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).