Heterogeneity of fatty acid distribution in nature: implications for consumers
Primary producers vary widely in their fatty acid composition across ecosystems (Fig. 2A-C), but there are some stark contrasts within and among ecosystems (Table S1). For example, vascular land plants, such as angiosperms and gymnosperms, often contain little to no n-3 LC-PUFA, whereas aquatic algae, such as diatoms and cryptophytes, are often laden with both EPA and DHA (Fig. 2A-C). However, a number of non-vascular and semi-aquatic plants, such as mosses, do contain EPA (e.g., Kalacheva et al. 2009; Fig. 2B). Terrestrial primary producers also contain significantly more fatty acids as ALA, the precursor to EPA and DHA, compared to marine primary producers (Fig. 2A; Table S1). In addition to these patterns with n-3 PUFA, terrestrial primary producers typically contain a higher proportion of n-6, such as LIN, relative to n-3 PUFA, like ALA, compared to aquatic primary producers (Hixson et al. 2015), but the reasons for this are unclear. One possible explanation for these patterns is the higher susceptibility of PUFA with more double bonds, and LC-PUFA in particular, to peroxidation (Halliwell and Gutteridge 1985; Mueller 2004; Møller et al. 2007), which is a greater risk in terrestrial environments. Another important and well-documented pattern is that marine primary producers have a significantly higher percentage of fatty acids as EPA compared to either freshwater or terrestrial primary producers (Fig. 2B; Table S1) as well as significantly more fatty acids as DHA compared to terrestrial primary producers (Fig. 2C; Table S1). The reasons for this pattern are also unclear, but might be partly due to EPA and DHA conferring protection against high salinity (Jiang and Chen 1999; Sui et al. 2010).
Within ecosystems, the distribution of PUFA of primary producers is typically attributed to both species differences (Taipale et al. 2013) and environmental conditions (Lang et al. 2011). For example, n-3 LC-PUFA are very abundant across several major groups of Eukaryotic algae (Mühlroth et al. 2013), but are absent in Cyanobacteria (Twining et al. 2016a). However, the composition and content of FAs can also be highly variable among closely related species and individuals of the same species (Lang et al. 2011; Galloway et al. 2012; Taipale et al. 2013; Charette and Derry 2016), possibly due to the strong influence of environmental conditions (Lang et al. 2011). LC-PUFA molecules are particularly unstable due to the susceptibility of their multiple double bonds to oxidation and attack by reactive oxygen species (Shchepinov et al. 2014). For instance, high temperatures increase reaction rates, such that LC-PUFA degrade faster in warm environments (Hixson and Arts 2016). In addition, phospholipids with double bonds, such as those found in PUFA, may help cells maintain membrane fluidity at lower temperatures (homeoviscous adaptation; Sinensky 1974; Feller et al. 2002). Thus, it may be beneficial for organisms to have more LC-PUFA when it is colder and more costly for them to protect LC-PUFA when it is warmer. In algae, n-3 LC-PUFA content is often negatively correlated with both temperature (Hixson and Arts 2016) and light levels (Amini Khoeyi et al. 2012; Hill et al. 2011), and influenced by inorganic nutrient concentration (e.g., Guschina and Harwood 2009; Piepho et al. 2012). At constant temperature and light levels, phosphorus limitation, for example, can decrease overall lipid content but increase n-3 LC-PUFA production, possibly reflecting the need to store lipids until growth conditions improve (Guschina and Harwood 2009). However, when light, temperature, and nutrients are simultaneously manipulated, fatty acid responses can be highly variable across species and systems (e.g., Piepho et al. 2012; Cashman et al. 2013; Guo et al. 2016b).
In consumers, the composition of PUFA reflects both the dietary sources of lipids (e.g., ecosystem origin, prey availability) and the capacity of consumers to metabolise different FA (Fig. 2, Hixson et al. 2015; Guo et al. 2017). Insect species with an early aquatic life stage often contain more n-3 LC-PUFA than those that are exclusively terrestrial (Twining et al. 2018a), and are thus important sources of EPA for insectivores, such as Eastern Phoebes (Sayornis phoebe ) (Twining et al. 2019). Many consumers acquire PUFA from multiple ecosystems in order to meet their own nutritional requirements. For example, mammalian carnivores can forage on aquatic resources to help increase their intake of DHA relative to linolenic acid (18:2n-6; LIN), which is an abundant n-6 PUFA in terrestrial primary producers (Koussoroplis et al. 2008). Migratory consumers can accumulate n-3 LC-PUFA from PUFA-rich ecosystems and use them for reproduction and offspring provisioning in more PUFA-depauperate ecosystems (e.g. salmon migrating from the ocean to freshwater streams; Heintz et al. 2004). Indeed, many species that experience wide temporal variation in resource quality often exhibit either plasticity (e.g., Katan et al. 2019) or genetic adaptation (Ishikawa et al. 2019) associated with fatty acid metabolism.
Within ecosystems, consumers often experience contrasting distributions of FA when foraging in multiple adjacent habitats. Within lakes, for example, ecotypes of Eurasian perch (Perca fluviatilis ) are known to specialize on either littoral macroinvertebrates, which are DHA-poor, or pelagic zooplankton, which have species (e.g. copepods) that are DHA-rich (Fig. 3A). Intriguingly, in spite of the fact that DHA is higher in pelagic prey, littoral perch typically have higher DHA than pelagic perch. This might indicate that perch can thrive on a low-DHA diet (Scharnweber et al., unpublished), via preferential DHA retention (e.g., Hessen and Leu 2006; Heissenberger et al. 2010) and/or DHA synthesis from precursors like ALA (e.g., Buzzi et al. 1996; Bell et al. 2001). In terrestrial systems, Tree Swallows vary widely in their access to aquatic prey (McCarty and Winkler 1999; Stanton et al. 2016; Michelson et al. 2018), which contain substantially more EPA than terrestrial prey (Twining et al. 2018a; Twining et al. 2019; Fig. 3B). Controlled diet studies show that Tree Swallow chicks, which are inefficient at synthesizing EPA and DHA from ALA (Twining et al. 2018b) grow faster, are in better condition, and have increased survival when they consume either more aquatic insects or diets containing more EPA and DHA (Twining et al. 2016b). Because nest sites vary considerably in their distance to aquatic ecosystems, adults might trade-off food quality with quantity when provisioning their young. Although unexplored, this trade-off could select for increased efficiency of ALA to EPA and DHA conversion in populations that breed in drier, upland habitats that have a lower availability of high-quality freshwater prey.
Contrasting distribution of FA can, in some cases, drive adaptive population divergence of consumers. For example, urban and rural populations of Great Tits (Parus major ) differ not only in their diet (Andersson et al. 2015) and their fatty acid composition (Andersson et al. 2015; Isaksson et al. 2017) but also in their expression of theElovl and Fads genes (Watson et al. 2017), which code for the enzymes used to convert ALA and LIN to n-3 and n-6 LC-PUFA, respectively. Specifically, rural tits have higher plasma EPA content while urban tits have plasma higher arachidonic acid (ARA, 20:4n-6) content (Andersson et al. 2015; Isaksson et al. 2017). The n-3 LC-PUFA have anti-inflammatory properties while n-6 LC-PUFA, which are synthesized from their shorter-chain n-6 precursor through the same pathway as n-3 PUFA, have pro-inflammatory properties (Calder et al. 2002). Urban tits experience greater oxidative stress than do rural tits (Isaksson et al. 2017; Watson et al. 2017) and also express Elovland Fads at lower rates compared to rural tits (Watson et al. 2017). Thus, urban tits appear to suppress the production of both n-3 and n-6 LC-PUFA in order to reduce inflammation and oxidative damage in a more stressful environment (Watson et al. 2017).