Exceptional preservation of nerve and muscle tissues in Late Devonian placoderm fish and their evolutionary implications

Abstract

In this paper, we show exceptional three-dimensionally preserved fossilized muscle tissues in 380-384 Myr old placoderm fish (Late Devonian), offering new morphological evidence supporting the hypothesis that placoderms are the sister group to all other gnathostomes. We describe the oldest soft tissue discovered in gnathostomes, which includes striated muscle fibres, circulatory and nerve tissues, preserved as phosphatized structures precipitated by microbial infilling of small, protected areas under the headshield of the arthrodire, Eastmanosteus calliaspis. Muscle impressions have also been found in the ptyctodontid, Austroptyctodus gardineri. The specimens display primitive vertebrate muscle structures; in particular, shallow W-shaped muscle blocks such as those observed in lampreys. New information from fossilized soft tissues thus elucidates the affinities of the placoderms and provides new insights into the evolution and radiation of gnathostomes.

Figure 1

Preserved soft-tissue recovered from under the infragnathal plate from the placoderm, Eastmanosteus calliaspis (WAM 00.3.1). (a) A striated muscle fibre showing banding replaced by individual calcium phosphate spherulites arranged in pairs, preserving the H and Z bands. (b) A neuron with motor end plates (indicated by arrow) attaching to muscle fibres. (c) A capillary running between muscle fibres. (d) Preservation style made up of coarse massive crystalline replacement by calcium phosphate. (e) A section of phosphatized muscle tissue made up of muscle bundles. (f) Individual muscle fibres enclosed by sarcolemmic membrane. (g) Fibre bundles (indicated by arrow). (h) Scavenger holes (indicated by arrow) in the headshield of E. calliaspis (visceral view and lateral view). (i) Muscle fibres in the ptyctodontid, Australolepis gardineri (WAM 86.9.662). (j) Line drawing of Australolepis gardineri (WAM 86.9.662) indicating the position and extent of muscle blocks. (k) Scavenger holes (indicated by arrow) in anterior median ventral plate. (l) Dorsal muscle fibres running parallel to the long axis of the body attached to myomeres (indicated by an arrow). (m) ‘W’-shaped muscle architecture in the ptyctodontid Australolepis gardineri (arrows indicate the points of flexure that give the W-shape).

Figure 2

Phylogenetic tree supporting the hypothesis that placoderms are the sister group to all other gnathostomes. See table 1 for list of characters.