Perspectives on hyperphalangy: patterns and processes

Abstract

Hyperphalangy is a digit morphology in which increased numbers of phalanges are arranged linearly within a digit beyond the plesiomorphic condition. We analyse patterns and processes of hyperphalangy by considering previous definitions and occurrences of hyperphalangy among terrestrial and secondarily aquatic extant and fossil taxa (cetaceans, ichthyosaurs, plesiosaurs and mosasaurs), and recent studies that elucidate the factors involved in terrestrial autopod joint induction. Extreme hyperphalangy, defined as exceeding a threshold condition of 4/6/6/ 6/6, is shown only to be found among secondarily aquatic vertebrates with a flipper limb morphology. Based on this definition, hyperphalangy occurs exclusively in digits II and III among extant cetaceans. Previous reports of cetacean embryos having more phalanges than adults is clarified and shown to be based on cartilaginous elements not ossified phalanges. Developmental prerequisites for hyperphalangy include lack of cell death in interdigital mesoderm (producing a flipper limb) and maintenance of a secondary apical ectodermal ridge (AER), which initiates digit elongation and extra joint patterning. Factors of the limb-patterning pathways located in the interdigital mesoderm, including bone morphogenetic proteins (BMPs), BMP antagonists, fibroblast growth factors (FGFs), growth/differentiation factor-5 (GDF-5), Wnt-14 and ck-erg , are implicated in maintenance of the flipper limb, secondary AER formation, digit elongation and additional joint induction leading to hyperphalangy.

Evolution of hyperphalangy and digit reduction in the cetacean manus

“…Hyperphalangy is defined here as an increased number of phalanges per digit beyond the plesiomorphic conditions of 2/3/4/5/4 for all amniotes and more specifically 2/3/3/3/3 for mammals (Richardson and Chipman, 2003;Fedak and Hall, 2004), which evolved from the primitive reptilian formula of 2/3/4/5/3-4 among cynodont synapsids (Richardson and Chipman, 2003). Some extinct marine reptiles exhibit hyperphalangy in all their digits (Fig.…”

“…Some extinct marine reptiles exhibit hyperphalangy in all their digits (Fig. 1E, Caldwell, 2002;Richardson and Chipman, 2003;Fedak and Hall, 2004); however hyperphalangy in toothed whales (odontocetes) is mostly restricted to the second and third digits ( Fig. 1A,B; Richardson and Oelschlä ger, 2002).…”

“…The cetacean manus has been the focus of numerous descriptive studies documenting the patterns of digit ossification and phalangeal counts in isolated taxa (e.g., Gihr et al, 1982;Benke, 1993;Watson et al, 1994;Calzada and Aguilar, 1996;Ortega-Ortiz and Villa-Ramirez, 2000;Richardson and Oelschlä ger, 2002;Dawson, 2003;Fedak and Hall, 2004), but only recently has a more synthetic view of digital evolution emerged. Using a limited number of taxa, Fedak and Hall (2004) hypothesized that the derived condition of hyperphalangy (unconventionally defined as exhibiting a phalangeal formula greater than 4/6/6/6/6 which is greater than the earliest known tetrapods and, therefore, represents a new tetrapod morphology) evolved three separate times within cetaceans.…”

“…Using a limited number of taxa, Fedak and Hall (2004) hypothesized that the derived condition of hyperphalangy (unconventionally defined as exhibiting a phalangeal formula greater than 4/6/6/6/6 which is greater than the earliest known tetrapods and, therefore, represents a new tetrapod morphology) evolved three separate times within cetaceans. While their sample included a limited number of cetacean species, Fedak and Hall (2004) set the stage for a broader and more detailed analysis of cetacean manus evolution.…”

“…Several hypotheses have been proposed regarding the developmental mechanisms underlying the acquisition of hyperphalangy (Caldwell, 2002;Richardson and Oelschl-ä ger, 2002;Fedak and Hall, 2004) but all remain untested, as the genes expressed during the formation of additional phalanges are unknown in cetaceans. However, a study of digital development in the pantropical spotted dolphin (Stenella attenuata) (Richardson and Oelschlä ger, 2002) revealed that additional phalanges were added to the distal ends of the second and third digits after the apical ectodermal ridge (AER) thickened and became isolated to the distal ends of just these digits.…”