Discussion
In a previous study, Issa et al. (2020) investigated the role of
dopamine in shaping life history responses to food abundance in D.
magna . This was done both through aqueous exposure to dopamine and to
the antidepressant bupropion, a dopamine reuptake inhibitor. Both
treatments led to higher population growth rates (calculated from
maternal life history traits) when food was restricted, without any
apparent costs to fitness. The higher dopamine exposure resulted however
in smaller offspring, which could potentially perform worse particularly
when facing restrictions in food availability (Gliwicz, 1990). Since
offspring survival is a crucial component of maternal fitness, this may
represent a fitness cost of higher maternal dopamine levels. In the
current study we tested this by exposing F0 D.
magna to aqueous dopamine and quantifying life-history responses of
mothers (F0) to food abundance as well as the starvation
resistance of their offspring (F1).
Similar to the findings of Issa et al. (2020), offspring size was larger
in mothers that had experienced restricted food abundance, a pattern
commonly observed in Daphnia (Garbutt & Little, 2014; Glazier,
1992), as well as in other organisms (Reznick et al., 1996;
Vijendravarma et al., 2010). This response was in the same direction for
both dopamine and control treatments but was considerably steeper for
the control treatment. The latter arose as a consequence of dopamine
exposure causing a reduction in offspring size when mothers experienced
restricted food ration, but not when mothers received ad libfood. In general, a larger investment in offspring size when food is
limited is expected to boost offspring survival and fitness (Gorbi et
al., 2011; Tessier & Consolatti, 1989). In support of this, we found
that the larger offspring of mothers having experienced restricted food
ration survived better under starvation across treatments. Mothers that
experience low food abundance tend to produce offspring with a larger
maternal lipid reserve, which can increase offspring starvation
resistance (Tessier et al., 1983). In contrast to our hypothesis,
however, maternal exposure to dopamine did not come at a cost to
offspring longevity. Surprisingly, offspring in the dopamine treatment
survived longer than controls across food rations. This was true even
for the offspring from mothers that had experienced restricted food
rations, where offspring size was smaller in the dopamine treatment than
in the controls. Hence, enhanced maternal dopamine levels increased
rather than decreased offspring survival.
Unlike the effects of dopamine exposure on offspring longevity, its
effects on maternal life-history reaction norms were overall as
predicted based on the findings of Issa et al. (2020). Specifically, at
restricted food ration, somatic growth rate decreased, and maturation
was delayed. However, dopamine exposure resulted in faster growth and
earlier age at maturation across food rations compared to the control.
Higher dopamine levels have been shown to promote cell proliferation
and/or increase cell volume, explaining the positive effect of dopamine
exposure on somatic growth rate (Huet & Franquinet, 1981; Weiss et al.,
2015). As in Issa et al. (2020), a smaller adult size was observed at
restricted food ration in the dopamine treatment, with potential costs
to adult survival and reproduction (Cleuvers et al., 1997; Lampert,
2001), as body size in Daphnia positively correlates with the
ability to satisfy metabolic requirements at low food levels.
Contrastingly, at high food ration, dopamine exposure increased adult
size, and hence Daphnia competitiveness (Brooks & Dodson, 1965),
compared to the control. The significant effects of dopamine treatment
on adult size and somatic growth rate (and consequently age at
maturation) at high food ration were surprising, given that treatment
effects were expected to occur at restricted food ration only (Issa et
al., 2020). There were however some differences in the setup between the
current study and the study by Issa et al. (2020) that may potentially
explain this: 1) in the present study, we performed exposure in groups,
thus allowing for interactions between individuals, whereas Issa et al.
(2020) exposed animals individually; 2) the present study used a
different clone than Issa et al. (2020). Previous research shows that
antidepressant effects on life history traits of Daphnia species
can vary between clones, if they differ in their growth and reproductive
performance (Campos et al., 2012). Yet, although the exact patterns may
depend on clonal identity and experimental protocols, the results of the
present study support the overall conclusion of Issa et al. (2020) that
important life-history responses to food abundance are shaped by the
dopamine system.
The observed increase in Daphnia growth and advanced timing of
reproduction from elevated dopamine levels may also be interpreted as a
stress response. Indeed, evidence shows that fast species (i.e.
short-lived species, producing many offspring early in life), such asDaphnia , respond to stressful environments by accelerating their
life cycle (Rochet et al., 2000; Trippel, 1995). Higher dopamine levels
may stress individuals through dopamine oxidation. Elevated
intracellular dopamine levels can promote the intracellular oxidation of
dopamine, by increasing the production of reactive quinones and free
radicals for a given rate of oxidation (Miyazaki & Asanuma, 2008; Sun
et al., 2018). In addition, increased extracellular dopamine can
overload the antioxidant capacity in the extracellular space, causing
dopamine oxidation (Blesa et al., 2015; LaVoie & Hastings, 1999;
Miyazaki & Asanuma, 2008). In the case of limited investment in
antioxidant defence, dopamine oxidation can then lead to oxidative
stress, which can potentially reduce longevity (Ishii et al., 1998;
Moskovitz et al., 2001). On the other hand, increased investment in
antioxidant defence may lower investment in immune defence (Takahashi et
al., 2017), ultimately increasing the susceptibility of individuals to
diseases and parasites. A higher investment in antioxidant defence may
also lower investment in reproduction (Speakman & Garratt, 2013). There
may also be ecological costs of rapid growth associated with enhanced
dopamine levels, due to biotic interactions. One such cost may be higher
predation risk from faster growth (Urban, 2007), as individuals become
more exposed to predators from increased feeding (Lankford et al. 2001;
Stoks et al., 2005). Thus, whether through oxidative stress, or
increased investment in antioxidant defence, dopamine oxidation may pose
a proximate restriction for why Daphnia do not produce more
endogenous dopamine. This in addition to more ultimate restrictions in
the form of reduced survival, from oxidative stress, reduced immunity or
increased predation risk, as well as lowered reproduction, may be
important to explore in order to understand the evolution of the
dopamine system.
In summary, maternal dopamine exposure boosted Daphnia offspring
survival in addition to accelerating its life cycle. Altogether, these
results emphasize the important role of dopamine as a regulator of
life-history responses to food abundance but leave open the question of
why D. magna do not evolve towards higher endogenous dopamine
levels despite the apparent fitness benefits. A potential proximate
cause may be that higher dopamine levels promote dopamine oxidation.
More ultimate causes involve the potential costs of dopamine oxidation
to reproduction and survival, as well as ecological costs of rapid
growth due to biotic interactions (predation). Hence, further
understanding of the evolution of the dopamine signalling system may
require a combined investigation of ultimate and proximate causes.