Placoid scales in bioluminescent sharks: Scaling their evolution using morphology and elemental composition

Abstract

Elasmobranchs are characterised by the presence of placoid scales on their skin. These scales, structurally homologous to gnathostome teeth, are thought to have various ecological functions related to drag reduction, predator defense or abrasion reduction. Some scales, particularly those present in the ventral area, are also thought to be functionally involved in the transmission of bioluminescent light in deep-sea environments. In the deep parts of the oceans, elasmobranchs are mainly represented by squaliform sharks. This study compares ventral placoid scale morphology and elemental composition of more than thirty deep-sea squaliform species. Scanning Electron Microscopy and Energy Dispersive X-ray spectrometry, associated with morphometric and elemental composition measurements were used to characterise differences among species. A maximum likelihood molecular phylogeny was computed for 43 shark species incuding all known families of Squaliformes. Character mapping was based on this phylogeny to estimate ancestral character states among the squaliform lineages. Our results highlight a conserved and stereotypical elemental composition of the external layer among the examined species. Phosphorus-calcium proportion ratios (Ca/P) slightly vary from 1.8-1.9, and fluorine is typically found in the placoid scale. By contrast, there is striking variation in shape in ventral placoid scales among the investigated families. Character-mapping reconstructions indicated that the shield-shaped placoid scale morphotype is likely to be ancestral among squaliform taxa. The skin surface occupied by scales appears to be reduced in luminous clades which reflects a relationship between scale coverage and the ability to emit light. In luminous species, the placoid scale morphotypes are restricted to pavement, bristle-and spine-shaped except for the only luminescent somniosid, Zameus squamulosus, and the dalatiid Mollisquama mississippiensis. These results, deriving from an unprecedented sampling, show extensive morphological diversity in placoid scale shape but little variation in elemental composition among Squaliformes.

Illuminating the evolution of bioluminescence in sharks

“…Evolutionary, ecological and functional inferences on the last common ancestor of bioluminescent sharks might be benefited from future analyses incorporating information relative to their squamation patterns (Ferrón & Botella 2017; Lourtie et al . 2022) and physiology (Claes & Mallefet 2009 b ; Duchatelet et al . 2021 b ).…”

“…2021; Lourtie et al . 2022), embryology and ontogeny (Claes & Mallefet 2008, 2009 c ; Duchatelet et al . 2019 c ; Van den Bossche 2020) and function in living forms (Reif 1985; Munk & Jørgensen 1988; Widder 1998; Claes & Mallefet 2009 b ; Claes et al .…”

Photophore Morphogenesis and Extraocular Encephalopsin Expression during the Embryogenesis of Smalleye Pygmy Shark (Squaliolus aliae)

“…Little information is available on the scale development in luminous sharks, which does not allow a comparison between the different luminous shark families (i.e., Dalatiidae, Etmopteridae, and Somniosidae). Across the deep-sea species, dalatiid and etmopterid species have been shown to display a low placoid scale coverage (i.e., less than 40% of the skin) [37]. The scale shape of dalatiids (pavement-shaped) and etmopterids (pavement-, spine-, bristle-shaped) regarding scale densities and space between scales would then allow a higher luminescence propagation than other covering and tight scale shapes, such as shield-shaped scales [37,41].…”

“…Across the deep-sea species, dalatiid and etmopterid species have been shown to display a low placoid scale coverage (i.e., less than 40% of the skin) [37]. The scale shape of dalatiids (pavement-shaped) and etmopterids (pavement-, spine-, bristle-shaped) regarding scale densities and space between scales would then allow a higher luminescence propagation than other covering and tight scale shapes, such as shield-shaped scales [37,41]. The hypothesis of a space trade-off was suggested, reducing the putative defense or hydrodynamic scale function to allow a better light emission [19,37,41].…”

“…Both photophore types are less complex than Etmopterus spinax, displaying a unique photocyte, embedded between pigmented cells and surmounted by lens cells [19,[32][33][34][35][36], and a less dense ILS is also present. Somniosidae present atypical bioluminescent squamation with overlapping honeycomb placoid scales translucent to light, while dalatiids generally have pavement-shape placoid scales [19,37].…”