Correction to 'A key environmental driver of osteichthyan evolution and the fish-tetrapod transition?'

[This corrects the article DOI: 10.1098/rspa.2020.0355.].

Tides: A key environmental driver of osteichthyan evolution and the fish-tetrapod transition?

Tides are a major component of the interaction between the marine and terrestrial environments, and thus play an important part in shaping the environmental context for the evolution of shallow marine and coastal organisms. Here, we use a dedicated tidal model and palaeogeographic reconstructions from the Late Silurian to early Late Devonian (420 Ma, 400 Ma and 380 Ma, Ma = millions of years ago) to explore the potential significance of tides for the evolution of osteichthyans (bony fish) and tetrapods (land vertebrates). The earliest members of the osteichthyan crown-group date to the Late Silurian, approximately 425 Ma, while the earliest evidence for tetrapods is provided by trackways from the Middle Devonian, dated to approximately 393 Ma, and the oldest tetrapod body fossils are Late Devonian, approximately 373 Ma. Large tidal ranges could have fostered both the evolution of air-breathing organs in osteichthyans to facilitate breathing in oxygen-depleted tidal pools, and the development of weight-bearing tetrapod limbs to aid navigation within the intertidal zones. We find that tidal ranges over 4 m were present around areas of evolutionary significance for the origin of osteichthyans and the fish-tetrapod transition, highlighting the possible importance of tidal dynamics as a driver for these evolutionary processes.

The humerus of Eusthenopteron: a puzzling organization presaging the establishment of tetrapod limb bone marrow.

Because of its close relationship to tetrapods, Eusthenopteron is an important taxon for understanding the establishment of the tetrapod body plan. Notably, it is one of the earliest sarcopterygians in which the humerus of the pectoral fin skeleton is preserved. The microanatomical and histological organization of this humerus provides important data for understanding the evolutionary steps that built up the distinctive architecture of tetrapod limb bones. Previous histological studies showed that Eusthenopteron's long-bone organization was established through typical tetrapod ossification modalities. Based on a three-dimensional reconstruction of the inner microstructure of Eusthenopteron's humerus, obtained from propagation phase-contrast X-ray synchrotron microtomography, we are now able to show that, despite ossification mechanisms and growth patterns similar to those of tetrapods, it also retains plesiomorphic characters such as a large medullary cavity, partly resulting from the perichondral ossification around a large cartilaginous bud as in actinopterygians. It also exhibits a distinctive tubular organization of bone-marrow processes. The connection between these processes and epiphyseal structures highlights their close functional relationship, suggesting that either bone marrow played a crucial role in the long-bone elongation processes or that trabecular bone resulting from the erosion of hypertrophied cartilage created a microenvironment for haematopoietic stem cell niches.

A mathematical model for mechanotransduction at the early steps of suture formation.

Growth and patterning of craniofacial sutures is subjected to the effects of mechanical stress. Mechanotransduction processes occurring at the margins of the sutures are not precisely understood. Here, we propose a simple theoretical model based on the orientation of collagen fibres within the suture in response to local stress. We demonstrate that fibre alignment generates an instability leading to the emergence of interdigitations. We confirm the appearance of this instability both analytically and numerically. To support our model, we use histology and synchrotron X-ray microtomography and reveal the fine structure of fibres within the sutural mesenchyme and their insertion into the bone. Furthermore, using a mouse model with impaired mechanotransduction, we show that the architecture of sutures is disturbed when forces are not interpreted properly. Finally, by studying the structure of sutures in the mouse, the rat, an actinopterygian (Polypterus bichir) and a placoderm (Compagopiscis croucheri), we show that bone deposition patterns during dermal bone growth are conserved within jawed vertebrates. In total, these results support the role of mechanical constraints in the growth and patterning of craniofacial sutures, a process that was probably effective at the emergence of gnathostomes, and provide new directions for the understanding of normal and pathological suture fusion.

A uniquely specialized ear in a very early tetrapod.

The Late Devonian genus Ichthyostega was for many decades the earliest known tetrapod, and the sole representative of a transitional form between a fish and a land vertebrate. However, despite being known since 1932 (ref. 1) from a large collection of specimens, its morphology remained enigmatic and not what was expected of a very primitive tetrapod. Its apparent specializations led it to be considered as a "blind offshoot" or "sidebranch" off the tetrapod family tree, and recent cladistic analyses have disagreed about its exact phylogenetic position within the tetrapod stem group. In particular, its braincase and ear region defied interpretation, such that conventional anatomical terms seemed inapplicable. Using new material collected in 1998 (ref. 9), preparation of earlier-collected material, and high-resolution computed tomography scanning, here we identify and interpret these problematic anatomical structures. They can now be seen to form part of a highly specialized ear, probably a hearing device for use in water. This represents a structurally and functionally unique modification of the tetrapod otic region, unlike anything seen in subsequent tetrapod evolution. The presence of deeply grooved gill bars as in its contemporary Acanthostega suggest that Ichthyostega may have been more aquatically adapted than previously believed.

A primitive sarcopterygian fish with an eyestalk.

The discovery of two Early Devonian osteichthyan (bony fish) fossils has challenged established ideas about the origin of osteichthyans and their divergence into actinopterygians (teleosts and their relatives) and sarcopterygians (tetrapods, coelacanths, lungfishes and related groups). Psarolepis from China and an unnamed braincase from Australia combine derived sarcopterygian and actinopterygian characters with primitive features previously restricted to non-osteichthyans, suggesting that early osteichthyan evolution may have involved substantial parallellism between sarcopterygians and actinopterygians. But interpretation of these fossils has been hampered by poor phylogenetic resolution. Here we describe a basal sarcopterygian fish, Achoania gen, et sp. nov., that fills the morphological gap between Psarolepis and higher sarcoptergyians. We also report the presence of eyestalk attachments in both Achoania and Psarolepis, showing that this supposedly non-osteichthyan feature occurs in basal sarcopterygians as well as the actinoptergyian-like Australian braincase.

Zebrafish in context: uses of a laboratory model in comparative studies.

With the recent interest in the reintegration of evolutionary and developmental biology has come a growing need for understanding the phylogenetic relations and degree of generality of the model organisms upon which we rely so heavily. In vertebrate biology the zebrafish Danio rerio has become a paradigmatic system for studies at levels of organization from molecular to interspecific. Studies of model systems in development are often techniques-driven rather than questions-based; however, informative hypotheses for developmental research can be derived from phylogenetic distributions of characters. With some understanding of how general the characters of interest are, a thoughtful comparison of the requirements of the questions with the lists of available embryos, reagents, and protocols can guide choices of new vertebrate models. We describe here the phylogenetic placement of zebrafish within the vertebrate world and discuss how generally observations on zebrafish can be taken to apply. We outline a practical protocol for investigating development in a comparative context, illustrated with an example from an ongoing study of teleost tail fin evolution. The principles and procedures presented here apply equally well to any comparative study with an interest in evolution, at any level of phylogeny from intraspecific studies to comparisons across phyla.