Growth trajectories of prenatal embryos of the deep‐sea shark Chlamydoselachus anguineus (Chondrichthyes)

Abstract

Chlamydoselachus anguineus, Garman 1884, commonly called the frilled shark, is a deep-sea shark species occurring up to depths of 1300 m. It is assumed to represent an ancient morphotype of sharks (e.g., terminal mouth opening, more than five gill slits) and thus is often considered to represent plesiomorphic traits for sharks. Therefore, its early ontogenetic developmental traits are important for understanding the evolution of its particular phenotype. Here, we established six stages for prenatal embryos and used linear measurements and geometric morphometrics to analyse changes in shape and size as well as their timing during different embryonic stages. Our results show a change in head shape and a relocation of the mouth opening at a late stage of development. We also detected a negative allometric growth of the head and especially the eye compared to the rest of the body and a sexual dimorphism in total body length, which differs from the known data for adults. A multivariate analysis of covariance shows a significant interaction of shape related to the logarithm of centroid size and developmental stage. Geometric morphometrics results indicate that the head shape changes as a covariate of body size while not accounting for differences between sexes. The growth pattern of stages 32 and 33 indicates a shift in head shape, thus highlighting the moment in development when the jaws start to elongate anteriorly to finally achieve the adult condition of terminal mouth opening rather than retaining the early embryonic subterminal position as is typical for sharks. Thus, the antero-terminal mouth opening of the frilled shark has to be considered a derived feature.

Early shape divergence of developmental trajectories in the jaw of galeomorph sharks

“…This suggests that underlying differences between both species are strongly established probably from very early in their development. By observing the embryonic development among elasmobranchs, the external morphology is similar up to specific stages, when divergent features (e.g., pectoral fin expansion in batoids) become more noticeable [ 37 , 44 , 52 – 55 ]. Differences in developmental timing and trajectories contribute to establish the marked morphological features of the lower jaw in the bamboo shark and catshark.…”

Insights into ontogenetic scaling and morphological variation in sharks from near-term brown smooth-hound (Mustelus henlei) embryos

“…One potential limitation that has not yet been addressed in the literature is that existing ecomorphological studies of scaling in elasmobranchs focus predominantly on postnatal ontogeny, despite the evolutionary and ecological significance of morphological changes occurring during prenatal ontogeny. Those studies that do address embryogenic scaling focus on developing staging tables without much focus on the ecomorphology of scaling itself (Tomita et al, 2018; López-Romero et al, 2020; Byrum et al, 2023). They may, as in other ontogenetic stages (Gayford et al, 2023b) act to maximise fitness in the context of the trophic and spatial ecology of this taxon post-partum.…”

Embryonic development in the bonnethead (Sphyrna tiburo), a viviparous hammerhead shark

“…including the small-spotted catshark Scyliorhinus canicula, 15,16 the winter skate Leucoraja ocellata, 17 the little skate Leucoraja erinacea, 18 the Atlantic sharpnose Rhizoprionodon terraenovae, 19 the brownbanded bamboo shark Chiloscyllium punctata, 20 and the frilled shark Chlamydoselachus anguineus. 21 Such work has been particularly valuable for the catshark and little skate, which have become popular models in experimental biology, in part because their eggs can be easily produced, collected, maintained, and observed in captivity, 18,22,23 making them widely used in multiple studies. Developmental staging series allows for the identification of emerging features for experimentation and provide a comparative reference for other published work.…”

“…While aspects of elasmobranch development have long been of interest, 13,14 publications featuring developmental staging series tracking the growth of elasmobranchs have only appeared in the past 30 years. including the small‐spotted catshark S cyliorhinus canicula , 15,16 the winter skate Leucoraja ocellata , 17 the little skate Leucoraja erinacea , 18 the Atlantic sharpnose Rhizoprionodon terraenovae , 19 the brownbanded bamboo shark Chiloscyllium punctata , 20 and the frilled shark Chlamydoselachus anguineus 21 . Such work has been particularly valuable for the catshark and little skate, which have become popular models in experimental biology, in part because their eggs can be easily produced, collected, maintained, and observed in captivity, 18,22,23 making them widely used in multiple studies.…”