Fossils are the preserved remains of animals, plants or other organisms. The most highly prized fossils are those that retain their original three-dimensional shape and provide details needed to identify what species it represents, and what its closest living relatives might be. However, even fossils with the most beautifully preserved external anatomy can lack the internal structures that also help to identify its evolutionary history. “Mineralized” fossils are particularly useful for researchers as they form in a process that helps to preserve the internal anatomy of the organism. This type of fossil forms when mineral-laden water surrounds an organism’s body so that the minerals are deposited in its cells and turn soft tissues to stone.

In the 1940s, Swiss scientist Eduard Handschin used eight mineralized fossil specimens to describe a 25-40 million-year-old beetle species called Onthophilus intermedius. On the basis of the external anatomy of the two best-preserved specimens, Handschin claimed this species was distinct from, but closely related to a beetle species called O. striatus that is found in Europe today.

Since then, fossil examination methods have greatly advanced and include three-dimensional X-ray based imaging techniques that reveal the internal structures of a fossil while leaving it intact. One such technique is called X-ray computed tomography, in which numerous X-ray images of a solid object are taken from different angles. These images are then reassembled using computer software to create a virtual three-dimensional model of the object.

Here, Schwermann et al. used this X-ray technique to re-examine the beetle fossils originally reported by Handschin. This analysis revealed many new details of these specimens’ external and internal anatomies, including their gut, genitals and airways. These new insights place Onthophilus intermedius into a different evolutionary lineage to O. striatus. They also suggest that mineralized fossils could provide a rich source of data for studies on fossil insects and other arthropods, even if they appear to be poorly preserved on the outside.

An organism’s morphology represents a complex solution to myriad ecological and environmental challenges it and its ancestors have confronted over evolutionary time. Inferring a comprehensive evolutionary history of a lineage requires consideration of a wide range of morphological features, and how they may have been shaped by selection, drift, and developmental constraints. While external characters predominate in ecomorphological and systematic studies, internal characters also play critical roles (Perreau and Tafforeau, 2011). In fossil specimens, however, these characters are usually not preserved or difficult to access (Siveter et al., 2007). While combined phylogenetic analyses of extant species frequently utilize internal anatomy, analyses including fossil taxa are generally limited to external characters. Moreover, it is often difficult to distinguish whether unobserved morphological characters were originally absent or lost due to taphonomic processes, potentially leading to misinterpretations of character evolution and erroneous phylogenetic placements (Sansom, 2015).

Several types of preservation or certain combinations of them are known for arthropod fossils. These are adpressions (compressions or impressions) (Wedmann et al., 2007; 2011), casts, voids, embeddings, mineral replications, charcoalified remains, or inclusions in amber (Grimaldi et al., 1994; Martı́nez-Delclòs et al., 2004; Grimaldi and Engel, 2005; Dunlop and Garwood 2014; Penney and Jepson, 2014). Amber inclusions are famous for exquisitely preserving three-dimensional external shape and sometimes internal characters (Perreau and Tafforeau, 2011). Three-dimensional arthropods may also be preserved within concretions (e.g. in siderite nodules [Nitecki, 1979; Garwood et al., 2009]), calcareous incrustations (e.g. in travertine [Rosendahl et al., 2013]), encapsulations in minerals (e.g. in onyx-marble [Pierce, 1951], chert [Anderson and Trewin, 2003], or gypsum crystals [Schlüter et al., 2003]), and mineral replications (e.g. as calcite [McCobb et al., 1998], silica [Miller and Lubkin, 2001], goethite [Grimaldi, 2009; Barling et al., 2014], pyrite [Grimaldi and Engel, 2005], or phosphate [Duncan and Briggs, 1996; Hellmund and Hellmund, 1996; Waloszek, 2003]). Some of these preservation types have revealed surprisingly detailed insights into the internal and soft tissue anatomy of several arthropods, for instance from several Paleozoic marine deposits (e.g. Siveter et al., 2007; 2013; 2014; Ma et al., 2014; Cong et al., 2014; Edgecombe et al., 2015). For insects, e.g. eyes (Duncan and Briggs, 1996) and muscle fibers (Grimaldi, 2009) have been reported.

Abundant arthropod fossils preserved by mineralization of calcium phosphate are known from the Oligocene fissure fillings of Ronheim (Hellmund and Hellmund, 1996), the Late Oligocene/Early Miocene limestones of Riversleigh (QLD, Australia) (Duncan and Briggs, 1996) and from Paleogene deposits at Quercy (south-central France) (Filhol, 1877; Gervais, 1877; Flach, 1890; Thévenin, 1903; Handschin, 1944). These localities have long been famous for their rich vertebrate fossils as well (e.g. Legendre et al., 1997; Laloy et al., 2013). The arthropod fossils of Quercy were documented by Swiss entomologist Eduard Handschin (1944). He described the hister beetle Onthophilus intermedius (Coleoptera: Histeridae) from eight specimens, and considered it distinct but closely related to the extant European species O. striatus (Forster, 1771). The description, however, was vague and based mainly on the external morphology of the two best-preserved specimens (Handschin, 1944).

X-ray microtomography has become established for the detailed examination of both extant (e.g. Betz et al., 2007; Bosselaers et al., 2010; van de Kamp et al., 2011; 2014; 2015; Brehm et al., 2015; Sombke et al., 2015) and extinct (Sutton, 2008; Sutton et al., 2014) arthropods, including fossils preserved in amber (Lak et al., 2009; Pohl et al., 2010; Soriano et al., 2010; Perreau and Tafforeau, 2011; Riedel et al., 2012). We explored the application of this technique to mineralized fossils by re-examination of Handschin's specimens of Onthophilus intermedius. To ensure a direct morphological comparison, we performed tomographic scans (Figure 1) of ethanol-fixed and air-dried O. striatus using the same experimental setup. Furthermore we tested the hypothesis that the two are closely related with a global phylogenetic analysis of Onthophilus Leach, 1817.

Figure 1

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We found internal characters in all fossils (Table 1). Three specimens show remains of inner organs, especially of the sclerotized genitalia, allowing their identification as two males and one female. The outer surfaces of most specimens appear smooth (Figure 2); the distinct punctuation found in extant Onthophilus species (Kovarik and Caterino, 2005) is faint.

Figure 2

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The specimen F1994 (Figures 1A,D,G, 2, 3, Supplementary file 1) differs from all other samples by the presence of a stony matrix, covering the ventral part of the beetle. Its dorsal part and head are exposed; the elytra are missing and were probably detached before embedding. The exposed surface is partly eroded, especially in the anterior region of the head, and no appendages are visible from the outside. The matrix, however, concealed the best-preserved fossil from the collection, which we examine here in detail.

Figure 3

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The ventral portion of the beetle covered by the matrix reveals an extraordinary preservation of exoskeletal fine structures and internal anatomy (Figures 3, 4 and 5; Supplementary file 1). While some fractions of the cuticle appear to be mineralized, the latter is mostly represented by air-filled spaces in the fossil (Figure 1A,D,G). The surface of the exoskeleton is preserved as a three-dimensional imprint of remarkable detail; the body sclerites show characteristic punctuation of the genus. The right foreleg is not preserved; the left one is truncated from the trochanter; distal parts of the leg were lost prior to fossilization. The right mid and hind legs are eroded at the edge of the matrix, but their encrusted left counterparts appear complete except for the most distal part of the metafemur of the hind leg that would protrude from the matrix. Moreover, many anatomical characters can be recognized inside the fossil (Figure 3D). Apart from internal invaginations of the exoskeleton (e.g. tentorium, furcal arms and metendosternite), large parts of the alimentary canal and tracheal system are visible. The oesophagus appears to be shrunken and is connected to the crop, which is truncated posteriorly. The anterior part of the hindgut is hollow, while the middle part is apparently filled with mineral matrix but well-defined. Conspicuous spherical particles may constitute remnants of gut content (Figure 1G). The hindmost part of the gut can be roughly retraced by aggregations of tiny holes inside the mineral matrix. Like in the alimentary canal, some large tracheae appear to be filled with matrix, while others are hollow. Except for the musculature connecting the right pro- and mesofurcal arms (Figure 1D), most muscles can only be recognized by remnants at the insertion areas (Figure 1G). The genitals are extraordinary well-preserved (Figure 3F). While testes and Ductus ejaculatorius could not be recognized, other soft tissues such as the spiral accessory glands and parts of the gland ducts are conspicuous. The genital sclerites, including aedeagus, median lobe, gonopore, tergites 8-10 and sternites 8 & 9 are almost perfectly preserved as imprints.

Figure 4

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Figure 5

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The remarkable preservation state of the fossil is emphasized when its morphological characters are compared to those of an extant ethanol-fixed specimen of the same genus (Figures 1, 3E,F and 4). The new anatomical data from this specimen facilitated an extended description of the species according to modern taxonomic standards (Appendix 1).

Handschin (1944) hypothesized a close relationship (‘particularly striking similarity’) between Onthophilus intermedius and O. striatus based on then-observable external morphology. However, phylogenetic analysis (Material and methods) of the more diverse character set now accessible places these species in distinct clades. The analysis resulted in 72 most parsimonious trees of length 185 (CI 0.27, RI 0.61). The strict consensus of these trees (Figure 6) is well resolved apart from a few rearrangements of some outgroup taxa and within a relatively derived group related to O. niponensis Lewis, 1907. O. intermedius is part of a trichotomy involving O. silvae Lewis, 1884 and a large group of species descended from the common ancestor of O. giganteus Heleva, 1978 and O. niponensis, though in reweighted trees it is resolved as sister to O. silvae alone. In all analyses O. striatus is nested within a lineage of Nearctic and far-eastern Palaearctic species, including O. flavicornis Lewis, 1884, O. flohri Lewis, 1888 and others.

Figure 6

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Inclusion of diverse characters revealed by microtomography of Onthophilus intermedius yields a well-supported topology and a more comprehensive picture of the biogeographic and morphological history of the group. Of the characters scored for both O. intermedius and O. striatus, there are seven by which their states differ, three external and four internal. Of these, two external (chars. 29 & 30) and one internal (char. 36) are reconstructed as autapomorphies (Figure 6). Only one external synapomorphy (char. 22) separates them, while three of the four genitalic differences (chars. 35, 40, and 41) represent synapomorphies of their respective lineages. Exclusion of internal characters for O. intermedius did not affect the topology, but did prevent genitalic characters from supporting its larger containing clade. Critical diagnostic differences in external morphology, such as mesoventral proportions and pygidial sculpturing, were also revealed by visualization of features previously obscured by matrix.

Based on our examinations we can reconstruct the probable fossilization process of the Quercy Onthophilus specimens, which culminates in a partial mineralization of inner organs in combination with the cuticle preserved as voids. An accurate three-dimensional conservation of soft tissues does not occur if the specimens are dried in air (Figure 1C,F,I). Therefore, the fixation process must have occurred fast, possibly due to the animal being immediately penetrated and enclosed by phosphate rich water. In arthropods, this type of fossilization is only known from a handful of localities, which are better known for a rich vertebrate fauna (Riversleigh: Duncan and Briggs, 1996; Ronheim: Hellmund and Hellmund, 1996; Quercy: Handschin, 1944). Replication of soft tissues by phosphatization may be accomplished over a period of weeks (Martı́nez-Delclòs et al., 2004). Possible sources for high phosphorous concentrations in water circulating through the fissure fill are rocks or abundant phosphate-rich vertebrate bones, which may have been deposited along with them (Handschin, 1944; Hellmund and Hellmund, 1996). After encrustation and internal mineralization, the cuticle largely decayed, leaving air-filled spaces. Erosion processes probably removed the outer stony matrix of most specimens, including fragile appendages and the imprint of the outer surface of the exoskeleton, leaving a mineralized endocast. Thus, the exterior of the fossils merely represents the inner surface of the exoskeleton – the deep grooves (Figure 2) actually being inner folds or apophyses. While the smooth dorsal part of F1994 resembles the other fossils in appearance, its ventral surface covered by the mineral matrix shows a distinct surface sculpturing as present in extant species of the genus. In contrast, an artificial ‘digital endocast’ created from the tomographic data of F1994 (Material and methods) bears a striking resemblance to the other fossils (Figure 5), on which Handschin based his original description. Summing up, the Quercy hister beetles represent three-dimensional ‘hybrid’ fossils, comprising cuticle imprints and mineralized soft tissue, combining to preserve both exoskeletal fine structure and internal anatomical characters.

Fissure filling fossils preserving three-dimensional internal anatomy will help to overcome taphonomic biases in available fossil data (Allison and Bottjer, 2011). To date, fossilized insect internal character information has mainly been obtained from well-preserved amber inclusions (e.g. Pohl, et al., 2010; Perreau and Tafforeau, 2011). However, the origination of amber as tree resin causes a representational bias toward generally arboreal taxa (Martı́nez-Delclòs et al., 2004). The fossil arthropods of Quercy represent an assemblage of taxa more typically associated with forest floor communities (Handschin, 1944), as exemplified by Onthophilus, typically a predator in various decaying organic materials (Kovarik and Caterino, 2005; Bajerlein et al., 2011). Such communities are less commonly preserved than those of many other environments (Kidwell and Flessa, 1996). Beyond anatomical data on these species, clearer interpretations of evolutionary relationships of these fossils will improve inferences about the evolution of these ecological communities. Thus, reexamination of the Quercy fossils, and likely also of similar mineralized fossils from other localities (which may represent different ecosystems and/or time periods), may provide a highly complementary source of information on the evolutionary history of arthropods.

With regard to the methods employed here, we can offer some guidance on improving future imaging attempts on similar materials. Based on our experience, a fast tomography setup combining filtered polychromatic radiation and an optimized detector system (dos Santos Rolo et al., 2014) is well-suited to achieve sufficient image quality in most fossil specimens. Thus, scan duration per tomogram may be reduced to a couple of seconds (Material and methods), facilitating high-throughput screening of large sample numbers in short time.

Our results demonstrate that mineralized arthropod fossils from a sedimentary context may three-dimensionally preserve soft tissue and other internal anatomical characters in remarkable detail, which allows determinations and phylogenetic analyses according to the standards for Recent organisms. Reevaluation of relationships with modern taxa in this extended morphological context will substantially improve estimates of rates and modes of arthropod evolution. This exceptionally detailed preservation may be aided by the presence of a surrounding stony matrix, hinting that encrusted specimens, which therefore were originally considered to be of poor quality, could contain particularly well-preserved external and internal characters. Our findings may trigger the reinvestigation of numerous similar fossils from various localities.

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Author details

1. Achim H Schwermann

   Steinmann Institute for Geology, Mineralogy and Paleontology, University of Bonn, Bonn, Germany

   Contribution

   AHS, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   For correspondence

   achim.schwermann@uni-bonn.de

   Competing interests

   The authors declare that no competing interests exist.

2. Tomy dos Santos Rolo

   ANKA/Institute for Photon Science and Synchrotron Radiation, Karlsruhe Institute of Technology, Eggenstein-Leopoldshafen, Germany

   Contribution

   TdSR, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

3. Michael S Caterino

   Department of Agricultural and Environmental Sciences, Clemson University, Clemson, United States

   Contribution

   MSC, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

4. Günter Bechly

   State Museum of Natural History Stuttgart, Stuttgart, Germany

   Contribution

   GB, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

5. Heiko Schmied

   Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, Germany

   Contribution

   HS, Conception and design, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

6. Tilo Baumbach

   1. ANKA/Institute for Photon Science and Synchrotron Radiation, Karlsruhe Institute of Technology, Eggenstein-Leopoldshafen, Germany
   2. Laboratory for Applications of Synchrotron Radiation, Karlsruhe Institute of Technology, Karlsruhe, Germany

   Contribution

   TB, Acquisition of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

7. Thomas van de Kamp

   1. ANKA/Institute for Photon Science and Synchrotron Radiation, Karlsruhe Institute of Technology, Eggenstein-Leopoldshafen, Germany
   2. Laboratory for Applications of Synchrotron Radiation, Karlsruhe Institute of Technology, Karlsruhe, Germany

   Contribution

   TvdK, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   For correspondence

   thomas.vandekamp@kit.edu

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0001-7390-1318

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