Discussion
The relative brain volume, i.e. after controlling for fish FL,
was larger in lake habitats compared to streams. In addition, volumes of
telencephalon and optic tectum were, in relation to other brain regions,
disproportionately larger in lakes compared to streams, while volumes of
other brain regions changed in close correlation to the overall brain
volume. The telencephalon of stream fish was even smaller than
telencephalon of hatchery individuals. Similarly to the study of Ahmed
et al. (2017) on wild populations of stickleback, our findings do
not support the hypothesis that in brown trout volume of brain and
regions important for navigation and decision-making increases in
physically complex stream compared to simpler lake and hatchery habitat.
We posit that the discrepancy between theoretical predictions and our
findings can be explained by two main mutually non-exclusive factors.
First is the non-linear association between physical habitat complexity
and selection for larger brains, particularly for larger telencephala
and optic tecta (Boogert et al. , 2018). This explanation assumes
that habitat complexity beyond a certain threshold may favor simple
behavioural strategies to operate effectively in those complex
environments, because their success probability is comparable to more
complicated and cognitively demanding behaviours requiring costly
investment in brain development (Morand-Ferron et al. 2015). Therefore,
the high complexity of the rapidly changing stream habitat may favour
simpler behavioural strategies than the less complex lake habitat.
Stationary behaviour and a sit-and-wait foraging strategy of stream
dwelling trout (Jonsson & Jonsson 2011) is an example of such simple
behavioural adaptations to the complex stream habitat. In contrast,
alternation in foraging between pelagic and littoral zone and more
common piscivory of lake-dwelling brown trout (Sánchez-Hernández 2020)
may induce selection for large telencephala and optic tecta due to the
need for visual cues processing and relatively complex navigation and
decision-making skills that they require (Edmunds et al. , 2016).
The second possible explanation for differences in brain size between
the habitats is differences in available diet quality, which limit the
nutrient supply for brain development. Lake-dwelling trout feeding on
zooplankton or other fish acquire more n-3 LC-PUFA than stream-dwelling
trout, which rely on a mix of macro-zoobenthos and n-3 LC-PUFA-poor
terrestrial insect (Heissenberger et al. , 2010; Sánchez-Hernández
& Cobo 2016). Previous laboratory studies that have shown that
availability of dietary n-3 LC-PUFA has positive effect on overall brain
size (Lund et al. , 2012) and on size of optic tecta (Ishizakiet al. , 2001). Therefore, the higher dietary intake of these
nutrients may facilitate brain size development in lake-dwelling brown
trout, compared to their conspecifics from stream habitats. An extremely
n-3 LC-PUFA-rich diet is also typical for hatchery-reared fish
(Heissenberger et al. , 2010). This high-quality diet may loosen
the selection trade-off between the cost of brain development and
benefits of high cognitive capacity that typically shapes brain
morphology in wild animals (Morand-Ferron et al. 2015; Boogert et
al. , 2018). Thus, a high-quality diet, which enables rapid brain growth
in hatchery fish, can explain the findings of this and other studies
(Näslund et al. , 2012; Kotrschal et al., 2012) that
hatchery salmonids can have similar or larger brain and telencephalon
volume than stream-dwelling salmonids, despite the low physical
complexity of hatchery habitat. The relative brain size (i.e. ,
encephalization) of hatchery trout was in our study difficult to compare
with the wild fish due to the difference of allometric relationship
between the FL and brain in hatchery and wild individuals, but it
appears that hatchery fish brain was of intermediate size between fish
of stream and lake origin. The lack of positive correlation between the
brain size and FL in hatchery individuals is unusual for wild fishes
where body size is a strong predictor of brain volume (e.g. ,
Triki et al. 2021). Previous studies on evolution of encephalization in
mammals have suggested that relative brain size depends on selection
pressure on size of the brain as well as on the overall body size
(Smaers et al. 2012). Therefore, high-quality diet and selection for
fast body growth in hatchery fish could uncouple the developmental link
between the brain and the rest of the body (Kotrschal et al.,2012; Smaers et al. 2012).
Other factors that have been shown to influence brain size and
morphology in fishes and were not explicitly considered in our
comparative study are predation pressure (Kotrschal et al. ,
2017), sex (Kolm et al. , 2009; Näslud 2018), and ontogeny
(Abrahao et al. 2021). Potential predators, that is eel and large trout,
were present in all sampled wild populations (see method section), and
thus were unlikely to explain differences between the lake and stream
habitat. Proportion of males and females in brown trout populations in
generally even (e.g. , Baglinière et al.1989) and thus should not
differ between the groups compared in this study, but some studies
suggest that female brown trout are more common in pelagic lake habitat
(e.g. , Jonsson 1989). There were clearly ontogenetic differences
between the compared groups, as hatchery trout were young-of-year, while
the sizes of all wild trout corresponded to adults. In addition, lake
trout were larger than stream trout, and thus some of lake individuals
could have been older than the rest of the sample, but these differences
could also stem from differences in growth rates in lake and stream
trout (Jonsson & Jonsson 2011; Sánchez-Hernández 2020). The differences
in growth rates among the environments compared in this study makes it
impossible to collect individuals of the same body size and age, and
thus confounding of these two factors is an inherent shortcoming of any
such comparative study.
In conclusion, our study provides an example of among population
variability of brain size and morphology, which is a topic still widely
understudied in the wild. We suggest that besides the cognitive demands
of the environment (e.g., habitat complexity) future studies
should also consider the availability of dietary essential fatty acids
as a possible key driver of brain evolution and development in wild
fishes.