An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain

School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, 7 York Road, Parktown, 2193, Johannesburg, Republic of South Africa.
Biological Reviews (Impact Factor: 9.67). 06/2006; 81(2):293-338. DOI: 10.1017/S1464793106007019
Source: PubMed


This review examines aspects of cetacean brain structure related to behaviour and evolution. Major considerations include cetacean brain-body allometry, structure of the cerebral cortex, the hippocampal formation, specialisations of the cetacean brain related to vocalisations and sleep phenomenology, paleoneurology, and brain-body allometry during cetacean evolution. These data are assimilated to demonstrate that there is no neural basis for the often-asserted high intellectual abilities of cetaceans. Despite this, the cetaceans do have volumetrically large brains. A novel hypothesis regarding the evolution of large brain size in cetaceans is put forward. It is shown that a combination of an unusually high number of glial cells and unihemispheric sleep phenomenology make the cetacean brain an efficient thermogenetic organ, which is needed to counteract heat loss to the water. It is demonstrated that water temperature is the major selection pressure driving an altered scaling of brain and body size and an increased actual brain size in cetaceans. A point in the evolutionary history of cetaceans is identified as the moment in which water temperature became a significant selection pressure in cetacean brain evolution. This occurred at the Archaeoceti - modern cetacean faunal transition. The size, structure and scaling of the cetacean brain continues to be shaped by water temperature in extant cetaceans. The alterations in cetacean brain structure, function and scaling, combined with the imperative of producing offspring that can withstand the rate of heat loss experienced in water, within the genetic confines of eutherian mammal reproductive constraints, provides an explanation for the evolution of the large size of the cetacean brain. These observations provide an alternative to the widely held belief of a correlation between brain size and intelligence in cetaceans.

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Available from: Paul Manger, Sep 29, 2015
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    • "In comparison to a dolphin skull, such as Tursiops, Pontoporia has a long narrow bony rostrum, with a concave ventral profile in lateral view, and exhibits the most symmetrical skull of any extant odontocetes (Ness 1967, Barnes 1985, Cranford et al. 1996) (Fig. 1). The small braincase with one of the smallest brains among toothed whales (Schwerdtfeger et al. 1984, Manger 2006) may correlate with the elongation of Pontoporia's nasal complex. Huggenberger et al. (2010) have noted that this elongation is marked by topographical relations of the dorsal bursae with the cranial vault and melon, which is located further caudally in relation to the brain case. "
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    ABSTRACT: Franciscana dolphins (Pontoporia blainvillei) are the most endangered species of the western South Atlantic Ocean. The major cause of their vulnerability is incidental bycatch in fishery gill nets. Ontogenetic changes of biosonar relevant structures in Pontoporia were analyzed in five specimens (one female neonate, two male neonates and two male adults) using digital imaging technology (MRI, CT) and macroscopic dissections to compare structures involved in sound production and reception. These data were compared to an ontogenetic series of 69 macerated skulls of Pontoporia in order to elucidate the correlation between soft tissue structures and bones of the epicranial complex and to describe the development-related changes in the mandible. Postnatal developmental shape changes of the posterior part of the right vestibular air sac followed bone formation and the melon with its right branch elongated, paralleling the flatter facial depression of adults. Minor postnatal developmental modifications were verified in the tympano-periotic complex but a shape change of the mandible was visible by a ventral deviation of the posterior part of the mandible in adults. These results reveal postnatal changes in allometry and shape of biosonar relevant structures that may be one of the causes that increase bycatch of neonate and young Pontoporia individuals.
    Marine Mammal Science 04/2015; 31(3). DOI:10.1111/mms.12211 · 1.94 Impact Factor
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    • "With the discovery of specific endogenous markers to visualize immature neurons and thus adult hippocampal neurogenesis (using antibodies directed against doublecortin , DCX; Kempermann 2012), we decided to look for evidence of adult hippocampal neurogenesis and evaluate the absolute and relative size of the cetacean hippocampus in comparison to a broad range of other mammalian species. Hippocampal size and the presence or absence of adult hippocampal neurogenesis in the cetaceans would provide substantive information to the debate surrounding the purported cognitive complexity of species belonging to this mammalian order (Manger 2006, 2013; Marino et al. 2008). "
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    ABSTRACT: The hippocampus is essential for the formation and retrieval of memories and is a crucial neural structure sub-serving complex cognition. Adult hippocampal neurogenesis, the birth, migration and integration of new neurons, is thought to contribute to hippocampal circuit plasticity to augment function. We evaluated hippocampal volume in relation to brain volume in 375 mammal species and examined 71 mammal species for the presence of adult hippocampal neurogenesis using immunohistochemistry for doublecortin, an endogenous marker of immature neurons that can be used as a proxy marker for the presence of adult neurogenesis. We identified that the hippocampus in cetaceans (whales, dolphins and porpoises) is both absolutely and relatively small for their overall brain size, and found that the mammalian hippocampus scaled as an exponential function in relation to brain volume. In contrast, the amygdala was found to scale as a linear function of brain volume, but again, the relative size of the amygdala in cetaceans was small. The cetacean hippocampus lacks staining for doublecortin in the dentate gyrus and thus shows no clear signs of adult hippocampal neurogenesis. This lack of evidence of adult hippocampal neurogenesis, along with the small hippocampus, questions current assumptions regarding cognitive abilities associated with hippocampal function in the cetaceans. These anatomical features of the cetacean hippocampus may be related to the lack of postnatal sleep, causing a postnatal cessation of hippocampal neurogenesis.
    Brain Structure and Function 01/2015; 220(1):361. DOI:10.1007/s00429-013-0660-1 · 5.62 Impact Factor
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    • "Testes and brain tissues are energetically expensive, so a reduction in the mass of one or the other would evolve in species that did not need or was unable to maintain large amounts of costly tissue (Pitnick et al. 2006). Thermogenesis was suggested as a possible explanation for the evolution of large brains in cetaceans (Manger 2006), but there is overwhelming evidence suggesting that cetacean brain size is linked with cognitive capacities (Herman 1980; Ridgeway 1986; Connor et al. 1992; Marino 1998; Connor 2007; Marino et al. 2007). There was no significant correlation between residual testes mass and residual brain mass after controlling for phylogeny, which weakens support for the Machavellian intelligence or sexual conflict hypothesis that predicts increased brain mass with increasing sperm competition. "
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    ABSTRACT: Little is known about their mating systems, but odontocetes may utilize the same types of mating systems as terrestrial mammals. Species with relatively large testes are likely to be polygynandrous, while species with smaller testes and greater sexual size dimorphism (SSD) are predicted to be polygynous. The sexual conflict/Machiavellian intelligence hypothesis predicts that polygynadrous species also evolved larger brains both to coerce conspecifics to mate and resist mating attempts by undesirable mates. The costly tissue hypothesis predicts that species investing heavily in testes invest less in brain tissue and vice versa in order to conserve energy. Residual testes and brain mass measurements were used to test the sexual conflict and costly tissue hypotheses in 40 species of odontocetes. Correlations were performed on both raw data and independent contrasts to control for phylogeny. There was a significant positive correlation between residual testes mass and SSD in both data sets, and between residual testes mass and residual brain mass in the non-phylogenetically controlled data set. Results indicate a negative relationship between increased testes masses and SSD in odontocetes. There was no support for the costly tissue hypothesis. Support for sexual conflict/Machiavellian intelligence hypothesis was found only when phylogenetic effects were not considered.
    Canadian Journal of Zoology 06/2014; 92(8):721-726. DOI:10.1139/cjz-2014-0044 · 1.30 Impact Factor
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