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).