Feather-like development of Triassic diapsid skin appendages
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- Voigt, S., Buchwitz, M., Fischer, J. et al. Naturwissenschaften (2009) 96: 81. doi:10.1007/s00114-008-0453-1
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Of the recent sauropsid skin appendage types, only feathers develop from a cylindrical epidermal invagination, the follicle, and show hierarchical branching. Fossilized integuments of Mesozoic diapsids have been interpreted as follicular and potential feather homologues, an idea particularly controversially discussed for the elongate dorsal skin projections of the small diapsid Longisquama insignis from the Triassic of Kyrgyzstan. Based on new finds and their comparison with the type material, we show that Longisquama’s appendages consist of a single-branched internal frame enclosed by a flexible outer membrane. Not supporting a categorization either as feathers or as scales, our analysis demonstrates that the Longisquama appendages formed in a two-stage, feather-like developmental process, representing an unusual early example for the evolutionary plasticity of sauropsid integument.
KeywordsFossilized integumentSkin appendageFeather evo-devoLongisquama
The only skeletal specimen of the diapsid Longisquama insignis was discovered in lacustrine deposits of the Triassic Madygen Formation and described by A. G. Sharov in 1970. It features a series of seven elongated skin projections attached in fan-like arrangement along the animal’s back. These have been ambivalently assessed either as modified scales with corrugated surfaces (Sharov 1970; Reisz and Sues 2000; Prum 2001; Unwin and Benton 2001) or pennaceous feathers with outwardly fused barbs (Jones et al. 2000). Given their complexity and transitional state, the appendages attracted some attention when feathers and reptilian skin came into the focus of evolutionary developmental biology (e.g., Chuong et al. 2003; Wu et al. 2004). The unsolved status of the skin structures and the lack of a comprehensive description and reconstruction after Sharov’s initial approach have motivated our study and the search for further fossil evidence.
Here, we provide a detailed analysis of Longisquama’s appendages involving the type series and the recent finds. We are addressing crucial aspects of their structure, including their alleged high-level homology with avian feathers. Following the description, we are demonstrating how the complex morphology of the skin projections constrains feasible developmental scenarios and derive a model of development that we compare to feather morphogenesis. As functional and phylogenetic interpretations have been linked by some authors (Jones et al. 2000; Martin 2004), we discuss the appendage function briefly at the end.
Materials and methods
In addition to the holotype PIN 2584/4 (PIN for Palaeontological Institute of the Russian Academy of Sciences) and four specimens with fragmentarily preserved isolated appendages, representing the paratype series (PIN 2584/5–7, -9), we introduce three more specimens of the elongated skin projections: FG 596/V/1, -2, and -3 (FG for Geological Institute of the TU Bergakademie Freiberg) have been recovered at the Madygen type locality in southwest Kyrgyzstan during fieldwork in 2007.
In both lobes of the distal section, individual rugae of the slab and counter slab correspond in a convex–convex/concave–concave fashion, creating a series of more voluminous chambers and less voluminous interjacent zones. As noted by Reisz and Sues (2000), up to the distal end of the appendage, the rugae become narrower and more filigree mimicking barbs of a feather vane. In PIN 2584/5 (Fig. 1c–e), a fragmentary distal appendage of high fidelity, the middle axis forms a prominent roof-like ridge on the right slab and a deep furrow on the counter slab. The most striking feature of the distal section, preserved only in this specimen, is a series of about 20, up to 1.5-mm-long, spine-like impressions on the anterior lobe of the right slab. They root close to the middle axis and branch off obliquely (Fig. 1d, arrows). Corresponding structures on the counter slab are short, rounded impressions that run directly into the groove of the middle axis. We interpret them as the negative relief of rigid spines. If these were connected to the rod-like middle axis, they formed a single-branched internal frame. The insertion of the spines appears to be synchronous to the corrugation pattern, suggesting that the voluminous internal chambers and possibly intervening tissue enclosed them entirely in life.
The transition from the proximal to the distal section represents a major morphological changeover. For the specimen FG 596/V/1, covering both portions of an appendage, we measure the parameters curvature, total width, percentage of the anterior and posterior lobes, and tilting angle and density of the rugae in order to quantify the morphological change along the proximal–distal axis (Fig. 2b). These parameters are highly correlated and data points for the proximal and distal sections form distinct clusters (see electronic supplementary material S3). This is in agreement with a single switch-over in the development of a unidirectionally growing appendage. A characteristic feature related to the proximal–distal transition of the appendage is a narrow, slightly curved seam running from the posterior margin of the proximal section to the middle axis of the distal section, thereby crossing the rugae of the rear lobe (in PIN 2584/4–5, -7; FG 596/V/1, see Figs. 1a and 2a). This structure probably represents a breakage trail caused by the diagenetic compression of the appendage where it is transitional from a rather tubular, straight proximal to a flattened, increasingly curved distal section.
Subdivision of the proximal section into three lobes begins above a short, proximally tapering basis—a feature emphasized by Jones et al. (2000)—which appears to be attached right to the bone of the thoracal vertebral spines (in appendages no. 2–4 of PIN 2584/4). A slight convexity of the proximalmost section led to its interpretation as having a tubular shape (Jones et al. 2000; Reisz and Sues 2000; Prum 2001). This is in agreement with the proximally thicker sediment core in FG 596/V/1. Of the three longitudinal lobes in the proximal section, only the middle lobe, which accounts for 40–60% of the total width, bears a relief of rugae and deeper encarved interstices. Our analysis shows that the proximal rugae vary considerably in appearance: They are square-edged with a parallelepiped outline and merlon-like arranged in FG 596/V/1 (Fig. 1b), but roundish convex folds are found in PIN 2584/4 and PIN 2584/6, described by Sharov (1970) as “rosary-bead-like.” In all specimens, the long axes of the rugae are dipping caudoventrally transversal to the trend of the proximal–distal axis. The rugae run in and overlap with an anterior and posterior longitudinal bar forming, a latter-like pattern. This complex relief of the middle lobe occurs mirror-inverted on the left and right sides of the proximal section—rugae and interstices are synchronously arranged in a convex–convex/concave–concave fashion as in the distal section (Fig. 2c). The relief of the proximal section varies in distinctness, probably affected by the preservation of a smooth outer lamella. That such an envelope exists has been suggested by Jones et al. (2000) for the third appendage of the holotype in which a proximal cover layer with shallow relief only flimsily reproduces the topography of the underlying tripartite structure.
Following our description, Longisquama’s appendages possess several anatomical features that do not occur in recent elongate reptilian scales but are reminiscent of avian feathers and their developmental stages: (1) a proximal–distal differentiation with a single major morphological transition, (2) distinctive internal and external structures, (3) a complex internal organization with voluminous chambers and a branched frame in the distal section, and (4) a high length/proximal width ratio—up to 50 in FG 596/V/1. Thus, we are interpreting aspects of the appendage development in analogy to that of feathers (as characterized by Lucas and Stettenheim 1972; Widelitz et al. 2003; Yu et al. 2004): Their growth was unidirectional, requiring a clearly defined zone of cell proliferation. The appendages descended from a multilayered epidermal collar whose differentiation governed the shaping of the complex appendage topography. A switch from distal to proximal section marks the succession of distinct developmental phases analogous to the transition from feather vane to calamus. Furthermore, the deep anchoring and the probable tubular nature of the proximal section, also described by Jones et al. (2000), Reisz and Sues (2000), and Prum (2001), may be indicative for derivation from a cylindrical epidermal invagination, i.e., a follicle (Jones et al. 2000; Martin 2004). However, a cylindrical organization also occurs in nonfollicular appendages, such as the dorsal frill scales of recent iguanids (Wu et al. 2004).
Remaining discrepancies, in particular the flexible enveloping membrane and the lateral position of the middle axis, demonstrate the phylogenetic distance of Longisquama’s appendages to avian feathers. Considering the occurrence of derived and possibly follicular skin appendages in some archosaur groups, which are only distantly related to birds (Ji and Yuan 2002; Wang et al. 2002; Mayr et al. 2002), and the uncertain archosaurian relationship of Longisquama (as discussed by Unwin et al. 2000; Senter 2004), we agree with others that the dorsal appendages are unlikely to be homologous with avian feathers (Reisz and Sues 2000; Unwin and Benton 2001; Prum 2001; Prum and Brush 2002). The question of whether the convergent acquisition of a certain morphological feature, such as a tubular basis or branching, is sufficient to call the structures “feathers” has been raised and answered in the negative (Chuong et al. 2003). In agreement with Prum and Brush (2002), we advocate the restriction of the term “feather” to skin derivates regarded as homologous with avian feathers at least on the level of the feather follicle. Distinct from both, feathers and scales, Longisquama’s highly derived skin projections exemplify the plurality of sauropsid integument evolution.
This work was supported by the German Research Foundation (DFG II - VO 1466/1–1) and by the Society of Vertebrate Paleontology (Patterson Memorial Grant to JF). We are thankful to Evgenii N. Kurochkin and Vladimir R. Alifanov for access to the type material in Moscow in February 2007, to Susan Turner and Jörg W. Schneider for suggestions and comments, and to Ilja Kogan for his help with the translation of Russian publications and reports.