifts’ (secretions deposited in the brood ball along with the egg) are also more similar to larval gut communities than to those of males. Maternal secretions and maternally provisioned brood balls, as well as dung, were important factors shaping the larval gut community. Differences between gut microbiota in the adults and larvae are likely to contribute to differences in nutrient assimilation from ingested dung at different life history stages.

    

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4. Incipient hybrid inferiority between recently introduced, diverging dung beetle populations

   https://doi.org/10.1093/biolinnean/blaa228  

   Macagno, Anna L ; Edgerton, Trevor J ; Moczek, Armin P ( January 2021 , Biological Journal of the Linnean Society)

   null (Ed.)

   Abstract Understanding why and how certain clades emerge as speciation hotspots is a fundamental objective of evolutionary biology. Here we investigate divergences between exotic Onthophagus taurus, a dung beetle introduced into the USA and Australia in the 1970s, as a potential model for the widespread recent speciation events characterizing the genus Onthophagus. To do so, we hybridized O. taurus derived from Eastern US (EUS) and Western Australian (WA) populations, and assessed fitness-relevant trait expression in first- and second-generation hybrids. We found that dams invest more in offspring provisioning when paired with a sire from the same population, and that WA dams crossed with EUS sires produce smaller and lighter F1 hybrids, with an unexpectedly male-biased sex ratio. Furthermore, fewer F2 hybrids with vertically inherited WA cytoplasm and microbiome emerged compared with WA backcrosses with WA cytoplasm/microbiome, suggesting that combinations of nuclear genome, cytoplasm and/or microbiome may contribute to hybrid viability. Lastly, we document a dominance of WA genotypes over body size at the point of inflection between minor and major male morphs, a trait of significance in mate competition, which has diverged remarkably between these populations. We discuss our results in light of the evolutionary ecology of onthophagine beetles and the role of developmental evolution in clade diversification. 

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5. Transgenerational developmental effects of species‐specific, maternally transmitted microbiota in Onthophagus dung beetles

   https://doi.org/10.1111/een.12703  

   Parker, Erik S. ; Dury, Guillaume J. ; Moczek, Armin P. ( November 2018 , Ecological Entomology)

   1. The significance of host–microbe interactions is increasingly appreciated across biological disciplines, yet to what extent these interactions influence developmental outcomes within and across generations remains poorly understood.

   2. This study investigated the putative role of host–microbe interactions in the adaptive diversification ofOnthophagusdung beetles, one of the most species‐rich and ecologically successful genera of insects.Onthophagusmothers vertically transmit growth‐ and fitness‐enhancing gut symbionts to their offspring through a faecal secretion known as the pedestal.

   3. Pedestals were reciprocally exchanged between two ecologically similar congenericOnthophagusspecies to assess the degree to which pedestal microbiota from one species can substitute for those of another.

   4. It was found that the presence of a heterospecific pedestal delays development and increases mortality, and that the fitness costs of non‐host‐specific microbiota are maintained transgenerationally.

   5. Collectively, these results support the hypothesis thatOnthophagusbeetles maintain, interact with, and are dependent upon host species‐specific microbial communities to support normal growth and development. The implications of these results are discussed in the context of host microbiota coevolution.

    

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