Gut microbial diversity increases with social rank in the African cichlid fish, Astatotilapia burtoni

被引:7
作者
Singh, Avehi [1 ]
Faber-Hammond, Joshua J. [1 ]
O'Rourke, Cynthia E. [1 ]
Renn, Suzy C. P. [1 ]
机构
[1] Reed Coll, Dept Biol, 3203 SE Woodstock Blvd, Portland, OR 97202 USA
基金
美国国家科学基金会;
关键词
cichlid; microbiome; microbiota; social hierarchy; CHAIN FATTY-ACIDS; REPRODUCTIVE SUCCESS; HAPLOCHROMIS-BURTONI; METABOLIC-RATE; DIRTY MICE; STRESS; DOMINANCE; HEALTH; DIET; PLASTICITY;
D O I
10.1016/j.anbehav.2019.04.003
中图分类号
B84 [心理学]; C [社会科学总论]; Q98 [人类学];
学科分类号
03 ; 0303 ; 030303 ; 04 ; 0402 ;
摘要
Social dominance hierarchies are a common system of within-group social ranking. Animals occupying subordinate and dominant ranks within these hierarchies differ in their access to food and mating opportunities. Thus, these animals often have different levels of stress, energy reserves and metabolic activity, leading to distinctive behavioural and physiological phenotypes. We hypothesized that phenotypes associated with social rank would affect the gut microbiome, a community of microbes intimately involved in host physiological and metabolic processes. Using male Astatotilapia burtoni, a well-studied species of cichlid, we implemented noninvasive sampling techniques to track microbial variation within individuals occupying different ranks. Our results indicated a lag between the behavioural and physiological changes and microbial community shifts associated with rank change. Given this, subordinate males had higher levels of pathogenic clades and decreased overall community diversity (alpha diversity) while dominant males had higher levels of protective clades and increased alpha diversity. The distributions of several differentially abundant operational taxonomic units (OTUs) were highly correlated with alpha diversity, suggesting that these clades might be involved in structuring the community as a whole. Taken together, our results indicate that behavioural and phenotypic states associated with social rank induce dynamic, population-level shifts in microbiome composition, an effect putatively mediated by the presence of certain bacterial clades. This study is one of the first to evaluate and track the effects of social rank on teleost microbiomes and highlights the importance of integrating microbiome-derived physiological effects into future studies of behaviour. (C) 2019 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.
引用
收藏
页码:79 / 91
页数:13
相关论文
共 126 条
  • [11] Structural & functional consequences of chronic psychosocial stress on the microbiome & host
    Bharwani, Aadil
    Mian, M. Firoz
    Foster, Jane A.
    Surette, Michael G.
    Bienenstock, John
    Forsythe, Paul
    [J]. PSYCHONEUROENDOCRINOLOGY, 2016, 63 : 217 - 227
  • [12] Animal models of social stress: Effects on behavior and brain neurochemical systems
    Blanchard, RJ
    McKittrick, CR
    Blanchard, DC
    [J]. PHYSIOLOGY & BEHAVIOR, 2001, 73 (03) : 261 - 271
  • [13] AN ANALYSIS OF TRANSFORMATIONS
    BOX, GEP
    COX, DR
    [J]. JOURNAL OF THE ROYAL STATISTICAL SOCIETY SERIES B-STATISTICAL METHODOLOGY, 1964, 26 (02) : 211 - 252
  • [14] Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling?
    Buchanan, KL
    Evans, MR
    Goldsmith, AR
    Bryant, DM
    Rowe, LV
    [J]. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2001, 268 (1474) : 1337 - 1344
  • [15] Rapid behavioral and genomic responses to social opportunity
    Burmeister, SS
    Jarvis, ED
    Fernald, RD
    [J]. PLOS BIOLOGY, 2005, 3 (11) : 1996 - 2004
  • [16] The role of short chain fatty acids in appetite regulation and energy homeostasis
    Byrne, C. S.
    Chambers, E. S.
    Morrison, D. J.
    Frost, G.
    [J]. INTERNATIONAL JOURNAL OF OBESITY, 2015, 39 (09) : 1331 - 1338
  • [17] Food availability affects the strength of mutualistic host-microbiota interactions in Daphnia magna
    Callens, Martijn
    Macke, Emilie
    Muylaert, Koenraad
    Bossier, Peter
    Lievens, Bart
    Waud, Michael
    Decaestecker, Ellen
    [J]. ISME JOURNAL, 2016, 10 (04) : 911 - 920
  • [18] Social stress results in altered glucocorticoid regulation and shorter survival in simian acquired immune deficiency syndrome
    Capitanio, JP
    Mendoza, SP
    Lerche, NW
    Mason, WA
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1998, 95 (08) : 4714 - 4719
  • [19] QIIME allows analysis of high-throughput community sequencing data
    Caporaso, J. Gregory
    Kuczynski, Justin
    Stombaugh, Jesse
    Bittinger, Kyle
    Bushman, Frederic D.
    Costello, Elizabeth K.
    Fierer, Noah
    Pena, Antonio Gonzalez
    Goodrich, Julia K.
    Gordon, Jeffrey I.
    Huttley, Gavin A.
    Kelley, Scott T.
    Knights, Dan
    Koenig, Jeremy E.
    Ley, Ruth E.
    Lozupone, Catherine A.
    McDonald, Daniel
    Muegge, Brian D.
    Pirrung, Meg
    Reeder, Jens
    Sevinsky, Joel R.
    Tumbaugh, Peter J.
    Walters, William A.
    Widmann, Jeremy
    Yatsunenko, Tanya
    Zaneveld, Jesse
    Knight, Rob
    [J]. NATURE METHODS, 2010, 7 (05) : 335 - 336
  • [20] Sirtuins mediate mammalian metabolic responses to nutrient availability
    Chalkiadaki, Angeliki
    Guarente, Leonard
    [J]. NATURE REVIEWS ENDOCRINOLOGY, 2012, 8 (05) : 287 - 296