host-associated microbial communities, such as algae surfaces (Burke et al. 2011),
salamander skin (Barnes et al. 2020), bovine rumen (Weimer 2015), and the adult
human intestine (Rakoff-Nahoum et al. 2014). The prevalence of this redundancy
model is unsurprising, since theory predicts that redundancy will evolve in all
ecosystems through a combination of competition, and stochastic processes
(Scheffer and van Nes 2006, but see Barabás et al. 2013, Vergnon et al. 2013),
and it has been proposed as a paradigm in microbial ecology where functional
diversity and variability are constrained by energetic and stoichiometric factors
(such as the availability of electron acceptors for respiration, Raes et al. 2011,
Nelson et al. 2016, Louca et al. 2016b).
In contrast to these positive diversity–function relationships, some hosts maintain
species-poor microbial communities. For example, insects with specific diets, such
as bees and aphids, are often found in association with low diversity microbial
communities (Cariveau et al. 2014; Smith et al. 2015; Gauthier et al. 2015). Because
increased diversity or changes in composition potentially reduce function and thus
impact host’s fitness, these hosts have little variation in their microbial communities.
Therefore, we will probably not find these hosts harboring a diverse community, and
test its effect on fitness. Nonetheless, we can follow a simple thought experiment to
explore what is going on here: imagine a scenario where the functional and efficient
species is a poor competitor, and its functional rates and abundance decrease if local
resources are occupied by other, less functional species. Then, it would be beneficial
for the host to strictly control membership to functional species, constraining
recruitment of other taxa.
This scenario corresponds to the negative selection model where increased
diversity results in diminishing ecosystem function rates (Fig. 17.2c, Jiang et al.
2008). Negative selection has been registered in environmental bacteria, where
certain functions decrease along biodiversity gradients. For example, single species
often provide important rate-limiting functions such as chitin and cellulose degradation that drive processes like litter decomposition and nutrient cycling in lakes
(Peter et al. 2011). Functions under negative selection have more specific metabolic
pathways, narrow phylogenetic constraints, or energetically expensive reactions
(Delgado-Baquerizo et al. 2016). A potential example in host–microbe interactions
is nitrogen fixation by rhizobia in association with Acacia sp. plants. Barrett and
collaborators (Barrett et al. 2015) used a manipulative experiment to show that
increased rhizobia diversity resulted in lower nitrogen provision due to increase
competition. Nitrogen fixation is extremely energetically intensive and few taxa
maintain the genes for the necessary nitrogenase enzyme (see Chap. 8 in this
volume).
Studies that manipulate host-associated microbial diversity provide direct insight
into how diversity influences microbiome function. Most of these experiments
include the inoculation of sterile hosts with microbial isolates, while controlling
for diversity (number of species) and composition (species identities). A common
finding is that, while diversity correlates with function, species composition also has
an important effect, suggesting that many functions are driven by specific species or
specific networks of species. For example, Faith et al. (2014) found that germ-free
17 Diversity–Function Relationships and the Underlying Ecological Mechanisms in. . .
307
salamander skin (Barnes et al. 2020), bovine rumen (Weimer 2015), and the adult
human intestine (Rakoff-Nahoum et al. 2014). The prevalence of this redundancy
model is unsurprising, since theory predicts that redundancy will evolve in all
ecosystems through a combination of competition, and stochastic processes
(Scheffer and van Nes 2006, but see Barabás et al. 2013, Vergnon et al. 2013),
and it has been proposed as a paradigm in microbial ecology where functional
diversity and variability are constrained by energetic and stoichiometric factors
(such as the availability of electron acceptors for respiration, Raes et al. 2011,
Nelson et al. 2016, Louca et al. 2016b).
In contrast to these positive diversity–function relationships, some hosts maintain
species-poor microbial communities. For example, insects with specific diets, such
as bees and aphids, are often found in association with low diversity microbial
communities (Cariveau et al. 2014; Smith et al. 2015; Gauthier et al. 2015). Because
increased diversity or changes in composition potentially reduce function and thus
impact host’s fitness, these hosts have little variation in their microbial communities.
Therefore, we will probably not find these hosts harboring a diverse community, and
test its effect on fitness. Nonetheless, we can follow a simple thought experiment to
explore what is going on here: imagine a scenario where the functional and efficient
species is a poor competitor, and its functional rates and abundance decrease if local
resources are occupied by other, less functional species. Then, it would be beneficial
for the host to strictly control membership to functional species, constraining
recruitment of other taxa.
This scenario corresponds to the negative selection model where increased
diversity results in diminishing ecosystem function rates (Fig. 17.2c, Jiang et al.
2008). Negative selection has been registered in environmental bacteria, where
certain functions decrease along biodiversity gradients. For example, single species
often provide important rate-limiting functions such as chitin and cellulose degradation that drive processes like litter decomposition and nutrient cycling in lakes
(Peter et al. 2011). Functions under negative selection have more specific metabolic
pathways, narrow phylogenetic constraints, or energetically expensive reactions
(Delgado-Baquerizo et al. 2016). A potential example in host–microbe interactions
is nitrogen fixation by rhizobia in association with Acacia sp. plants. Barrett and
collaborators (Barrett et al. 2015) used a manipulative experiment to show that
increased rhizobia diversity resulted in lower nitrogen provision due to increase
competition. Nitrogen fixation is extremely energetically intensive and few taxa
maintain the genes for the necessary nitrogenase enzyme (see Chap. 8 in this
volume).
Studies that manipulate host-associated microbial diversity provide direct insight
into how diversity influences microbiome function. Most of these experiments
include the inoculation of sterile hosts with microbial isolates, while controlling
for diversity (number of species) and composition (species identities). A common
finding is that, while diversity correlates with function, species composition also has
an important effect, suggesting that many functions are driven by specific species or
specific networks of species. For example, Faith et al. (2014) found that germ-free
17 Diversity–Function Relationships and the Underlying Ecological Mechanisms in. . .
307