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elephant-nose fishes

The African mormyrids or elephant-nose fishes were noted for having unusually large brains already more than a century ago (Erdl, 1846). For a mean body mass of 26 g, the mean brain weight of Gnathonemus petersii reaches 0.53 g, almost three times its expected mean value of 0.19 g, as calculated from the relationship between brain size and body size in teleost fish (Kaufman, 2003).  

This character is probably, at least in part, related to their ability to sense prey and to communicate by generating and perceiving electric fields (Nieuwenhuys and Nicholson, 1969).  In contrast with mammals, it is the cerebellum, and not the telencephalon that is greatly enlarged in these fishes.  More precisely, the most enlarged part of the mormyrids cerebellum (or ¡°gigantocerebellum¡±, Nieuwenhuys and Nicholson, 1969) is the valvulla cerebelli (fig. 2).  This rostral protrusion of the cerebellum is only present in actinopterygian fish.  In elephant-nose fishes, the valvula cerebelli covers most of the rest of the brain (fig. 2).  In contrast, in another highly derived brain such as the human brain, it is the telencephalon, and more specifically the neocortex, a telencephalic structure unique to mammals, that entirely covers the rest of the brain (fig. 3).
Brains are always costly organs in terms of energy consumption.  What are then the challenges faced by humans and mormyrids?  
Vertebrates show remarkably constant ratios of brain to body O2 consumption, the brain using 2–8 % of resting body O2 consumption, suggesting that evolution has put limits on the energetic cost of brain functions (Mink et al., 1981).  Only man is an exception to this rule.  The adult human brain accounts for 2% of the total body mass but consumes some 20 % of the O2 taken up by the resting body.  This represents an exceptionally high rate of energy use among vertebrates and appears to have remained undisputed.  
The results of Nilsson (1996) however suggest that, in the electric fish Gnathonemus petersii, the brain is responsible for approximately 60% of body O2 consumption, a figure three times higher than that for any other vertebrate studied so far, including human.

The exceptionally high energetic cost of the Gnathonemus petersii brain appears to be a consequence both of the brain being very large and of the fish being ectothermic (Nilsson, 1996).  At the same temperature and body size, total energy expenditures of ectothermic vertebrates are about 1/13 of those of endotherms but brain energy expenditures are quite similar.  When considering the whole-body energy budget, it is thus comparatively more expensive for an ectothermic vertebrate to have a large brain. This may be a reason why most ectothermic vertebrates have relatively small brains.  

Consequently, the fact that Gnathonemus petersii is an ectothermic vertebrate and has such a huge brain makes this organ an exceptionally expensive part of the whole body (Nilsson, 1996).  To some extent, Gnathonemus petersii therefore faces an ecophysiological challenge unparalled in the animal kingdom, including human.

Differences in cognition and relative brain size are among the most striking differences between humans and their closest primate relatives. The Energy Trade-Off Hypothesis predicts that a major shift in energy allocation across tissues occurred during human origins in order to support the remarkable expansion of a metabolically expensive brain. Recent genetic studies, based on genome wide scans for signatures of adaptation and comparative brain transcriptomics, suggest a role for metabolic genes in human evolution consistent with the Energy Trade-Off Hypothesis. However, the genetic and molecular mechanisms underlying this hypothesis remain unknown and experimental evidence is lacking. Despite the numerous advantages of studying great apes, including extensive genomic and medical data, there are ethical and practical limitations to performing controlled experiments. Fortunately, human is not the only species that has experienced increased brain size. For instance, it has been shown that the brain of the elephant-nose fish (Gnathonemus petersii) from the Mormyridae family is extremely enlarged and consumes proportionally three times more oxygen than the human brain. Because the Mormyrids also exhibit spectacular variation in brain size, they offer a unique opportunity to study the genetic bases of the Energy Trade-Off Hypothesis with laboratory tractable organisms. I will focus on two species with significant brain size differences: G. petersii and Brienomyrus brachyistius. Using a combination of comparative transcriptomics across multiple tissues and computational approaches, I will identify genes involved in a metabolic trade-off. Overlaid with previous genomic studies on primates, these results will contribute to a better understanding of human origins. This project is also a necessary first step to develop a genetic model for studying the Energy Trade-Off Hypothesis.