Lamprey-like gills in a gnathostome-related Devonian jawless vertebrate

Abstract

So far, the Palaeozoic fossil jawless vertebrates have not provided any direct evidence for the organization of the gills, apart from vague impressions--supposedly left by gill filaments--on the bony surface of the gill chamber in certain armoured forms or 'ostracoderms' (for example, osteostracans and heterostracans). The latter are currently regarded as more closely related to the living jawed vertebrates (crown gnathostomes) than to the living jawless vertebrates (hagfish and lampreys, or cyclostomes). Here we report the first direct evidence for the position of the gill filaments--possibly supported by gill rays--enclosed by gill pouches in a 370-million year (Myr)-old jawless vertebrate, Endeiolepis, from the Late Devonian fossil fish site of Miguasha, Quebec, Canada. This extinct jawless fish has much the same gill organization as living lampreys, although it possesses an unusually large number of gill pouches--a condition unlike that in any extant vertebrates and that raises questions about gill development. Endeiolepis is currently regarded as a close relative of anaspids, a group of 410-430-Myr-old 'ostracoderms'. Assuming that current vertebrate phylogeny is correct, this discovery demonstrates that pouches enclosing the gills are primitive for vertebrates, but have been subsequently lost in jawed vertebrates.

Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons

“…Gegenbaur drew parallels between the organization of the gill arch skeleton with that of the paired appendage skeletons of gnathostomes, homologizing the appendage girdle with the proximal branchial arch, and the endoskeleton of paired fins proper with the distal branchial rays. Mapping the presence of branchial ray elements on existing phylogenetic trees supports the notion that they are likely an ancestral feature of jawed fishes, as evidenced by their presence in the stem gnathostome Euphanerops, the stem osteichthyan Acanthodes, and all extant chondrichthyans (4,5). Branchial rays (not to be confused with the gill rakers of osteichthyans) have been lost, however, in extant agnathans and osteichthyans, leaving chondrichthyans as the only organisms in which ray development might be examined and hypotheses of homology tested (6).…”

“…The fossil record and comparative anatomy unambiguously indicate the sequential appearance of gills, median fins, and paired fins in deuterostome evolution (4)(5)(6)40). Although the fossil record cannot unequivocally resolve the order of appearance of branchial rays and median fins, both appear before the origin of gnathostomes and paired appendages.…”

“…We hypothesize that these are ancestral features of gnathostome branchial arch development that functioned primitively to direct branchial ray outgrowth and that the differing expression patterns observed in osteichthyans [i.e., the restriction of Shh expression to arches 2 and 3 (18,24)] are a derived condition, corresponding with the near-complete loss of lateral outgrowth-the loss of branchial rays-in these taxa. Our hypothesis rests on the notion that branchial ray-supported gills are a primitive anatomical feature of gnathostomes-a notion supported by the presence of branchial rays in all extant chondrichthyans, a stem osteichthyan, and a stem gnathostome (4,5,25).…”

A primitive fish from the Cambrian of North America

“…Primitive serial homology is often used as a starting point in discussions on the origin of jaws, although Metaspriggina is too basal (Fig. 3) 22 , in these Late Devonian period (Frasnian) agnathans the branchial arches have fused into single sinuous units and are now associated with an array of small rods and 'copular elements'. This may prefigure 21 the complex basket of extant lampreys 7 , a configuration that had apparently stabilized by the latest Devonian period (Famennian) 23 .…”

Great Canadian Lagerstätten 4. The Devonian Miguasha Biota (Québec): UNESCO World Heritage Site and a Time Capsule in the Early History of Vertebrates

“…Recent investigations have focused on exceptional cases of fossilization where preservation of soft tissues such as digestive tracts, stomachs, spiral intestines, lungs, gill filaments, blood vessels (Fig. 10b) or muscles is involved (Arsenault et al 2004;Janvier et al 2006;Cloutier 2009;Janvier and Arsenault 2009;Arsenault and Janvier 2010). In addition, preliminary studies on nonmineralized parts of the Bothriolepis body suggest that 'skin preservation' results from the presence of a bacterial mat outlining the surface of the carcass (Fig.…”