Developmental sequence of the chondrocranium in the obligate carnivorous larvae of Lepidobatrachus laevis (Amphibia: Ceratophryidae)

Abstract

The vertebrate head and its skull represent a significant innovation that has played a key role in the evolutionary and ecological success of vertebrates. For a global and integral understanding of the evolution of the head skeleton, it is essential to have reliable information on the development of chondrocranium in a wide range of vertebrate species. Therefore, we studied the cranial chondrogenesis of the larva of the Budgett frog, Lepidobatrachus laevis (Ceratophryidae, Neobatrachia). We studied the development using several methods, including histological preparation of transverse sections of the chondrocranium, morphological analysis of three different states of development (mesenchymal aggregation, differentiation, and chondrification), and three-dimensional digital reconstructions. As a result, we observed that the Anlage of the chondrocranium at Gosner stage 19 is laterally compressed, that is, it is initially higher than wide. It gradually flattens, enlarges, and differentiates until reaching a very wide and flat shape at Gosner stage 26. Furthermore, we show that the chondrocranial development of L. laevis takes place in a mosaic pattern, which differs to nontetrapod vertebrates in which an anterior to posterior gradient of chondrification is observed. We identified 19 developmental stages in L. laevis according to the chondrification state of its cranial structures. The first element reaching the differentiation-into-chondroblast stage is the hypobranchial plate of the branchial basket, and chondrification, that is, final differentiation, occurs simultaneously in several structures of the neurocranium and viscerocranium. We hypothesize that the rapid chondrification of L. laevis' chondrocranium is an adaptation to the semi-arid climate conditions from its type locality, El Gran Chaco in South America. Due to the only temporary availability of suitable water accumulations this apparent accelerated development would make sense to ensure the tadpoles are froglets by the time the water body disappears. Here, we provide novel information on chondrocranial development in L. laevis. We compare our results to the developmental sequences, previously known from other vertebrate taxa, particularly within the amphibian phylogeny, in an attempt to understand developmental variability and the evolutionary history of the vertebrate head skeleton.