The Oldest Actinopterygian Highlights the Cryptic Early History of the Hyperdiverse Ray-Finned Fishes

Abstract

Osteichthyans comprise two divisions, each containing over 32,000 living species [1]: Sarcopterygii (lobe-finned fishes and tetrapods) and Actinopterygii (ray-finned fishes). Recent discoveries from China highlight the morphological disparity of early sarcopterygians and extend their origin into the late Silurian [2-4]. By contrast, the oldest unambiguous actinopterygians are roughly 30 million years younger, leaving a long temporal gap populated by fragments and rare body fossils of controversial phylogenetic placement [5-10]. Here we reinvestigate the enigmatic osteichthyan Meemannia from the Early Devonian (∼415 million years ago) of China, previously identified as an exceptionally primitive lobe-finned fish [3, 7, 11, 12]. Meemannia combines "cosmine"-like tissues taken as evidence of sarcopterygian affinity with actinopterygian-like skull roof and braincase geometry, including endoskeletal enclosure of the spiracle and a lateral cranial canal. We report comparable histological structures in undoubted ray-finned fishes and conclude that they are general osteichthyan features. Phylogenetic analysis places Meemannia as an early-diverging ray-finned fish, resolving it as the sister lineage of Cheirolepis [13] plus all younger actinopterygians. This brings the first appearance of ray-fins more in line with that of lobe-fins and fills a conspicuous faunal gap in the otherwise diverse late Silurian-earliest Devonian vertebrate faunas of the South China Block [4].

The dermal skeleton of the jawless vertebrateTremataspis mammillata(Osteostraci, stem‐Gnathostomata)

“…Gross () and Thomson () highlighted the similarity between the mesh canals of Tremataspis and the pore canal system in extinct sarcopterygians. A pore canal system is plesiomorphic for osteichthyans (Lu et al, ), and similar canal systems appear in acanthodians (Gross, ) and heterostracans (‘intermediate canals’). The homology of these structures among early vertebrates remains unresolved; equally mysterious is their function.…”

A new osteichthyan from the late Silurian of Yunnan, China

“…Both Guiyu and Sparalepis are known from articulated specimens whereas the disarticulated remains of Psarolepis are sufficiently comparable to these forms to reconstruct a substantial proportion of its anatomy [15,27,28]. The other two Silurian genera, Lophosteus and Andreolepis , are highly fragmentary as is Meemannia from the Lockhovian [45], recently posited as a stem-actinopterygian [46]. The Early Devonian Dialipina is known from complete specimens [47] that display an unusual (for an osteichthyan) dermal configuration of numerous small cranial and gnathal plates, presenting difficulties in determining homologies with other bony fishes [25] and possibly suggesting some degree of anatomical specialization.…”

A critical appraisal of appendage disparity and homology in fishes

“…The presence of a single dorsal fin has been considered as an actinopterygian synapomorphy (Cloutier & Arratia, 2004). However, since its description, phylogenetic investigations have placed Dialipina sometimes as a stem actinopterygian (Giles, Darras, Clement, Blieck, & Friedman, 2015;Long et al, 2015;Schultze & Cumbaa, 2001;Taverne, 1997;Zhu & Schultze, 2001;Zhu, Yu, Wang, Zhao, & Jia, 2006;, and other times as a stem osteichthyan (Brazeau, 2009;Brazeau & de Winter, 2015;Burrow et al, 2016;Davis et al, 2012;Dupret et al, 2014;Friedman, 2007;Lu, Giles, Friedman, den Blaauwen, & Zhu, 2016;Qiao et al, 2016). However, since its description, phylogenetic investigations have placed Dialipina sometimes as a stem actinopterygian (Giles, Darras, Clement, Blieck, & Friedman, 2015;Long et al, 2015;Schultze & Cumbaa, 2001;Taverne, 1997;Zhu & Schultze, 2001;Zhu, Yu, Wang, Zhao, & Jia, 2006;, and other times as a stem osteichthyan (Brazeau, 2009;Brazeau & de Winter, 2015;Burrow et al, 2016;Davis et al, 2012;Dupret et al, 2014;Friedman, 2007;Lu, Giles, Friedman, den Blaauwen, & Zhu, 2016;Qiao et al, 2016).…”