Brain size and brain morphology may provide insights into shark behavior, particularly in species that are often difficult to study behaviorally due to their rarity and/or the extreme habitat in which they live. Of high ecological importance, the Greenland (Somniosus microcephalus) and Pacific sleeper (S. pacificus) sharks are the only non-lamnid shark species found in the Arctic, with a high prevalence of pinnipeds as a key component of their diet. In this study, the brain of these two unique species was examined as a way of predicting the relative importance of different sensory modalities. These sharks have a reduction in overall brain size and a marked reduction in the size of brain regions associated with higher cognitive functions, such as spatial learning and memory (e.g. the telencephalon77). They also possess relative reductions of the regions that receive the majority of afferents arising from the retinal ganglion cells (optic tectum) and one of the largest olfactory bulbs of any species described to date (comprising >30% of the brain), suggestive of a more olfactory-mediated, rather than a visually-mediated lifestyle.

As proposed by Jerison11, selection for larger brains (and/or enlargement of a particular brain region) are predicted to afford a functional advantage. However, little experimental evidence exists to empirically demonstrate this12,78,79. Thus, comparative studies of brain size and brain organization make the key assumption that there are correlations between brain regions and the functions or behaviors those regions modulate. However, correlatory evidence does not necessary reflect a causal relationship. It is important to note that this study is not a functional analysis; rather, it represents an attempt to use patterns of brain organization as a framework for exploring the relative importance of different sensory systems in poorly understood shark species. The extent to which morphological variation in the brain can directly confer differences in functional performance is of critical importance, but requires further study.

Within the cartilaginous fishes examined to date, S. microcephalus had a smaller than expected brain for its large body size (R br = −1.54; Fig. 3). The only other published account of brain size in S. microcephalus documented a specimen of 280 kg body mass that had a brain size of 10.29g71, which is in line with allometric expectations for the S. microcephalus specimens examined in this study. A relatively small brain is a common characteristic for other deep-sea shark species10, including other members of Somniosidae (Fig. 3B). As brain tissue is energetically costly, a relatively small brain may reflect its lower metabolic rate80,81.

Although the degree to which brain size reflects enhanced cognitive capabilities continues to be highly contentious82,83, it is a common suggestion that encephalization informs behavioral complexity to some degree84. Of the few studies to date to explore a direct link between brain size and a cognitive task, guppies (Poecilia reticulata) selected for a 10% increase in brain size outperform smaller-brained individuals in cognitive learning tasks, which suggests a larger brain confers some cognitive advantages12,79, with tradeoffs between these cognitive benefits and energetic costs80. Although not empirically shown, reductions in brain size in cartilaginous fishes have been attributed to a number of factors, including more opportunistic, passive predation strategies85,86, a close association with the substrate30,75, and lower activity levels (reviewed in3). These behaviors have been suggested to lend themselves to sensory and motor requirements that are likely less cognitively demanding, as compared to agile hunters that occupy more spatially complex habitats, such as coral reefs26,27,30. Across other vertebrate groups, species with larger brains similarly tend to exhibit behavioral innovations in the form of increased sociality, complex learning, tool use, and foraging ecology, than do animals with small brainse.g.17,21,78,87,88.

In addition to a low degree of encephalization, the brain of S. microcephalus occupies only a small proportion of available endocranial space. A relatively small brain is a common attribute of many mature large-bodied shark species, such as Carcharodon carcharias, Rhincodon typus, and Cetorhinus maximus30,86,89, with a correspondingly small brain-to-endocranial-volume ratio86,89,90,91. The low levels of encephalization in large-bodied sharks may reflect an evolutionary increase in body growth without a concurrent increase in brain size, as opposed to an absolute reduction in brain size (termed “gigantism”84). However, small brains housed within expansive crania are not a consistent characteristic across all large-bodied cartilaginous fishes. Some of the most encephalized species, such as the great hammerhead, Sphyrna mokarran30 and mobulid rays3,74, can grow up to body sizes of 6 m in total length (Sphyrna)43 or >7 m in disc width (Manta birostris92) and possess brains that are either tightly housed in the chondrocranium (Sphyrna; Yopak, pers. obs) or are situated within an expansive cranial cavity (Manta74).

Encephalization is also correlated with a high degree of maternal investment in cartilaginous fishes, which exhibit the most diverse array of reproductive strategies of any vertebrate group93. These strategies range from egg-laying (lecithotrophy), with no investment beyond the yolk sac, to live-bearing (matrotrophy), where the developing embryo receives additional provisioning from the mother. Matrotrophic cartilaginous fishes have brains that are 20–70% larger than lecithotrophic species28, where the increased provisioning from the mother may provide a developing embryo with a cognitive advantage at birth. Although our knowledge of reproduction in Somniosus spp is limited, they are known to produce a high number of follicles52,94, although litter sizes are relatively low in both species examined here, with approximately 8–10 pups per litter44. S. microcephalus and S. pacificus are believed to be lecithotrophic live-bearers46,52, where embryos are nourished via a yolk-sac and pups are live19. This low reproductive output and lack of additional provisioning from mother to offspring may explain the low degree of encephalization in Somniosus, but more work is required on the reproductive biology of these sharks.

Unlike S. microcephalus, the brain of the S. pacificus examined in this study is relatively large in comparison to other somniosids and oxynotids and average-sized in comparison to all cartilaginous fishes examined (R br = 1.86; Fig. 3). Although maturity was not assessed directly in S. pacificus, its body size (1.38 m TL; 25.6 kg) suggests this animal was a juvenile, as documented studies on the reproductive organs assert that S. pacificus matures at 3.65 m TL52. Cartilaginous fishes (as well as jawless and bony fishes, some amphibians and reptiles) experience indeterminate growth95. As such, their brains continue to grow throughout their lifespan, unlike other vertebrates that experience very little adult neurogenesis96. Although the brain grows through adulthood, the steepest period of growth is often during the early juvenile stages97,98, as seen in some jawless99 and bony fishes100,101 and reptiles102. Since the brain from an adult specimen of S. pacificus was not available for this study for comparison, the degree of encephalization documented in this study for S. pacificus may not be representative of the adult condition.

If natural selection is acting on a particular behavior or sensory characteristic of a species, there may be selective pressures similarly acting on the neural substratum that modulates that modality15,16. Previous studies on other members of Somniosidae have shown that they possess relatively small brains, with small telencephalons, small, smooth cerebellums10,30, and relatively large olfactory bulbs29 and medullas10,70. Like other somniosids, both S. microcephalus and S. pacificus possess a relatively small telencephalon and a relatively large medulla, which occupies between 17% (S. microcephalus) and 15% (S. pacificus) of the brain. S. microcephalus and S. pacificus have among the smallest telencephalons of any species described to date, including other deep-sea sharks and chimaerids10.

The telencephalon is implicated in multimodal sensory integration, complex behavioral control75,103,104, and higher cognitive functions, including allocentric place learning, avoidance learning, and long term memory77,105,106,107, as in teleosts108. In cartilaginous fishes, the telencephalon can comprise from 15–20% of the brain (e.g. in Harriotta raleighana and Deania calcea10) up to as much as 67% of the brain in Sphryna mokarran30. Given this variability, it has been proposed that telencephalon size may be indicative of behavioral complexity, whereby enlargement of this region is documented in shark species with increased sociality, strategic hunting, and navigating in spatially complex habitats3,10,27,30,74. The telencephalon is also one of the few brain regions to scale with positive allometry with brain size (Fig. 4E), such that larger brains become disproportionately composed of this structure, as similarly documented in mammals26. Functionally, lesions to various regions of the telencephalon, specifically the pallium, in some shark species have been shown to impair different types of learning105,106,107, which supports the assertion that the size of this structure likely reflects spatial learning and memory capabilities77. A small telencephalon in Somniosus is in line with phylogenetic expectations for this group and is also consistent with relative reduction of this structure in solitary species that do not dwell in spatially complex habitats30.

Olfaction is a critical sense in the aquatic realm and the detection of dissolved odorants is believed to mediate tasks ranging from predator avoidance, prey detection, and chemosensory communication with conspecifics (reviewed in2,109). Histological analysis of the peripheral system supports a well-developed olfactory capability in S. microcephalus, with a relatively high lamellar surface area and a high rate of renewal of olfactory receptor neurons (ORNs) in the olfactory epithelium72,73. The olfactory bulbs (OBs) receive primary projections from the ORNs and are associated with processing olfactory information33,38. Given the important role of olfaction in feeding, whereby many species follow odor plumes to their prey1,2, there may be selection pressures on the olfactory system for some species in this context. Both S. microcephalus and S. pacificus possess relatively large OBs (Fig. 1A,B), comprising 33% and 31% of the brain, respectively. In particular, compared across a range of other cartilaginous fishes, the OBs of S. microcephalus are among the largest of any species described to date (R OB = 2.96), rivalled only by the tiger shark, Galeocerdo cuvier (R OB = 4.89) and white shark, Carcharodon carcharias (R OB = 3.50) (Fig. 4B), both large-bodied, highly migratory predators. The OBs can vary considerably in size and morphology across species29,110 and show a high degree of statistical independence from the rest of the brain26,29, a pattern also documented across other species, including bony fishes, amphibians, birds and mammals26,111,112,113. Correlations between OB variability and ecology has been widely used to confer olfactory capability in vertebrates114,115,116, although uncertainties exist regarding whether peripheral and central organization reflects functional specialization in cartilaginous fishes38. Variation in OB size may not be indicative of functional variability, and instead may reflect a tighter coupling between other, more highly-interconnected, regions of the brain117.

Previous work has shown relatively large OBs in shark species living in conditions where the use of visual information is in some way compromised, such as the deep-sea, or in species (e.g. G. cuvier and C. carcharias) that may follow chemosensory cues over long distances to locate cetacean carcasses29,97,118. Like G. cuvier and C. carcharias, S. microcephalus and S. pacificus also have a high prevalence of marine mammals in their diet50,52,61,62,65. Pinnipeds can create considerable odoriferous material and the resultant odor trails can likely be tracked over considerable distances by large marine predators119,120. In this context, a well-developed olfactory system would be evolutionarily advantageous in the Greenland and Pacific sleeper sharks, who may be relying on chemoreceptive cues to prey on pinnipeds.

In addition to foraging and locating conspecifics, olfaction has been proposed to play a role in linking locations in olfactory space for both short and long-distance navigation121. Accordingly, Jacobs121 proposes OB size should co-vary with navigational demand29, supported by enlarged OBs documented in migratory birds122, bats with enlarged wingspans18, and mammals with large home ranges123. Although there is not a large enough dataset to test this hypothesis directly in sharks29, the largest OBs are, in fact, found in highly migratory sharks, including G. cuvier and C. carcharias (Fig. 4). Similarly, both S. microcephalus and S. pacificus occupy a broad depth niche from the surface down to 2200 m, and can make daily vertical migrations, in addition to long-range latitudinal movements48,49,58,124. Should a function of the olfactory system be to map patterns of odorants in olfactory space, a correspondingly large OB might support this behavior in somniosids.

The optic tectum in S. microcephalus and S. pacificus is notably reduced, and occupies ~2.5% of the brain; this relative reduction in tectum size is characteristic for deep-sea dwelling somniosids (Fig. 4H). The superficial layers of the optic tectum receive the majority of primary projections arising from the retinal ganglion cells and are associated with visual processing125,126,127, in addition to receiving projections from other sensory modalities128. Despite its role as a multimodal integration center, variability in the size of the optic tectum is suggested to reflect visual specialization in non-mammalian species8,69,88 and often scales with a number of other aspects of the peripheral nervous system in fishes, including eye size, retinal area, the number of retinal ganglion cells and optic nerve axons, and overall retinal area88,129,130. In addition to living in low-light environments, among the most distinctive characteristic of S. microcephalus and S. pacificus is the presence of ocular lesions, generated by the large ectoparasitic copepod Ommatokoita elongata, which attaches to the cornea54,55,56. This parasite has a very high rate of occurrence in the Arctic sleeper sharks; it is documented in the majority of specimens of S. microcephalus caught in East Greenland, Baffin Island58, Cumberland Sound, and Svalbard, Norway46. Histological assessment of the attachment of these parasites (and subsequent larval deposition and/or infection) shows corneal lacerations, damage, and visual impairment54,56. Although whether O. elongata fully blinds its host is uncertain, these animals may only be capable of light/dark discrimination56. Despite the potential visual impairment caused by O. elongata and a relatively small eye131, Somniosus spp. clearly remain capable of capturing active prey, including pinnipeds62,68. Previous work has proposed these sharks depend primarily on chemoreception to find prey from a distance and only use motion detection and visual cues at close range56. Patterns of brain morphology in S. microcephalus and S. pacificus, with relatively large olfactory bulbs and relatively reduced optic tectums, similarly support an olfactory-mediated rather than a visually-mediated lifestyle. However, experimental evidence on both the visual and olfactory system is required to confirm this.

Cerebellar development in S. microcephalus and S. pacificus is noteworthy. Although the function of the cerebellum has been an area of considerable speculation throughout gnathostomes132, it is generally agreed that the cerebellum regulates motor control and motor learning133. Morphologically, the corpus cerebellum varies substantially in size, level of convolution (a.k.a. foliation) and symmetry in cartilaginous fishes27,30,74,134,135,136, and it has been suggested that this may reflect performance differences in cerebellar-dependent functions and behaviors132. Both S. microcephalus and S. pacificus possess a relatively small, smooth corpus, with low levels of cerebellar foliation - a pattern consistent with that previously described for squalomorph sharks30,75. In contrast, high levels of foliation have been documented in active, agile predators, such as C. carcharias30, species with extreme motor specializations, such as Alopias spp., which uses a rapid strike of the upper lobe of the caudal fin30,118, or large-bodied species that make long-distance migrations, such as R. typus and C. maximus86,89. In contrast, low levels of foliation are common in small, benthic species that rest on the seafloor or benthopelagic species that inhabit the deep-sea, suggestive of lower activity levels10,30. Foliation has been proposed to be an identifying feature of highly encephalized brains26 and that species with larger, more complex cerebella might have the ability to perform more multi-faceted motor tasks than their close relatives lacking these convolutions137. Although the exact mechanism for this characteristic is unknown in sharks, cerebellar foliation likely allows for an increased cerebellar surface area, while reducing the length of neuronal connections26, which may provide an energetically efficient means of coordinating larger body sizes or may serve to improve motor agility at the central level.

To our knowledge, Somniosus spp. are the only large-bodied (>3 m TL) shark species examined to date that have a smooth cerebellar corpus. An increase in foliation is correlated with an increase in cerebellum size, brain size, and body size (Table S3) across this group, where S. microcephalus, in particular, showed a marked deviation from expectation (Fig. 5). The lack of cerebellar complexity may reflect a reduction in fine-tuned motor behavior26,30, as Greenland sharks exhibit the slowest swimming speed for their body size compared to other representative cartilaginous fishes59. Tail beat frequency data also suggests a sluggish cruising speed of between 0.22 and 0.34 m/s58,59 and a maximum speed of 0.74 m/s59 for S. microcephalus, which is much slower than those estimated for species such as C. carcharias120,138 and G. cuvier139,140. Importantly, acceleration during burst swimming speeds for S. microcephalus (0.008 m/s2) are much lower than those recorded in pinnipeds59, which makes this species unlikely to achieve the high swimming speeds necessary for active pursuit of seals.

Ferrando et al.72,73 have proposed that S. microcephalus has well-developed olfactory capabilities and might rely heavily on chemoreception during foraging, which would include predating on marine mammals. Although it has been considered whether seals are being fed upon as carrion, characteristic corkscrew wounds found on living or deceased stranded animals suggest these pinnipeds are still being bitten while alive in the water52,61,62,65. Whole, intact small seals that appeared to be healthy at the time of ingestion also support the assertion that the seals were taken live65. Previous studies speculated that S. microcephalus may actively feed at ice holes (e.g. on over wintering Delphinapterus leucas46) and could be attracted to seal ice holes via a suite of olfactory, acoustic and visual cues, possibly using stealth and camouflage to approach and capture seals at the surface58. Other research suggest that Somniosus sp. may ambush sleeping seals59,68. Arctic seals often sleep in water, either underwater or at the surface141,142. It has been hypothesized that this sleeping behavior allows them to avoid predation by polar bears (Ursus maritimus) that feed on seals primarily on the sea ice59,68. However, unlike cetaceans or otariids, who employ unique unihemispheric sleep patterns as a means to remain active while one half of the brain is in a sleeping state143,144, phocid seals exhibit bilaterally symmetrical (bihemispheric) sleep patterns, characteristic of terrestrial mammals141. Although protected from being hunted on the ice by U. maritimus, an immobilized state during sleep, may leave Arctic seals vulnerable to cryptic predators in the water, including Somniosus.