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

Abstract

One of the major events in vertebrate evolution involves the transition from jawless (agnathan) to jawed (gnathostome) vertebrates, including a variety of cranial and postcranial innovations. It has long been assumed that characters such as the pelvic girdles and fins, male intromittent organs independent from the pelvic girdles, as well as a regionalized axial skeleton first appeared in various basal gnathostome groups if not at the origin of gnathostomes. Here we describe the first occurrence of pelvic girdles and intromittent organs in the Late Devonian jawless anaspid‐like fish Euphanerops longaevus Woodward (Miguasha Lagerstätte, eastern Canada), associated with a morphologically differentiated region of the axial skeleton. Morphological differentiation of the axial skeleton is also described for the first time in an extant jawless fish, the sea lamprey Petromyzon marinus Linnaeus. Our data indicate that regionalization of the axial skeleton occurred earlier in vertebrate evolutionary history than previously appreciated. This regionalization is coupled with modifications of the appendicular skeleton in Euphanerops. These new observations combined with a new phylogenetic analysis of early vertebrates provide a more precise understanding of how the appendicular and axial skeletons developed and evolved within vertebrate evolutionary history.

A critical appraisal of appendage disparity and homology in fishes

“…The structural and functional similarities between the median and paired fins in coelacanths provide another example of the possible redeployment of developmental mechanisms. This hypothesis may be extended to other appendages as well: pelvic claspers are considered as a synapomorphy of extant chondrichthyans Grogan et al, 2012;Maisey, 1986;Schaeffer & Williams, 1977), but intromittent organs have also been identified in various placoderms (Goujet, 1984(Goujet, , 2001Miles & Young, 1977;Trinajstic et al, 2014;Young, 1986) and more recently in the anaspid Euphanerops (Chevrinais et al, 2018). Fin-forming fields could also explain how some fins might have evolved more than once independently during the evolutionary history of fishes.…”

“…Ahlberg (1992) hypothesized that these similarities may be owing to a homeotic switch in gene expression whereby paired fin developmental mechanisms were re-expressed in the posterior dorsal and anal fins. In Euphanerops, the intromittent organs are associated with the pelvic girdles despite the fact that pelvic fins are absent (Chevrinais et al, 2018). Indeed, despite similarities in structure and morphology, the adipose fin has been shown to have evolved independently multiple times within teleosteans (Stewart & Hale, 2013;Stewart et al, 2014).…”

“…A few species (e.g., Birkenia elegans, Kerreralepis carinata, Pterygolepis nitida) possess a series of plates or spines inserted anteriorly to the anus, which Blom (2012) interpreted as a possible median preanal fin. A recent re-investigation of the Euphanerops material confirms that a long and low dorsal fin is indeed present (Chevrinais et al, 2018). In Euphanerops longaevus, a dorsal fin has been reported either as present (Arsenault & Janvier, 1991;Stensiö, 1939;Woodward, 1900a) or absent (Janvier & Arsenault, 2007;Sansom, Gabbott, & Purnell, 2013).…”

“…These appendages, which can be found in some anaspids and thelodonts, have variously been described using terms such as (ventro)lateral fins or fin-folds (e.g., Blom, 2008;Blom, Märss, & Miller, 2002;Ritchie, 1964;Ritchie, 1968aRitchie, , 1980, paired anteroventral fins (Chevrinais et al, 2018), pectoral swimming appendages (Stensiö, 1964), paired or pectoral flaps (e.g., Dineley & Loeffler, 1976;Donoghue & Smith, 2001;Märss, Turner, & Karatajūtē-Talimaa, 2007;Turner, 1982Turner, , 1991 and suprabranchial fins (e.g., Johanson, 2010;Wilson et al, 2007). These appendages, which can be found in some anaspids and thelodonts, have variously been described using terms such as (ventro)lateral fins or fin-folds (e.g., Blom, 2008;Blom, Märss, & Miller, 2002;Ritchie, 1964;Ritchie, 1968aRitchie, , 1980, paired anteroventral fins (Chevrinais et al, 2018), pectoral swimming appendages (Stensiö, 1964), paired or pectoral flaps (e.g., Dineley & Loeffler, 1976;Donoghue & Smith, 2001;Märss, Turner, & Karatajūtē-Talimaa, 2007;Turner, 1982Turner, , 1991 and suprabranchial fins (e.g., Johanson, 2010;Wilson et al, 2007).…”

“…Furthermore, these ventrolateral paired fins are subdivided into a series of finlets, each composed of a radial, a meso-or metapterygial-like element and several fin-rays (Chevrinais et al, 2018). Janvier …”