Environmental Complexity and Social Organization Sculpt the Brain in Lake Tanganyikan Cichlid Fish

Abstract

Complex brains and behaviors have occurred repeatedly within vertebrate classes throughout evolution. What adaptive pressures drive such changes? Both environmental and social features have been implicated in the expansion of select brain structures, particularly the telencephalon. East African cichlid fishes provide a superb opportunity to analyze the social and ecological correlates of neural phenotypes and their evolution. As a result of rapid, recent, and repeated radiations, there are hundreds of closely-related species available for study, with an astonishing diversity in habitat preferences and social behaviors. In this study, we present quantitative ecological, social, and neuroanatomical data for closely-related species from the (monophyletic) Ectodini clade of Lake Tanganyikan cichlid fish. The species differed either in habitat preference or social organization. After accounting for phylogeny with independent contrasts, we find that environmental and social factors differentially affect the brain, with environmental factors showing a broader effect on a range of brain structures compared to social factors. Five out of seven of the brain measures show a relationship with habitat measures. Brain size and cerebellar size are positively correlated with species number (which is correlated with habitat complexity); the medulla and olfactory bulb are negatively correlated with habitat measures. The telencephalon shows a trend toward a positive correlation with rock size. In contrast, only two brain structures, the telencephalon and hypothalamus, are correlated with social factors. Telencephalic size is larger in monogamous species compared to polygamous species, as well as with increased numbers of individuals; monogamy is also associated with smaller hypothalamic size. Our results suggest that selection or drift can act independently on different brain regions as the species diverge into different habitats and social systems.

Social fishes and single mothers: brain evolution in African cichlids

“…Habitat has also been shown to influence brain size in bats (Safi & Dechmann 2005) and, in Tanganyikan cichlids, habitat complexity was found to be associated with larger brains and larger cerebella, while the telencephalon showed a similar trend (Pollen et al 2007). Habitat complexity was further shown to be correlated with the number of species and number of individuals (Pollen et al 2007); however, we found that habitat and diet are correlated, but Pollen et al (2007) did not include diet in their analyses, thus its influence on brain size cannot be ruled out.…”

“…bottom-dwelling invertebrates and crustaceans) as 3; plankton and zooplankton as 4; invertebrates and crustaceans found in the water column as 5; and fishes as 6. Habitat reflected variation in complexity, previously shown to be correlated with brain structure (Pollen et al 2007): benthic and benthopelagic habitats were coded as 1; semi-pelagic as 2; sandy or shallow vegetated habitats as 3; rocky or rubble as 4; and rock habitat as 5. Pollen et al (2007) showed that sandy, rocky or rubble (intermediate) and rock habitat differ significantly in several quantitative measures of complexity, thus the categorization adequately reflects complexity.…”

“…Two previous studies have analysed the correlates of brain size and structure in African cichlid fishes and their results suggest an influence of diet and habitat (Huber et al 1997;Pollen et al 2007). Interestingly, results from one study suggest a potential effect of mating pattern on telencephalon size ( Pollen et al 2007).…”

“…However, neural structures within the brain evolve in concert in response to specific cognitive challenges as shown by the presence of 'cerebrotypes' that highlight convergent response of brain architecture to specific selection pressures (Clark et al 2001;de Winter & Oxnard 2001;Iwaniuk & Hurd 2005), such changes are expected to be reflected in total brain size. As an example of this, in Tanganyikan cichlids, whole brain size explained 50-76 per cent of the variation in all brain structures, except for the dorsal medulla where the variance explained was 18-32 per cent (Pollen et al 2007). Thus, the resulting correlates of brain size should point to factors that have a notable influence on one or several neural structures.…”

Orientation from open water to settlement habitats by coral reef fish: behavioral flexibility in the use of multiple reliable cues

“…Various species of reef fish have larvae that navigate through multiple coastal ecosystems before settling (Nagelkerken 2009). For example, reef species that are associated with mangroves and seagrass beds during only their early life stage need to navigate as larvae from the open ocean, across coastal shelves that harbor coral reefs, towards bays or lagoons that harbor juvenile habitats (Pollen et al 2007, Pollux et al 2007. Potentially, larvae of such species consecutively use auditory, olfactory, and visual cues to navigate from the open ocean towards their settlement habitats (Huijbers et al 2012).…”