Ontogenetic Shifts in Brain Size and Brain Organization of the Atlantic Sharpnose Shark, <b><i>Rhizoprionodon terraenovae</i></b>

Abstract

Throughout an animal’s life, species may occupy different environments and exhibit distinct life stages, known as ontogenetic shifts. The life histories of most sharks (class: Chondrichthyes) are characterized by these ontogenetic shifts, which can be defined by changes in habitat and diet as well as behavioral changes at the onset of sexual maturity. In addition, fishes experience indeterminate growth, whereby the brain and body grow throughout the organism’s life. Despite a presupposed lifelong neurogenesis in sharks, very little work has been done on ontogenetic changes in the brain, which may be informative about functional shifts in sensory and behavioral specializations. This study quantified changes in brain-body scaling and the scaling of six major brain regions (olfactory bulbs, telencephalon, diencephalon, optic tectum, cerebellum, and medulla oblongata) throughout ontogeny in the Atlantic sharpnose shark, &lt;i&gt;Rhizoprio­nodon terraenovae&lt;/i&gt;. As documented in other fishes, brain size increased significantly with body mass throughout ontogeny in this species, with the steepest period of growth in early life. The telencephalon, diencephalon, optic tectum, and medulla oblongata scaled with negative allometry against the rest of the brain throughout ontogeny. However, notably, the olfactory bulbs and cerebellum scaled hyperallometrically to the rest of the brain, whereby these structures enlarged disproportionately as this species matured. Changes in the relative size of the olfactory bulbs throughout ontogeny may reflect an increased reliance on olfaction at later life history stages in &lt;i&gt;R. terraenovae&lt;/i&gt;, while changes in the relative size of the cerebellum throughout ontogeny may be indicative of the ability to capture faster prey or an increase in migratory nature as this species moves to offshore habitats, associated with the onset of sexual maturity.

Gill surface area provides a clue for the respiratory basis of brain size in the blacktip shark (Carcharhinus limbatus)

“…Since fishes (like other ectothermic vertebrates) grow indeterminately, their brains may exhibit lifelong neurogenesis and brain growth to match the neural demands of the body (Leonard et al ., 1978; Ngwenya et al ., 2013; Zupanc, 2006). For example, our estimate of the brain mass allometric slope was similar to those reported in various other intraspecific studies of fishes, which reported slopes of 0.48–0.57 (Bauchot et al ., 1976) and 0.5 (95% CI 0.46–0.54; Gonda et al ., 2011) for bony fishes and 0.427 (95% CI 0.374–0.480; Lisney et al ., 2017) and 0.46 (95% CI 0.43–0.49; Laforest et al ., 2020) for cartilaginous fishes. Our slope estimate was also similar to evolutionary allometric slopes across cartilaginous fishes broadly (slope = 0.43; Yopak et al ., 2019) and Carcharhiniformes specifically, where brain mass changes with body mass with a slope of 0.52 (Myagkov, 1991).…”

“…Using gill surface area as a proxy for oxygen consumption and energetic demand on evolutionary time scales, we found that C. limbatus individuals with a large gill surface area for their body mass may be able to support a higher energetic turnover and, in turn, a larger brain for their body mass. However, brain size is highly variable at large body sizes in cartilaginous fishes (Laforest et al ., 2020). Thus, although our results suggest that individuals with a large brain for a given body mass may also have a large gill surface area, more data is needed spanning the full range of body sizes in C. limbatus .…”

“…In addition to exhibiting lifelong neurogenesis, fishes grow throughout their lives ( i.e ., indeterminately), with both brain mass and gill surface area changing with body mass throughout ontogeny (Bigman et al ., 2018; Laforest et al ., 2020). Therefore, both brain mass and gill surface area must be studied in an allometric context and any comparison between brain mass and gill surface area throughout ontogeny must also account for body mass (Bigman et al ., 2018; Laforest et al ., 2020; Lisney et al ., 2017).…”

“…In addition to exhibiting lifelong neurogenesis, fishes grow throughout their lives ( i.e ., indeterminately), with both brain mass and gill surface area changing with body mass throughout ontogeny (Bigman et al ., 2018; Laforest et al ., 2020). Therefore, both brain mass and gill surface area must be studied in an allometric context and any comparison between brain mass and gill surface area throughout ontogeny must also account for body mass (Bigman et al ., 2018; Laforest et al ., 2020; Lisney et al ., 2017). Although explanations for the rate at which brain mass changes with body mass ( i.e ., the allometric slope for brain mass) within a species and across ontogeny are rare, some explanations have been proposed for allometric slopes across species ( i.e ., evolutionary allometries).…”

“…Third, chondrichthyans occupy a basal position on the evolutionary tree of jawed vertebrates ( i.e ., gnathostomes) and are the first group to exhibit the fundamental and highly homologous vertebrate brain plan (Yopak, 2012). However, despite their basal place in vertebrate evolution, chondrichthyan brains have been poorly studied in comparison to other vertebrate groups, with brain mass data only available for about 16% of all currently described chondrichthyan species (Yopak, 2012), and even less is understood about intraspecific variation in brain size in this group (Laforest et al ., 2020; Lisney et al ., 2007, 2017). For these reasons, we chose to study the blacktip shark Carcharhinus limbatus (Valenciennes 1839) from the western Atlantic Ocean.…”