A New 13 Million Year Old Gavialoid Crocodylian from Proto-Amazonian Mega-Wetlands Reveals Parallel Evolutionary Trends in Skull Shape Linked to Longirostry

Abstract

Gavialoid crocodylians are the archetypal longirostrine archosaurs and, as such, understanding their patterns of evolution is fundamental to recognizing cranial rearrangements and reconstructing adaptive pathways associated with elongation of the rostrum (longirostry). The living Indian gharial Gavialis gangeticus is the sole survivor of the group, thus providing unique evidence on the distinctive biology of its fossil kin. Yet phylogenetic relationships and evolutionary ecology spanning ~70 million-years of longirostrine crocodylian diversification remain unclear. Analysis of cranial anatomy of a new proto-Amazonian gavialoid, Gryposuchus pachakamue sp. nov., from the Miocene lakes and swamps of the Pebas Mega-Wetland System reveals that acquisition of both widely separated and protruding eyes (telescoped orbits) and riverine ecology within South American and Indian gavialoids is the result of parallel evolution. Phylogenetic and morphometric analyses show that, in association with longirostry, circumorbital bone configuration can evolve rapidly for coping with trends in environmental conditions and may reflect shifts in feeding strategy. Our results support a long-term radiation of the South American forms, with taxa occupying either extreme of the gavialoid morphospace showing preferences for coastal marine versus fluvial environments. The early biogeographic history of South American gavialoids was strongly linked to the northward drainage system connecting proto-Amazonian wetlands to the Caribbean region.

Fig 1. Miocene fossiliferous localities in the Iquitos region, northeastern Peru.

Spatial distribution of the Molluscan Zones (MZ) [28] and fossil bearing localities (IQ) within the Pebas Formation and the “Uppermost Pebas Formation” is shown. Geological data from [33].

Fig 2. Gryposuchus pachakamue sp. nov.

Photograph and schematic drawing of the skull (holotype, MUSM 1981) in dorsal (A), ventral (B), and lateral (C) view. (D) Photograph of the right mandible (MUSM 987) and schematic drawing in dorsal view. Details of the skull (E,F). (E) MUSM 900 in lateral view. (F) MUSM 1681 in occipital view. Abbreviations: an, angular; ar, articular; bo, basioccipital; d, dentary; d4, d22, dentary tooth positions; ec, ectopterygoid; ec.j, jugal surface for ectopterygoid; ec.mx, maxilla surface for ectopterygoid; EN, external nares; eo, exoccipital; f, frontal; fo, foramen; IF, incisive foramen; j, jugal; j.mx, maxilla surface for the jugal; l, lacrimal; ls, laterosphenoid; m22, maxillary tooth position 22; mcq, medial condyle of the quadrate; mx, maxilla; mx.j, jugal surface for maxilla; n.mx, maxilla surface for nasal; n, nasal; OR, orbit; p, parietal; pa, palatine; pf, prefrontal; pm, premaxilla; p2, premaxillary tooth position 2; po, postorbital; ppo, paraoccipital process; pt, pterygoid; ptb, pterygoid bullae; q, quadrate; qj, quadratojugal; qj.q, quadrate surface for quadratojugal;; rac, retroarticular crest; sp, splenial; sa, surangular; so, supraoccipital; sq, squamosal; SOF, suborbital fenestra; STF, supratemporal fenestra. Scale bars, 5 cm.

Fig 3. Cranial and mandibular specimens referred to Gryposuchus pachakamue sp. nov.

(A-C,E-O) Gryposuchus pachakamue from the Middle Miocene of the Pebas Formation, Peru and (D) Gryposuchus cf. pachakamue from the Late Miocene of Urumaco, Venezuela. (A,E) Skull in dorsal (A) and lateral (E) view (MUSM 1681); (B,F) Skull in dorsal (B) and lateral (F) view (MUSM 2032); (C,G,H) Skull in dorsal (C), lateral (G), and occipital (H) view, juvenile (MUSM 1988); (D) Skull in dorsal view (AMU CURS 12). (I,J) Snout in dorsal (I) and (J) ventral view (MUSM 1681). (K,L) Snout in dorsal (K) and ventral (L) view, juvenile (MUSM 1727). (M) Symphyseal mandible in dorsal view (MUSM 2407). (N) Symphyseal mandible in dorsal view, juvenile (MUSM 1439). (O) Symphyseal mandible in dorsal view, juvenile (MUSM 1682). Abbreviations: cqg, cranio-quadrate groove; d, dentary; d4, d11, d18, dentary tooth positions; ec, ectopterygoid; EN, external nares; eo, exoccipital; f, frontal; fcp, foramen carotideum posterior; IF, incisive foramen; ITF, infratemporal fenestra; j, jugal; l, lacrimal; m1, maxillary tooth position 1; mx, maxilla; n, nasal; OP, occlusal pits; OR, orbit; p, parietal; p1, p2, p4, premaxillary tooth positions; pm, premaxilla; po, postorbital; pr, prefrontal; pt, pterygoid; PTF, post-temporal fenestra; q, quadrate; qj, quadratojugal; so, supraoccipital; sp, splenial; sq, squamosal; STF, supratemporal fenestra; v, foramen vagus. Scale bars, 5 cm.

Fig 4. Comparisons between distal snouts of selected gavialoids.

(A,F) Gryposuchus pachakamue in dorsal (A) and ventral (F) view (MUSM 1981). (B,G) Piscogavialis jugaliperforatus in dorsal (B) and ventral (G) view (SMNK 1282 PAL). (C,H) Eogavialis africanus in dorsal (C) and ventral (H) view (AMNH 5075). (D,I) Gavialis gangeticus in dorsal (D) and ventral (I) view (MNHN A5321). (E) Gryposuchus colombianus in dorsal view (IGM 184696). Red and blue horizontal bars indicate the posterior limit of the premaxillae and anterior limit of the nasals, respectively. Abbreviations: m2, m3, m4, m5, m6, maxillary tooth positions; p1-p4, p1-p5, premaxillary tooth series. Scale bar, 5 cm.

Fig 5. Noteworthy anatomical features of Gryposuchus pachakamue.

(A) Suborbital fenestra region of the holotype skull (MUSM 1981) in lateroventral view showing the pterygoid bullae (ptb). (B) Post-symphyseal mandible (MUSM 987) in posteromedial view showing a foramen (fo), that probably is the aperture of the foramen intermandibularis oralis. (C,D) Posterior portion of the right mandible (MUSM 1440) in dorsomedial (C) and lateral (D) view. Abbreviations: an, angular; ar, articular; d17, d21, dentary tooth positions; ec, ectopterygoid; EMF, external mandibular fenestra; fo, foramen; SOF, suborbital fenestra; j, jugal, mx, maxilla; p, parietal; pa, palatines; po, postorbital; ptb, pterygoyd bullae; rac, retroarticular crest; rar, retroarticular process of the mandible; sa, surangular; sp, splenial; sq, squamosal; sy, symphysis. Scale bars, 5 cm.

Fig 6. Comparisons between post-symphyseal mandibles of selected gavialoids.

(A,B) Gryposuchus pachakamue (MUSM 987) in lateral (A) and medial (B) view. (C,D) Gavialis gangeticus (MNHN A-5312) in lateral (C) and medial (D) view. (E,F) Piscogavialis jugaliperforatus (MUSM 449) in lateral (E) and medial (F) view. The arrows in (B) and (F) show the ventral process of the surangular in medial view. Abbreviations: an, angular (green color in lateral views); anp, angular process; ar, articular (fuchsia color); co, coronoid; d, dentary; rac, retroarticular crest; sa, surangular (purple color in lateral views); sp, splenial. Scale bars, 5 cm.

Fig 7. Phylogenetic position of Gryposuchus pachakamue within crocodylians.

(A) Strict consensus cladogram of 45 most parsimonious trees based on parsimony analysis of the complete data matrix (S1 Appendix). Apomorphic character states associated with a “telescoped” orbit condition are plotted on the cladogram as black lines (i.e., 137–2, 138–1, and 190–1). (B) Strict consensus cladogram of 24 optimal trees in a second parsimony analysis performed after removing character state 137–2 and character 138 from the data matrix (S2 Fig). (C) Parallel acquisition of a fully “telescoped” orbit condition (TO) in advanced South American Gryposuchus and Indian Gavialis. Selected character states of the circumorbital region are indicated with arrows. From left to right: Gryposuchus colombianus (IGM 184696), Gryposuchus pachakamue (MUSM 900), Piscogavialis jugaliperforatus (SMNK 1282 PAL), Gavialis gangeticus (MNHN A5321), and Argochampsa krebsi (OCP DEK-GE 333). Scale bars, 5 cm.

Fig 8. Phylogenetic relationships of Crocodylia mapped onto the circumorbital morphospace defined by PC1 and PC2.

Deformation grids depict extreme values along each axis and blue vectors indicate the position of the mean relative to the landmark variation. PC1 correlates mainly with the width of the pre- and post-orbital regions, and orbit length. Species on the positive extreme of PC1 present slender skull tables and interorbital bridge, long orbits and prefrontals, and laterally oriented anterior processes of the jugals, whereas those on the negative extreme bear broad skull tables, wide posterior portion of the interorbital bridge and orbits, short orbits, short prefrontals, and medially oriented anterior processes of the jugals. PC2 correlates with the relative length of the pre-orbital bones, involving mostly the frontal and lacrimals and the width of the prefrontals. Species with higher PC2 scores have comparatively longer and more slender frontals and a narrow interorbital bridge. Taxa with lower scores present short frontal and lacrimal bones and short and wide anterior portion of the interorbital bridge. The phylogenetic morphospace of the orbital and circumorbital region in Miocene South American gavialoids covers most of the variation of the whole clade. Taxon abbreviations: Bor., Borealosuchus; Pal., Paleosuchus; The., Thecachampsa; Tho., Thoracosaurus (S1 Appendix).

Fig 9. Time calibrated phylogenetic tree of the Gavialoidea and relevant paleogeographic distributions associated with the evolution and diversification of gavialoids in marine and freshwater settings.

During the Late Paleocene-Early Eocene interval, peaks of sea surface temperature (SST) and global sea surface level (GSL) occurred together with tropical marine connections through the Tethys Ocean and Caribbean Sea [59,60]. During the Neogene, distinct biomes dominated tropical South America: (A) Acre Phase, after the onset of the eastern-draining Amazon and northward-draining Orinoco river systems; and (B) Pebas Mega-Wetland System, with its drainage northward to the Caribbean Sea. Abbreviations: Olig., Oligocene; Ple., Pleistocene; Pli., Pliocene. Global and South American schematic paleogeography adapted from Blakey [60] and Hoorn et al. [61], respectively.