Predation drives the evolution of brain cell proliferation and brain allometry in male Trinidadian killifish, Rivulus hartii. Kent D. Dunlap, Joshua H. Corbo, Margarita M. Vergara, Shannon M. Beston and Matthew R. Walsh. Proceedings of the Royal Society B, Volume 286, Issue 1917, December 18 2019. https://doi.org/10.1098/rspb.2019.1485
Abstract: The external environment influences brain cell proliferation, and this might contribute to brain plasticity underlying adaptive behavioural changes. Additionally, internal genetic factors influence the brain cell proliferation rate. However, to date, researchers have not examined the importance of environmental versus genetic factors in causing natural variation in brain cell proliferation. Here, we examine brain cell proliferation and brain growth trajectories in free-living populations of Trinidadian killifish, Rivulus hartii, exposed to contrasting predation environments. Compared to populations without predators, populations in high predation (HP) environments exhibited higher rates of brain cell proliferation and a steeper brain growth trajectory (relative to body size). To test whether these differences in the wild persist in a common garden environment, we reared first-generation fish originating from both predation environments in uniform laboratory conditions. Just as in the wild, brain cell proliferation and brain growth in the common garden were greater in HP populations than in no predation populations. The differences in cell proliferation observed across the brain in both the field and common garden studies indicate that the differences are probably genetically based and are mediated by evolutionary shifts in overall brain growth and life-history traits.
1. Introduction
Researchers have devoted much attention to assessing whether changes in adult neurogenesis in response to the environment might be a mechanism of adaptive brain plasticity [1,2]. While the precise functional significance of adult neurogenesis is still debated, there is substantial evidence from many model systems that environmental stimuli alter neurogenic rates in specific brain regions, and that such neurogenic changes have behavioural consequences [3]. For example, complex odour environments increase neurogenesis in the olfactory bulb of rodents [4], and these new neurons enhance odour discrimination abilities [5]. Similarly, seasonal changes in day length promote neurogenesis in the song nuclei in the brains of several bird species, and these neurons are linked to seasonal song production [6].
Most of our understanding of environmental influences on adult neurogenesis comes from laboratory studies in which researchers manipulate environmental stimuli and document effects over the timescale of days to months. That is, they demonstrate an external factor driving phenotypic plasticity in the neurogenic rate. However, the neurogenic rate can also be influenced by intrinsic genetic factors [7–9], and thus, over evolutionary timescales, the environment can modify the neurogenic rate via natural selection acting within populations. Selection could act directly on the neurogenic rate if enhanced (or reduced) brain plasticity confers an advantage in responding to environmental change. Additionally, in species with indeterminate growth, such as most fishes, the brain grows in tandem with the body throughout adulthood [10,11], and selection on body growth trajectories could indirectly affect brain growth and the underlying cellular processes of brain growth [12]. Thus, population variation in the neurogenic rate could arise from phenotypic responses to different environments, or from evolved genetic divergence owing to direct selection on brain growth rate or as an indirect, correlated response to selection on body growth (figure 1). We evaluated these alternative explanations by examining one stage of adult neurogenesis, brain cell proliferation, in killifish (Rivulus hartii) populations from different predator environments. By measuring brain cell proliferation rates in populations exposed to differential predation pressure in the field as well as those same populations reared in a common laboratory environment, we assessed whether population variation in brain cell proliferation is attributable to natural environmental differences versus intrinsic population differences. Finally, we evaluated the predator effects on brain cell proliferation within the context of lifetime growth trajectories of the brain and body in populations [13–16] to assess how population variation in brain cell proliferation fits into the overall evolved difference in life history.
[Figure 1. Three alternative causal chains linking the environment with variation in brain cell proliferation.]
In Trinidad, R. hartii are found in sites where they are the only species present (Rivulus only (RO) sites) and lack predators as well as in sites where they are exposed to predatory fish such as Hoplias malabaricus and Crenicichla frenata (high predation (HP) sites). RO sites are typically located upstream from HP sites above barrier waterfalls that truncate the distribution of large piscivores [13,14,16,17]. These sites are located near each other and thus do not differ in physical habitat and environmental variables (i.e. water temperature and dissolved oxygen) [14]. In HP sites, Rivulus suffer increased mortality, are found at lower densities, and, in turn, they exhibit faster rates of individual growth (HP sites also have a more open canopy) [13,18]. Rivulus can also be bred and reared in the laboratory, allowing us to identify intrinsic (probably genetic) differences between populations that are independent of the environment, and many previous studies have indeed demonstrated that increased predation pressure is associated with evolutionary changes in life-history traits [13,15,19].
Recent work on Rivulus showed that divergent patterns of predation lead to evolutionary shifts in brain size [20]. Increased predation rates in HP sites are associated with the evolution of smaller brains in male (but not in female) Rivulus. Given this negative association between predator environment and brain size in male Rivulus and the negative effect of predators on brain cell proliferation in another freshwater teleost [21,22], we predicted that Rivulus from HP populations would have lower rates of brain cell proliferation than those from RO populations. In fact, we found the opposite: brain cell proliferation was higher in HP populations than in RO populations. These differences were maintained in first-generation laboratory-reared fish, indicating that they probably arise from evolved genetic divergence rather than through phenotypic plasticity. Population differences in cell proliferation were found across all sampled brain regions and correlated with population differences in overall brain allometry, suggesting that they evolved as part of broader evolutionary changes in overall brain growth rather than as a mechanism serving a specific behavioural adaptation.
By examining the impact of economic conditions on a broad range of social ills for 40 rich countries for the period 2000–2015, this study represents the most up-to-date and comprehensive examination of the famous inequality hypothesis. To our knowledge, this is also the first aggregate-level study in which a larger number of potential mediators between economic conditions and social ills has been put to an empirical test. Descriptively, while the ranking of countries according to their number of social ills largely matches that presented in The Spirit Level, our finding that social ills have decreased over time in all but two countries is a genuinely new finding that contradicts the widely accepted diagnose of social malaise in the developed world (Eckersley 2012; Elchardus and De Keere 2013). While some of our results provide partial support for the inequality hypothesis, others contradict it. We begin our discussion with the supporting evidence, which stems exclusively from the cross-sectional analysis.
The first confirmatory finding is that cross-sectionally the scale of income inequality is positively associated—year by year—with social ills, an association that holds when economic prosperity is considered at the same time (confirming H1). This association is found in our two sets of rich countries, the global (full) sample, which is culturally more diverse, and the subset of European countries (confirming H3). There thus seems to be no need to confine the inequality hypothesis to the Western world. In light of the criticism that Wilkinson and Pickett especially received for disregarding cultural peculiarities (Saunders and Evans 2010; Snowdon 2010), this is a most relevant finding.
A second and at least partly theory-confirming finding concerns potential mediators. Our cross-sectional results lend some support, first of all, to the idea that status anxiety mediates between economic conditions and social ills. Two qualifications, however, are essential. While average levels of status anxiety are systematically higher in less affluent countries, they are not higher in more unequal ones, as The Spirit Level presumes. Secondly, our cross-sectional finding that the characteristics of social cohesion perform better as mediators suggests that it is the erosion of social life more generally which evokes health and social problems, not status anxiety specifically. Interestingly, this conclusion resonates well with the thrust of Wilkinson’s (1996, 1999) older works.
As regards the findings that challenge the inequality hypothesis and the spirit level theory, most importantly, changing income inequality does not cause changes in the number of social ills (disconfirming H4). Our study thus joins those that find a link between inequality and social ills cross-sectionally, but not longitudinally (e.g. Beckfield 2004; Leigh and Jencks 2007; Avendano 2012; Hu et al. 2015). Our results further indicate that economic prosperity is related to lower social ills—cross-sectionally in both subsets of rich nations, and longitudinally in Europe, in both cases while simultaneously considering the income distribution. This questions the exclusive focus on inequality that many scholars advocate. The positive impact of prosperity on societies is already observable at the beginning of the 2000s according to our data; and so it was not a new phenomenon that appeared after The Spirit Level was published. Seen in conjunction with the mounting evidence that individual quality of life is also better in richer countries (e.g., Hagerty and Veenhoven 2003; Deaton 2008; Delhey and Steckermeier 2016), it appears premature to declare economic resources ineffective for making lives and societies better, and even more so, as in the study at hand increases in economic prosperity over time decrease social ills, at least in Europe. In our data, the causal effect on social ills is actually exerted by economic prosperity, not by changes in the income distribution. Still, we do not want to gloss over the finding that in the European sub-sample the cross-sectional association between economic prosperity and social ills became weaker in later years of the period studied. This might mean that some rich societies are experiencing diminishing returns from economic resources, but still have positive returns—in particular in Europe—so “wealthier is healthier” (Biggs et al. 2010) is still a valid slogan for contemporary rich societies.
The mediation analysis could only be performed for Europe. Here, a genuinely new finding is that the same mechanisms that mediate in cross-sectional analysis between inequality and social ills also mediate between economic prosperity and social ills, namely satisfaction with social life and experienced social exclusion (largely in support of the cross-sectional part of H6); and further, that the mechanism prominently proposed by the spirit level theory—feelings of inferiority—only mediates the attenuating effect of economic prosperity. This suggests that prosperity exerts its positive effect on social ills by improving the social climate within societies (cf. Welzel 2013; Delhey and Dragolov 2016). Nevertheless, the longitudinal mediation analysis could not ultimately clarify the experienced quality-of-life mechanism through which economic prosperity has an effect on social ills. Future research, ideally based on larger case numbers, might yield more conclusive results on this issue.
Our results for economic prosperity raise the important question of why we unearthed a robust prosperity-social ills nexus when Wilkinson and Pickett did not. Re-running our analysis for the set of 21 countries from The Spirit Level, we find two explanations: country selection and methods. Indeed, there is no significant correlation between economic prosperity and our ISI index for the 21 countries in any of the years 2000–2015. In other words, it is Wilkinson and Pickett’s—disputable—compilation of countries which produces a non-correlation. Furthermore, when estimating pooled OLS regressions of ISI on inequality and prosperity for their 21 countries over the full period of 16 years, there is a robust social ills attenuating effect of prosperity, entirely in line with our results, but contrary to Wilkinson and Pickett. This demonstrates how unadvisable it is to draw conclusions based on zero-order correlations alone.
A limitation of our study is that the mediation analysis could only be performed for Europe. European societies are in the vanguard of value change toward self-expression values (Inglehart and Welzel 2005; Welzel 2013). Provided this peculiarity rubs off on the social production functions of these societies, we cannot rule out that the focus on Europe in the mediation analysis overemphasizes the role of social mediators and underemphasizes the role of material ones, such as economic strain. Moreover, a multi-level framework could be applied to the best-performing mechanisms from our analysis to determine whether they imply contextual effects of inequality and prosperity, or rather composition effects (for status anxiety, see, for example, Whelan and Layte 2014). Further research is also needed to explore potential cultural conditions that breed or prevent social ills. Although we have established that the impact of income inequality is not weaker in the culturally diverse global sample, it is still conceivable that cultural forces play their part in the generation of health and social problems.
In conclusion, while from a cross-sectional perspective the inequality hypothesis seems accurate but one-sided, in a longitudinal perspective it appears to be wrong. This news might be hard to digest for those who assume that creating a ‘better’ society is, definitely and primarily, a matter of income redistribution. For policymakers, our study instead suggests that economic prosperity should be prioritized over income redistribution as an instrument to achieving a less problem-ridden society. Naturally, tackling inequalities might still be of paramount importance for achieving other valuable goals, such as to enhance social justice.