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.