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. 2022 Apr;604(7907):684-688.
doi: 10.1038/s41586-022-04622-3. Epub 2022 Apr 20.

Pterosaur melanosomes support signalling functions for early feathers

Aude Cincotta  1   2   3   4 , Michaël Nicolaï  5 , Hebert Bruno Nascimento Campos  6 , Maria McNamara  7   8 , Liliana D'Alba  5   9 , Matthew D Shawkey  5 , Edio-Ernst Kischlat  10 , Johan Yans  11 , Robert Carleer  12 , François Escuillié  13 , Pascal Godefroit  14
Affiliations

Pterosaur melanosomes support signalling functions for early feathers

Aude Cincotta et al. Nature. 2022 Apr.

Abstract

Remarkably well-preserved soft tissues in Mesozoic fossils have yielded substantial insights into the evolution of feathers1. New evidence of branched feathers in pterosaurs suggests that feathers originated in the avemetatarsalian ancestor of pterosaurs and dinosaurs in the Early Triassic2, but the homology of these pterosaur structures with feathers is controversial3,4. Reports of pterosaur feathers with homogeneous ovoid melanosome geometries2,5 suggest that they exhibited limited variation in colour, supporting hypotheses that early feathers functioned primarily in thermoregulation6. Here we report the presence of diverse melanosome geometries in the skin and simple and branched feathers of a tapejarid pterosaur from the Early Cretaceous found in Brazil. The melanosomes form distinct populations in different feather types and the skin, a feature previously known only in theropod dinosaurs, including birds. These tissue-specific melanosome geometries in pterosaurs indicate that manipulation of feather colour-and thus functions of feathers in visual communication-has deep evolutionary origins. These features show that genetic regulation of melanosome chemistry and shape7-9 was active early in feather evolution.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Details of the cranial crest of MCT.R.1884, a new specimen of Tupandactylus cf. imperator (Pterosauria: Tapejaridae) from the Lower Cretaceous Crato Formation, Brazil.
a, Incomplete cranium showing preserved soft tissue crest. b–f, Detail of the integumentary structures associated with the posterior part of the skull. b, Monofilaments. c, Branched feathers. d, Detail of curved branched feather in c. e, f, Straight branched feather (e) with detail (f). White arrowhead in e indicates the basal calamus. g–i, SEM of melanosomes in the soft tissues of MCT.R.1884. g, Ovoid melanosomes from the elongate fibres of the soft tissue crest. h, Elongate melanosomes from a monofilament. i, Ovoid melanosomes from a branched feather. c, cristae; p, postmaxillary process; op, occipital process; s, skin. Scale bars, 50 mm (a); 5 mm (b); 2 mm (c); 250 μm (d–f); 2 μm (g–i).
Fig. 2
Fig. 2. Time-tree phylogeny of Avemetatarsalia.
The phylogeny shows the results of ancestral-state estimations for the origin of feathers with the highest likelihood (−72.52), in addition to the lowest AICc (168.32) and the highest AICc weighting (64.56). Only the most complex integumentary structure present is shown for each taxon. Feathers are reconstructed as ancestral to the common avemetatarsalian ancestor of dinosaurs and pterosaurs. Branch lengths are estimated using the mbl branch length estimation and reconstructed according to the best model (that is, with the highest likelihood, lowest AICc and highest AICc weighing), which estimates trait transition rates following ordered evolution. The pie charts at the nodes show the scaled likelihoods of different integumentary structures. The likelihood values for model parameters are shown in Extended Data Table 2. The Tupandactylus silhouette is drawn by E. Boucher from www.phylopic.org. Silhouettes of integumentary appendages are reproduced from ref. , Springer Nature Limited.
Extended Data Fig. 1
Extended Data Fig. 1. Location of the samples collected from the soft tissue cranial crest, monofilaments and branched feathers and sedimentary matrix.
The soft tissue crest is characterized by elongate brown fibres. The posterodorsal part of the crest is darker than the rest of the crest and the brown fibres are faint or not evident in that area. Scale bar, 100 mm.
Extended Data Fig. 2
Extended Data Fig. 2. Distribution of feather types in the tapejarid pterosaur Tupandactylus cf. imperator (MCT.R.1884).
a, Schematic illustration of MCT.R.1884. Monofilaments (red) are restricted to the region immediately adjacent to the proximal part of the occipital process and the branched feathers (blue) to the region adjacent to the distal part of the occipital process. The cranial soft tissue crest is shown in dark grey and the preserved bones are shown in white. The proximal part of the skull (in black) is not present on the slab. b, Reconstruction of MCT.R.1884 showing the distribution of feathers along the occipital process (colours are not reconstructed here). Image credit, Julio Lacerda. Scale bar in (a), 100 mm.
Extended Data Fig. 3
Extended Data Fig. 3. Taphonomic scenarios to explain the origin of the splayed appearance of the branched feathers, based on different styles of feather branching and stiffness.
Only scenario 3, in particular scenario 3b, with a stiff central shaft and stiff barbs of equal length, can explain the particular structures observed in Tupandactylus feathers. a–c, Branched feathers from MCT.R.1884. c, Close-up of the splayed structure in (b) showing branching and a thin shaft at the point of flexure of the barbs (arrow). Scale bars, 1 mm (a, b), 250 μm (c).
Extended Data Fig. 4
Extended Data Fig. 4. Integumentary structures of the cranial crest of MCT.R.1884.
a, Ventral part of the soft tissue crest separated from the occipital process (op) by a zone lacking soft tissue and showing only sediment (s). b, c, Detail of the basal part of the cranial crest showing dark brown structures at the base of the fibres (see arrows). d, Posterodorsal part of the cranial crest. e, f, Details of regions indicated in (d). The brown fibres of the soft tissue crest are oriented perpendicular to prominent wrinkles, expressed as variation in the topography of the specimen. Scale bars, 10 mm (a, d); 2 mm (b, c); 5 mm (e, f). op, occipital process; s, sediment; w, wrinkle.
Extended Data Fig. 5
Extended Data Fig. 5. Time-tree phylogeny of Avemetatarsalia, estimated using the ‘mbl’ branch-length estimation and reconstructed according to the ‘equal rates’ evolutionary model.
The likelihood values for model parameters are shown in Extended Data Table 2. The different categories of integumentary structures represent: scales, monofilaments, brush-like filaments, tufts of filaments joined basally, open pennaceous vane lacking secondary branching and closed pennaceous feathers comprising a rachis-like structure associated with lateral branches (see material and methods in the main text for more details). Tupandactylus silhouette by Evan Boucher from www.phylopic.org. Silhouettes of integumentary appendages are reproduced from ref. . (Fig. 3).
Extended Data Fig. 6
Extended Data Fig. 6. Time-tree phylogeny of Avemetatarsalia, estimated using the ‘mbl’ branch-length estimation and reconstructed according to the ‘SYM’ evolutionary model.
The likelihood values for model parameters are shown in Extended Data Table 2. The different categories of integumentary structures represent: scales, monofilaments, brush-like filaments, tufts of filaments joined basally, open pennaceous vane lacking secondary branching and closed pennaceous feathers comprising a rachis-like structure associated with lateral branches (see material and methods in the main text for more details). Tupandactylus silhouette by Evan Boucher from www.phylopic.org. Silhouettes of integumentary appendages are reproduced from ref. . (Fig. 3).
Extended Data Fig. 7
Extended Data Fig. 7. Time-tree phylogeny of Avemetatarsalia, estimated using the ‘mbl’ branch-length estimation and reconstructed according to the ‘all rates different’ (ARD) evolutionary model.
The likelihood values for model parameters are shown in Extended Data Table 2. The different categories of integumentary structures represent: scales, monofilaments, brush-like filaments, tufts of filaments joined basally, open pennaceous vane lacking secondary branching and closed pennaceous feathers comprising a rachis-like structure associated with lateral branches (see material and methods in the main text for more details). Tupandactylus silhouette by Evan Boucher from www.phylopic.org. Silhouettes of integumentary appendages are reproduced from ref. . (Fig. 3).
Extended Data Fig. 8
Extended Data Fig. 8. Scanning electron micrographs of melanosomes in the soft tissues of MCT.R.1884.
a–c, Elongate melanosomes from monofilaments. d–f, Ovoid melanosomes from the branched feathers. g–i, Ovoid melanosomes from the soft tissue crest (area 1, Extended Data Table 2). Scale bars, 2 μm.
Extended Data Fig. 9
Extended Data Fig. 9. Scatterplots of melanosome geometry in amniotes and ancestral-state estimation of the diversity of melanosome geometries within Avemetatarsalia.
a–d, Melanosome geometry in amniotes; data from refs. ,. and this study. a, Mammal hair (n = 1984). b, Squamate skin (n = 734). c, Pterosaur skin (this study, n = 2115; melanosomes imaged from ten independent samples; purple datapoints) and pterosaur feathers (n = 2173; orange datapoints, this study (n = 1284; melanosomes imaged from four independent samples); black and yellow datapoints, previous studies,). d, extinct and extant bird feathers (n = 3643). Data from non-avialan dinosaurs are not shown here. Polygon with dark grey shading in (a–d) shows the range of melanosome geometries known for extant and extinct bird feathers. Darker shades in (a) and (d) indicate more than one data point with similar measurements. e, Simplified time-tree phylogeny estimated using the ‘mbl’ branch-length estimation and reconstructed according to the best evolutionary model, i.e.‘equal rates’ (ER) model. The different categories (or ‘states’) of melanosome geometry are: one geometry (in black), two geometries (in red) and three geometries (in green). Only taxa for which melanosome length and aspect ratio was known have been included in our dataset (n = 20). *taxa showing spheroidal melanosomes in addition to any other category. Tupandactylus silhouette (in e) by Evan Boucher from www.phylopic.org.
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