Brain morphology of the threespine stickleback (Gasterosteus aculeatus) varies inconsistently with respect to habitat complexity: A test of the Clever Foraging Hypothesis

Abstract

The Clever Foraging Hypothesis asserts that organisms living in a more spatially complex environment will have a greater neurological capacity for cognitive processes related to spatial memory, navigation, and foraging. Because the telencephalon is often associated with spatial memory and navigation tasks, this hypothesis predicts a positive association between telencephalon size and environmental complexity. The association between habitat complexity and brain size has been supported by comparative studies across multiple species but has not been widely studied at the within‐species level. We tested for covariation between environmental complexity and neuroanatomy of threespine stickleback (Gasterosteus aculeatus) collected from 15 pairs of lakes and their parapatric streams on Vancouver Island. In most pairs, neuroanatomy differed between the adjoining lake and stream populations. However, the magnitude and direction of this difference were inconsistent between watersheds and did not covary strongly with measures of within‐site environmental heterogeneity. Overall, we find weak support for the Clever Foraging Hypothesis in our study.

Brain differences in ecologically differentiated sticklebacks

“…It is possible that these patterns with total brain size are due to the Enos Lake limnetic-like fish being male and most of the other fish tested being female. For example, sexual dimorphism in total brain size has been detected in other populations of threespine stickleback fish from British Columbia ( Samuk et al 2014 , but see Ahmed et al 2017 ), although we did not detect it in our Paxton Lake benthic fish.…”

“…Stickleback fish are increasingly being used to study brain and cognitive evolution, and several other studies have asked how different environments correlate with brain morphology. For example, comparing populations with varying habitat complexity has found small differences in telencephalon shape ( Park and Bell 2010 ) and the size of other areas ( Gonda et al 2009 , 2011 ; Ahmed et al 2017 ), suggesting some degree of local adaptation, even though effect sizes were modest in most studies. Overall brain size differences have also been detected for populations of threespine ( Samuk et al 2014 ; Ahmed et al 2017 ) and ninespine stickleback ( Gonda et al 2009 , 2011 ).…”

“…We scanned 5 benthic and 2 limnetic fish from Paxton Lake ( Table 1 ). We mostly used females to make comparisons more straightforward, because sexual dimorphism in brain size has been described in some populations of threespine sticklebacks from British Columbia ( Samuk et al 2014 , but see Ahmed et al 2017 ). However, we were unable to do this for Enos Lake limnetic fish, as they are now particularly rare in nature and the females are especially hard to collect, limiting access.…”

“…We use a powerful method to quantify variation in brain regions that underpin these senses. To date, the most common method for measuring brain region size variation is estimating volume from photographs of the brain’s exterior (e.g., Pollen et al 2007 ; Gonda et al 2009 ; Gonzalez-Voyer et al 2009 ; Eifert et al 2014 ; Schulz-Mirbach et al 2016 ; Ahmed et al 2017 ), which gives relatively coarse information and requires an assumption that the structure is ellipsoid, but it can be done easily and cheaply in large numbers. Histology is less frequently used (e.g., Kotrschal and Palzenberger 1992 ; Day et al 2005 ), and although it can provide quite detailed information, it requires careful slicing, staining, and then imaging of the brain structures, and can be prone to distortions as the slices are mounted onto slides, making measurements of volume inaccurate.…”

Gene expression stasis and plasticity following migration into a foreign environment

“…Our result is thus somewhat puzzling, in that we observe greater transcriptomic plasticity in lake fish, which inhabit the more temporally stable habitat. While stream habitats are generally very diverse (flow regime, overhead foliage, substrate, spatial distribution of prey), lake habitats generally have large and smooth transitions between any variation in environmental variables (and in most cases very little variation (Ahmed, Thompson, Bolnick, & Stuart, ; Stuart et al., ). However, lakes may be less predictable in other ways.…”