Brain Size Evolution (marine mammals)

The study of brain size among three major living groups of marine mammals, cetaceans, pinnipeds, and sirenians, is a studv in contrasts. Phylogenetic and ecological factors have shaped the course of brain evolution in each group in distinct ways. The resulting diversity of brains provides an illustration of the different successful paths that were taken in the evolution of marine mammals.

I. The Meaning of Encephalization

Brain size evolution is embodied in the concept of encephalization, which was originally put forth as an encephalization quotient (EQ) by psychologist Harry Jerison. Jerison widely applied this measure to comparisons across different species. EQ is a measure of observed brain size relative to expected brain size derived from a regression of brain weight on body weight for a sample of species. EQ values of one, less than one, and greater than one indicate a relative brain size that is average, below average, and above average, respectively. For example, a species with an EQ of 2.0 possesses a brain twice as large as expected for an animal of its body size. The EQ values reported here are based on a large sample of living mammalian species from Jerison (1973).

In addition to the whole brain, changes in the size of various brain components have also occurred throughout marine mammal evolution and contribute to changes in the overall brain size. Some of these changes are measurable, but undoubtedly many changes in the relative size of structures occurred in all marine mammals that are not apparent from the fossil record.

II. Accessing the Fossil Record

Studies of brain size evolution in fossil marine mammals have depended on measuring the volume of the endocranial cavity in fossil specimens. Because the specific gravity of brain tissue is nearly the value of water, volumetric data have been typically converted to units of weight. In addition to the general problem of finding intact fossil crania, early studies were hampered by difficulties accessing the sediment-filled endocranium. Researchers have taken advantage of the fortuitous occurrence of intact natural endocasts but these are rare. Also, earlier studies often resulted in overestimates of brain mass from endocranial volume because they did not take into account that total endocranial volume is partly composed of non-neural, e.g., vascular, components. Cetaceans, for instance, possess a massive endocranial system of blood vessels, called the rete mirabile, that surrounds the brain and can sometimes account for nearly 20% of total endocranial volume. Most recent studies take these vascular structures into account when estimating brain size from endocranial volume. Computed tomography (CT) has proven to be an important tool in the study of fossil endocranial features because it is nondestructive and enables more accurate, precise, and reliable measurement of endocranial features than traditional methods.

III. Brain Sizes in Fossils and Modern Species

A. Brain Size Evolution in Archaeocetes

The fossil record of early cetacean brain evolution includes the transition from the immediate land ancestor of cetaceans to the extinct aquatic forms known as archaeocetes. The best candidates for the cetacean land ancestor are the Paleocene and early Eocene Mesonychia. With EQs from 0.18 to 0.51. the mesonychians were not particularly encephalized compared with modern mammals. The range of EQs estimated for early, middle, and late archaeocetes is from 0.25 to 0.49 (Table I and Fig. 1). Therefore, archaeocetes appear to have experienced little increase in encephalization above their land precursors.

B. Brain Size Evolution in Odontocetes

The suborder Odontoceti appeared during the early Oligocene and radiated rather dramatically in that epoch and into the Miocene. Despite the existence of a fair number of specimens, there is surprisingly little systematic data on brain size in fossil odontocetes. Those data that do exist suggest that by the early-mid Miocene at least several odontocete species possessed encephalization levels substantially above that of archaeocetes and within the midrange of living species (Table I and Fig. 1). These data imply that some important changes in brain size occurred during the Oligocene after the turnover from archaeocetes to early odontocetes. Unfortunately, there are no brain size data on odontocetes during the Oligocene. Data on brain size in odontocetes during the Pliocene and Pleistocene are likewise lacking.

The EQs of living odontocetes are generally on a par with nonhuman primates, but some species have achieved a level of encephalization second only to modern humans (EQ ~ 7.0) and equal to or above that of the recent hominid ancestor Homo habilis (EQ ~ 4.4). Therefore, a number of odontocetes species are significantly more encephalized than other mammals, including nonhuman primates. There is, however, a range of encephalization levels within the odontocetes. The sperm whale (Physeter inacrocephalus), with an EQ of 0.58, is an example of an odontocete species subject to disproportionate body enlargement for which the measure of EQ is not particularly meaningful. The Delphinidae, however, are the family that contains several species with exceptionally high EQs above 4.0. These include the bottlenose dolphin (Tursiops truncatus), the tucuxi (Sotalia fluviatilis), the Pacific white-sided dolphin (.Lagenorhynchus obliquidens), and the shortbeaked common dolphin (Delphinus delphis).

Odontocete brain evolution was also characterized by increased foreshortening and widening of the brain, which coincided with telescoping of the skull. There was a trend toward increased relative size of auditory processing regions, such as the acoustic cranial nerve and inferior colliculus. In living odontocetes this is evident in the larger relative size of the inferior colliculus to the analogous midbrain visual processing area, the superior colliculus. In addition, structures associated with the processing of olfactory information regressed. Furthermore, the cerebral cortex of odontocetes (and cetaceans in general) has achieved an extremely high level of gyrification. Although surface morphology is not always discernible from fossil endo-casts, it is generally thought that this was not a feature of archaeocete brains.

C. Brain Size Evolution in Mysticetes

The suborder Mysticeti appeared and diversified in the Oligocene and consisted of primitive toodied taxa in addition to the earliest baleen-bearing whales. Extant groups appeared in the mid-late Miocene. There are two problems associated with examining brain size evolution in mysticetes. First, data on fossil and living mysticete brain size are scarce. This is partly due to the difficulties associated with extracting and measuring such large brains. Second, mysticete brains tend to be smaller than expected relative to body size despite their large absolute size. This is partly due to the enormous body masses achieved by mysticetes. As in the sperm whale, mysticete bodies are greatly enlarged in ways that do not necessarily require a concomitant increase in neural tissue. EQs of living mysticetes are therefore unrepresentative of actual brain enlargement, with all values falling substantially below 1.0 (Table I and Fig. 1). For this reason, although encephalization has probably occurred throughout mysticete evolution, EQ is not an appropriate measure of it in this group, particularly in comparison widi terrestrial mammals. In fact, to the extent that disproportionate increases in body size have played a role in body enlargement in any fully aquatic species, EQ will be underestimated relative to terrestrial mammals.

Many of the changes in morphology and size of brain components that occurred in odontocetes also characterize mysticete brain evolution, but to a lesser extent. For instance, unlike in odontocetes, olfactory tracts have remained in some mysticete species and the hypertrophy of the auditory processing regions is not as extreme as in odontocetes.

D. Brain Size Evolution in Sirenia

Sirenian brain evolution has been markedly conservative regarding relative brain size. Fossil endocasts of early Eocene sirenians (among the earliest) were small in relation to the skull and already very similar to modern forms. Sirenian encephalization levels are among the lowest of modern mammals. According to the same formula used to derive cetacean encephalization quotients in cetaceans, the Florida manatee (Trichechus manatus) possesses an EQ of about 0.35 and the dugong (Dugong dugon) about 0.5. The EQ of the extinct Steller’s sea cow (Hydrodamalis gigas) was approximately 0.25 (Table I). Body size enlargement explains some of the reason for these low EQs, but, given that cetaceans of the same body size possess higher EQs, not all.

Unlike odontocetes, sirenians do possess olfactory bulbs. Perhaps the most striking contrast, however, is the fact that cetacean and sirenian brains anchor the two ends of the spectrum of cortical gyrification. Whereas the cetacean cerebral cortex is thin and highly convoluted, the sirenian cortex is unusually thick and almost lissencephalic (smooth). Interestingly, despite these differences, the relative volume of the cerebral

TABLE 1

Estimates of Brain and Body Weight and EQ for Some Fossil and Living Marine Mammal Species

“Based on a reference group of modem mammals from Jerison (1973).

!’For living species, estimated brain and body weights are averaged across several specimens in most cases-

cBody weight estimates for fossil specimens are often general estimates of adult species-specific values and are not necessarily from the same speciinen(s) for which brain weight estimates are obtained-

cortex in both sirenians and cetaceans is on a par with nonhu-man primates.

E. Brain Size Evolution in Pinnipedia

Pinnipeds diverged from terrestrial carnivores during the early Miocene. This is a relatively more recent date than cetaceans and sirenians diverged from their land ancestors. The pinniped brain, therefore, still resembles that of terrestrial carnivores. Living pinnipeds possess EQs that hover around the average for terrestrial mammals. For instance, the ringed seal (Pusa hispida) possesses an EQ of 1.75, the harbor seal (.Phoca vitulina) 2.08, and the Weddell seal (Leptonychotes weddellii) 0.76 (Table I). These values are fairly representative of pinniped EQ in general. Pinniped olfactory structures are reduced but not to the same degree as in cetaceans. The cerebral cortex is highly convoluted (and more so than most terrestrial carnivores) but lies somewhere in between the extreme degrees of gyrification and thickness found in cetaceans and sirenians. The pinniped brain is somewhat more spherical in shape than in terrestrial carnivores but did not undergo the dramatic change in overall morphology exhibited in cetaceans.

Figure 1 Pattern of change in encephalization over geological time in Mesonychia, archaeocetes, and extinct odontocetes compared with living odontocetes and mysticetes. Encephalization is plotted as EQ where the reference group is a large sample of living mammals.

IV. Conclusions

Much more information is needed before we can obtain a complete picture of patterns of brain size evolution in marine mammals. However, what does seem clear is that the different marine mammal groups evolved along distinct paths that led to a great variety of levels of encephalization in modern species. For instance, among odontocetes there was a substantial increase in encephalization in the Oligocene lineages, which has led to the existence of a number of dolphin and porpoise species with relative brain sizes challenging only the hominid mammalian line. The relationship between mass and organization must be explored further, as well as the phylogenetic and ecological factors that led to the differential development of brain size among the various marine mammal groups.