Bayesian Morphological Clock Methods Resurrect Placoderm Monophyly and Reveal Rapid Early Evolution in Jawed Vertebrates

Abstract

The phylogeny of early gnathostomes provides an important framework for understanding one of the most significant evolutionary events, the origin and diversification of jawed vertebrates. A series of recent cladistic analyses have suggested that the placoderms, an extinct group of armoured fish, form a paraphyletic group basal to all other jawed vertebrates. We revised and expanded this morphological data set, most notably by sampling autapomorphies in a similar way to parsimony-informative traits, thus ensuring this data (unlike most existing morphological data sets) satisfied an important assumption of Bayesian tip-dated morphological clock approaches. We also found problems with characters supporting placoderm paraphyly, including character correlation and incorrect codings. Analysis of this data set reveals that paraphyly and monophyly of core placoderms (excluding maxillate forms) are essentially equally parsimonious. The two alternative topologies have different root positions for the jawed vertebrates but are otherwise similar. However, analysis using tip-dated clock methods reveals strong support for placoderm monophyly, due to this analysis favoring trees with more balanced rates of evolution. Furthermore, enforcing placoderm paraphyly results in higher levels and unusual patterns of rate heterogeneity among branches, similar to that generated from simulated trees reconstructed with incorrect root positions. These simulations also show that Bayesian tip-dated clock methods outperform parsimony when the outgroup is largely uninformative (e.g., due to inapplicable characters), as might be the case here. The analysis also reveals that gnathostomes underwent a rapid burst of evolution during the Silurian period which declined during the Early Devonian. This rapid evolution during a period with few articulated fossils might partly explain the difficulty in ascertaining the root position of jawed vertebrates.

Neurocranial anatomy of the petalichthyid placodermShearsbyaspis oepikiYoung revealed by X‐ray computed microtomography

“…D, topology 3 tests the result with a monophyletic Placodermi as found by King et al . (). E, topology 4 presents a monophyletic Placodermi with Shearsbyaspis resolved as sister to arthrodires.…”

“…; King et al . ; Zhu et al . ), the phylogenetic interpretation of the parapshenoid in Kosoraspis is unclear.…”

Evolution of vertebrate postcranial complexity: axial skeleton regionalization and paired appendages in a Devonian jawless fish

“…; but see King et al . ). This confirms these characters as primitive for jawed vertebrates, but with pelvic girdles and intromittent organs apparently absent among jawless vertebrates.…”

Unique diversity of acanthothoracid placoderms (basal jawed vertebrates) in the Early Devonian of the Prague Basin, Czech Republic: A new look at Radotina and Holopetalichthys

“…Only scarce fragments of placoderm fossils can be found nowadays. Contra King et al [12], who argue that phylogenetically basal placoderms were benthic, we suggest that the Lochkovian acanthothoracids were most probably nektonic active swimmers, considering the shape of their crania and trunk armours, and the lateral position of the orbits [25, 28]. The environment in the Lochkovian of the Černá rokle is supposed to be relatively deep water [43].…”

“…In evolutionary terms, the gnathostome stem group encompasses the origin of jaws and associated major changes in facial architecture [3,5,7]; in phylogenetic terms, it is a segment of the vertebrate tree whose content and topology has long been the subject of debate [9,10,11,1,2,3,4,6,7]. A key development in the understanding of this stem group has been the recognition that the placoderms (armoured jawed fishes of Silurian to Devonian age), which until recently were regarded as a clade branching off the gnathostome stem group, probably form a paraphyletic segment of that stem group [2,7,8] (but see [12]). Some groups of placoderms appear to be very primitive and close to jawless vertebrates [7] whereas others possess what were previously regarded as osteichthyan autapomorphies (notably a maxilla, premaxilla and dentary) and are probably close to the gnathostome crown-group node [6, 13].…”