On the sequence heterochrony of cranial ossification of bats in light of Haeckel's recapitulation theory

Abstract

Haeckel's recapitulation theory has been a controversial topic in evolutionary biology. However, we have seen some recent cases applying Haeckel's view to interpret the interspecific variation of prenatal ontogeny. To revisit the validity of Haeckel's recapitulation theory, we take bats that have undergone drastic morphological changes and possess a characteristic ecology as a case study. All members of Rhinolophoidea and Yangochiroptera can generate an ultrasonic pulse from the larynx to interpret surrounding objects (laryngeal echolocation) whereas Pteropodidae lacks such ability. It is known that the petrosal bone is particularly derived in shape and expanded in laryngeal echolocators. If Haeckel's recapitulation theory holds, the formation of this derived trait should occur later than those of other bones. Therefore, we compared the prenatal ossification timing of the petrosal in 15 bat species and five outgroup species. We found that the ossification of the petrosal is accelerated in laryngeal echolocators while it is the last bone to ossify in non‐laryngeal echolocating bats and non‐volant mammals, which runs counter to the prediction generated by Haeckel's recapitulation theory. We point out the evolutionarily labile nature of trait developmental timing and emphasize that Haeckel's recapitulation theory does not hold in many cases. We caution that generating predictions on ancestral conditions and evolutionary history leading from Haeckel's recapitulation theory is not well supported.

Evolution, conservatism and overlooked homologies of the mammalian skull

“…In mammals, ossification sequences can be determined by studying various stages of prenatal and perinatal samples using whole-mount clearing-and-staining, histological sections, and microCT imaging. A growing body of evidence indicates that the ossification sequence is highly speciesspecific and variable among species [77,[90][91][92][93]. Evolutionary changes in ossification timing have been frequently linked to the changes in life history awaiting the newborn [94,95].…”

“…However, the functional significance of ossification heterochrony is largely unstudied, despite the considerable interspecific diversity of the ossification sequence reported to date [96]. Some studies have linked ossification heterochrony to evolutionary changes in relative bone sizes [96][97][98], but many High interspecific variation in ossification heterochrony is known for the mammalian skull [77,92,93,98,103,104]. Although the evolutionary drivers of this diversity are still largely unexplained, Koyabu et al [77] contended that the ossification timing of the skull roof bones may be related to brain size evolution.…”

“…High interspecific variation in ossification heterochrony is known for the mammalian skull [77,92,93,98,103,104]. Although the evolutionary drivers of this diversity are still largely unexplained, Koyabu et al [77] contended that the ossification timing of the skull roof bones may be related to brain size evolution.…”

Beyond recapitulation: Past, present, and future

“…On the other hand, the evidence against the recapitulative tendency has also been provided. Taking bats' skulls as an example, Nojiri et al (2021) examined the temporal sequence of ossification and showed that the order did not follow the recapitulative tendency. Notably, in this paper, they caution on the danger of assuming that ancestral features are observed at earlier developmental stages when compared with more derived features.…”

Morphological association between muscle attachments and ossification sites in the late cartilaginous skull of tuatara embryos

“…Ossification studies in vertebrate embryology mainly concentrate on deciphering the timing of onset of ossification (Arendt & Wilson, 2000; Koyabu et al, 2014; Nojiri et al, 2018; Nojiri, Tu, et al, 2021; Nojiri, Wilson, et al, 2021; Ollonen et al, 2018; Spiekman & Werneburg, 2017; Weisbecker & Nilsson, 2008; Werneburg & Sánchez‐Villagra, 2015). This causes a bias in explaining specific phenomena.…”