Evolution of median fin patterning and modularity in living and fossil osteichthyans

PLOS ONE RESEARCH ARTICLE Evolution of median fin patterning and modularity in living and fossil osteichthyans France Charest ID1,2☯*, Jorge Mondéjar Fernández3,4☯, Thomas Grünbaum1, Richard Cloutier1☯ 1 Département de Biologie, Chimie et Géographie, Université du Québec à Rimouski, Rimouski, Québec, Canada, 2 Parc National de Miguasha, Nouvelle, Québec, Canada, 3 Senckenberg Forschungsinstitut und Naturmuseum Frankfurt, Frankfurt am Main, Germany, 4 Centre de Recherche en Paléontologie–Paris, Département Origines & Évolution, Muséum National d’Histoire Naturelle, UMR 7207 (MNHN–Sorbonne Université–CNRS), Paris, France a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 ☯ These authors contributed equally to this work. * Abstract OPEN ACCESS Citation: Charest F, Mondéjar Fernández J, Grünbaum T, Cloutier R (2023) Evolution of median fin patterning and modularity in living and fossil osteichthyans. PLoS ONE 18(3): e0272246. https://doi.org/10.1371/journal.pone.0272246 Editor: Michael Schubert, Laboratoire de Biologie du Développement de Villefranche-sur-Mer, FRANCE Received: July 15, 2022 Accepted: February 24, 2023 Published: March 15, 2023 Copyright: © 2023 Charest et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Morphological and developmental similarities, and interactions among developing structures are interpreted as evidences of modularity. Such similarities exist between the dorsal and anal fins of living actinopterygians, on the anteroposterior axis: (1) both fins differentiate in the same direction [dorsal and anal fin patterning module (DAFPM)], and (2) radials and lepidotrichia differentiate in the same direction [endoskeleton and exoskeleton module (EEM)]. To infer the evolution of these common developmental patternings among osteichthyans, we address (1) the complete description and quantification of the DAFPM and EEM in a living actinopterygian (the rainbow trout Oncorhynchus mykiss) and (2) the presence of these modules in fossil osteichthyans (coelacanths, lungfishes, porolepiforms and ‘osteolepiforms’). In Oncorhynchus, sequences of skeletal elements are determined based on (1) apparition (radials and lepidotrichia), (2) chondrification (radials), (3) ossification (radials and lepidotrichia), and (4) segmentation plus bifurcation (lepidotrichia). Correlations are then explored between sequences. In fossil osteichthyans, sequences are determined based on (1) ossification (radials and lepidotrichia), (2) segmentation, and (3) bifurcation of lepidotrichia. Segmentation and bifurcation patterns were found crucial for comparisons between extant and extinct osteichthyan taxa. Our data suggest that the EEM is plesiomorphic at least for actinopterygians, and the DAFPM is plesiomorphic for osteichthyans, with homoplastic dissociation. Finally, recurrent patterns suggest the presence of a Lepidotrichia Patterning Module (LPM). Data Availability Statement: All relevant data are within the manuscript and its Supporting Information files. Funding: This project was supported by a NSERC Discovery grant to RC. NSERC-RGPIN 06133 https://www.nserc-crsng.gc.ca Additional funding was provided to FC: Fondation UQAR, Caisse Desjardins de la Baie-des-Chaleurs, AMNH and FMNH travel grants. https://fondationuqar.ca/ https://www.desjardins.com/votre-caisse/index. jsp?transit=81540001 https://www.amnh.org/ Introduction In the past two decades, the median fins [i.e., dorsal, anal, and caudal fins] of fishes have been the focus of an overwhelming body of research in evolutionary developmental biology. Primary interest for these so-called unpaired fins lies in their locomotor functions [1–3], ecological implications [4, 5], comparative morpho-anatomy [6], molecular [7] and developmental PLOS ONE | https://doi.org/10.1371/journal.pone.0272246 March 15, 2023 1 / 38 PLOS ONE https://www.fieldmuseum.org/ JMF was supported by the Louis Gentil - Jacques Bourcart prize of the French Academy of Sciences. https://www. academie-sciences.fr/ The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Median fin patterning in osteichthyans [8] patterning, as well as morphological disparity [9]. Indeed, among median fins, the dorsal and anal fins of piscine osteichthyans (bony fishes) show a great morphological disparity, reflecting the evolvability of this system [9–11]. The fins of vertebrates can be described as membranous outgrowths of the body walls reinforced internally by elongated elements, which can be of endoskeletal (e.g., radial bones) or dermal (e.g., fin rays) origin. Osteichthyans primitively display two dorsal fins and a single anal fin [12]. Independently and repeatedly in actinopterygians (ray-finned fishes) and sarcopterygians (lobe-finned fishes), the number of dorsal fins is reduced by loss or fusion with the caudal fin [9, 11, 13]. The loss of the anal fin is less frequent in piscine osteichthyans, although loss or fusion with the caudal fin occurs in some teleosts and dipnoans [11, 14]. Among ‘elpistostegalians’, the extinct transitional taxa between fishes and tetrapods, the condition is poorly documented (e.g., Panderichthys, Tiktaalik). However, Elpistostege, considered a basal tetrapod, has lost the dorsal fin while an anal fin is present [15]. And finally, the absence of both the dorsal and anal fins is considered a synapomorphy shared by aquatic and terrestrial tetrapods [14] with the exception of Elpistostege [15]. Even with such morphological disparity, the structure and development of the median fins is expected to be broadly similar among osteichthyans because these fins have similar constituents. In a forerunner comparative study, Mabee et al. [16] revealed the recurrence of similar developmental patterning (i.e., sequences and direction of development among endoskeletal and exoskeletal elements) in the dorsal and anal fins among living actinopterygians, which they interpreted as evidence of modularity. They found out that the similar patterning of these fins might be indicative of two modules: (1) the Dorsal and Anal Fin Patterning Module (DAFPM), where the skeletal elements (radial bones and lepidotrichia) of both fins differentiate in the same direction (on the anteroposterior (AP) axis) and (2) the Endoskeleton and Exoskeleton Module (EEM), where the directions of development (AP axis) of the endoskeleton (radials) and exoskeleton (lepidotrichia) are similar. The DAFPM and EEM are considered to be maintained during actinopterygian evolutionary history [16] but a phylogenetic inference across osteichthyans was not possible owing to the absence of comparative data on early actinopte (...truncated)