Environmental enrichment, sexual dimorphism, and brain size in sticklebacks

Abstract

Evidence for phenotypic plasticity in brain size and the size of different brain parts is widespread, but experimental investigations into this effect remain scarce and are usually conducted using individuals from a single population. As the costs and benefits of plasticity may differ among populations, the extent of brain plasticity may also differ from one population to another. In a common garden experiment conducted with three‐spined sticklebacks (Gasterosteus aculeatus) originating from four different populations, we investigated whether environmental enrichment (aquaria provided with structural complexity) caused an increase in the brain size or size of different brain parts compared to controls (bare aquaria). We found no evidence for a positive effect of environmental enrichment on brain size or size of different brain parts in either of the sexes in any of the populations. However, in all populations, males had larger brains than females, and the degree of sexual size dimorphism (SSD) in relative brain size ranged from 5.1 to 11.6% across the populations. Evidence was also found for genetically based differences in relative brain size among populations, as well as for plasticity in the size of different brain parts, as evidenced by consistent size differences among replicate blocks that differed in their temperature.

Variation in sexual brain size dimorphism over the breeding cycle in the three-spined stickleback

“…In comparison to field sampling across the breeding cycle, this experiment conducted under controlled environmental conditions allowed us to evaluate to what degree variation in brain SSD is attributable to developmental, sex-specific or populationspecific sources. As to the latter, large population differences that are constant over all three sampling points would provide evidence for the importance of fixed differences in SSD among populations, and support the hypothesis that the large variance in brain SSD among stickleback populations observed in earlier studies (Herczeg et al, 2015;Kotrschal et al, 2012a;Samuk et al, 2014;Toli et al, 2017) is mainly attributable to population differentiation (see Toli et al, 2017). On the contrary, constant ( parallel) changes in brain SSD over different sampling periods in all replicate populations would provide strong evidence for a developmental component to brain SSD, and indicate that the large variance in brain SSD observed in earlier studies (see above) could owe to differences in timing of sampling relative to the breeding cycle.…”

“…The sex-specific increase in brain size over the breeding cycle was similar in all four replicate populations used in this study, confirming the ubiquity of a developmental component to brain SSD. This finding also excludes geographic variation as the unique source for the observed between-population variation in the degree of brain SSD (Herczeg et al, 2015;Kotrschal et al, 2012a;Samuk et al, 2014;Toli et al, 2017). In essence, we conclude that studies using snapshot sampling for brain size measurements from different populations at different time points over the reproductive season need to be interpreted with caution.…”

“…It is the male that builds and defends an elaborate nest, courts females and cares for offspring, whereas the female's role in reproduction is restricted to choosing a male with a nest to lay her eggs in. Interestingly, recent studies indicate that the degree of SSD in the stickleback brain can vary from 4% to more than 20% depending on the population studied (Herczeg et al, 2015;Kotrschal et al, 2012a;Samuk et al, 2014;Toli et al, 2017). However, it is unclear whether these widely varying estimates of brain SSD reflect genetic differences between populations, or whether they are attributable to developmental plasticity; if brain SSD exhibits breeding cycle dependent developmental plasticity, heterogeneity in timing of sampling in relation to breeding cycle in different populations could explain among-population variation in brain SSD (see Herczeg et al, 2015).…”

“…However, it is unclear whether these widely varying estimates of brain SSD reflect genetic differences between populations, or whether they are attributable to developmental plasticity; if brain SSD exhibits breeding cycle dependent developmental plasticity, heterogeneity in timing of sampling in relation to breeding cycle in different populations could explain among-population variation in brain SSD (see Herczeg et al, 2015). Although a genetic component to brain size SSD has been demonstrated in a common garden experiment (Toli et al, 2017), there are good reasons to assume that a developmental component to SSD variation in the stickleback brain may also be important. First, the brain is amongst the most energetically expensive organs to develop and maintain, and adaptive phenotypic plasticity in brain anatomy can therefore be expected.…”

The effect of environmental enrichment on behavioral variability depends on genotype, behavior, and type of enrichment

“…Salmon living in enriched tanks were faster in escaping mazes and showed increased expression of a pro-neurogenic gene (Salvanes et al, 2013). There is conflicting evidence for the effect of enrichment on brain size in fish, with enrichment having no effect on three-spined sticklebacks, but decreasing brain size in eastern mosquitofish (Toli et al, 2017;Turschwell and White, 2016). Early studies in D. melanogaster have found that changing the social milieu affects the size of brain structures, with social isolation leading to decreased sizes and numbers of Kenyon cell fibers (Barth and Heisenberg, 1997;Heisenberg et al, 1995;Technau, 1984).…”