Zilber-Rosenberg and Rosenberg 2008; Brinker et al. 2019). Resulting host–microbe
interactions may be the key to understand major animal and plant evolutionary
events (McFall-Ngai et al. 2013; Foster et al. 2017). For example, the radiation of
ruminants (McFall-Ngai et al. 2013), specialization of insects’ diets (Janson et al.
2008; Hongoh 2010) or the invasion of land by plants (Martin et al. 2017), were
likely triggered by microbes giving hosts access to otherwise inaccessible nutrients.
In these and other niche diversification events, microbial communities altered host
evolutionary trajectories by persistently performing complex functions. Even though
it seems key to understanding the evolution of life on Earth (Foster et al. 2017; Zeng
et al. 2017; Henry et al. 2019; van Vliet and Doebeli 2019), we still struggle to
identify the ecological mechanisms that maintain function in host-associated microbial communities.
With the advent of better and cheaper molecular techniques, we have moved
beyond regarding microbes as a “black box,” and started considering complex
interactions between microbial species and their environment in closer detail (Blaser
2014; Widder et al. 2016; Julliand and Grimm 2016). In the last 20 years, studies
taking advantage of new sequencing technologies have revealed how microbial
diversity and composition change in time and space (Gonzalez et al. 2012; Lauber
et al. 2013; Shade et al. 2013). In fact, the microbial communities associated with
hosts vary dramatically in composition and function across time and space
(Turnbaugh and Gordon 2009; Costello et al. 2009; Louca et al. 2016a). Part of
this variation responds to changes in the host’s development, health status, and the
surrounding environment (Kraal et al. 2014; Oh et al. 2016; Dunphy et al. 2019), yet
a large proportion remains unexplained (Huttenhower and The Human Microbiome
Project Consortium 2012; Louca et al. 2016a, Cao et al. 2017). This lack of
explanatory power highlights important gaps in our understanding of microbial
community dynamics and their consequences for host–microbe interactions.
An important aspect of this gap is the role diversity plays in shaping microbial
function. In the literature, microbial diversity is often equated to function (Reese and
Dunn 2018). Traditionally, gut microbial communities with high diversity are
assumed to be more efficient contributors to digestion and harder to invade by
pathogens, just as more diverse forests and coral reefs are considered to be more
productive and unlikely to recruit invasive species (Balser et al. 2006; Allison and
Martiny 2008). Within their guts and other body parts, most hosts maintain diverse
communities that are assumed to correlate with high functional stability, functional
diversity and, in general, benefits to host fitness (Hongoh 2010; Philippot et al. 2013;
McFall-Ngai et al. 2013). However, diverse microbial communities have also been
linked to a higher likelihood of cheater strains, opportunistic pathogens, and unstable
dynamics (Coyte et al. 2015; Foster et al. 2017; Coyte and Rakoff-Nahoum 2019).
Some hosts filter the incoming microbes to such extent that community membership
is restricted to one or few species. An extreme example is the Bobtail Squid’s
selection of a single species, a highly functional symbiont within its light organ
(Nyholm and McFall-Ngai 2004). We need to consider this mismatch between
diversity and function if we aim to understand when hosts should maintain diverse
298
C. Cuellar-Gempeler
interactions may be the key to understand major animal and plant evolutionary
events (McFall-Ngai et al. 2013; Foster et al. 2017). For example, the radiation of
ruminants (McFall-Ngai et al. 2013), specialization of insects’ diets (Janson et al.
2008; Hongoh 2010) or the invasion of land by plants (Martin et al. 2017), were
likely triggered by microbes giving hosts access to otherwise inaccessible nutrients.
In these and other niche diversification events, microbial communities altered host
evolutionary trajectories by persistently performing complex functions. Even though
it seems key to understanding the evolution of life on Earth (Foster et al. 2017; Zeng
et al. 2017; Henry et al. 2019; van Vliet and Doebeli 2019), we still struggle to
identify the ecological mechanisms that maintain function in host-associated microbial communities.
With the advent of better and cheaper molecular techniques, we have moved
beyond regarding microbes as a “black box,” and started considering complex
interactions between microbial species and their environment in closer detail (Blaser
2014; Widder et al. 2016; Julliand and Grimm 2016). In the last 20 years, studies
taking advantage of new sequencing technologies have revealed how microbial
diversity and composition change in time and space (Gonzalez et al. 2012; Lauber
et al. 2013; Shade et al. 2013). In fact, the microbial communities associated with
hosts vary dramatically in composition and function across time and space
(Turnbaugh and Gordon 2009; Costello et al. 2009; Louca et al. 2016a). Part of
this variation responds to changes in the host’s development, health status, and the
surrounding environment (Kraal et al. 2014; Oh et al. 2016; Dunphy et al. 2019), yet
a large proportion remains unexplained (Huttenhower and The Human Microbiome
Project Consortium 2012; Louca et al. 2016a, Cao et al. 2017). This lack of
explanatory power highlights important gaps in our understanding of microbial
community dynamics and their consequences for host–microbe interactions.
An important aspect of this gap is the role diversity plays in shaping microbial
function. In the literature, microbial diversity is often equated to function (Reese and
Dunn 2018). Traditionally, gut microbial communities with high diversity are
assumed to be more efficient contributors to digestion and harder to invade by
pathogens, just as more diverse forests and coral reefs are considered to be more
productive and unlikely to recruit invasive species (Balser et al. 2006; Allison and
Martiny 2008). Within their guts and other body parts, most hosts maintain diverse
communities that are assumed to correlate with high functional stability, functional
diversity and, in general, benefits to host fitness (Hongoh 2010; Philippot et al. 2013;
McFall-Ngai et al. 2013). However, diverse microbial communities have also been
linked to a higher likelihood of cheater strains, opportunistic pathogens, and unstable
dynamics (Coyte et al. 2015; Foster et al. 2017; Coyte and Rakoff-Nahoum 2019).
Some hosts filter the incoming microbes to such extent that community membership
is restricted to one or few species. An extreme example is the Bobtail Squid’s
selection of a single species, a highly functional symbiont within its light organ
(Nyholm and McFall-Ngai 2004). We need to consider this mismatch between
diversity and function if we aim to understand when hosts should maintain diverse
298
C. Cuellar-Gempeler