Conserved developmental processes constrain evolution of lungfish dentitions

Abstract

Although the 3 genera of living lungfish have different‐shaped adult tooth plates, their larval stages have similar patterns of development. The sequence in the pattern of initiation of teeth and their modification through ontogeny in Neoceratodus hatchlings provides a developmental model for fossil hatchling tooth plates (smallest 1–2 mm) recovered as 3‐dimensional dentitions from Andreyevichthys. This Late Devonian lungfish demonstrates that these also have a similar dentition pattern and suggests strongly conserved developmental processes. We postulate that a specific pattern of development, derived within lungfish, has been conserved in extant forms through evolution from the earliest known lungfish. The most basal early dipnoan, Diabolepis speratus, is also known from juveniles with tooth plates formed in this pattern. The lungfish pattern is in marked contrast to the typical linear rows of teeth with lingual replacement for each tooth position, characteristic of most osteichthyan and chondrichthyan dentitions. Uniquely for lungfish, teeth are only added to the lateral ends of the radial rows in the palatal and lingual dentition and are consolidated into dental plates without loss through shedding. It is proposed that this tooth pattern is set up from primordial teeth at the patterning stage of the dentition, one in each dentate region of the larval jaws. Although in post‐Devonian lungfish marginal dentate bones are absent in the adult, in both the fossil and extant hatchling, teeth are present and function on some of the marginal bones. This pattern of development and loss is described and we conclude that in both forms it is also based on a radial pattern of successive tooth initiation. We propose that this ontogenetic pattern constrained the phylogenetic pattern of adult form, through evolution of dipnoan dentitions from 360 MYBP until the present. The universality amongst dipnoans and the implications for such a conserved constraint in the developmental module for the dentition is discussed.

Vertebrate dentitions at the origin of jaws: when and how pattern evolved

“…One particular example of conservation of developmental pattern, unique for one taxon across 360 million years, can be observed in the ontogeny of fossil and recent lungfish dentitions (Reisz and Smith 2001;Smith and Krupina 2001;Smith et al 2002). It is assumed here that part of the module for dentition patterning is conserved within gnathostomes, that is, the morphogenetic unit, or primordium for denticle, or tooth, involving epithelial-mesenchymal interactions between an inductive epithelium (endoderm) and mesenchyme derived from cranial neural crest (ectomesenchyme).…”

The cranial morphology of a new genus of lungfish (Osteichthyes: Dipnoi) from the Upper Jurassic Morrison Formation of North America

“…The partial skull of Ceratodus sturii from the Late Triassic (Carnian) of Austria has alternately been attributed to the genus Ceratodus (Kemp, 1998;Cavin et al, 2007) and placed in the genus Tellerodus (Lehman, 1975;Schultze, 1981), but has since been returned to the genus Ceratodus based on dental similarities with the holotypic material of the genotype, C. latissimus Agassiz (Kemp, 1998;Schultze, 2004). Similarities exist between the dental plates associated with this skull and with other dental plates attributed to the genus Ceratodus, but diversity within the genus Ceratodus and conservatism in dental morphology throughout Mesozoic lungfishes (Smith and Krupina, 2001;Smith et al, 2002;Ahlberg et al, 2006;Pardo, 2007) hinder further inference concerning constancy of skeletal morphology and monophyly of the genus. This is particularly perplexing because fossils attributed to the genus Ceratodus span the entire Mesozoic and are found on every continent.…”

“…No cranial material was collected or described, and the generic diagnosis was necessarily brief. Unfortunately, the dentition of post-Devonian lungfishes is highly stereotypical (Smith and Krupina, 2001;Smith et al, 2002), and the systematic utility of dental plate morphology is poor. To date, many taxa have been described on the basis of dental plate heuristics (e.g., Vorobyeva and Minikh, 1968), a practice that fills in the poor Mesozoic lungfish skeletal record at the cost of diluting systematically and phylogenetically informative data.…”

Fate mapping in embryos of Neoceratodus forsteri reveals cranial neural crest participation in tooth development is conserved from lungfish to tetrapods

“…Uniquely for Neoceratodus only these marginal teeth of the whole tooth row are lost during the juvenile period of lungfish ontogeny and never replaced (for this reason referred to as transitional), even the dentary bone never forms. Conversely, all teeth of the lingual and palatal toothplates are retained and fused to the dermal bones (Kemp 1999;Smith and Krupina 2001). Although there is great disparity among lungfish dentitions in the early Devonian Period when the clade originates (Ahlberg et al 2006) the developmental pattern of tooth addition is conserved from this time for more than 400 Myr (Reisz and Smith 2001) including the three extant genera.…”

“…Although lungfish have evolved a unique toothed phenotype, represented by a dentition of retained (statodont) teeth, this dentition is assembled from separate teeth which fuse together in diverging radial rows into palatal (vomerine and pterygoid) and lingual (prearticular) toothplates (Smith and Krupina 2001). This palato-lingual part of the dentition begins to develop before, but almost simultaneously with, a single row of teeth along the lower jaw margin in the position of the dentary.…”