A primitive placoderm sheds light on the origin of the jawed vertebrate face

Abstract

Extant vertebrates form two clades, the jawless Cyclostomata (lampreys and hagfishes) and the jawed Gnathostomata (all other vertebrates), with contrasting facial architectures. These arise during development from just a few key differences in the growth patterns of the cranial primordia: notably, the nasal sacs and hypophysis originate from a single placode in cyclostomes but from separate placodes in gnathostomes, and infraoptic ectomesenchyme migrates forward either side of the single placode in cyclostomes but between the placodes in gnathostomes. Fossil stem gnathostomes preserve cranial anatomies rich in landmarks that provide proxies for developmental processes and allow the transition from jawless to jawed vertebrates to be broken down into evolutionary steps. Here we use propagation phase contrast synchrotron microtomography to image the cranial anatomy of the primitive placoderm (jawed stem gnathostome) Romundina, and show that it combines jawed vertebrate architecture with cranial and cerebral proportions resembling those of cyclostomes and the galeaspid (jawless stem gnathostome) Shuyu. This combination seems to be primitive for jawed vertebrates, and suggests a decoupling between ectomesenchymal growth trajectory, ectomesenchymal proliferation, and cerebral shape change during the origin of gnathostomes.

Copulation in antiarch placoderms and the origin of gnathostome internal fertilization

“…These structures are not associated with pelvic fins. The clasper morphology resembles that of ptyctodonts, a more crownward placoderm group [7][8] , suggesting that all placoderm claspers are homologous and that internal fertilization characterized all placoderms. This implies that external fertilisation and spawning, which characterizes most extant aquatic gnathostomes, must be derived from internal fertilisation, even though this transformation has been thought implausible.…”

“…The discovery in arthrodiran 3 and ptyctodont placoderms 2,4 of copulatory structures (claspers) originally 3, 12 but incorrectly 4 interpreted as modified pelvic fins implied that any placoderms lacking pelvic appendages would have also lacked claspers, and therefore reproduced externally by spawning. This was thought to be the case with the antiarchs, recently considered the sister group of all other jawed vertebrates [5][6][7][8] . Deposits where small antiarch juveniles suffered mass mortality have been interpreted as nurseries associated with mass spawning events 13 .…”

“…It is commonly argued that internal fertilization can evolve from external, but not the reverse. Male copulatory claspers are present in certain placoderms [2][3][4] , fossil jawed vertebrates retrieved as a paraphyletic segment of the gnathostome stem group in recent studies [5][6][7][8] . This suggests that internal fertilization could be primitive for gnathostomes, but such a conclusion depends on demonstrating that copulation was not just a specialized feature of certain placoderm subgroups.…”

“…This suggests that internal fertilization could be primitive for gnathostomes, but such a conclusion depends on demonstrating that copulation was not just a specialized feature of certain placoderm subgroups. The reproductive biology of antiarchs, consistently identified as the least crownward placoderms [5][6][7][8] and thus of great interest in this context, has until now remained unknown. Here we show that certain antiarchs possessed dermal claspers in the males, while females bore paired dermal plates inferred to have facilitated copulation.…”

“…Based on similarities in position (behind and independent of pelvic region), and materials (dermal bone), the claspers of antiarchs, ptyctodonts and arthrodires are most probably homologous with each other, but not homologous with the claspers of chondrichthyans. To evaluate the evolution of claspers and reproductive biology across gnathostomes, we expanded upon a recently published phylogenetic analysis 8 with the addition of 14 placoderm taxa, three new characters (256-258), and one character (122) split into two (122, 159) (Supplementary Information: C7,8). Our analyses of both expanded and original data sets yielded very similar trees, which supported placoderm paraphyly and placed antiarchs as the sister group to all other gnathostomes (Extended Data, Figs.…”