The first dinosaur egg from the Lower Cretaceous of ...

Historical Biology An International Journal of Paleobiology

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The first dinosaur egg from the Lower Cretaceous of Western Siberia, Russia Pavel P. Skutschas, Valentina D. Markova, Elizaveta A. Boitsova, Sergey V. Leshchinskiy, Stepan V. Ivantsov, Evgeny N. Maschenko & Alexander O. Averianov To cite this article: Pavel P. Skutschas, Valentina D. Markova, Elizaveta A. Boitsova, Sergey V. Leshchinskiy, Stepan V. Ivantsov, Evgeny N. Maschenko & Alexander O. Averianov (2017): The first dinosaur egg from the Lower Cretaceous of Western Siberia, Russia, Historical Biology, DOI: 10.1080/08912963.2017.1396322 To link to this article: http://dx.doi.org/10.1080/08912963.2017.1396322

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Date: 06 November 2017, At: 00:47

Historical Biology, 2017 https://doi.org/10.1080/08912963.2017.1396322

The first dinosaur egg from the Lower Cretaceous of Western Siberia, Russia Pavel P. Skutschasa,b , Valentina D. Markovac, Elizaveta A. Boitsovaa, Sergey V. Leshchinskiyb, Stepan V. Ivantsovb, Evgeny N. Maschenkod and Alexander O. Averianovb,e,f a

Faculty of Biology, Department of Vertebrate Zoology, Saint Petersburg State University, Saint Petersburg, Russia; bLaboratory of Mesozoic and Cenozoic Continental Ecosystems, Tomsk State University, Tomsk, Russia; cSaint Petersburg City Palace of Youth Creativity, Saint Petersburg, Russia; dBorissiak Paleontological Institute of the Russian Academy of Sciences, Moscow, Russia; eZoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia; fInstitute of Geology and Petroleum Technology, Kazan Federal University, Kazan, Russia

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ABSTRACT

The Lower Cretaceous Ilek Formation in Western Siberia (Russia) has yielded various vertebrate fossils, including skeletal remains of dinosaurs. Here we report on a fragmentary theropod egg from the vertebrate locality Shestakovo 3 of the Ilek Formation in Kemerovo Province. We assign the specimen to the oogenus Prismatoolithus (oofamily Prismatoolithidae) as Prismatoolithus ilekensis oosp. nov., on the basis of the following unique combination of characters: ovoid-shaped egg; thin eggshell 300–330 μm thick; angustiprismatic morphotype; eggshell with three different layers; gradual transition between mammillary layer and prismatic layer; abrupt contact between prismatic layer and external layer; mammillary layer to prismatic layer to external layer thickness ratio is 1:3:0.6; prismatic layer with ill-defined squamatic texture; angusticanaliculate pore system; and smooth outer surface. Like other Early Creataceous Prismatoolithus, the egg of Prismatoolithus ilekensis oosp. nov. was laid by a small bodied theropod dinosaur (troodontid or primitive bird) and this taxonomic attribution is supported by results of our phylogenetic analysis. Prismatoolithus ilekensis oosp. nov. is the first Early Cretaceous ootaxon from Russia.

ARTICLE HISTORY

Received 4 July 2017 Accepted 20 October 2017 KEYWORDS

Fossil eggs; Theropoda; Early Cretaceous; Ilek Formation; Russia

http://zoobank.org/urn:lsid:zoobank.org:act:734EAD40-86C3-488B-A61E-B5FF7378BC0E

Introduction The continental Lower Cretaceous Ilek Formation is widely distributed in Western Siberia, (Russia) and vertebrate localities of this geological unit yield a variety of vertebrate fossils, including dinosaur bone remains (Alifanov et al. 1999; Leshchinskiy et al. 2001, 2003; Averianov et al. 2006; Averianov and Lopatin 2015). Among vertebrate localities of Ilek Formation, the Shestakovo 3 locality in Kemerovo Province (Figure 1) is famous by findings of numerous articulated skeletons of primitive ceratopsian Psittacosaurus sibiricus (Averianov et al. 2006; Lopatin et al. 2015). The other non-avian dinosaurs from Shestakovo 3 are troodontids represented by rare partially articulated and isolated bones (Alifanov et al. 1999) and large tetanuran theropods known by isolated teeth (pers. obs.). Additionally to non-avian dinosaurs, the confuciornithiform-like bird Evgenavis nobilis was described from Shestakovo 3 on the basis of an isolated tarsometatarsus (O’Connor et al. 2014). In August of 2008, a partial fossil egg was found by one of us (ENM) during excavations of the Tomsk State University on the Shestakovo 3 locality. Mesozoic fossil eggs (including dinosaur eggs) were previously unreported from the Lower Cretaceous deposits of Russia. The previous findings of dinosaur eggshells in Russia were made only at the Late Cretaceous Kakanaut locality in Chukotka, northeastern Russia (Godefroit et al. 2009).

Here, we describe this fossil egg from the Shestakovo 3 locality, wich also represents the first report of fossil egg from the Early Cretaceous of Russia. Institutional Abbreviations. LMCCE, Laboratory of Mesozoic and Cenozoic Continental Ecosystems, Tomsk State University, Tomsk, Russia.

Geological setting and associated vertebrate assemblage The partial egg was found in the deposits of the Lower Cretaceous Ilek Formation exposed at the Shestakovo 3 locality, Kemerovo Province, Western Siberia, Russia (Figure 1). The stratigraphic section of this locality is divided into six layers (Figure 2): Layer 1: Fine to medium-grained greenish-grey sand with cross-bedded laminated and fine-lenticular structure. The top of the layer is laminated horizontally and it is composed of unsorted sand with numerous light-grey flow silt pebbles and carbonate concretions. In addition, thin laminas of greenish-brown sandy clay occur rarely in the layer top. The interlayer of poorly lithified fine-grained sandstone with variable thickness (0–0.2 m) is present just below the bedding surface. The visible thickness of the layer is more than 0.7 m. The bedding surface is slightly undulate. The layer demonstrates the regular bedding with the deposits of the Layer 2.

CONTACT Pavel P. Skutschas [email protected], [email protected] Supplemental data for this article can be accessed https://doi.org/10.1080/08912963.2017.1396322 © 2017 Informa UK Limited, trading as Taylor & Francis Group


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P. P. SKUTSCHAS ET AL.

Figure 1. Map showing the position of the Shestakovo 3 and other vertebrate localities of the Lower Cretaceous Ilek Formation in Russia (A) and in Kemerovo Province, Western Siberia (B). (A). 1 – Shestakovo 1; 2 – Shestakovo 2; 3 – Shestakovo 3; 4 – Smolenskii Yar; 5 – Ust’-Kolba.

Layer 2: Fine-grained blueish-grey sand with a fine wavy lamination. Thin laminas and interlayers (up to 7 cm) of greenish-brown sandy clay with numerous carbonate concretions (up to 9 × 7 × 4 cm) occur often. The layer contains the vertebrate remains, including isolated skulls, skeletal parts in anatomical association and complete skeletons (e.g. Averianov et al. 2006). A thickness of the layer depends on the position of the upper bedding surface and may change from 0.3 to 1 m. The bedding surface is uneven with obvious signs of erosion. Layer 3: Deposits of the complicated genesis composed of the mixture of reddish-brown clay (more than 70%) and fine-grained blueish-grey sand (less than 30%). The layer contains a numerous unrounded carbonate concretions (from 1 mm to 7 cm in diameter) with a tuberculous surface. The absence of material sorting, deformed lamina, capturing and dragging blocks of the underlying deposits reflect the post-depositional changes, possibly, subaqueous landslide. Deformed mudcracks (from 0.1 to 0.5 m deep and up to 3 cm wide), filled with medium-grained bluish-grey sand, and numerous plant root marks are observed in reddish-brown clay of the middle and top parts of the layer. The superface of layer is marked by small lenses (from 0.25 to

0.8 m long and 5 to 15 cm thickness) formed by thin-laminated (1–20 mm) blueish-grey sand and silt, reddish-brown and brickred sandy clay. These lenses filled depressions on the bottom of paleobasin, and occur periodically. The distance between the centers of lenses is from 0.4 to 2 m). The deposits comprise the vertebrate remains (including skulls, skeletons and their fragments, e.g. Lopatin et al. 2015) and coprolites. The thickness of the layer is very variable (1–1.8 m), due to the position of subface of layer. The deposits of the layer were probably covered by non-depositional hiatus. The studied egg LMCCE 4/6 was found in this layer. Layer 4: Horizontally laminated brick-red clay with rare laminas of pinkish-brown and chocolate colored clay, and blueish-grey silt. The thickness of laminas varies from 1 to 30 mm. The thickness of the layer is around 0.8 to 1 m. Deposits lay horizontally and they are continuous along the strike and conformably covered by the deposits of the Layer 5. Layer 5: Horizontally laminated blueish-grey silt and finegrained sand with interbeds and laminas of reddish-brown clay are continuous along the strike. The thickness of interlayers and laminas is from 5 mm to 5 cm. The deposits contain the vertebrate remains (including skeleton fragments). The thickness of the layer varies from 0.8 to 2 m and more. The layer superface position is considerably uneven and indistinct. Layer 6: Deposits are similar in composition, structure and genesis to that of the Layer 3. The layer contains the vertebrate remains (including skulls and skeleton fragments). The visible thickness of the layer is more than 1.5 m. Above the Cretaceous section there is Quaternary–Holocene colluvial sediments and soil. The visible thickness of this member is more than 0.6 m. The Ilek Formation was deposited under continental environments in the fluvial-lacustrine semi-desert plain (Nesterov 1976). The dating of the Shestakovo 3 locality within the Lower Cretaceous remains controversial: it has been dated as Berriasian (Alifanov et al. 1999), Aptian–Albian (Averianov et al. 2006), and Barremian–Aptian (Kurochkin et al. 2011) based on vertebrates.

Material and methods Two eggshell fragments were removed from the central part of the fossil egg LMCCE 4/6 from Shestakovo 3 for preparing of standard petrographic thin sections and studied under normal and polarized light using an optical microscope (Leica 4500, Leica Microsystems, Wetzlar, Germany) in the ‘Geomodel’ Research Center at the Saint Petersburg State University, Saint Petersburg (Russia). Additionally, two fragments (original positions within the egg are unknown) were examined and photographed using the scanning electron microscope Hitachi S-3400 N in the ‘Geomodel’ Research Center. Eggshells were identified in terms of parataxonomy, following Mikhailov et al. (1996) and Mikhailov (1997). The partial egg LMCCE 4/6 from Shestakovo 3 is housed in Laboratory of Mesozoic and Cenozoic Continental Ecosystems, Tomsk State University, Tomsk, Russia, while the thin-sections used in study are housed in the histological collection of the Department of Vertebrate Zoology of Saint Petersburg State University, Saint Petersburg (Russia).


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Figure 2. The lithological section of the deposits of Ilek Formation at Shestakovo 3 locality. (A) Picture of the outcrop with interpretation. (B) Drawing of the lithological section. Sedimentary structures: a – red-brown clay; b – deposits of the complex genesis composed of the mixture of reddish-brown clay (more than 70%) and fine-grained blueish-grey sand; c – blueish-grey silt and fine-grained sand; d – fine-grained blueish-grey sand; e – fine-to medium-grained light greenish-grey sand. Sedimentary textures: f – parallel lamination; g – wavy lamination; h – fine-lenticular texture; i – cross-bedded lamination; j – disturbed relics of layers; k – post-sedimental textures; l – pebbles of silt; m – carbonate concretions; n – ichnofossils; o – vertebrate remains; partial egg.

Systematic paleontology Oofamily PRISMATOOLITHIDAE Hirsch, 1994 Oogenus PRISMATOOLITHUS Zhao and Li, 1993 sensu Zelenitsky and Hills, 1996 Type oospecies. Prismatoolithus gebiensis Zhao and Li, 1993; Djadokhta Formation (Upper Cretaceous); Bayan Mandahu, Inner Mongolia, China. Referred oospecies. P. gebiensis Zhao and Li, 1993, P. matellensis Vianey-Liaud and Crochet, 1993, P. tenuis Vianey-Liaud and Crochet, 1993, P. levis Zelenitsky and Hills, 1996, P. hanshuiensis Zhou et al., 1998, P. jenseni Bray, 1999, P. caboti Garcia et al., 2000, P. hukouensis Zhao, 2000, P. heyuanensis Lü et al., 2006, P. hirschi Jackson and Varricchio, 2010, P. tiantaiensis Wang et al., 2011 and P. trempii Sellés et al., 2014. PRISMATOOLITHUS ILEKENSIS oosp. nov. Holotype. LMCCE 4/6, partial egg. Type Locality and Horizon. Shestakovo 3, approximately 40 km south of Mariinsk City, Chebula District, Kemerovo Province, Russia; Ilek Formation, Lower Cretaceous. Etymology. In reference to the Ilek Formation where the holotype was found. Diagnosis. Prismatoolithid egg characterized by the following combination of characters: ovoid-shaped egg; thin eggshell

300–330 μm thick; angustiprismatic morphotype; eggshell with three structural layers; gradual transition between mammillary layer and prismatic layer; abrupt contact between prismatic layer and external layer; the mammillary layer to prismatic layer to external layer thickness ratio is 1:3:0.6; prismatic layer with ill-defined squamatic texture; angusticanaliculate pore system; and smooth outer surface.

Description An incomplete egg LMCCE 4/6 (Figure 3) from the Shestakovo 3 locality measures about 2 cm wide. According to the preserved portion, the LMCCE 4/6 was ovoid-shaped, presumably slightly asymmetric, with estimated length about 3.5–4 cm. Eggshell thickness ranges between 300 and 330 μm. The outer surface is smooth. The eggshell unit has a broad columnar shape with three distinct structural layers: mammillary, prismatic and external (Figures 4 and 5). The prisms are visible throughout the prismatic and external layers. The prisms in the prismatic layer have ill-defined squamatic texture. The eggshell displays a columnar extinction pattern under polarized light. The transition between mammillary and prismatic layers is gradual, while external layer is separated from prismatic layer by a distinct line (so the eggshell

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Figure 3. Holotype (LMCCE 4/6) of Prismatoolithus ilekensis oosp. nov. (A), (B) Partial egg in clay block.

Figure 4. Eggshell of Prismatoolithus ilekensis oosp. nov. (A), (B) Radial thin sections of eggshell under normal light, showing the boundary between the mammillary layer and prismatic layer (black bar) and abrupt contact between prismatic layer and external layer (arrow). Note numerous continuous horizontal growth lines in the prismatic layer. (C) Radial thin section of eggshell under polarized light, showing a columnar extinction pattern. Abbreviations: el – external layer, ml – mammillary layer, pl – prismatic layer.

of LMCCE 4/6 displays partial detachment of the external layer). The mammillary layer to prismatic layer thickness ratio is about 1:3. The mammillary layer is formed of wedge-like crystals of calcite that radiate from the base of the shell units. The mammillary cones are relatively broad (50–70 μm) and barrel-shaped. The numerous continuous horizontal growth lines are present in the inner part of the prismatic layer. The straight pore canals are very narrow, sparse and widely spaced (= angusticanaliculate pore system).

Comparison The new oospecies from Shestakovo 3 shares with prismatoolithid eggs (oogenera Preprismatoolithus Hirsch, 1994, Prismatoolithus Zhao and Li, 1993, Protoceratopsidovum Mikhailov, 1994, Spheruprismatoolithus Bray, 1999, Sankofa López-Martínez and Vicens, 2012, and Trigonoolithus Moreno-Azanza et al., 2014) the presence of columnar shape of shell units, the presence of continuous horizontal growth lines, the gradual transition between mammillary and prismatic layers (Hirsch 1994; Zelenitsky and

Hills 1996; Moreno-Azanza et al. 2014) and can be placed within the oofamily Prismatoolithidae Hirsch, 1994. The described material on the new oospecies resembles in important details (smooth outer surface, angustiprismatic morphotype, and angusticanaliculate pore system) those of Prismatoolithus Zhao and Li, 1993 (Vianey-Liaud and López-Martínez, 1997; Jackson and Varricchio 2010; Sellés et al. 2014) and, thus, can be assigned to this oogenus. Additionally, the new oospecies from Shestakovo 3 significantly differs from Spheruprismatoolithus and Sankofa in the mammillary layer to prismatic layer thickness ratio (1:3 in the new Prismatoolithus oospecies from Shestakovo 3 vs. 1:1 in Spheruprismatoolithus and 1:7–1:10 in Sankofa) (Bray 1999; López-Martínez and Vicens 2012; Sellés et al. 2014). It differs from Trigonoolithus in having smooth outer surface (triangular and/or rounded protuberances in Trigonoolithus) (MorenoAzanza et al. 2014). The new oospecies Prismatoolithus ilekensis oosp. nov. differs from all other oospecies of Prismatoolithus by the mammillary layer to prismatic layer thickness ratio 1:3 (1:6–1:10 in P. gobiensis, P. matellensis, P. tenuis, P. levis, P. jenseni, P. caboti; 1:2–1:2.5


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Figure 5. Scanning electron microscope photographs of eggshell of Prismatoolithus ilekensis oosp. nov. (A), (B) Radial views showing eggshell ultrastructure. Note the gradual boundary between the mammillary layer and prismatic layer (black bar) and abrupt contact between prismatic layer and external layer (arrow). (C), (D) Close-ups of the prismatic layer. Note ill-defined squamatic structure with vesicles. Abbreviations: el – external layer, ml – mammillary layer, pl – prismatic layer.

in P. hirschi, 1:4–1:5 in P. trempii and 1:5 in P. tiantaiensis); differs from all Prismatoolithus oospecies (except P. tenuis and P. trempii) by eggshell thickness 300–330 μm (eggshell is thicker in other oospecies); differs from all Prismatoolithus oospecies (probably except P. levis) by the presence of three structural layers (vs. two in other oospecies) (Vianey-Liaud and Crochet 1993; Zhao and Li 1993; Zelenitsky and Hills 1996; Zhou et al. 1998; Bray 1999; Garcia et al. 2000; Zhao 2000; Lü et al. 2006; Jackson and Varricchio 2010; Moreno-Azanza et al. 2014; Sellés et al. 2014; Table 1). Additionally, Prismatoolithus ilekensis oosp. nov. differs from the Cretaceous avian eggs with smooth outer surface and the three structural layers by the proportionally thicker prismatic and by thinner external layer (the mammillary layer to prismatic layer to external layer thickness ratio is 1:3:0.6 in Prismatoolithus ilekensis oosp. nov. vs. 1:1:1.6 in Pachycorioolithus Lawver et al.,

2016, 1:1.5:1.5 in Styloolithus Varricchio and Barta, 2015, 1:1:0.44 in Plagioolithus Imai and Azuma, 2015, 1:1.6:0.4 in Neuquén enantiornithine eggshells from Argentina and by the presence of ill-defined squamatic texture (vs. well-defined squamatic texture s in the Cretaceous avian eggs, including Parvoolithus Mikhailov, 1996, Pachycorioolithus, Plagioolithus, Styloolithus and Neuquén enantiornithine eggshells) (Schweitzer et al. 2002; Imai and Azuma 2015; Varricchio and Barta 2015; Lawver et al. 2016).

Number of structural layers in Prismatoolithus ilekensis oosp. nov. The presence of three structural layers of eggshell is a potential synapomorphy of birds (the most of birds have three-layered eggshells; Board and Sparks 1991; Mikhailov 1997; Kohring 1999) or more exclusive theropod clade that includes birds and some

Table 1. Comparisons of oospecies of Prismatoolithus. Abbreviations: ML – mammillary layer, PL – prismatic layer. Oospecies P. gebiensis Zhao and Li, 1993 P. matellensis Vianey-Liaud and Crochet, 1993 P. tenuis Vianey-Liaud and Crochet, 1993 P. levis Zelenitsky and Hills, 1996 P. hanshuiensis Zhou, 1998 P. jenseni Bray, 1999 P. caboti Garcia et al., 2000 P. hukouensis Zhao, 2000 P. heyuanensis Lü et al., 2006 P. hirschi Jackson and Varricchio, 2010 P. trempi Sellés et al., 2014 P. tiantaiensis Wang et al. 2011 P. ilekensis oosp. nov.; this study

Shell thickness (mm) 0.7–0.9 1.06–1.22

Ml:Cl ratio 1:7 1:10

Pore system Angusticanaliculate Angusticanaliculate

Smooth Smooth

Ornament

No of structural layers Two Two

0.24–0.6

1:6–1:10

Angusticanaliculate

Smooth to dispersituberculate

Two

0.7–1.0 1.0–1.2 0.83–1.16 0.5–0.6 0.7–1.0 0.52 0.5–0.56 0.25–0.53 0.4–0.6 0.3–0.33

1:6–1:8 – 1:6–1:7 1:8–1:10 – – 1:2–1:2.5 1:4–1:5 1:5 1:3

Angusticanaliculate Angusticanaliculate Angusticanaliculate Angusticanaliculate Angusticanaliculate Angusticanaliculate Angusticanaliculate Angusticanaliculate Angusticanaliculate Angusticanaliculate

Smooth Smooth Smooth Dispersituberculate Smooth Smooth Smooth Smooth to dispersituberculate Smooth? Smooth

Two or three Two Two Two Two Two Two Two Two Three


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closely related non-avian theropods (e.g. troodontids) (Jackson et al. 2010). This ambiguity is a result of controversial interpretations of the number of structural layers (two or three) for many Mesozoic fossil eggs, including oospecies Prismatoolithus levis (eggs of Troodon formosus) (see Jackson et al. 2010 and references therein). Moreover, thin (thickness less than 500 μm) prismatic eggshells from Cretaceous deposits with three layers and smooth outer surface will be almost automatically interpreted as a bird eggshell (e.g. Imai and Azuma 2015), while two-layered eggshell will be ambiguously associated with small non-avian or avian theropods (Tanaka et al. 2016). The different interpretation of the number of structural layers produces different results of parsimony analyses (see below). We interpret a thin third layer in the eggshell of Prismatoolithus ilekensis oosp. nov. as a structural external layer (not a diagenetic layer) by following reasons: pore canals are present through the both prismatic (= second) and third layers and the columnar extinction pattern (under polarized light) continues through the third layer (Figure 4). Phylogenetic analysis Three parsimony analyses with one thousand repetitions of the parsimony ratchet (island hopper) algorithm were carried out using NONA v. 2.0 (Goloboff 1999), run with the WINCLADA v. 1.00.08 interface (Nixon 1999) to assess the phylogenetic position of Prismatoolithus ilekensis oosp. nov. We used the most recent matrix of Vila et al. (2017), with the addition of one new ootaxon (Prismatoolithus ilekensis oosp. nov.). Multistate characters were treated as unordered. According to the controversial interpretations of the number of structural layers for oospecies Prismatoolithus levis (see above), two analyses were different in coding states of character 7 (external zone: absent (0); present (1)) for Prismatoolithus levis and Troodon eggs; the third analysis run without this character. The first analysis (character 7(0) for P. levis and Troodon eggs) recovered one most parsimonious tree (tree length 41; consistency index 0.65; retention index 0.9) where Prismatoolithus ilekensis oosp. nov. is placed as the sister ootaxon of bird eggs included in this analysis (Figure 6(A)), sharing the presence of three structural layers. The second analysis (character 7(1) for P. levis and Troodon eggs) recovered seven most parsimonious trees (tree length 42; consistency index 0.64; retention index 0.89) where Prismatoolithus ilekensis oosp. nov. is placed in the one clade with advanced non-avian theropod eggs, but relationships of the new ootaxon with these ootaxa is only partly resolved in the strict consensus tree (Figure 6(B)). The placement of Prismatoolithus ilekensis oosp. nov., according to the third analysis (with removing of character 7 from the matrix; three most parsimonious trees, tree length 41; consistency index 0.66; retention index 0.9) (Figure 6(C)) is generally similar to that of the second analysis. The results of the phylogenetic analyses depend on interpretations of number of structural layers (two or three) for Prismatoolithus levis/eggs of Troodon formosus and two hypotheses about the phylogenetic position/taxonomic attribution arise: (1) the egg-layer of Prismatoolithus ilekensis oosp. nov. was a primitive bird or (2) the egg-layer of Prismatoolithus ilekensis oosp. nov. was a non-avian theropod, presumably troodontid. The microstructure of the eggshell of Prismatoolithus ilekensis

oosp. nov. fits intermediate position between non-avian and avian theropods and both hypotheses are almost equally parsimonious: the first hypothesis is supported by the presence of the confuciornithiform-like bird (Evgenavis nobilis) in Shestakovo 3, by the presence of three structural layers in the eggshell, by a small egg size and thin eggshell; the second hypothesis is supported by the presence of troodontids in Shestakovo 3, by the resemblance in eggshell microstructure with eggs of Troodon formosus (= Prismatoolithus levis), including the presence of ill-defined squamatic texture in the prismatic layer (well-defined in birds). Taxonomic affinity The prismatoolithid eggs are attributed to non-avian theropods on the basis of the discovery of this type of eggs (oospecies Prismatoolithus levis) with embryos of the troodontid Troodon formosus from the Two Medicine Formation in Montana, USA, and on the basis of the considerable resemblances with some avian eggshells (Varricchio et al. 2002; Zelenitsky et al. 2002). According to some recent phylogenetic analyses including oological characters, the Prismatoolithus and Protoceratopsidovum eggs form a clade that most likely has troodontid affinities, taking in account the association of Prismatoolithus levis eggs with the embryonic bones of Troodon formosus (Varricchio and Jackson 2004; Tanaka et al. 2011; Vila et al. 2017). Mikhailov in the original description of Protoceratopsidovum and in subsequent studies (Mikhailov 1994, 2000, 2014) proposed ceratopsian affinities of prismatoolithid Protoceratopsidovum eggs on the basis of egg type without any accompanying skeletal material. The phylogenetic analyses including oological characters did not support this taxonomic attribution and placed the Protoceratopsidovum eggs within a theropod egg clade with possible troodontid affinities (see above). The problem of theropod/ceratopsian affinities of Protoceratopsidovum eggs could be finally solved by findings of ceratopsian eggs containing embryos. Unfortunately, such unquestionable ceratopsian eggs have not been found – the only one reported ‘neoceratopsian’ embryo with poorly-developed embryonic bones within a three-layered eggshell (Balanoff et al. 2008) could belong to a theropod dinosaur (Jackson and Varricchio 2010; Mikhailov 2014) or more likely enantiornithine bird (Varricchio et al. 2015). As a result, we still do not know the morphology of ceratopsian eggs and microstructure of ceratopsian eggshells. If assignment of Protoceratopsidovum to the theropod dinosaurs is correct, then it arises a question why the ceratopsian eggs are absent in the beds containing numerous ceratopsian (namely Protoceratops) bones and theropod eggs? The possible answers are that: (1) this is a result of a specific taphonomic condition; (2) this is completely random situation and ceratopsian eggs will be found in these beds during future prospecting; (3) the absence of ceratopsian eggs in the beds with bones or/and skeletons of ceratopsians (e.g. Protoceratops in the Late Cretaceous of Mongolia; Psittacosaurus in the Early Cretaceous of China) could be result of a specific structure of ceratopsian egg not typical for other dinosaurs, namely the leathery (or weakly calcified) eggshells; and (4) this is a result of specific reproductive behaviors (e.g. selective environmental behaviors) (e.g. Dong and Currie 1993; Sellés and Galobart 2016). The alternative (and for our opinion

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HISTORICAL BIOLOGY

Figure 6. The most parsimonious tree (A) and two strict consensus trees (B, C) obtained by three different phylogenetic analyses showing possible phylogenetic positions of Prismatoolithus ilekensis oosp. nov. (A) The most parsimonious tree obtained by the first analysis where the state (0) was coded for the character 7 (external zone: absent (0); present (1)) for Prismatoolithus levis and Troodon eggs. (B) The strict consensus of the seven most parsimonious trees obtained by the second analysis where the state (1) was coded for the character 7 (external zone: absent (0); present (1)) for Prismatoolithus levis and Troodon eggs. (C) The strict consensus of the three most parsimonious trees obtained by the third analysis where the character 7 (external zone: absent (0); present (1)) was removed.


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less parsimonious) hypothesis that should be tested in future is that there is an amazing result of convergent evolution then the ceratopsians and theropods have similar eggs and the prismatoolithid oofamily is polyphyletic, containing both ceratopsian and theropod eggs. The Shestakovo 3 locality contains bone remains of both groups (basal ceratopsian Psittacosaurus and theropod dinosaurs (troodontids and birds); Alifanov et al. 1999; Averianov et al. 2006; O’Connor et al. 2014), but taking in account results of the recent phylogenetic analyses including oological characters (e.g. Tanaka et al. 2011; Vila et al. 2017; this study), the possible egglayer of Prismatoolithus ilekensis oosp. nov. is a small theropod dinosaur.

Acknowledgements

Early Cretaceous distribution of Prismatoolithus

The laboratory research was supported by the state task of the Ministry of Education and Science of the Russian Federation, Project 5.4217.2017/4.6. The work is performed according to the Russian Government Program of Competitive Growth of Kazan Federal University [2017]. ENM was supported by the Program of the Presidium of Russian Academy of Science [2014–2017].

Comparing with the abundant and widely distributed Late Cretaceous fossil record of Prismatoolithus, the Early Cretaceous fossil record of this oogenus is scarce and is limited to one European locality (Prismatoolithus sp. in the La Cantalera locality in Spain) and to two localities in Asia (Prismatoolithus sp. in the lower part of the ‘Lower Formation’ of the Sasayama Group, Japan; Prismatoolithus ilekensis oosp. nov. in the Shestakovo 3 locality, Western Siberia) (Canudo et al. 2010; Tanaka et al. 2016; this paper). All these Early Cretaceous Prismatoolithus eggs are characterized by relatively small size, according to thin eggshell (0.23 mm in the Japanese egg; 0.4 mm in the Spanish egg and the 0.3–0.33 mm in the Shestakovo egg) and were laid by small bodied forms (non-avian or avian theropods) (Canudo et al. 2010; Tanaka et al. 2016; this study). In contrast, the most of Late Cretaceous oospecies of Prismatoolithus had thicker eggshells (usually 0.5–1 mm) and larger eggs, except P. tenuis (eggshell thickness 0.24–0.6 mm) and P. trempii (0.25–0.53 mm) (see Table 1 and references therein).

Conclusions The fragmentary fossil egg from the Lower Cretaceous the Shestakovo 3 locality is historically important (at least for the national paleontology) as the first Early Cretaceous egg found in Russia. It can be referred to the oofamily Prismatoolithidae on the basis of its columnar organization of shell units, the presence of continuous horizontal growth lines and the gradual transition between mammillary and prismatic layers. The egg from the Shestakovo 3 shares the smooth outer surface, angustiprismatic morphotype and angusticanaliculate pore system with Prismatoolithus and can be assigned to this oogenus. The Shestakovo egg is characterized by thin eggshell (300–330 μm), by the presence of three structural layers with abrupt contact between prismatic layer and external layer and by the mammillary layer to prismatic layer to external layer thickness ratio is about 1:3:0.6. All these features support the erection of a new oospecies, Prismatoolithus ilekensis oosp. nov. The egg of Prismatoolithus ilekensis oosp. nov. was laid by small bodied theropod (primitive bird or non-avian theropod, presumably troodontid).

We thank all the participants of excavations at Shestakovo 3 in 2008 for field assistance and good company. We are very grateful to the staff of the “Geomodel” Research Center at the Saint Petersburg State University (Saint Petersburg, Russia), for their help in preparing images of the thin sections and for taking the SEM micrographs. The authors thank Daniel Barta and two anonymous reviewers for providing helpful comments that improved the quality of the manuscript.

Disclosure statement No potential conflict of interest was reported by the authors.

Funding

ORCID Pavel P. Skutschas http://orcid.org/0000-0001-8093-2905 Alexander O. Averianov http://orcid.org/0000-0001-5948-0799

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