Extreme evolutionary shifts in developmental timing establish the miniature Danionella as a novel model in the neurosciences

Abstract

Background: Species of Danionella rank among the smallest of all vertebrates and their miniature size is correlated with an extreme case of progenesis, resulting in tiny, transparent sexually mature individuals. Progenesis has affected the entire skeleton of Danionella, in which 60 skeletal elements are absent, including some of the skull roofing bones. This lack of a skull roof combined with the presence of a fully formed hearing and sound producing apparatus has led to Danionella being used as an important model for neurophysiological studies. Results: Using both rank based and PGi analyses we investigate sequence heterochrony in the development of the skeleton of Danionella dracula and close relatives. Extreme heterochronic shifts affect the appearance of bony elements in Danionella dracula. This includes a delay in the appearance of most chondral skull bones, and a reduction or loss of dermal bones that would otherwise form the skull roof. In contrast, formation of the anterior region of the vertebral column, including the functionally important elements of the Weberian apparatus, is greatly accelerated. Conclusions: Here we show that the anatomical conditions that favor Danionella for brain research are the result of extreme heterochronic shifts that have acted differentially across the skeleton.

Whole-brain optical access in small adult vertebrates with two- and three-photon microscopy

“…A prior anatomical study enabled us to clearly identify the bone at the bottom of the brain in the SHG channel (Fig. 4) [24]. To compare the performance of 2PM and 3PM, we collected images through the entire depth of the brain.…”

“…Smaller adult vertebrates with translucent young including zebrafish (Danio rerio) and the smaller relatives of zebrafish, Danionella, offer the prospect of imaging throughout the brain of a vertebrate as well as throughout life [19,20,22,23]. Danionella dracula adults, studied here, reach approximately 11 to 18 mm in length and have a transparent body with a poorly ossified skull above the brain [24,25]. Like other Danionella species, they produce sounds during social interactions making them especially promising for identifying neural mechanisms underlying adult vertebrate reproductive behavior [25].…”

Evolutionary divergence of locomotion in two related vertebrate species

“…However, studies on ossification in Danionella sp. demonstrate that most bones affected by truncation are formed later in the development of ZF 5,6 . Hence, in the early stages of their development, DT and ZF are highly comparable.…”

The emerging vertebrate model species for neurophysiological studies is Danionella cerebrum, new species (Teleostei: Cyprinidae)

“…The five species of Danionella are textbook examples for the link between miniaturization via developmental truncation and evolutionary morphological novelty, as proposed by Hanken and Wake 2 and discussed in detail for this genus by Rüber et al 17 and Britz and Conway 9 . Specifically for Danionella , Conway et al 10 have shown that it is the dramatic disparity in heterochronic shifts between different parts of the skeleton that has resulted in a vertebrate with an open, larval skull roof, but a fully developed Weberian apparatus. Both features render species of Danionella ideal candidates as neurophysiological model organisms.…”

“…So far, four species of the genus Danionella , maturing at sizes of 10–15 mm in length and including some of the smallest fishes and vertebrates, have been described from Myanmar and northeastern India 3 – 6 . Though progenesis may act at the level of an individual character or character complex, leading to a mosaic of paedomorphic features in the adult, Danionella is unusual in that it shows organism–wide progenesis or developmental truncation, a heterochronic change that leads to tiny adult organisms with an overall larval appearance 7 – 10 .…”