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. 2017 Sep 13;284(1862):20170556.
doi: 10.1098/rspb.2017.0556.

Exceptional preservation and the fossil record of tetrapod integument

Affiliations

Exceptional preservation and the fossil record of tetrapod integument

Chad M Eliason et al. Proc Biol Sci. .

Abstract

The fossil record of exceptionally preserved soft tissues in Konservat-Lagerstätten provides rare yet significant insight into past behaviours and ecologies. Such deposits are known to occur in bursts rather than evenly through time, but reasons for this pattern and implications for the origins of novel structures remain unclear. Previous assessments of these records focused on marine environments preserving chemically heterogeneous tissues from across animals. Here, we investigate the preservation of skin and keratinous integumentary structures in land-dwelling vertebrates (tetrapods) through time, and in distinct terrestrial and marine depositional environments. We also evaluate previously proposed biotic and abiotic controls on the distribution of 143 tetrapod Konservat-Lagerstätten from the Permian to the Pleistocene in a multivariate framework. Gap analyses taking into account sampling intensity and distribution indicate that feathers probably evolved close to their first appearance in the fossil record. By contrast, hair and archosaur filaments are weakly sampled (five times less common than feathers), and their origins may significantly pre-date earliest known occurrences in the fossil record. This work suggests that among-integument variation in preservation can bias the reconstructed first origins of integumentary novelties and has implications for predicting where, and in what depositional environments, to expect further discoveries of exquisitely preserved tetrapod integument.

Keywords: Lagerstätten; feathers; hair; soft tissue preservation; taphonomy; terrestrial.

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Conflict of interest statement

We declare we have no competing interests.

Figures

Figure 1.
Figure 1.
Distribution of tetrapod Konservat-Lagerstätten through time and space (n = 143). (a) Numbers of Lagerstätten found in fluvial (light green), lacustrine (medium green), near-shore marine (blue) and other terrestrial depositional environments (dark green) are shown on the y-axis by period as well as epoch (for the Mesozoic and Cenozoic). For all statistical analyses, we used 10 My time bins after assessing the influence of time bin size on our statistical results (see electronic supplementary material, figure S7). (b) Global distribution of Lagerstätten found in different depositional environments. Pies show relative numbers in different depositional environments (colours of pie) and absolute number per country (size of pie). (c) Earliest skin impressions in Saurerpeton [49]. (d) Earliest putative filaments in Eudimorphodon rosenfeldi [50]. (e) Scales in the ornithischian dinosaur Kulindadromeus zabaikalicus [24]. (f) Earliest known feathers in Anchiornis huxleyi [51]. (g) Earliest preserved hair in Rugosodon eurasiaticus [52]. Image credits: (c) Smokeybjb (CC BY-SA 3.0), (d) Tommy from Arad (CC BY 2.0), (e) Tomopteryx (CC BY-SA 4.0), (f) Kumiko (CC BY-SA 2.0), (g) Zhe-Xi Luo (University of Chicago). (Online version in colour.)
Figure 2.
Figure 2.
Comparative time-series analysis of Lagerstätten preservation through time. Vertical panels show time series of palaeoenvironmental data and number of Lagerstätten for different (a) depositional environments and (b) integument types. Dendrograms show hierarchical clustering of time-series data with Euclidean distances on the x-axis (e.g. two variables directly connected by a short path indicate similar trends with time). Variables were scaled to have a standard deviation of unity prior to computing Euclidean distances and running a clustering analysis. Lagerstätten counts were integrated over 10 My bins (see electronic supplementary material. figure S1). Note that curves for climatic/tectonic variables are smoothed here to make it easier to visualize trends in the data, but unsmoothed per bin values were used in all statistical analyses. Sea level estimates are from composite of [31] and [32], as presented in [34]. Global terrestrial rock outcrop area is from [39]. Atmospheric CO2 data taken are from [36] and are an average of global proxies. See electronic supplementary material, figure S12 for units and more detailed information. (Online version in colour.)
Figure 3.
Figure 3.
The fossil record of integumentary innovations in tetrapods. Panels correspond to (a) filaments (light purple) and feathers (dark purple), (b) skin (pink) and scales (red) and (c) hair (brown). Grey polygons (secondary y-axis) show a proxy for tetrapod biodiversity (number of families) [40]. Age ranges for the earliest first appearances of an integumentary type based on gap analyses using three different methods [–47,54] are shown as horizontal bars: (a) method of [45,54]; (b) method of [46]; (c) method of [47]. Arrowheads represent 90% CIs for estimated earliest occurrence in the fossil record, vertical lines represent 50% CIs and dashed lines indicate uncertainty in these intervals estimated by Marshall [46] (see key). In some cases, lower bounds on the 90% CI estimated by Marshall [46] could not be calculated due to limited fossil data (indicated by missing arrowheads). For visualization purposes, cases where the lower bound of 90% CI extend beyond the x-axis range are indicated with grey arrowheads. Gap analyses were performed using the mean age range of individual Lagerstätten (see electronic supplementary material, table S7 for results using minimum and maximum of age ranges). Vertical dashed lines present early body or trace fossils as context for the integumentary records: in (a), archosauromorph Eorasaurus [55], 260 Ma; in (b), indet. stem tetrapod tracks, 397 Ma [56], reviewed in [57]; in (c), synapsid Eocasea martini, 315 Ma [58,59] and oldest known crown mammal, Megaconus mammaliaformis, 161 Ma [60]. Vertical dotted lines are molecular divergence estimates for (a) crown archosaurs (241 Ma), (b) tetrapods (344 Ma) [61] and (c) crown mammals (185 Ma) [62]. (Online version in colour.)

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