Metabolic adaptation and consumer diversification
The network structure of fatty acid metabolism, including the modularity
and degree of pleiotropy, has important consequences for understanding
how organisms evolve and diversify over time. For instance, while the
primary photosynthetic pathways of plants are highly conserved, some of
its components have diversified widely, culminating in lineage-specific
pathway regulation and structure
(Maeda 2019). As a
consequence of network structure, evolutionary changes at early steps
within photosynthesis can have more substantial effects on final
products than those that occur in later steps (Kacser and Burns 1981;
Wright and Rausher 2010; Olson-Manning et al. 2012). In consumers, the
evolution of metabolic networks has allowed them to utilize new
resources or synthesize essential organic compounds that were previously
required from diet (Borenstein et al. 2008; Wagner 2012). Within a
lineage, species can differ in the number and connectivity of modules in
metabolic networks as well as in synthesis activities across the
network. The evolution of carotenoid networks in birds, for example, has
led to considerable variation in the structure (i.e., gain and loss of
modules) and connectivity of functional modules
(Morrison and Badyaev
2016), and, interestingly, has been implicated in the diversification
of avian color patterns
(Badyaev et al. 2019a).
In the 1940s, Simpson posited that species could enter new ‘adaptive
zones’ (Simpson 1945; Simpson 1953) via specific events, including
dispersal into new habitats, extirpation of predators, or through ‘key
innovations’, namely those that relax or fundamentally change the
prevailing environmental sources of natural selection
(Miller 1949; Rabosky
2017). While microevolutionary dynamics might shape the existing
structure or control of metabolic networks (Figs. 4-5), large structural
changes in the network itself, such as the internalization of an
external dependency (e.g., the ability to synthesize a formerly
essential dietary fatty acid), might present a species with novel
ecological opportunity. In other words, the evolution of fatty acid
metabolism might afford species new opportunities to exploit novel
resources (e.g. terrestrial plants containing only ALA), and allow them
to persist and diversify in ‘adaptive zones’. For example, freshwater
threespine stickleback have reduced their external dependency on
DHA-rich resources, which are limited outside of marine habitats (Fig.
3A), by increasing their endogenous conversion rates from ALA to DHA, a
key innovation. Badyaev et al. (2019a) propose that such evolution in
the control of metabolic networks is fundamentally associated with
macroscale patterns of species diversity. Specifically, local metabolic
adaptation can culminate in shifts in network topologies, potentially
opening new opportunities for evolutionary diversity
(Badyaev 2019b). Currently,
this is unexplored in the context of fatty-acid metabolism, but there is
considerable potential to do so in light of the heterogeneity of FA
within and among ecosystems (Fig. 2), genetic variation and fitness
relevance of FA acquisition and metabolism traits, and examples of key
innovations facilitating consumer diversification (Ishikawa et al.
2019).