A time-lagged association between the gut microbiome, nestling weight and nestling survival in wild great tits.

fitness great tit gut microbiome microbial diversity microbiota survival viability weight

Journal

The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574

Informations de publication

Date de publication:
04 2021
Historique:
received: 29 09 2020
accepted: 21 12 2020
pubmed: 23 1 2021
medline: 20 4 2021
entrez: 22 1 2021
Statut: ppublish

Résumé

Natal body mass is a key predictor of viability and fitness in many animals. While variation in body mass and therefore juvenile viability may be explained by genetic and environmental factors, emerging evidence points to the gut microbiota as an important factor influencing host health. The gut microbiota is known to change during development, but it remains unclear whether the microbiome predicts fitness, and if it does, at which developmental stage it affects fitness traits. We collected data on two traits associated with fitness in wild nestling great tits Parus major: weight and survival to fledging. We characterised the gut microbiome using 16S rRNA sequencing from nestling faeces and investigated temporal associations between the gut microbiome and fitness traits across development at Day-8 (D8) and Day-15 (D15) post-hatching. We also explored whether particular microbial taxa were 'indicator species' that reflected whether nestlings survived or not. There was no link between mass and microbial diversity on D8 or D15. However, we detected a time-lagged relationship where weight at D15 was negatively associated with the microbial diversity at D8, controlling for weight at D8, therefore reflecting relative weight gain over the intervening period. Indicator species analysis revealed that specificity values were high and fidelity values were low, suggesting that indicator taxa were primarily detected within either the survived or not survived groups, but not always detected in birds that either survived or died. Therefore these indicator taxa may be sufficient, but not necessary for determining either survival or mortality, perhaps owing to functional overlap in microbiota. We highlight that measuring microbiome-fitness relationships at just one time point may be misleading, especially early in life. Instead, microbial-host fitness effects may be best investigated longitudinally to detect critical development windows for key microbiota and host traits associated with neonatal weight. Our findings should inform future hypothesis testing to pinpoint which features of the gut microbial community impact on host fitness, and when during development this occurs. Such confirmatory research will shed light on population level processes and could have the potential to support conservation.

Identifiants

pubmed: 33481278
doi: 10.1111/1365-2656.13428
doi:

Substances chimiques

RNA, Ribosomal, 16S 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

989-1003

Informations de copyright

© 2021 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.

Références

Alberdi, A., Aizpurua, O., Bohmann, K., Zepeda-Mendoza, M. L., & Gilbert, M. T. P. (2016). Do vertebrate gut metagenomes confer rapid ecological adaptation? Trends in Ecology & Evolution, 31(9), 689-699. https://doi.org/10.1016/j.tree.2016.06.008
Amato, K. R. (2013). Co-evolution in context: The importance of studying gut microbiomes in wild animals. Microbiome Science and Medicine, 1(1). https://doi.org/10.2478/micsm-2013-0002
Angelakis, E., & Raoult, D. (2010). The increase of Lactobacillus species in the gut flora of newborn broiler chicks and ducks is associated with weight gain. PLoS ONE, 5, https://doi.org/10.1371/journal.pone.0010463
Arnold, K. E., Ramsay, S. L., Donaldson, C., & Adam, A. (2007). Parental prey selection affects risk-taking behaviour and spatial learning in avian offspring. Proceedings of the Royal Society B: Biological Sciences, 274(1625), 2563-2569. https://doi.org/10.1098/rspb.2007.0687
Backhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F., & Gordon, J. I. (2004). The gut microbiota as an environmental factor that regulates fat storage. Proceedings of the National Academy of Sciences of the United States of America, 101(44), 15718-15723. https://doi.org/10.1073/pnas.0407076101
Banerjee, S., Sar, A., Misra, A., Pal, S., Chakraborty, A., & Dam, B. (2018). Increased productivity in poultry birds by sub-lethal dose of antibiotics is arbitrated by selective enrichment of gut microbiota, particularly short-chain fatty acid producers. Microbiology, 164(2), 142-153. https://doi.org/10.1099/mic.0.000597
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48.
Bateson, P., Gluckman, P., & Hanson, M. (2014). The biology of developmental plasticity and the Predictive Adaptive Response hypothesis. The Journal of Physiology, 592(11), 2357-2368. https://doi.org/10.1113/jphysiol.2014.271460
Beaumont, M., Goodrich, J. K., Jackson, M. A., Yet, I., Davenport, E. R., Vieira-Silva, S., Debelius, J., Pallister, T., Mangino, M., Raes, J., Knight, R., Clark, A. G., Ley, R. E., Spector, T. D., & Bell, J. T. (2016). Heritable components of the human fecal microbiome are associated with visceral fat. Genome Biology, 17(1), 189. https://doi.org/10.1186/s13059-016-1052-7
Bender, R., & Lange, S. (2001). Adjusting for multiple testing-when and how? Journal of Clinical Epidemiology, 54(4), 343-349. https://doi.org/10.1016/S0895-4356(00)00314-0
Biagi, E., Franceschi, C., Rampelli, S., Severgnini, M., Ostan, R., Turroni, S., Consolandi, C., Quercia, S., Scurti, M., Monti, D., Capri, M., Brigidi, P., & Candela, M. (2016). Gut microbiota and extreme longevity. Current Biology, 26(11), 1480-1485. https://doi.org/10.1016/j.cub.2016.04.016
Blomberg, E. J., Sedinger, J. S., Gibson, D., Coates, P. S., & Casazza, M. L. (2014). Carryover effects and climatic conditions influence the postfledging survival of greater sage-grouse. Ecology and Evolution, 4(23), 4488-4499. https://doi.org/10.1002/ece3.1139
Both, C., Visser, M. E., & Verboven, N. (1999). Density-dependent recruitment rates in great tits: The importance of being heavier. Proceedings of the Royal Society of London. Series B: Biological Sciences, 266(1418), 465-469. https://doi.org/10.1098/rspb.1999.0660
Bowen, W. D., den Heyer, C. E., McMillan, J. I., & Iverson, S. J. (2015). Offspring size at weaning affects survival to recruitment and reproductive performance of primiparous gray seals. Ecology and Evolution, 5(7), 1412-1424. https://doi.org/10.1002/ece3.1450
Callahan, B. J., McMurdie, P. J., & Holmes, S. P. (2017). Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. The ISME Journal, 11(12), 2639-2643. https://doi.org/10.1038/ismej.2017.119
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581-583. https://doi.org/10.1038/nmeth.3869
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11(4), 265-270.Retrieved from www.jstor.org/stable/4615964
Coates, M. E., Cole, C. B., Fuller, R., Houghton, S. B., & Yokota, H. (1981). The gut microflora and the uptake of glucose from the small intestine of the chick. British Poultry Science, 22(3), 289-294. https://doi.org/10.1080/00071688108447888
Cox, L. M., Yamanishi, S., Sohn, J., Alekseyenko, A. V., Leung, J. M., Cho, I., Kim, S. G., Li, H., Gao, Z., Mahana, D., Zárate Rodriguez, J. G., Rogers, A. B., Robine, N., Loke, P., & Blaser, M. J. (2014). Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell, 158(4), 705-721. https://doi.org/10.1016/j.cell.2014.05.052
Crino, O. L., & Breuner, C. W. (2015). Developmental stress: Evidence for positive phenotypic and fitness effects in birds. Journal of Ornithology, 156(1), 389-398. https://doi.org/10.1007/s10336-015-1236-z
David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., Ling, A. V., Devlin, A. S., Varma, Y., Fischbach, M. A., Biddinger, S. B., Dutton, R. J., & Turnbaugh, P. J. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature, 505(7484), 559-563. https://doi.org/10.1038/nature12820
Davidson, G. L., Raulo, A., & Knowles, S. C. L. (2020). Identifying microbiome-mediated behaviour in wild vertebrates. Trends in Ecology & Evolution, https://doi.org/10.1016/j.tree.2020.06.014
Davidson, G. L., Somers, S. E., Wiley, N., Johnson, C. N., Reichert, M. S., Ross, R. P., Stanton, C., & Quinn, J. L. (2020). Data from: A time-lagged association between the gut microbiome, nestling weight and nestling survival in wild great tits [Dataset]. Dryad, https://doi.org/10.5061/dryad.bk3j9kd9g
Davidson, G. L., Wiley, N., Cooke, A. C., Johson, C. N., Fouhy, F., Reichert, M. S., de la Hera, I., Crane, J. M. S., Kulahci, I. G., Ross, R. P., Stanton, C., & Quinn, J. L. (2020). Diet induces parallel changes to the gut microbiota and problem solving performance in a wild bird. Scientific Reports, 10, 20783. https://doi.org/10.1038/s41598-020-77256-y
De Caceres, M., & Legendre, P. (2009). Associations between species and groups of sites: Indices and statistical inference. Ecology. https://doi.org/10.1890/08-1823.1
De Cáceres, M., Legendre, P., & Moretti, M. (2010). Improving indicator species analysis by combining groups of sites. Oikos, 119(10), 1674-1684. https://doi.org/10.1111/j.1600-0706.2010.18334.x
Drissi, F., Raoult, D., & Merhej, V. (2017). Metabolic role of lactobacilli in weight modification in humans and animals. Microbial Pathogenesis, 106, 182-194. https://doi.org/10.1016/j.micpath.2016.03.006
Eisenhofer, R., Minich, J. J., Marotz, C., Cooper, A., Knight, R., & Weyrich, L. S. (2019). Contamination in low microbial biomass microbiome studies: Issues and recommendations. Trends in Microbiology, 27(2), 105-117. https://doi.org/10.1016/j.tim.2018.11.003
Fettweis, J. M., Serrano, M. G., Brooks, J. P., Edwards, D. J., Girerd, P. H., Parikh, H. I., Huang, B., Arodz, T. J., Edupuganti, L., Glascock, A. L., Xu, J., Jimenez, N. R., Vivadelli, S. C., Fong, S. S., Sheth, N. U., Jean, S., Lee, V., Bokhari, Y. A., Lara, A. M., … Buck, G. A. (2019). The vaginal microbiome and preterm birth. Nature Medicine, 25(6), 1012-1021. https://doi.org/10.1038/s41591-019-0450-2
Ford, D. J., & Coates, M. E. (1971). Absorption of glucose and vitamins of the B complex by germ-free and conventional chicks. The Proceedings of the Nutrition Society, 30(1), 10a-11a.
García-Navas, V., Ferrer, E. S., & Sanz, J. J. (2012). Prey selectivity and parental feeding rates of blue tits Cyanistes caeruleus in relation to nestling age. Bird Study, 59(2), 236-242. https://doi.org/10.1080/00063657.2012.662939
Gatesoupe, F. J. (1999). The use of probiotics in aquaculture. Aquaculture, 180(1), 147-165. https://doi.org/10.1016/S0044-8486(99)00187-8
Gillingham, M. A. F., Béchet, A., Cézilly, F., Wilhelm, K., Rendón-Martos, M., Borghesi, F., Nissardi, S., Baccetti, N., Azafzaf, H., Menke, S., Kayser, Y., & Sommer, S. (2019). Offspring microbiomes differ across breeding sites in a panmictic species. Frontiers in Microbiology, 10, 35. https://doi.org/10.3389/fmicb.2019.00035
Gomes, B. C., Rodrigues, M. R., Winkelströter, L. K., Nomizo, A., & de Martinis, E. C. (2012). In vitro evaluation of the probiotic potential of bacteriocin producer Lactobacillus sakei 1. Journal of Food Protection, 75(6), 1083-1089. https://doi.org/10.4315/0362-028x.Jfp-11-523
Götmark, F. (2002). Predation by sparrowhawks favours early breeding and small broods in great tits. Oecologia, 130(1), 25-32. https://doi.org/10.1007/s004420100769
Hansen, C. H. F., Nielsen, D. S., Kverka, M., Zakostelska, Z., Klimesova, K., Hudcovic, T., Tlaskalova-Hogenova, H., & Hansen, A. K. (2012). Patterns of early gut colonization shape future immune responses of the host. PLoS ONE, 7(3), e34043. https://doi.org/10.1371/journal.pone.0034043
Hartig, F. (2019). DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.3.1.
Heintz-Buschart, A., & Wilmes, P. (2018). Human gut microbiome: Function matters. Trends in Microbiology, 26(7), 563-574. https://doi.org/10.1016/j.tim.2017.11.002
Highet, A. R., Berry, A. M., Bettelheim, K. A., & Goldwater, P. N. (2014). Gut microbiome in sudden infant death syndrome (SIDS) differs from that in healthy comparison babies and offers an explanation for the risk factor of prone position. International Journal of Medical Microbiology, 304(5-6), 735-741. https://doi.org/10.1016/j.ijmm.2014.05.007
Holzapfel, W. H., & Schillinger, U. (2002). Introduction to pre- and probiotics. Food Research International, 35(2), 109-116. https://doi.org/10.1016/S0963-9969(01)00171-5
Hooper, L. V., Littman, D. R., & Macpherson, A. J. (2012). Interactions between the microbiota and the immune system. Science, 336(6086), 1268-1273. https://doi.org/10.1126/science.1223490
Hõrak, P., Lea, T., Ots, I., & Møller, A. P. (1999). Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia, 121(3), 316-322. https://doi.org/10.1007/s004420050934
Keller, L. F., & Van Noordwijk, A. J. (1994). Effects of local environmental-conditions on nestling growth in the Great Tit Parus major. Ardea, 82(2), 349-362.
Khan, G., Kangro, H. O., Coates, P. J., & Heath, R. B. (1991). Inhibitory effects of urine on the polymerase chain reaction for cytomegalovirus DNA. Journal of Clinical Pathology, 44(5), 360-365. https://doi.org/10.1136/jcp.44.5.360
Kinross, J. M., Darzi, A. W., & Nicholson, J. K. (2011). Gut microbiome-host interactions in health and disease. Genome Medicine, 3(3), 14. https://doi.org/10.1186/gm228
Knowles, S. C. L., Eccles, R. M., & Baltrūnaitė, L. (2019). Species identity dominates over environment in shaping the microbiota of small mammals. Ecology Letters, 22(5), 826-837. https://doi.org/10.1111/ele.13240
Koenig, J. E., Spor, A., Scalfone, N., Fricker, A. D., Stombaugh, J., Knight, R., Angenent, L. T., &Ley, R. E. (2010). Succession of microbial consortia in the developing infant gut microbiome. Proceedings of the National Academy of Sciences of the United States of America, 108(Suppl 1), 4578-4585. https://doi.org/10.1073/pnas.1000081107
Kohl, K. D., Brun, A., Bordenstein, S. R., Caviedes-Vidal, E., & Karasov, W. H. (2018). Gut microbes limit growth in house sparrow nestlings (Passer domesticus) but not through limitations in digestive capacity. (1749-4877; Electronic).
Lan, Y., Verstegen, M. W. A., Tamminga, S., & Williams, B. A. (2005). The role of the commensal gut microbial community in broiler chickens. World's Poultry Science Journal, 61(1), 95-104. https://doi.org/10.1079/WPS200445
Le Chatelier, E., Nielsen, T., Qin, J., Prifti, E., Hildebrand, F., Falony, G., Almeida, M., Arumugam, M., Batto, J.-M., Kennedy, S., Leonard, P., Li, J., Burgdorf, K., Grarup, N., Jørgensen, T., Brandslund, I., Nielsen, H. B., Juncker, A. S., Bertalan, M., … Pedersen, O. (2013). Richness of human gut microbiome correlates with metabolic markers. Nature, 500(7464), 541-546. https://doi.org/10.1038/nature12506
LeBlanc, J. G., Chain, F., Martín, R., Bermúdez-Humarán, L. G., Courau, S., & Langella, P. (2017). Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microbial Cell Factories, 16(1), 79. https://doi.org/10.1186/s12934-017-0691-z
Liu, H., Wang, J., He, T., Becker, S., Zhang, G., Li, D., & Ma, X. (2018). Butyrate: A double-edged sword for health? Advances in Nutrition, 9(1), 21-29. https://doi.org/10.1093/advances/nmx009
Lloyd-Price, J., Abu-Ali, G., & Huttenhower, C. (2016). The healthy human microbiome. Genome Medicine, 8(1), 51. https://doi.org/10.1186/s13073-016-0307-y
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K., & Knight, R. (2012). Diversity, stability and resilience of the human gut microbiota. Nature, 489(7415), 220-230. https://doi.org/10.1038/nature11550
Martin, T. E. (2015). Age-related mortality explains life history strategies of tropical and temperate songbirds. Science, 349(6251), 966. https://doi.org/10.1126/science.aad1173
Maurice, C. F., Cl Knowles, S., Ladau, J., Pollard, K. S., Fenton, A., Pedersen, A. B., & Turnbaugh, P. J. (2015). Marked seasonal variation in the wild mouse gut microbiota. The ISME Journal, 9(11), 2423-2434. https://doi.org/10.1038/ismej.2015.53
McKnight, D. T., Huerlimann, R., Bower, D. S., Schwarzkopf, L., Alford, R. A., & Zenger, K. R. (2019). Methods for normalizing microbiome data: An ecological perspective. Methods in Ecology and Evolution, 10(3), 389-400. https://doi.org/10.1111/2041-210X.13115
McMurdie, P. J., & Holmes, S. (2013). phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 8(4), e61217. https://doi.org/10.1371/journal.pone.0061217
Merila, J. (1996). Genetic variation in offspring condition: An experiment. Functional Ecology, 10(4), 465-474. https://doi.org/10.2307/2389939
Mikaela, A. J. B., Mark, G. M., Robertson, D. R., & McCormick, M. I. (2002). Larval growth predicts the recruitment success of a coral reef fish. Oecologia, 131(4), 521-525.Retrieved from http://www.jstor.org/stable/4223286
Monrós, J. S., Belda, E. J., & Barba, E. (2002). Post-fledging survival of individual great tits: The effect of hatching date and fledging mass. Oikos, 99(3), 481-488. https://doi.org/10.1034/j.1600-0706.2002.11909.x
Motiei, A., Brindefalk, B., Ogonowski, M., El-Shehawy, R., Pastuszek, P., Ek, K., Liewenborg, B., Udekwu, K., & Gorokhova, E. (2020). Disparate effects of antibiotic-induced microbiome change and enhanced fitness in Daphnia magna. PLoS ONE, 15(1), e0214833. https://doi.org/10.1371/journal.pone.0214833
Norris, K. (1993). Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature, 362(6420), 537-539. https://doi.org/10.1038/362537a0
O'Hara, A. M., & Shanahan, F. (2006). The gut flora as a forgotten organ. EMBO Reports, 7(7), 688-693. https://doi.org/10.1038/sj.embor.7400731
Oksanen, J., Guillaume Blanchet, F., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R, O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E., & Wagner, H. (2019). vegan: Community ecology package (version R package version 2.5-6).
Olszak, T., An, D., Zeissig, S., Vera, M. P., Richter, J., Franke, A., Glickman, J. N., Siebert, R., Baron, R. M., Kasper, D. L., & Blumberg, R. S. (2012). Microbial exposure during early life has persistent effects on natural killer T cell function. Science, 336(6080), 489-493. https://doi.org/10.1126/science.1219328
O'Shea, W., O'Halloran, J., & Quinn, J. L. (2018). Breeding phenology, provisioning behaviour, and unusual patterns of life history variation across an anthropogenic heterogeneous landscape. Oecologia, 188, 953-964. https://doi.org/10.1007/s00442-018-4155-x
Patrick, S. C., & Weimerskirch, H. (2014). Personality, foraging and fitness consequences in a long lived seabird. PLoS ONE, 9(2), e87269. https://doi.org/10.1371/journal.pone.0087269
Patterson, J. A., Orban, J. I., Sutton, A. L., & Richards, G. N. (1997). Selective enrichment of bifidobacteria in the intestinal tract of broilers by thermally produced kestoses and effect on broiler performance. Poultry Science, 76(3), 497-500. https://doi.org/10.1093/ps/76.3.497
Pickett, S. R. A., Weber, S. B., McGraw, K. J., Norris, K. J., & Evans, M. R. (2013). Environmental and parental influences on offspring health and growth in great tits (Parus major). PLoS ONE, 8(7), e69695. https://doi.org/10.1371/journal.pone.0069695
Potti, J., Moreno, J., Yorio, P., Briones, V., García-Borboroglu, P., Villar, S., & Ballesteros, C. (2002). Bacteria divert resources from growth for magellanic penguin chicks. Ecology Letters, 5(6), 709-714. https://doi.org/10.1046/j.1461-0248.2002.00375.x
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2012). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590-D596. https://doi.org/10.1093/nar/gks1219
R Core Team. (2019). R: A language and environment for statistical computing (version 3.5.1). R Foundation for Statistical Computing.
Ranstam, J. (2019). Hypothesis-generating and confirmatory studies, Bonferroni correction, and pre-specification of trial endpoints. Acta Orthopaedica, 90(4), 297. https://doi.org/10.1080/17453674.2019.1612624
Ratajczak, W., Rył, A., Mizerski, A., Walczakiewicz, K., Sipak, O., & Laszczyńska, M. (2019). Immunomodulatory potential of gut microbiome-derived short-chain fatty acids (SCFAs). Acta Biochimica Polonica, 66(1), 1-12. https://doi.org/10.18388/abp.2018_2648
Rauw, W. M. (2012). Immune response from a resource allocation perspective. Frontiers in Genetics, 3, 267. https://doi.org/10.3389/fgene.2012.00267
Ringsby, T. H., Saether, B.-E., & Solberg, E. J. (1998). Factors affecting juvenile survival in house sparrow Passer domesticus. Journal of Avian Biology, 29(3), 241-247. https://doi.org/10.2307/3677106
Rosshart, S. P., Vassallo, B. G., Angeletti, D., Hutchinson, D. S., Morgan, A. P., Takeda, K., Hickman, H. D., McCulloch, J. A., Badger, J. H., Ajami, N. J., Trinchieri, G., Pardo-Manuel de Villena, F., Yewdell, J. W., & Rehermann, B. (2017). Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell, 171(5), 1015-1028.e1013. https://doi.org/10.1016/j.cell.2017.09.016
Rowland, I., Gibson, G., Heinken, A., Scott, K., Swann, J., Thiele, I., & Tuohy, K. (2018). Gut microbiota functions: Metabolism of nutrients and other food components. European Journal of Nutrition, 57(1), 1-24. https://doi.org/10.1007/s00394-017-1445-8
Schwagmeyer, P. L., & Mock, D. W. (2008). Parental provisioning and offspring fitness: Size matters. Animal Behaviour, 75(1), 291-298. https://doi.org/10.1016/j.anbehav.2007.05.023
Shannon, C. E. (1948). A mathematical theory of communication. Bell System Technical Journal, 27(3), 379-423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Sherwin, E., Bordenstein, S. R., Quinn, J. L., Dinan, T. G., & Cryan, J. F. (2019). Microbiota and the social brain. Science, 366(6465). https://doi.org/10.1126/science.aar2016
Shutt, J. D., Nicholls, J. A., Trivedi, U. H., Burgess, M. D., Stone, G. N., Hadfield, J. D., & Phillimore, A. B. (2020). Gradients in richness and turnover of a forest passerine's diet prior to breeding: A mixed model approach applied to faecal metabarcoding data. Molecular Ecology, 29(6), 1199-1213. https://doi.org/10.1111/mec.15394
Song, S. J., Sanders, J. G., Delsuc, F., Metcalf, J., Amato, K., Taylor, M. W., Mazel, F., Lutz, H. L., Winker, K., Graves, G. R., Humphrey, G., Gilbert, J. A., Hackett, S. J., White, K. P., Skeen, H. R., Kurtis, S. M., Withrow, J., Braile, T., Miller, M., … Knight, R. (2020). Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. MBio, 11(1), e02901-02919. https://doi.org/10.1128/mBio.02901-19
Spencer, K. A., Evans, N. P., & Monaghan, P. (2009). Postnatal stress in birds: A novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology, 150(4), 1931-1934. https://doi.org/10.1210/en.2008-1471
Stige, L. C., Rogers, L. A., Neuheimer, A. B., Hunsicker, M. E., Yaragina, N. A., Ottersen, G., Ciannelli, L., Langangen, Ø., & Durant, J. M. (2019). Density- and size-dependent mortality in fish early life stages. Fish and Fisheries, 20(5), 962-976. https://doi.org/10.1111/faf.12391
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X.-N., Kubo, C., &Koga, Y. (2004). Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. The Journal of Physiology, 558(1), 263-275. https://doi.org/10.1113/jphysiol.2004.063388
Suzuki, T. A. (2017). Links between natural variation in the microbiome and host fitness in wild mammals. Integrative and Comparative Biology, 57(4), 756-769. https://doi.org/10.1093/icb/icx104
Teyssier, A., Lens, L., Matthysen, E., & White, J. (2018). Dynamics of gut microbiota diversity during the early development of an avian host: Evidence from a cross-foster experiment. Frontiers in Microbiology, 9, 1524. https://doi.org/10.3389/fmicb.2018.01524
Teyssier, A., Rouffaer, L. O., Hudin, N. S., Strubbe, D., Matthysen, E., Lens, L., & White, J. (2018). Inside the guts of the city: Urban-induced alterations of the gut microbiota in a wild passerine. Science of The Total Environment, 612, 1276-1286. https://doi.org/10.1016/j.scitotenv.2017.09.035
Therneau, T. M. (2020). coxme: Mixed effects cox models (version R package version 2.2-16). Retrieved from https://CRAN.R-project.org/package=coxme
Torok, V. A., Hughes, R. J., Mikkelsen, L. L., Perez-Maldonado, R., Balding, K., MacAlpine, R., Percy, N. J., & Ophel-Keller, K. (2011). Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials. Applied and Environmental Microbiology, 77(17), 5868-5878. https://doi.org/10.1128/AEM.00165-11
Trevelline, B. K., Fontaine, S. S., Hartup, B. K., & Kohl, K. D. (2019). Conservation biology needs a microbial renaissance: A call for the consideration of host-associated microbiota in wildlife management practices. Proceedings of the Royal Society B: Biological Sciences, 286(1895), 20182448. https://doi.org/10.1098/rspb.2018.2448
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006). An obesity-associated gut microbiome with increased capacity for energy harvest. Nature, 444, 1027-1031. https://doi.org/10.1038/nature05414
Van Noordwijk, A. J., McCleery, R. H., & Perrins, C. M. (1995). Selection for the timing of great tit breeding in relation to caterpillar growth and temperature. Journal of Animal Ecology, 64(4), 451-458. https://doi.org/10.2307/5648
Vargas-Pellicer, P., Watrobska, C., Knowles, S., Schroeder, J., & Banks-Leite, C. (2019). How should we store avian faecal samples for microbiota analyses? Comparing efficacy and cost-effectiveness. Journal of Microbiological Methods, 165, 105689. https://doi.org/10.1016/j.mimet.2019.105689
Vásquez, A., Forsgren, E., Fries, I., Paxton, R. J., Flaberg, E., Szekely, L., & Olofsson, T. C. (2012). Symbionts as major modulators of insect health: Lactic acid bacteria and honeybees. PLoS ONE, 7(3), e33188. https://doi.org/10.1371/journal.pone.0033188
Videvall, E., Song, S. J., Bensch, H. M., Strandh, M., Engelbrecht, A., Serfontein, N., Hellgren, O., Olivier, A., Cloete, S., Knight, R., & Cornwallis, C. K. (2019). Major shifts in gut microbiota during development and its relationship to growth in ostriches. Molecular Ecology, 28(10), 2653-2667. https://doi.org/10.1111/mec.15087
Videvall, E., Song, S. J., Bensch, H. M., Strandh, M., Engelbrecht, A., Serfontein, N., Hellgren, O., Olivier, A., Cloete, S., Knight, R., & Cornwallis, C. K. (2020). Early-life gut dysbiosis linked to juvenile mortality in ostriches. Microbiome, 8(1), 147. https://doi.org/10.1186/s40168-020-00925-7
Videvall, E., Strandh, M., Engelbrecht, A., Cloete, S., & Cornwallis, C. K. (2018). Measuring the gut microbiome in birds: Comparison of faecal and cloacal sampling. Molecular Ecology Resources, 18(3), 424-434. https://doi.org/10.1111/1755-0998.12744
Vispo, C., & Karasov, W. H. (1997). The interaction of avian gut microbes and their host: An elusive symbiosis. (pp. 116-155). R. I. Mackie & B. A. White (Eds.). Springer.
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261-5267. https://doi.org/10.1128/AEM.00062-07
Warnecke, F., Luginbühl, P., Ivanova, N., Ghassemian, M., Richardson, T. H., Stege, J. T., Cayouette, M., McHardy, A. C., Djordjevic, G., Aboushadi, N., Sorek, R., Tringe, S. G., Podar, M., Martin, H. G., Kunin, V., Dalevi, D., Madejska, J., Kirton, E., Platt, D., … Leadbetter, J. R. (2007). Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature, 450(7169), 560-565. https://doi.org/10.1038/nature06269
Wasielewski, H., Alcock, J., & Aktipis, A. (2016). Resource conflict and cooperation between human host and gut microbiota: Implications for nutrition and health. Annals of the New York Academy of Sciences, 1372(1), 20-28. https://doi.org/10.1111/nyas.13118
Weber, B. M., Bowers, E. K., Terrell, K. A., Falcone, J. F., Thompson, C. F., & Sakaluk, S. K. (2018). Pre- and postnatal effects of experimentally manipulated maternal corticosterone on growth, stress reactivity and survival of nestling house wrens. Functional Ecology, 32(8), 1995-2007. https://doi.org/10.1111/1365-2435.13126
West, A. G., Waite, D. W., Deines, P., Bourne, D. G., Digby, A., McKenzie, V. J., & Taylor, M. W. (2019). The microbiome in threatened species conservation. Biological Conservation, 229, 85-98. https://doi.org/10.1016/j.biocon.2018.11.016
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer-Verlag.
Youngblut, N. D., Reischer, G. H., Walters, W., Schuster, N., Walzer, C., Stalder, G., Ley, R. E., & Farnleitner, A. H. (2019). Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nature Communications, 10(1), 2200. https://doi.org/10.1038/s41467-019-10191-3
Zaneveld, J. R., McMinds, R., & Vega Thurber, R. (2017). Stress and stability: Applying the Anna Karenina principle to animal microbiomes. Nature Microbiology, 2(9), 17121. https://doi.org/10.1038/nmicrobiol.2017.121
Zhu, L., Wu, Q., Dai, J., Zhang, S., & Wei, F. (2011). Evidence of cellulose metabolism by the giant panda gut microbiome. Proceedings of the National Academy of Sciences of United States of America, 108(43), 17714. https://doi.org/10.1073/pnas.1017956108
Zimmer, C., Boogert, N. J., & Spencer, K. A. (2013). Developmental programming: Cumulative effects of increased pre-hatching corticosterone levels and post-hatching unpredictable food availability on physiology and behaviour in adulthood. Hormones and Behavior, 64(3), 494-500. https://doi.org/10.1016/j.yhbeh.2013.07.002

Auteurs

Gabrielle L Davidson (GL)

School of Biological, Earth and Environmental Sciences, University College Cork, Cork, Ireland.
Department of Psychology, University of Cambridge, Cambridge, UK.

Shane E Somers (SE)

School of Biological, Earth and Environmental Sciences, University College Cork, Cork, Ireland.

Niamh Wiley (N)

APC Microbiome Ireland, University College Cork, Cork, Ireland.
Teagasc Food Research Centre, Moorepark, Ireland.

Crystal N Johnson (CN)

APC Microbiome Ireland, University College Cork, Cork, Ireland.
Teagasc Food Research Centre, Moorepark, Ireland.

Michael S Reichert (MS)

School of Biological, Earth and Environmental Sciences, University College Cork, Cork, Ireland.
Department of Integrative Biology, Oklahoma State University, Stillwater, OK, USA.

R Paul Ross (RP)

APC Microbiome Ireland, University College Cork, Cork, Ireland.
Teagasc Food Research Centre, Moorepark, Ireland.

Catherine Stanton (C)

APC Microbiome Ireland, University College Cork, Cork, Ireland.
Teagasc Food Research Centre, Moorepark, Ireland.

John L Quinn (JL)

School of Biological, Earth and Environmental Sciences, University College Cork, Cork, Ireland.
Environmental Research Institute, University College Cork, Cork, Ireland.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH