The origin of the Pycnodonteinae and relationship between gryphaeas and true pycnodontes

Berriasian (Early Cretaceous) oyster Pycnogryphaea weberae from Crimea is one of the earliest known pycnodonteine oysters. Examination of shell morphology and microstructure of this species shows that it shares characters of the subfamilies Gryphaeinae and Pycnodonteinae. Shell microstructure of Pycnogryphaea weberae lacks vesicular structure and is similar to microstructure of the genus Gryphaea . At the same time the shell of this species possesses morphological characters typical of pycnodonteins: development of chomata and well-defined circumferential curb. Pycnogryphaea weberae is regarded as a transitional taxon between the subfamilies Gryphaeinae and Pycnodonteinae and referred herein to a new genus Pycnogryphaea within the Pycnodonteinae. This suggests that the subfamily Pycnodonteinae likely originated from the Late Jurassic representatives of the genus Gryphaea (Gryphaeinae) in Berriassian. First pycnodonteins preserved shell microstructure of the genus Gryphaea but developed chomata along all the perimeter of both valves.


Introduction
The subfamily Pycnodonteinae was first proposed by Stenzel in 1959.Its original diagnosis includes: well-defined commissural shelf, proximally delimited by a circumferential curb; chomata short to long, branching and vermiculate; occurrence of vesicular structure; and absence of prismatic shell layer, except for the genus Neopycnodonte Stenzel, 1971 (Fig. 1).The subfamily Pycnodonteinae ranges from the Early Cretaceous to Recent (Stenzel 1971).Stenzel (1971 emphasized that the main morphological characteristic of the subfamily Pycnodonteinae is the occurrence of vesicular shell layer.Harry (1985), Malchus (1990), Cooper (1992), and Ivanov (1995) later clarified the diagnoses of supraspecific taxa within the subfamily Pycnodonteinae.Cooper (1992) was the first to propose a hypothesized relationships within the subfamily Pycnodonteinae on the basis of the shell morphology.In this model, genus Bilobissa Stenzel, 1971 (Cooper considered Bilobissa as a genus within the Pycno donteinae; herein Bilobissa is considered as a subgenus of Gryphaea [Gryphaeinae] as in original description of Stenzel [1971]) and genus Texigryphaea Stenzel, 1959 are closely related (Cooper 1992: fig.1).Furthermore, the phylogenetic affinities of the subgenus Bilobissa as closely related to the Pycnodonteinae were already proposed by Stenzel (1971 in its subgeneric description.However, the stratigraphic distribution of subgenus Bilobissa and genus Texigryphaea ranges from Middle to Late Jurassic, and Albian to Cenomanian, respectively, whereas other oysters from the subfamily Pycnodonteinae were absent through Berriasian and Albian successions.This problem of a large temporal gap in the occurrence of Pycnodontein oysters was later resolved with the discovery of the species Pycnodonte miranda Bog danova, 1980, in the Berriasian-Valanginian successions of the Mangyshlak Region (north-western Kazakhstan), as well as Gryphaea weberae Yanin in Tschelzova, 1969 in the Berriasian of Crimea.Later, Bogdanova (in Arkadiev et al. 1997) and Yanin (in Arkadiev et al. 2012) transferred G. weberae to the genus Pycnodonte Fisher de Waldheim, 1835.Thus, Pycno donte weberae is one of the earliest pycnodontein oysters.
The aim of this study is to re-examine the morphology and microstructure of the species Pycnodonte weberae in order to understand its taxonomic affinities, and more generally the early evolution of the Pycnodonteinae.In this work, previously published data (Tschelzova 1969;Arkadiev et al. 1997Arkadiev et al. , 2012) )  Nomenclatural acts.-Theelectronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature, and hence the new names contained herein are available under that Code from the electronic edition of this article.This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN.The LSID for this publication is: urn:lsid:zoobank.org:act:DE9CA5C3-1579-460D-85CD-65A10233558F.The electronic edition of this work was published in a journal with an ISSN 0567-7920, eISSN 1732-2421, and has been archived and is available from the following digital repository: APP archive: http://www.app.pan.pl/article/item/app004942018.html.

Material and methods
The studied material was collected by Tamara N. Bogdanova (VSEGEI) in the Berriasian sections of Crimean Mountains (Pseudosubplanites grandis Subzone in the section Sarysu river; Dalmasiceras tauricum Subzone in the section Balki village; lower part of Riasanites crassicostatum Subzone in the section Chernokamenka village; beds with Symphythyris arguinensis in sections Balki village and Kuchki village; beds with Zeillerina baksanensis corresponding the uppermost Berriasian in the section Mezhgorye village) (Figs. 2,  3).The material consists of 83 left and 39 right valves of the species Pycnogryphaea weberae.
In order to understand the intraspecific variability of the species Pycnogryphaea weberae, the following morphometric parameters were measured on specimens from the Dalmasiceras tauricum Subzone (the section Balki village): shell height, shell length and convexity of the shell; calculated parameters include: elongation coefficient and convexity coefficient.Distributions graphs were prepared on the basis of the previously mentioned parameters using the freely distributed software Past 3 (Hammer et al. 2001) The microstructure of the shells was examined in thin sections under light microscope Olympus BX60.Shell photographs were made after whitening with ammonium chloride (NH 4 Cl) using a camera Canon EOS 60D.
The morphological and microstructure terminology is taken from Stenzel (1971), Carter (1990), Carter et al. (2012) and Koppka (2015).The term "furcate" microstructure comes from the work of Tschelzova (1969).In longitudinal section, furcate microstructure consists on a system of treelike branching of vertical, large, irregular calcite crystals producing irregular embranchment in the upper part of the layer (Tschelzova 1969: 25, fig. 13).Interspaces between vertical and inclined crystals are filled by thin parallel calcite lamellas (0.01-0.02 mm), which in turn are more or less parallel to the shell surface.Extinction is heterogeneous.
The Late Jurassic Circunula Koppka, 2015, questionably referred by Koppka (2015) to the Pycnodonteinae, recorded from the Oxfordian to Kimmeridgian of Switzerland and France, the Kimmeridgian of Germany and Crimea and the Tithonian of Czech Republic, differs from Pycnogryphaea by a large attachment area, the disappearance of chomata in adult growth stage and the non gryphaeoid shell shape.
Stratigraphic and geographic range.-Berriasian of Crimea.
Description.-Leftvalve gryphaeoid, moderately to highly convex (convexity coefficient Conv/L in studied samples varies from 0.36 to 0.80; see Fig. 5C), triangular to oval in outline, sometimes with opisthogyrate beak, larger than the right valve; right valve flat or slightly concave.Examined specimens up to 66 mm high and up to 72 mm long (Fig. 5A); elongation coefficient (L/H) varies in studied sample from 0.66 to 1.22 (Fig. 5B).Left valve covered by commarginal growth lines; well-defined posterior sulcus.Attachment area very small (diameter up to 10 mm in shell with 42 mm high and 47 mm long; usually not distinguishable).Right valve with well-defined commarginal growth lines and antimarginal grooves.
Ligament area: small, triangular; initially prosogyrate in some specimens; resilifer triangular, weakly concave with slightly convex bourrelets on both valves, less elevated on the right valve.Plane of ligament area depends on the degree of beak development: from almost perpendicular to the commissure plane in shells with a well-developed beak, to subparallel to the commissure plane in shells having a non-developed beak.
Internal shell characters: Umbonal cavity absent.Poste rior adductor muscle rounded, relatively small, posterodorsal.Quenstedt muscle scar well distinguishable on the right valve, approximately located approximately under the resilifer (Fig. 4A-C, E, F).Commissural shelf narrow, well-defined, delimited by the circumferential curb.Chomata developed on commissural shelf all along the circumferential curb.Elongated chomata located near the ligament area, simple lath chomata developed below the elongated chomata.
Remarks.-The species Pycnogryphaea weberae was for the first time described by Yanin in the book by Tschelzova (1969), and was attributed to the genus Gryphaea.Tschelzova (1969) studied the microstructure of Pycnogryphaea weberae and showed that inner shell layer was defined by a regular foliated microstructure with rare empty chambers and subrhombic microstructure, which includes various types of irregular complex crossed foliated microstructure.Furcate microstructure was observed on the outer shell layer.Such microstructures are typical for the genus Gryphaea, and the species was included into Gryphaea by Yanin (in Tschelzova 1969).The current study of microstructure of Pycnogryphaea weberae agrees with the original description of Tschelzova (1969) (Figs. 6, 7).The presence of chomata mentioned on its original description (Yanin in Tschelzova, 1969), later encouraged Tamara N. Bogdanova (Arkadiev et al. 1997) and Boris T. Yanin (Arkadiev et al. 2012) to assign this species to the genus Pycnodonte.structure.It agrees with the idea of Stenzel (1971) that early primitive Pycnodonteinae are defined by simple chomata, whereas more advanced Pycnodonteinae are characterized by the development of large vermiculate chomata near the hinge.No transitional Early Cretaceous oysters were found filling the gap between the true gryphaeas and pycnodontes, and Stenzel noticed (Stenzel 1971 that: "…certain traits seemingly foreshadow transitions to Texigryphaea and Pycnodonte.These traits are a broad and deep posterior sulcus dividing the left valve, an ill-defined smooth rounded radial keel running down the main body of the left valve, a slight amount of compression of the left valve in anteroposterior direction, a three-dimensional spiral growth pattern, a more opisthogyral left beak, and sharp radial grooves or gashes on the right valve".Pycnogryphaea weberae shares all of the mentioned morphological characters typical for Late Jurassic representatives of Gryphaea (Bilobissa).It differs from the Late Jurassic Gryphaea (Bilobissa) by the development of chomata (character of the Pycnodonteinae).However, the species Pycnodonte weberae did not developed vesicular structure typical for most Pycnodonteinae (with a single exception "Pycnodonte" similis (Pusch, 1837) characterized by reduced (but not absent) vesicular structure (Machalski 1988).Thus, Pycnogryphaea weberae may be regarded as a transitional taxon between Late Jurassic Gryphaeinae and Cretaceous Pycnodonteinae.Comparisons made on shell morphology of Gryphaea (Bilobissa), Pycno gryphaea gen.nov., and Phygraea provide a basis for the reconstruction of phylogenetic line Gryphaea (Bilobissa) (Gryphaeinae; Late Jurassic) → Pycnogryphaea gen.nov.(Pycnodonteinae; Berriasian) → Phygraea (Pycnodonteinae; late Early Creta ceous).
Pycnogryphaea differs from Gryphaea by the appearance of chomata.Other morphological characters of Pycno gryphaea are typical for Gryphaeinae (circular posterodorsal adductor muscle scar, gryphaeoid shell shape, beaked umbo, posterior radial sulcus).The presence of chomata is a key morphological character that distinguished the Pycnodonteinae from the Gryphaeinae.On the other hand, chomata (as also shell chambers) independently appeared several times during the evolution of Ostreoidea in the subfamilies Exogyrinae Vialov, 1936, Pycnodonteinae Stenzel, 1959, and Liostreinae Vialov, 1983(Malchus 1998).However, other morphological characters of Pycnogryphaea are in common with Gry phaeinae and Pycnodonteinae and there are no doubts that the genus belongs to Gryphaeinae-Pycnodonteinae phylogenetic line.
The evolutionary trend from Pycnogryphaea gen.nov. to Phygraea includes the development of chambers filled by vesicular microstructure, increase of commissural shelf and the increase complexity from short simple chomata to long vermiculate chomata located only near the ligament area.
Finally, the Albian-Cenomanian genus Texigryphaea cannot be regarded as the earliest known Pycnodonteinae and may be considered as a specialized member arising from the pycnodontes branch and restricted to North and Central America (Stenzel 1971).
The Late Jurassic genus Circunula Koppka, 2015, is defined by chomata and was consequently previously questionably included in the subfamily Pycnodonteinae by Koppka (2015), but does not share morphological characters with the genera Gryphaea and Phygraea.Based on the present study, it cannot be regarded as an ancestor of the Pycnodonteinae.

Conclusions
Pycnogryphaea gen.nov. is proposed as a new genus within the subfamily Pycnodonteinae.It includes the species Pycnodonte weberae (Yanin in Tschelzova, 1969) previously attributed to the genus Pycnodonte and is defined by well-developed short simple chomata and circumferential curb (characters of the Pycnodonteinae), as well as a shell microstructure defined by irregularly complex crossed foliated and simple regularly foliated microstructures without chambering and vesicular structure (characters of the Gryphaeinae).The stratigraphic distribution of the subfamily Pycnodonteinae is extended to the early Berriasian (Berriasella jacobi Zone).The combination of typical gryphaeine shell microstructure and pycnodonteine morphology in the described specimens of the genus Pycnogryphaea suggest it may be considered as a transitional genus between both subfamilies, Gryphaeinae and Pycnodonteinae.

Fig. 1 .
Fig. 1.Schematic drawing illustrating shell morphology of Pycnogryphaea weberae Yanin in Tschelzova, 1969.Left valve in inner (A) and outer (B) views; right valve in inner (C) and outer (D) views.The image is given approximately in natural size.
are re-examined and backed by new data on the microstructure of the species Pycnodonte weberae from the Berriasian successions of Crimea.
Combination of two gryphaeid generic names Pycnodonte, and Gryphaea, since the new genus shares characteristics of both.Type species: Gryphaea weberae Yanin in Tschelzova, 1969, Berriasian of Crimea, section Sarysu river.Species included: Type species only.
Zakharov 1966 andKosenko 2017sic to Late Jurassic (or even Early Cretaceous according toZakharov 1966 andKosenko 2017) Gryphaea Lamarck, 1801, (Gryphaeinae) characterized by a gryphaeoid shell shape, orthogyrate beaked umbo, circular posterodorsally located posterior adductor muscle scar and radial grooves on the right valve, appears to be very similar to Pycnogryphaea.Pycnogryphaea differs from Gryphaea by chomata developed all along the circumferential curb.Due to the presence of chomata Pycnogryphaea is regarded here within the Pycnodonteinae.However, it differs from other genera of the Pycnodonteinae by the absence of vesicular structure in shell microstructure.