Within-species variation in the gut microbiome of medaka (Oryzias latipes) is driven by the interaction of light intensity and genetic background

10.24072/pcjournal.306 - Peer Community Journal, Volume 3 (2023), article no. e72.

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Unravelling evolution-by-environment interactions on the gut microbiome is particularly relevant considering the unprecedented level of human-driven disruption of the ecological and evolutionary trajectories of species. Here, we aimed to evaluate whether an evolutionary response to size-selective mortality influences the gut microbiome of medaka (Oryzias latipes), how environmental conditions interact with the genetic background of medaka on their microbiota, and the association between microbiome diversity and medaka growth-related traits. To do so, we studied two lineages of medaka with known divergence in foraging efficiency and life history raised under antagonistic size-selective regimes for 10 generations (i.e. the largest or the smallest breeders were removed to mimic fishing-like or natural mortality). In pond mesocosms, the two lineages were subjected to contrasting population density and light intensity (used as proxies of resource availability). We observed significant differences in the gut microbiome composition and richness between the two lines, and this effect was mediated by light intensity. The bacterial richness of fishing-like medaka (small-breeder line) was reduced by 34% under low-light conditions compared to high-light conditions, while it remained unchanged in natural mortality-selected medaka (large-breeder line). However, the observed changes in bacterial richness did not correlate with changes in adult growth-related traits. Given the growing evidence about the gut microbiomes importance to host health, more in-depth studies are required to fully understand the role of the microbiome in size-selected organisms and the possible ecosystem-level consequences.

Published online:
DOI: 10.24072/pcjournal.306
Keywords: communities, 16S rRNA gene sequencing, harvest-induced evolution, mesocosm, light, fish density
Evangelista, Charlotte 1, 2; Kamenova, Stefaniya 1, 3, 4; Diaz Pauli, Beatriz 1, 5; Sandkjenn, Joakim 1; Vøllestad, Leif Asbjørn 1; Edeline, Eric 6, 7; Trosvik, Pål 1; de Muinck, Eric Jacques 1

1 Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway
2 Current address: Aquatic Ecology Group, University of Vic - Central University of Catalonia, 08500, Vic, Spain
3 Departments of Ecology and Natural Resource Management, Norwegian University of Life Sciences, Ås, Norway
4 National Museum of Natural History, Sofia, Bulgaria
5 Department of Biological Science, University of Bergen, Norway
6 Sorbonne Université, CNRS, IRD, INRA, Institut d’écologie et des sciences de l’environnement (IEES), 4 place Jussieu, Paris 75005, France.
7 DECOD (Ecosystem Dynamics and Sustainability), INRAE, IFREMER, Institut Agro, Rennes, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     title = {Within-species variation in the gut microbiome of medaka {(\protect\emph{Oryzias} latipes}) is driven by the interaction of light intensity and genetic background},
     journal = {Peer Community Journal},
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     language = {en},
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%A Edeline, Eric
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Evangelista, Charlotte; Kamenova, Stefaniya; Diaz Pauli, Beatriz; Sandkjenn, Joakim; Vøllestad, Leif Asbjørn; Edeline, Eric; Trosvik, Pål; de Muinck, Eric Jacques. Within-species variation in the gut microbiome of medaka (Oryzias latipes) is driven by the interaction of light intensity and genetic background. Peer Community Journal, Volume 3 (2023), article  no. e72. doi : 10.24072/pcjournal.306. https://peercommunityjournal.org/articles/10.24072/pcjournal.306/

Peer reviewed and recommended by PCI : 10.24072/pci.microbiol.100012

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Alberdi, A.; Aizpurua, O.; Bohmann, K.; Zepeda-Mendoza, M. L.; Gilbert, M. T. P. Do Vertebrate Gut Metagenomes Confer Rapid Ecological Adaptation?, Trends in Ecology & Evolution, Volume 31 (2016) no. 9, pp. 689-699 | DOI

[2] Alberdi, A.; Gilbert, M. T. P. hilldiv: an R package for the integral analysis of diversity based on Hill numbers, bioRxiv, 2019 | DOI

[3] Alberdi, A.; Gilbert, M. T. P. A guide to the application of Hill numbers to DNA‐based diversity analyses, Molecular Ecology Resources, Volume 19 (2019) no. 4, pp. 804-817 | DOI

[4] Anderson, M. J.; Walsh, D. C. I. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing?, Ecological Monographs, Volume 83 (2013) no. 4, pp. 557-574 | DOI

[5] Bestion, E.; Jacob, S.; Zinger, L.; Di Gesu, L.; Richard, M.; White, J.; Cote, J. Climate warming reduces gut microbiota diversity in a vertebrate ectotherm, Nature Ecology & Evolution, Volume 1 (2017) no. 6 | DOI

[6] Bokulich, N. A.; Subramanian, S.; Faith, J. J.; Gevers, D.; Gordon, J. I.; Knight, R.; Mills, D. A.; Caporaso, J. G. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing, Nature Methods, Volume 10 (2013) no. 1, pp. 57-59 | DOI

[7] Bolnick, D. I.; Snowberg, L. K.; Hirsch, P. E.; Lauber, C. L.; Knight, R.; Caporaso, J. G.; Svanbäck, R. Individuals' diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch), Ecology Letters, Volume 17 (2014) no. 8, pp. 979-987 | DOI

[8] Bolnick, D. I.; Snowberg, L. K.; Caporaso, J. G.; Lauber, C.; Knight, R.; Stutz, W. E. Major Histocompatibility Complex class IIb polymorphism influences gut microbiota composition and diversity, Molecular Ecology, Volume 23 (2014) no. 19, pp. 4831-4845 | DOI

[9] Bouffet‐Halle, A.; Mériguet, J.; Carmignac, D.; Agostini, S.; Millot, A.; Perret, S.; Motard, E.; Decenciere, B.; Edeline, E. Density‐dependent natural selection mediates harvest‐induced trait changes, Ecology Letters, Volume 24 (2021) no. 4, pp. 648-657 | DOI

[10] Callahan, B. J.; McMurdie, P. J.; Rosen, M. J.; Han, A. W.; Johnson, A. J. A.; Holmes, S. P. DADA2: High-resolution sample inference from Illumina amplicon data, Nature Methods, Volume 13 (2016) no. 7, pp. 581-583 | DOI

[11] Chiu, C.-H.; Chao, A. Distance-Based Functional Diversity Measures and Their Decomposition: A Framework Based on Hill Numbers, PLoS ONE, Volume 9 (2014) no. 7 | DOI

[12] Conover, D. O.; Munch, S. B. Sustaining Fisheries Yields Over Evolutionary Time Scales, Science, Volume 297 (2002) no. 5578, pp. 94-96 | DOI

[13] Darimont, C. T.; Carlson, S. M.; Kinnison, M. T.; Paquet, P. C.; Reimchen, T. E.; Wilmers, C. C. Human predators outpace other agents of trait change in the wild, Proceedings of the National Academy of Sciences, Volume 106 (2009) no. 3, pp. 952-954 | DOI

[14] Diaz Pauli, B.; Garric, S.; Evangelista, C.; Vøllestad, L. A.; Edeline, E. Selection for small body size favours contrasting sex-specific life histories, boldness and feeding in medaka, Oryzias latipes, BMC Evolutionary Biology, Volume 19 (2019) no. 1 | DOI

[15] Diwan, A. D.; Harke, S. N.; Gopalkrishna; Panche, A. N. Aquaculture industry prospective from gut microbiome of fish and shellfish: An overview, Journal of Animal Physiology and Animal Nutrition, Volume 106 (2021) no. 2, pp. 441-469 | DOI

[16] Dutton, C. L.; Subalusky, A. L.; Sanchez, A.; Estrela, S.; Lu, N.; Hamilton, S. K.; Njoroge, L.; Rosi, E. J.; Post, D. M. The meta-gut: community coalescence of animal gut and environmental microbiomes, Scientific Reports, Volume 11 (2021) no. 1 | DOI

[17] Eckert, E. M.; Anicic, N.; Fontaneto, D. Freshwater zooplankton microbiome composition is highly flexible and strongly influenced by the environment, Molecular Ecology, Volume 30 (2021) no. 6, pp. 1545-1558 | DOI

[18] Edeline, E.; Terao, O.; Naruse, K. Empirical evidence for competition-driven semelparity in wild medaka, Population Ecology, Volume 58 (2016) no. 3, pp. 371-383 | DOI

[19] Evangelista C.; Kamenova S.; Diaz Pauli B.; Sandkjenn J.; Vøllestad Leif A.; Edeline E.; Trosvik P.; de Muinck E. J. Within-species variation in the gut microbiome of medaka (Oryzias latipes) is driven by the interaction of light intensity and genetic background. Dataset., Figshare, 2023 | DOI

[20] Evangelista, C.; Dupeu, J.; Sandkjenn, J.; Pauli, B. D.; Herland, A.; Meriguet, J.; Vøllestad, L. A.; Edeline, E. Ecological ramifications of adaptation to size-selective mortality, Royal Society Open Science, Volume 8 (2021) no. 10 | DOI

[21] Evangelista, C.; Vøllestad, L. A.; Diaz Pauli, B.; Edeline, E. Density-dependent consequences of size-selective induced life-history changes to population fitness in medaka (Oryzias latipes), Canadian Journal of Fisheries and Aquatic Sciences, Volume 77 (2020) no. 10, pp. 1741-1748 | DOI

[22] Fadrosh, D. W.; Ma, B.; Gajer, P.; Sengamalay, N.; Ott, S.; Brotman, R. M.; Ravel, J. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform, Microbiome, Volume 2 (2014) no. 1 | DOI

[23] Fouladi, F.; Bailey, M. J.; Patterson, W. B.; Sioda, M.; Blakley, I. C.; Fodor, A. A.; Jones, R. B.; Chen, Z.; Kim, J. S.; Lurmann, F.; Martino, C.; Knight, R.; Gilliland, F. D.; Alderete, T. L. Air pollution exposure is associated with the gut microbiome as revealed by shotgun metagenomic sequencing, Environment International, Volume 138 (2020) | DOI

[24] Frank, K. T.; Petrie, B.; Choi, J. S.; Leggett, W. C. Trophic Cascades in a Formerly Cod-Dominated Ecosystem, Science, Volume 308 (2005) no. 5728, pp. 1621-1623 | DOI

[25] Gallo, B. D.; Farrell, J. M.; Leydet, B. F. Fish Gut Microbiome: A Primer to an Emerging Discipline in the Fisheries Sciences, Fisheries, Volume 45 (2020) no. 5, pp. 271-282 | DOI

[26] Ghanbari, M.; Kneifel, W.; Domig, K. J. A new view of the fish gut microbiome: Advances from next-generation sequencing, Aquaculture, Volume 448 (2015), pp. 464-475 | DOI

[27] Graham, E. B.; Knelman, J. E.; Schindlbacher, A.; Siciliano, S.; Breulmann, M.; Yannarell, A.; Beman, J. M.; Abell, G.; Philippot, L.; Prosser, J.; Foulquier, A.; Yuste, J. C.; Glanville, H. C.; Jones, D. L.; Angel, R.; Salminen, J.; Newton, R. J.; Bürgmann, H.; Ingram, L. J.; Hamer, U.; Siljanen, H. M. P.; Peltoniemi, K.; Potthast, K.; Bañeras, L.; Hartmann, M.; Banerjee, S.; Yu, R.-Q.; Nogaro, G.; Richter, A.; Koranda, M.; Castle, S. C.; Goberna, M.; Song, B.; Chatterjee, A.; Nunes, O. C.; Lopes, A. R.; Cao, Y.; Kaisermann, A.; Hallin, S.; Strickland, M. S.; Garcia-Pausas, J.; Barba, J.; Kang, H.; Isobe, K.; Papaspyrou, S.; Pastorelli, R.; Lagomarsino, A.; Lindström, E. S.; Basiliko, N.; Nemergut, D. R. Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes?, Frontiers in Microbiology, Volume 7 (2016) | DOI

[28] Hammer, T. J.; Sanders, J. G.; Fierer, N. Not all animals need a microbiome, FEMS Microbiology Letters, Volume 366 (2019) no. 10 | DOI

[29] Hanning, I.; Diaz-Sanchez, S. The functionality of the gastrointestinal microbiome in non-human animals, Microbiome, Volume 3 (2015) no. 1 | DOI

[30] Hočevar, S.; Kuparinen, A. Marine food web perspective to fisheries‐induced evolution, Evolutionary Applications, Volume 14 (2021) no. 10, pp. 2378-2391 | DOI

[31] Jones, E. W.; Carlson, J. M.; Sivak, D. A.; Ludington, W. B. Stochastic microbiome assembly depends on context, Proceedings of the National Academy of Sciences, Volume 119 (2022) no. 7 | DOI

[32] Kormas, K. (. Getting closer to the host-microbe evolutionary relationship, Peer Community in Microbiology (2023) | DOI

[33] Laviad, S.; Halpern, M. Chironomids’ Relationship with Aeromonas Species, Frontiers in Microbiology, Volume 7 (2016) | DOI

[34] Le Rouzic, A.; Renneville, C.; Millot, A.; Agostini, S.; Carmignac, D.; Édeline, É. Unidirectional response to bidirectional selection on body size II. Quantitative genetics, Ecology and Evolution, Volume 10 (2020) no. 20, pp. 11453-11466 | DOI

[35] Lenth R.V. emmeans: estimated marginal means, aka least-squares means. R package version 1.6.3. , 2021 (https://CRAN.R-project.org/package=emmeans)

[36] Li, H.; Wu, S.; Wirth, S.; Hao, Y.; Wang, W.; Zou, H.; Li, W.; Wang, G. Diversity and activity of cellulolytic bacteria, isolated from the gut contents of grass carp (Ctenopharyngodon idellus) (Valenciennes) fed on Sudan grass (Sorghum sudanense) or artificial feedstuffs, Aquaculture Research, Volume 47 (2014) no. 1, pp. 153-164 | DOI

[37] Liu, C.; Cui, Y.; Li, X.; Yao, M. microeco: an R package for data mining in microbial community ecology, FEMS Microbiology Ecology, Volume 97 (2020) no. 2 | DOI

[38] Liu, H.; Guo, X.; Gooneratne, R.; Lai, R.; Zeng, C.; Zhan, F.; Wang, W. The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels, Scientific Reports, Volume 6 (2016) no. 1 | DOI

[39] McMurdie, P. J.; Holmes, S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data, PLoS ONE, Volume 8 (2013) no. 4 | DOI

[40] Moran, N. A.; Ochman, H.; Hammer, T. J. Evolutionary and Ecological Consequences of Gut Microbial Communities, Annual Review of Ecology, Evolution, and Systematics, Volume 50 (2019) no. 1, pp. 451-475 | DOI

[41] Navarrete, P.; Magne, F.; Araneda, C.; Fuentes, P.; Barros, L.; Opazo, R.; Espejo, R.; Romero, J. PCR-TTGE Analysis of 16S rRNA from Rainbow Trout (Oncorhynchus mykiss) Gut Microbiota Reveals Host-Specific Communities of Active Bacteria, PLoS ONE, Volume 7 (2012) no. 2 | DOI

[42] Nusslé, S.; Hendry, A. P.; Carlson, S. M. When Should Harvest Evolution Matter to Population Dynamics?, Trends in Ecology & Evolution, Volume 31 (2016) no. 7, pp. 500-502 | DOI

[43] Oksanen J. ; Blanchet F.G.; Friendly M.; Kindt R.; Legendre P.; McGlinn D.; Minchin P.; O’Hara R.; Simpson G.; Solymos P.; Stevens M.; Szöcs E.; Wagner H. vegan: community ecology package. R package version 2.5-7. , 2020 (https://CRAN.R-project.org/package=vegan)

[44] Piazzon, M. C.; Naya-Català, F.; Perera, E.; Palenzuela, O.; Sitjà-Bobadilla, A.; Pérez-Sánchez, J. Genetic selection for growth drives differences in intestinal microbiota composition and parasite disease resistance in gilthead sea bream, Microbiome, Volume 8 (2020) no. 1 | DOI

[45] Pootakham, W.; Mhuantong, W.; Yoocha, T.; Putchim, L.; Jomchai, N.; Sonthirod, C.; Naktang, C.; Kongkachana, W.; Tangphatsornruang, S. Heat‐induced shift in coral microbiome reveals several members of the Rhodobacteraceae family as indicator species for thermal stress in Porites lutea, MicrobiologyOpen, Volume 8 (2019) no. 12 | DOI

[46] R Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria , 2021 (https://www.R-project.org/)

[47] Reese, A. T.; Dunn, R. R. Drivers of Microbiome Biodiversity: A Review of General Rules, Feces, and Ignorance, mBio, Volume 9 (2018) no. 4 | DOI

[48] Renneville, C.; Millot, A.; Agostini, S.; Carmignac, D.; Maugars, G.; Dufour, S.; Le Rouzic, A.; Edeline, E. Unidirectional response to bidirectional selection on body size. I. Phenotypic, life‐history, and endocrine responses, Ecology and Evolution, Volume 10 (2020) no. 19, pp. 10571-10592 | DOI

[49] Revelle W. psych: Procedures for personality and psychological research, Northwestern University, Evanston, Illinois, USA, Version = 2.1.9, 2021 (https://CRAN.R-project.org/package=psych)

[50] Rohart, F.; Gautier, B.; Singh, A.; Lê Cao, K.-A. mixOmics: An R package for ‘omics feature selection and multiple data integration, PLOS Computational Biology, Volume 13 (2017) no. 11 | DOI

[51] Ruzzante, D. E.; Doyle, R. W. Evolution Of Social Behavior In A Resource-Rich, Structured Environment: Selection Experiments With Medaka (Oryzias Latipes), Evolution, Volume 47 (1993) no. 2, pp. 456-470 | DOI

[52] Sanderson, S.; Beausoleil, M.; O’Dea, R. E.; Wood, Z. T.; Correa, C.; Frankel, V.; Gorné, L. D.; Haines, G. E.; Kinnison, M. T.; Oke, K. B.; Pelletier, F.; Pérez‐Jvostov, F.; Reyes‐Corral, W. D.; Ritchot, Y.; Sorbara, F.; Gotanda, K. M.; Hendry, A. P. The pace of modern life, revisited, Molecular Ecology, Volume 31 (2021) no. 4, pp. 1028-1043 | DOI

[53] Schmidt, V. T.; Smith, K. F.; Melvin, D. W.; Amaral-Zettler, L. A. Community assembly of a euryhaline fish microbiome during salinity acclimation, Molecular Ecology, Volume 24 (2015) no. 10, pp. 2537-2550 | DOI

[54] Sepulveda, J.; Moeller, A. H. The Effects of Temperature on Animal Gut Microbiomes, Frontiers in Microbiology, Volume 11 (2020) | DOI

[55] Sevellec, M.; Derome, N.; Bernatchez, L. Holobionts and ecological speciation: the intestinal microbiota of lake whitefish species pairs, Microbiome, Volume 6 (2018) no. 1 | DOI

[56] Small, C. M.; Currey, M.; Beck, E. A.; Bassham, S.; Cresko, W. A. Highly Reproducible 16S Sequencing Facilitates Measurement of Host Genetic Influences on the Stickleback Gut Microbiome, mSystems, Volume 4 (2019) no. 4 | DOI

[57] Smith, C. C.; Snowberg, L. K.; Gregory Caporaso, J.; Knight, R.; Bolnick, D. I. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota, The ISME Journal, Volume 9 (2015) no. 11, pp. 2515-2526 | DOI

[58] Sonnenburg, J. L.; Sonnenburg, E. D. Vulnerability of the industrialized microbiota, Science, Volume 366 (2019) no. 6464 | DOI

[59] Spor, A.; Koren, O.; Ley, R. Unravelling the effects of the environment and host genotype on the gut microbiome, Nature Reviews Microbiology, Volume 9 (2011) no. 4, pp. 279-290 | DOI

[60] Stearns, S. The evolution of life histories, Oxford University Press, Oxford, 1992

[61] Sullam, K. E.; Essinger, S. D.; Lozupone, C. A.; O’connor, M. P.; Rosen, G. L.; Knight, R.; Kilham, S. S.; Russell, J. A. Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis, Molecular Ecology, Volume 21 (2012) no. 13, pp. 3363-3378 | DOI

[62] Sullam, K. E.; Rubin, B. E.; Dalton, C. M.; Kilham, S. S.; Flecker, A. S.; Russell, J. A. Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies, The ISME Journal, Volume 9 (2015) no. 7, pp. 1508-1522 | DOI

[63] Talwar, C.; Nagar, S.; Lal, R.; Negi, R. K. Fish Gut Microbiome: Current Approaches and Future Perspectives, Indian Journal of Microbiology, Volume 58 (2018) no. 4, pp. 397-414 | DOI

[64] Tarnecki, A.; Burgos, F.; Ray, C.; Arias, C. Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics, Journal of Applied Microbiology, Volume 123 (2017) no. 1, pp. 2-17 | DOI

[65] Terova, G.; Gini, E.; Gasco, L.; Moroni, F.; Antonini, M.; Rimoldi, S. Effects of full replacement of dietary fishmeal with insect meal from Tenebrio molitor on rainbow trout gut and skin microbiota, Journal of Animal Science and Biotechnology, Volume 12 (2021) no. 1 | DOI

[66] Teyssier, A.; Rouffaer, L. O.; Saleh Hudin, N.; Strubbe, D.; Matthysen, E.; Lens, L.; White, J. Inside the guts of the city: Urban-induced alterations of the gut microbiota in a wild passerine, Science of The Total Environment, Volume 612 (2018), pp. 1276-1286 | DOI

[67] Tomás, J. M. The Main Aeromonas Pathogenic Factors, ISRN Microbiology, Volume 2012 (2012), pp. 1-22 | DOI

[68] Trosvik, P.; Rueness, E. K.; de Muinck, E. J.; Moges, A.; Mekonnen, A. Ecological plasticity in the gastrointestinal microbiomes of Ethiopian Chlorocebus monkeys, Scientific Reports, Volume 8 (2018) no. 1 | DOI

[69] Uusi-Heikkilä, S.; Sävilammi, T.; Leder, E.; Arlinghaus, R.; Primmer, C. R. Rapid, broad-scale gene expression evolution in experimentally harvested fish populations, Molecular Ecology, Volume 26 (2017) no. 15, pp. 3954-3967 | DOI

[70] Uusi‐Heikkilä, S.; Whiteley, A. R.; Kuparinen, A.; Matsumura, S.; Venturelli, P. A.; Wolter, C.; Slate, J.; Primmer, C. R.; Meinelt, T.; Killen, S. S.; Bierbach, D.; Polverino, G.; Ludwig, A.; Arlinghaus, R. The evolutionary legacy of size‐selective harvesting extends from genes to populations, Evolutionary Applications, Volume 8 (2015) no. 6, pp. 597-620 | DOI

[71] Varg, J. E.; Kunce, W.; Outomuro, D.; Svanbäck, R.; Johansson, F. Single and combined effects of microplastics, pyrethroid and food resources on the life-history traits and microbiome of Chironomus riparius, Environmental Pollution, Volume 289 (2021) | DOI

[72] Wang, C.; Sun, G.; Li, S.; Li, X.; Liu, Y. Intestinal microbiota of healthy and unhealthy Atlantic salmon Salmo salar L. in a recirculating aquaculture system, Journal of Oceanology and Limnology, Volume 36 (2017) no. 2, pp. 414-426 | DOI

[73] Wang, Q.; Garrity, G. M.; Tiedje, J. M.; Cole, J. R. Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy, Applied and Environmental Microbiology, Volume 73 (2007) no. 16, pp. 5261-5267 | DOI

[74] van Wijk, S. J.; Taylor, M. I.; Creer, S.; Dreyer, C.; Rodrigues, F. M.; Ramnarine, I. W.; van Oosterhout, C.; Carvalho, G. R. Experimental harvesting of fish populations drives genetically based shifts in body size and maturation, Frontiers in Ecology and the Environment, Volume 11 (2013) no. 4, pp. 181-187 | DOI

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