Cetacean Brain Research Articles

Delphinid brain development from neonate to adulthood with comparisons to other cetaceans and artiodactyls

AbstractWhy do neonatal and adult delphinids have much larger brains than artiodactyls when they have common ancestors? We explore relationships between neonatal brain size, gestation duration, maternal body mass, and body growth. Cetacean brains grow fast in the womb and longer gestation results in a larger brain. Allometry shows that the larger the mother's body mass, the larger the neonatal brain. After birth, delphinid bodies grow much faster than brains, and the index of encephalization decreases even as brains grow beyond maturity. Delphinids’ larger brain growth during life at sea may be explained by at least three differences from artiodactyls’ life on land. First, the sea offers high calorie prey to support growth of a large brain. Second, life in water offers relief from gravity, allowing for a large head to contain a large brain. Third, sound in water may pass through an immersed body. This allows sounds from the water to reach the fetus, driving early development of delphinoid auditory brain parts. As an example of this, the dolphin ear bone is very large at birth. Furthermore, the auditory nervous system appears mature well before birth. Compared with artiodactyls, these three differences likely result in a larger delphinid brain.

The social and cultural roots of whale and dolphin brains.

Encephalization, or brain expansion, underpins humans' sophisticated social cognition, including language, joint attention, shared goals, teaching, consensus decision-making and empathy. These abilities promote and stabilize cooperative social interactions, and have allowed us to create a 'cognitive' or 'cultural' niche and colonize almost every terrestrial ecosystem. Cetaceans (whales and dolphins) also have exceptionally large and anatomically sophisticated brains. Here, by evaluating a comprehensive database of brain size, social structures and cultural behaviours across cetacean species, we ask whether cetacean brains are similarly associated with a marine cultural niche. We show that cetacean encephalization is predicted by both social structure and by a quadratic relationship with group size. Moreover, brain size predicts the breadth of social and cultural behaviours, as well as ecological factors (diversity of prey types and to a lesser extent latitudinal range). The apparent coevolution of brains, social structure and behavioural richness of marine mammals provides a unique and striking parallel to the large brains and hyper-sociality of humans and other primates. Our results suggest that cetacean social cognition might similarly have arisen to provide the capacity to learn and use a diverse set of behavioural strategies in response to the challenges of social living.

Is Cetacean Intelligence Special? New Perspectives on the Debate

In recent years, the interpretation of our observations of animal behaviour, in particular that of cetaceans, has captured a substantial amount of attention in the scientific community. The traditional view that supports a special intellectual status for this mammalian order has fallen under significant scrutiny, in large part due to problems of how to define and test the cognitive performance of animals. This paper presents evidence supporting complex cognition in cetaceans obtained using the recently developed intelligence and embodiment hypothesis. This hypothesis is based on evolutionary neuroscience and postulates the existence of a common information-processing principle associated with nervous systems that evolved naturally and serves as the foundation from which intelligence can emerge. This theoretical framework explaining animal intelligence in neural computational terms is supported using a new mathematical model. Two pathways leading to higher levels of intelligence in animals are identified, each reflecting a trade-off either in energetic requirements or the number of neurons used. A description of the evolutionary pathway that led to increased cognitive capacities in cetacean brains is detailed and evidence supporting complex cognition in cetaceans is presented. This paper also provides an interpretation of the adaptive function of cetacean neuronal traits.

Genetic basis of brain size evolution in cetaceans: insights from adaptive evolution of seven primary microcephaly (MCPH) genes

BackgroundCetacean brain size expansion is an enigmatic event in mammalian evolution, yet its genetic basis remains poorly explored. Here, all exons of the seven primary microcephaly (MCPH) genes that play key roles in size regulation during brain development were investigated in representative cetacean lineages.ResultsSequences of MCPH2–7 genes were intact in cetaceans but frameshift mutations and stop codons was identified in MCPH1. Extensive positive selection was identified in four of six intact MCPH genes: WDR62, CDK5RAP2, CEP152, and ASPM. Specially, positive selection at CDK5RAP2 and ASPM were examined along lineages of odontocetes with increased encephalization quotients (EQ) and mysticetes with reduced EQ but at WDR62 only found along odontocete lineages. Interestingly, a positive association between evolutionary rate (ω) and EQ was identified for CDK5RAP2 and ASPM. Furthermore, we tested the binding affinities between Calmodulin (CaM) and ASPM IQ motif in cetaceans because only CaM combined with IQ, can ASPM perform the function in determining brain size. Preliminary function assay showed binding affinities between CaM and IQ motif of the odontocetes with increased EQ was stronger than for the mysticetes with decreased EQ. In addition, evolution rate of ASPM and CDK5RAP2 were significantly related to mean group size (as one measure of social complexity).ConclusionsOur study investigated the genetic basis of cetacean brain size evolution. Significant positive selection was examined along lineages with both increased and decreased EQ at CDK5RAP2 and ASPM, which is well matched with cetacean complex brain size evolution. Evolutionary rate of CDK5RAP2 and ASPM were significantly related to EQ, suggesting that these two genes may have contributed to EQ expansion in cetaceans. This suggestion was further indicated by our preliminary function test that ASPM might be mainly linked to evolutionary increases in EQ. Most strikingly, our results suggested that cetaceans evolved large brains to manage complex social systems, consisting with the ‘social brain hypothesis’, as evolutionary rate of ASPM and CDK5RAP2 were significantly related to mean group size.

Vibrio parahaemolyticus- and V. alginolyticus-associated meningo-encephalitis in a bottlenose dolphin (Tursiops truncatus) from the Adriatic coast of Italy

A case of Vibrio parahaemolyticus- and V. alginolyticus-associated meningo-encephalitis in a bottlenose dolphin (Tursiops truncatus) found stranded along the Adriatic coast of Italy in 2016 is herein reported, along with a minireview on V. parahaemolyticus and V. alginolyticus infections in aquatic mammals.Macroscopically, two abscesses were found in the dolphin's forebrain, along with an extensive, bilateral, parasitic broncho-pneumonia. Histologically, a suppurative-to-pyogranulomatous meningo-encephalitis involved the brain but not the cerebellum. Microbiological investigations yielded isolation of V. parahaemolyticus and V. alginolyticus from the aforementioned abscesses and from the brain parenchyma, respectively, with simultaneous recovery of Shewanella algae from the heart and of Photobacterium damselae from a blowhole swab.Although V. parahaemolyticus and V. alginolyticus, which are widely distributed across marine ecosystems worldwide, likely played a role in the development of the suppurative meningo-encephalitis in this dolphin, we are not aware of previous isolations of any of these two bacteria neither from cetacean brain lesions, nor from abscesses in aquatic mammals.

Neuroanatomy of the killer whale (Orcinus orca): a magnetic resonance imaging investigation of structure with insights on function and evolution.

The evolutionary process of adaptation to an obligatory aquatic existence dramatically modified cetacean brain structure and function. The brain of the killer whale (Orcinus orca) may be the largest of all taxa supporting a panoply of cognitive, sensory, and sensorimotor abilities. Despite this, examination of the O. orca brain has been limited in scope resulting in significant deficits in knowledge concerning its structure and function. The present study aims to describe the neural organization and potential function of the O. orca brain while linking these traits to potential evolutionary drivers. Magnetic resonance imaging was used for volumetric analysis and three-dimensional reconstruction of an in situ postmortem O. orca brain. Measurements were determined for cortical gray and cerebral white matter, subcortical nuclei, cerebellar gray and white matter, corpus callosum, hippocampi, superior and inferior colliculi, and neuroendocrine structures. With cerebral volume comprising 81.51% of the total brain volume, this O. orca brain is one of the most corticalized mammalian brains studied to date. O. orca and other delphinoid cetaceans exhibit isometric scaling of cerebral white matter with increasing brain size, a trait that violates an otherwise evolutionarily conserved cerebral scaling law. Using comparative neurobiology, it is argued that the divergent cerebral morphology of delphinoid cetaceans compared to other mammalian taxa may have evolved in response to the sensorimotor demands of the aquatic environment. Furthermore, selective pressures associated with the evolution of echolocation and unihemispheric sleep are implicated in substructure morphology and function. This neuroanatomical dataset, heretofore absent from the literature, provides important quantitative data to test hypotheses regarding brain structure, function, and evolution within Cetacea and across Mammalia.

Forward shift of feeding buzz components of dolphins and belugas during associative learning reveals a likely connection to reward expectation, pleasure and brain dopamine activation.

For many years, we heard sounds associated with reward from dolphins and belugas. We named these pulsed sounds victory squeals (VS), as they remind us of a child's squeal of delight. Here we put these sounds in context with natural and learned behavior. Like bats, echolocating cetaceans produce feeding buzzes as they approach and catch prey. Unlike bats, cetaceans continue their feeding buzzes after prey capture and the after portion is what we call the VS. Prior to training (or conditioning), the VS comes after the fish reward; with repeated trials it moves to before the reward. During training, we use a whistle or other sound to signal a correct response by the animal. This sound signal, named a secondary reinforcer (SR), leads to the primary reinforcer, fish. Trainers usually name their whistle or other SR a bridge, as it bridges the time gap between the correct response and reward delivery. During learning, the SR becomes associated with reward and the VS comes after the SR rather than after the fish. By following the SR, the VS confirms that the animal expects a reward. Results of early brain stimulation work suggest to us that SR stimulates brain dopamine release, which leads to the VS. Although there are no direct studies of dopamine release in cetaceans, we found that the timing of our VS is consistent with a response after dopamine release. We compared trained vocal responses to auditory stimuli with VS responses to SR sounds. Auditory stimuli that did not signal reward resulted in faster responses by a mean of 151 ms for dolphins and 250 ms for belugas. In laboratory animals, there is a 100 to 200 ms delay for dopamine release. VS delay in our animals is similar and consistent with vocalization after dopamine release. Our novel observation suggests that the dopamine reward system is active in cetacean brains.

THE EVOLUTIONARY HISTORY OF CETACEAN BRAIN AND BODY SIZE

Cetaceans rival primates in brain size relative to body size and include species with the largest brains and biggest bodies to have ever evolved. Cetaceans are remarkably diverse, varying in both phenotypes by several orders of magnitude, with notable differences between the two extant suborders, Mysticeti and Odontoceti. We analyzed the evolutionary history of brain and body mass, and relative brain size measured by the encephalization quotient (EQ), using a data set of extinct and extant taxa to capture temporal variation in the mode and direction of evolution. Our results suggest that cetacean brain and body mass evolved under strong directional trends to increase through time, but decreases in EQ were widespread. Mysticetes have significantly lower EQs than odontocetes due to a shift in brain:body allometry following the divergence of the suborders, caused by rapid increases in body mass in Mysticeti and a period of body mass reduction in Odontoceti. The pattern in Cetacea contrasts with that in primates, which experienced strong trends to increase brain mass and relative brain size, but not body mass. We discuss what these analyses reveal about the convergent evolution of large brains, and highlight that until recently the most encephalized mammals were odontocetes, not primates.

Positive selection at the ASPM gene coincides with brain size enlargements in cetaceans

The enlargement of cetacean brain size represents an enigmatic event in mammalian evolution, yet its genetic basis remains poorly explored. One candidate gene associated with brain size evolution is the abnormal spindle-like microcephaly associated (ASPM), as mutations in this gene cause severe reductions in the cortical size of humans. Here, we investigated the ASPM gene in representative cetacean lineages and previously published sequences from other mammals to test whether the expansion of the cetacean brain matched adaptive ASPM evolution patterns. Our analyses yielded significant evidence of positive selection on the ASPM gene during cetacean evolution, especially for the Odontoceti and Delphinoidea lineages. These molecular patterns were associated with two major events of relative brain size enlargement in odontocetes and delphinoids. It is of particular interest to find that positive selection was restricted to cetaceans and primates, two distant lineages both characterized by a massive expansion of brain size. This result is suggestive of convergent molecular evolution, although no site-specific convergence at the amino acid level was found.

Neuroglobin of seals and whales: Evidence for a divergent role in the diving brain

Although many physiological adaptations of diving mammals have been reported, little is known about how their brains sustain the high demands for metabolic energy and thus O2 when submerged. A recent study revealed in the deep-diving hooded seal (Cystophora cristata) a unique shift of the oxidative energy metabolism and neuroglobin, a respiratory protein that is involved in neuronal hypoxia tolerance, from neurons to astrocytes. Here we have investigated neuroglobin in another pinniped species, the harp seal (Pagophilus groenlandicus), and in two cetaceans, the harbor porpoise (Phocoena phocoena) and the minke whale (Balaenoptera acutorostrata). Neuroglobin sequences, expression levels and patterns were compared with those of terrestrial relatives, the ferret (Mustela putorius furo) and the cattle (Bos taurus), respectively. Neuroglobin sequences of whales and seals only differ in two or three amino acids from those of cattle and ferret, and are unlikely to confer functional differences, e.g. in O2 affinity. Neuroglobin is expressed in the astrocytes also of P. groenlandicus, suggesting that the shift of neuroglobin and oxidative metabolism is a common adaptation in the brains of deep-diving phocid seals. In the cetacean brain neuroglobin resides in neurons, like in terrestrial mammals. However, neuroglobin mRNA expression levels were 4–15 times higher in the brains of harbor porpoises and minke whales than in terrestrial mammals or in seals. Thus neuroglobin appears to play a specific role in diving mammals, but seals and whales have evolved divergent strategies to cope with cerebral hypoxia. The specific function of neuroglobin that conveys hypoxia tolerance may either relate to oxygen supply or protection from reactive oxygen species. The different strategies in seals and whales resulted from a divergent evolution and an independent adaptation to diving.

Comparative analysis of encephalization in mammals reveals relaxed constraints on anthropoid primate and cetacean brain scaling

There is a well-established allometric relationship between brain and body mass in mammals. Deviation of relatively increased brain size from this pattern appears to coincide with enhanced cognitive abilities. To examine whether there is a phylogenetic structure to such episodes of changes in encephalization across mammals, we used phylogenetic techniques to analyse brain mass, body mass and encephalization quotient (EQ) among 630 extant mammalian species. Among all mammals, anthropoid primates and odontocete cetaceans have significantly greater variance in EQ, suggesting that evolutionary constraints that result in a strict correlation between brain and body mass have independently become relaxed. Moreover, ancestral state reconstructions of absolute brain mass, body mass and EQ revealed patterns of increase and decrease in EQ within anthropoid primates and cetaceans. We propose both neutral drift and selective factors may have played a role in the evolution of brain-body allometry.

Brains matter, bodies maybe not: the case for examining neuron numbers irrespective of body size

It is usually considered a paradox that the human brain, although smaller than elephant and cetacean brains, is the most cognitively able. The concept that humans are more encephalized than all other mammals appeared in the 1970s as a solution to that paradox: humans have a brain that is much larger than expected from their body mass. Such an "excess brain mass" would provide increased cognitive abilities across species, thus explaining our cognitive superiority. However, behind the paradox lies the assumption that large mammalian brains are scaled-up versions of smaller brains, always containing more neurons than smaller ones--an assumption that we have recently shown to be invalid. Here, it is proposed that the absolute number of neurons, irrespective of brain or body size, is a better predictor of cognitive ability--in which case, the cognitive superiority of humans would come as no paradox, surprise, or exception to evolutionary rules.

A Neurological Comparative Study of the Harp Seal (Pagophilus groenlandicus) and Harbor Porpoise (Phocoena phocoena) Brain

The cetacean brain is well studied. However, few comparisons have been done with other marine mammals. In this study, we compared the harp seal (Pagophilus groenlandicus) and the harbor porpoise brain (Phocoena phocoena). Stereological methods were applied to compare three areas of interest: the entire neocortex and two subdivisions of the neocortex, the auditory and visual cortices. The total number of neurons and glial cells in the three regions was estimated. The main results showed that the harbor porpoise have an estimated 14.9 × 10(9) neocortical neurons and 34.8 × 10(9) neocortical glial cells, whereas the harp seal have 6.1 × 10(9) neocortical neurons and 17.5 × 10(9) neocortical glial cells. The harbor porpoise have significantly more neurons and glial cells in the auditory cortex than in the visual cortex, whereas the pattern was opposite for the harp seal. These results are the first to provide estimates of the number of neurons and glial cells in the neocortex of the harp seal and harbor porpoise brain and offer new data to the comparative field of mammalian brain evolution.

Cetacean Brain Evolution: Dwarf Sperm Whale (Kogia sima) and Common Dolphin (Delphinus delphis) – An Investigation with High-Resolution 3D MRI

This study compares a whole brain of the dwarf sperm whale (Kogia sima) with that of a common dolphin (Delphinus delphis) using high-resolution magnetic resonance imaging (MRI). The Kogia brain was scanned with a Siemens Trio Magnetic Resonance scanner in the three main planes. As in the common dolphin and other marine odontocetes, the brain of the dwarf sperm whale is large, with the telencephalic hemispheres remarkably dominating the brain stem. The neocortex is voluminous and the cortical grey matter thin but expansive and densely convoluted. The corpus callosum is thin and the anterior commissure hard to detect whereas the posterior commissure is well-developed. There is consistency as to the lack of telencephalic structures (olfactory bulb and peduncle, olfactory ventricular recess) and neither an occipital lobe of the telencephalic hemisphere nor the posterior horn of the lateral ventricle are present. A pineal organ could not be detected in Kogia. Both species show a tiny hippocampus and thin fornix and the mammillary body is very small whereas other structures of the limbic system are well-developed. The brain stem is thick and underlies a large cerebellum, both of which, however, are smaller in Kogia. The vestibular system is markedly reduced with the exception of the lateral (Deiters’) nucleus. The visual system, although well-developed in both species, is exceeded by the impressive absolute and relative size of the auditory system. The brainstem and cerebellum comprise a series of structures (elliptic nucleus, medial accessory inferior olive, paraflocculus and posterior interpositus nucleus) showing characteristic odontocete dimensions and size correlations. All these structures seem to serve the auditory system with respect to echolocation, communication, and navigation.

Subglacial cetaceans and other mathematical mysteries: a Commentary on “A quantitative test of the thermogenesis hypothesis of cetacean brain evolution, using phylogenetic comparative methods” by C. Maximino

A recent paper published in this Journal purported to provide a quantitative test of the thermogenetic hypothesis of cetacean brain evolution. While using appropriate statistical analyses that account for phylogenetic inertia, errors in the raw data and in interpretation of the thermogenetic hypothesis raise concerns about the validity of the statistical results and the conclusions of the paper. In this commentary the errors in raw data, mathematical approaches, the lack of inclusion of certain data points and misinterpretation of the thermogenetic hypothesis are detailed. The conclusion being that the thermogenetic hypothesis has not been correctly tested by the study.

Reply to Manger’s Commentary on “A quantitative test of the thermogenesis hypothesis of cetacean brain evolution, using phylogenetic comparative methods”

In his Commentary (Manger PR. 2009. Subglacial cetaceans and other mathematical mysteries: a Commentary on “A quantitative test of the thermogenesis hypothesis of cetacean brain evolution, using phylogenetic comparative methods” by C. Maximino. Mar Fresh Behav Physiol. 42: 359–362) on my paper (Maximino C. 2009. A quantitative test of the thermogenesis hypothesis of cetacean brain evolution, using phylogenetic comparative methods. Mar Freshwater Behav Physiol. 42:1–17), Dr Paul Manger noted four errors in the quantitative analysis of the relationship between cetacean encephalization quotients (EQs) and water temperatures, which I suggested was a test of his thermogenesis hypothesis (Manger PR. 2006. An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain. Biol Rev Camb Philos Soc. 81:293–338). These referred to incorrect raw data on water temperatures for two species, odd use of midpoint temperatures as independent variable, lack of inclusion of data on Mysticeti and the use of a differently derived EQ and midpoints instead of the EQs proposed by Manger and temperature ranges; Dr Manger proposed that these errors invalidate the analysis, with special emphasis in an observation that, since my paper did not address the relationship between EQs and temperature range, it did not actually test the thermogenesis hypothesis. In this Reply, I apologize for the mistakes which were made, and show that re-analysis using all the proposed alterations do not qualitatively or quantitatively alter the final result. I also argue that the relationship between phylogenetically correct EQs and midpoint temperatures is a better test of the thermogenesis hypothesis than the relationship between non-phylogenetic EQs and temperature ranges.

A quantitative test of the thermogenesis hypothesis of cetacean brain evolution, using phylogenetic comparative methods

The present article tests one assumption of the thermogenesis hypothesis of cetacean brain evolution (Biol. Rev., Vol. 81, pp. 293–338, 2006) by analysing phylogenetically correct correlations between relative brain mass and environmental temperatures in 20 odontocetes, as well as undertaking a phylogenetic analysis of covariance of differences between the clades in brain mass. A simulation of trait evolution, under an Ornstein–Uhlenbeck process, yielded phylogenetically correct allometric slopes, which were used to correct the body size in correlations and ANCOVAs; the simulation also produced null distributions for these analyses. No significant correlation was found between environmental temperatures and relative brain masses, and neither was there a significant difference between clades in brain masses. These results challenge one of the central assumptions of the thermogenesis hypothesis, but other assumptions from this hypothesis are still to be explained. Alternative hypotheses are also discussed, but further studies will be necessary to judge their validity.

A claim in search of evidence: reply to Manger’s thermogenesis hypothesis of cetacean brain structure

In a recent publication in Biological Reviews, Manger (2006) made the controversial claim that the large brains of cetaceans evolved to generate heat during oceanic cooling in the Oligocene epoch and not, as is the currently accepted view, as a basis for an increase in cognitive or information-processing capabilities in response to ecological or social pressures. Manger further argued that dolphins and other cetaceans are considerably less intelligent than generally thought. In this review we challenge Manger's arguments and provide abundant evidence that modern cetacean brains are large in order to support complex cognitive abilities driven by social and ecological forces.

Beautiful Minds—For How Long?

Beautiful Minds—For How Long?

Neuroanatomy of the Subadult and Fetal Brain of the Atlantic White‐sided Dolphin (Lagenorhynchus acutus) from in Situ Magnetic Resonance Images

This article provides the first anatomically labeled, magnetic resonance imaging (MRI) -based atlas of the subadult and fetal Atlantic white-sided dolphin (Lagenorhynchus acutus) brain. It differs from previous MRI-based atlases of cetaceans in that it was created from images of fresh, postmortem brains in situ rather than extracted, formalin-fixed brains. The in situ images displayed the classic hallmarks of odontocete brains: fore-shortened orbital lobes and pronounced temporal width. Olfactory structures were absent and auditory regions (e.g., temporal lobes and inferior colliculi) were enlarged. In the subadult and fetal postmortem MRI scans, the hippocampus was identifiable, despite the relatively small size of this structure in cetaceans. The white matter tracts of the fetal hindbrain and cerebellum were pronounced, but in the telencephalon, the white matter tracts were much less distinct, consistent with less myelin. The white matter tracts of the auditory pathways in the fetal brains were myelinated, as shown by the T2 hypointensity signals for the inferior colliculus, cochlear nuclei, and trapezoid bodies. This finding is consistent with hearing and auditory processing regions maturing in utero in L. acutus, as has been observed for most mammals. In situ MRI scanning of fresh, postmortem specimens can be used not only to study the evolution and developmental patterns of cetacean brains but also to investigate the impacts of natural toxins (such as domoic acid), anthropogenic chemicals (such as polychlorinated biphenyls, polybrominated diphenyl ethers, and their hydroxylated metabolites), biological agents (parasites), and noise on the central nervous system of marine mammal species.