Towards an Evolutionary Model of Animal-Associated Microbiomes

Abstract

Second-generation sequencing technologies have granted us greater access to the diversity and genetics of microbial communities that naturally reside endo-and ecto-symbiotically with animal hosts. Substantial research has emerged describing the diversity and broader trends that exist within and between host species and their associated microbial ecosystems, yet the application of these data to our evolutionary understanding of microbiomes appears fragmented. For the most part biological perspectives are based on limited observations of oversimplified communities, while mathematical and/or computational modeling of these concepts often lack biological precedence. In recognition of this disconnect, both fields have attempted to incorporate ecological theories, although their applicability is currently a subject of debate because most ecological theories were developed based on observations of macro-organisms and their ecosystems. For the OPEN ACCESSEntropy 2011, 13 571 purposes of this review, we attempt to transcend the biological, ecological and computational realms, drawing on extensive literature, to forge a useful framework that can, at a minimum be built upon, but ideally will shape the hypotheses of each field as they move forward. In evaluating the top-down selection pressures that are exerted on a microbiome we find cause to warrant reconsideration of the much-maligned theory of multi-level selection and reason that complexity must be underscored by modularity.

The Howler Monkey as a Model for Exploring Host-Gut Microbiota Interactions in Primates

“…However, it is also possible that gut microbial communities co-diversifi ed and coevolved with their hosts, leading to specializations and increased dependence between the host and its microbial colonists (Kau et al 2011 ;Yeoman et al 2011 ). Recent studies analyzing bacterial 16S ribosomal RNA gene sequences from 60 mammalian species (Ley et al 2008a , b ) indicate that gut bacterial diversity may be affected by host phylogeny since the fecal microbial communities of conspecifi c hosts are more similar to each other than to the communities of more distantly related hosts.…”

Sex differences in the gut microbiome–brain axis across the lifespan

“…However, expansion of the human frontal cortex occurred at the cost of other metabolically expensive tissues, such as the gastrointestinal tract, suggesting coevolution of the gut and brain where expansion of the brain resulted in a corresponding reduction in overall size of the gut [1]. Paradoxically, the reduction of the mammalian gut was paralleled by increased capacity to synthesize essential amino acids, ferment complex carbohydrates and more efficiently extract energy, suggesting an essential coevolution between bacterial communities residing within the gut and increased metabolic demands necessary for an energetically expensive brain [4]. This coevolution between host and microbe has been recently suggested to impact the expression of an array of phenotypes across the lifespan, and the evolutionary processes driving these interactions have been the focus of a number of excellent reviews [5][6][7][8][9].…”

Co-evolution in context: The importance of studying gut microbiomes in wild animals

“…Because host-gut microbe relationships are influenced to some extent by host genotype, and gut microbial community composition differs according to host phylogeny [34][35][36], discussions of the co-evolution of host and gut microbiota are common in the current literature [7,[34][35][36][37]. Some researchers argue that since microbes are found in animals as simple as earthworms, the co-evolution of animals and bacteria has been Co-evolution in context: The importance of studying gut microbiomes in wild animals Abstract Because the gut microbiota contributes to host nutrition, health and behavior, and gut microbial community composition differs according to host phylogeny, co-evolution is believed to have been an important mechanism in the formation of the host-gut microbe relationship.…”

“…Changes in the composition of the gut microbial community are known to lead to changes in its function, which can alter host nutrition, health and behavior [6,[13][14][15][16][17][18][19][20][21][22][23]. Environmental factors such as diet or social contact are largely responsible for determining the composition of the gut microbial community [24][25][26][27][28][29][30][31], but host genotype also affects the abundances of some microbial genera [28,32,33].Because host-gut microbe relationships are influenced to some extent by host genotype, and gut microbial community composition differs according to host phylogeny [34][35][36], discussions of the co-evolution of host and gut microbiota are common in the current literature [7,[34][35][36][37]. Some researchers argue that since microbes are found in animals as simple as earthworms, the co-evolution of animals and bacteria has been Co-evolution in context: The importance of studying gut microbiomes in wild animals Abstract Because the gut microbiota contributes to host nutrition, health and behavior, and gut microbial community composition differs according to host phylogeny, co-evolution is believed to have been an important mechanism in the formation of the host-gut microbe relationship.…”