Introduction
Adaptive evolution of consumer metabolism in response to the spatiotemporal variation of dietary resources can contribute to the origin and maintenance of biological diversity. In natural populations, consumers often face mismatches between the dietary supply of, and physiological requirements for, both inorganic elements (e.g. carbon, nitrogen, and phosphorus) and essential organic compounds (e.g. amino acids, lipids, and vitamins). Ecosystem- and habitat-specific differences in the nutritional quality of prey can generate divergent selection, and thereby influence the evolutionary processes underlying ecological speciation and adaptive radiation (Schluter 2000; Nosil 2012). Moreover, key metabolic adaptations, such as the ability to synthesize essential compounds, can generate ecological opportunities that enable consumer species to transition into novel adaptive zones (Simpson 1945; Simpson 1953).
In natural populations of consumers, metabolic phenotypes in general, and lipid phenotypes in particular, are important components of fitness variation. Lipids are fundamentally important for energy storage, cell membrane structure, and cellular functions (Sunshine and Iruela-Arispe 2017). Within lipids, the omega-3 (n–3) and omega-6 (n–6) polyunsaturated fatty acids (PUFA) are important for somatic development, especially nervous and gonadal tissues (Arts and Kohler 2009; Guo et al. 2016a; Tocher et al. 2019), cognition (McCann and Ames 2005; Cunanne et al. 2009; Hoffman et al. 2009), reproduction (Martin-Creuzburg et al. 2009; Roqueta-Rivera et al. 2010; Chen et al. 2012; Sinendo et al. 2017), and survival (Matsunari et al. 2013; Fuiman and Perez 2015; Kim et al. 2016; Mesa-Rodriguez et al. 2018; Twining et al. 2018a).
Consumers likely face an allocation tradeoff involving their metabolic capacity to synthesize PUFA and their capacity to acquire fatty-acids (FA) from dietary sources. Indeed, the behavioral and metabolic strategies to meet PUFA requirements vary widely across the tree of life (Fig. 1). For example, detritivorous nematodes have a broad capacity to synthesize PUFA from dietary carbohydrates as well as short-chain fatty acid precursors (Watts and Browse 2002; Malcicka et al. 2018). However, all vertebrates and many major groups of invertebrates lack the ability to convert monounsaturated fatty acids (MUFA) such as oleic acid (OA) to n–3 and n–6 PUFA (Kabeya et al. 2018). Therefore, a finch consuming seeds that lack eicosapentaenoic acid (EPA, 20:5n-3) and docosahexaenoic acid (DHA, 22:6n–3) must metabolically derive these compounds from precursors (e.g., α-linolenic acid, ALA, 18:3n–3) through enzymatic conversion processes, including desaturation and elongation (Fig. 1C). However some species of obligate carnivores, such as cats and tuna (Fig. 1E), are entirely unable to convert short-chain (C18) into the long-chain (≥C20; LC) PUFA, and can only acquire EPA and/or DHA directly from their diet (Rivers et al. 1975; Betancor et al. 2020; Wang et al. 2020). Even those consumers that can synthesize some EPA and/or DHA from the precursor compounds available in low quality food (e.g., ALA), may face high metabolic costs that manifest as reduced population growth rates. For example, Daphniapopulations grow much slower (or not all) on a diet low in n-3 LC-PUFA (e.g. cyanobacteria) compared to a diet high in n-3 LC-PUFA (e.g.Nannochloropsis or Cryptomonas ; Fig. 1D; Martin-Creuzburg et al. 2009; Martin-Creuzburg and von Elert 2009).
At the base of food chains there are two fundamental contrasts in n-3 PUFA availability that are particularly relevant for understanding how spatiotemporal variation of resource quality can influence consumer adaptation (Fig. 2). First, aquatic primary producers often contain both EPA and DHA whereas terrestrial primary producers typically only contain shorter chain n-3 fatty acids, such as ALA (Hixson et al. 2015; Twining et al. 2016a; Colombo et al. 2017). As a result, terrestrial consumers are fundamentally more limited by EPA and DHA availability than aquatic consumers, and have evolved numerous adaptations to resolve this nutritional constraint. Second, within aquatic systems, primary producers in marine ecosystems have higher DHA content than in freshwater ecosystems (Fig. 2). This DHA disparity has driven multiple independent cases of consumer metabolic evolution associated with the adaptation from marine to freshwater ecosystems (Ishikawa et al. 2019). More generally, such fundamental nutritional contrasts among ecosystems, as well as others occurring within ecosystems (e.g. among habitats, and prey species), can contribute to evolutionary tradeoffs involving PUFA acquisition and metabolism.
Previous work has documented how PUFA vary in relation to ecosystem type, trophic level, taxonomy, and foraging behavior of species (e.g., Galloway and Winder 2015; Hixson et al. 2015; Colombo et al. 2017; Guo et al. 2017), but not how variation is important for understanding the prevailing diversity of consumer metabolism within and among species. Here, we review the distribution of n-3 LC-PUFA in both primary producers and consumers among major ecosystem (i.e., freshwater, marine, terrestrial), between adjacent habitats within ecosystems (e.g., nearshore-offshore, stream-forests), and among co-occurring prey species within habitats. We discuss how consumers can evolve in response to the spatial, seasonal, and community-level variation of prey quality. In doing so, we consider how the metabolic traits of consumers are hierarchically structured, from cell membrane function to maternal investment, and have strongly environment-dependent expression. Finally, we discuss the evolutionary genetic mechanisms that underlie the adaptation of consumers to PUFA limitation, and how such metabolic evolution can be an important driver of consumer diversification in ecosystems.