Osteology and phylogenetic interrelationships of sturgeons (Acipenseridae)

Sturgeons (Acipenseridae) are an ancient and unique assemblage of fishes historically important to discussions of actinopterygian evolution. Despite their basal position within Actinopterygii, rigorous comparative morphological studies of acipenserids have never been made, and most ideas about acipenserid evolution hinge on an untested impression that shovelnose sturgeons (Scaphirhynchini) are phylogenetically primitive. This impression promoted ideas that: (1) the earliest acipenserids were highly benthic and evolved secondarily into pelagic predators, and (2) paedomorphosis has dominated mechanisms affecting their morphological change. Using cladistic methods, this study examines generic level interrelationships within Acipenseridae. Representatives of the four acipenserid genera Huso, Acipenser, Pseudoscaphirhynchus, and Scaphirhynchus, as well as their acipenseriform outgroups Polyodontidae, Peipiaosteidae, and Chondrosteidae, were surveyed for skeletal characters. Sixty-nine characters are identified and described to support the first generic level cladogram of Acipenseridae. Huso is phylogenetically primitive within Acipenseridae and the sister group to a redefined subfamily Acipenserinae. Acipenser is not supported by any characters identified in this study, but the tribe Scaphirhynchini comprising Scaphirhynchus and Pseudoscaphirhynchus is found to be monophyletic. The cladogram contradicts historical ideas about acipenserid evolution because Huso defines an outgroup morphology and life history founded on pelagic habitats and piscivory. In contrast, acipenserines, and more markedly scaphirhynchines, are benthic predators possessing character complexes for benthic feeding, respiration, locomotion, and protection. Also, the pattern of character acquisition within Acipenseridae suggests that peramorphosis played a central role in acipenserid evolution. Peramorphic addition and enlargement of the skeleton and scalation defines most characters at all nodes within Acipenseridae, and repudiates paedomorphosis as a major trend in evolution within the family Acipenseridae.     

Age-Dependent Variation of Serum Protein Antigens in Sturgeons (Acipenseridae,Acipenseriformes)

We studied the variation of antigenic properties of proteins in two sturgeon species at different stages of postembryonic development. The deepest changes occurred in individual components of albumins and -globulins (transferrins) and were mostly related to an increased proportion of the protein accounting for these antigens. Transformation of the main component of albumins A1 into adult antigens was completed in 5-month old juveniles. The main component of -globulins A (component of transferrins) appeared in the blood flow much later than other proteins and could retain the juvenile features until the age of 3–4 years. Other antigens belonging to ₁- and ₂-globulins and the second component of transferrins were more stable and did not undergo substantial changes. The direction of ontogenetic variation of serum antigens in sturgeon juveniles did not depend on the habitat of adult fish in fresh or sea water.     

Variability of some blood serum beta-globulins in the life cycle of the true sturgeons (Acipenseridae)

Blood proteins of true sturgeons of three genera Acipenser, Huso, and Pseudocaphirhynchus preserving unidirectional variability in ontogenesis regardless of peculiarities of the fish ecology can indicate unity of origin of the current species. Age-related protein transformations have heterochronous character. The slowest ontogenetic development lasting 4-6 years is peculiar to one of antigens of beta-globulins. Analysis of variability of beta-globulins in the age diapason beginning from the 4-month-old fry and including adult spawned individuals indicates different functional significance of their individual components. The beta A-globulin absent at early postembryonic stages becomes the second, after albumin, quantitatively predominant antigen in the adult fish blood. The amount of beta B-globulin, like antigens of alpha 1- and alpha 2-globulins preserving relative ontogenetic stability, can decrease significantly in freshwater sturgeons due to their preparation for spawning.     

Cranial morphology of the Stellate Sturgeon,Acipenser stellatus Pallas 1771 (Acipenseriformes,Acipenseridae), with notes on the skulls of other sturgeons

Extant members of Acipenseridae are generally classified in four genera: Scaphirhynchus, Pseudoscaphirhynchus, Huso and “Acipenser,” which is widely recognized to be paraphyletic. Advances have been made in understanding the systematic relationships among sturgeons based on both morphological and molecular data. Analysis of mitochondrial DNA data suggested that Pseudoscaphirhynchus should be regarded as nested within “Acipenser,” specifically as sister group to the Stellate Sturgeon, A. stellatus. Recent morphological analyses also recovered this relationship, supported by a number of osteological synapomorphies, although these results were based on few and relatively small individuals. Here we describe the anatomy of the skull of A. stellatus based on newly prepared specimens of adult individuals, as well as examination of a large number of preserved individuals representing a broad range of ontogenetic stages. We present new anatomical data from all regions of the skull (dermatocranium, neurocranium, viscerocranium) and offer interpretations of these and other characters. In particular, we describe the allometry in the snout of A. stellatus, which undergoes substantial elongation relative to other sturgeons. Aspects of the skull of A. stellatus are compared to other members of the family, specifically the course of the occipital sensory canal and the morphology and distribution of cranial spines.     

中国鲟科一新记录种——小体鲟

在中国,小体鲟(Acipenser ruthenus)被认为自然分布于额尔齐斯河,但至今尚无发现该种的文献报道,在额尔齐斯河是否确有分布还存疑问。2019年9月,在中国额尔斯斯河下游(185团)采集到鲟类标本1尾,全长91.5 cm,体重5 520 g。标本背骨板11,侧骨板64,腹骨板12;口腹位,较小,口下唇中间断裂;鳃耙数17,符合小体鲟的形态特征。利用线粒体DNA Cyt b基因序列(1 141 bp),对鲟属10个物种的亲缘关系及系统发育进行分析,该种与分布于鄂毕河、多瑙河的小体鲟遗传距离最近(序列分歧为0～0.000 2),并在进化树中聚为一支,应属于种内关系。基于以上研究结果,可以确定该标本即为小体鲟,在额尔齐斯河首次被发现,为中国鲟科分布新记录种,标本保存于中国水产科学研究院黑龙江水产研究所鱼类标本馆(标本号80092871)。     

Polymorphism of the myogens locus in some representatives of sturgeons (Acipenseridae)

This study investigates muscle proteins in Russian (Acipenser gueldensiaedtii Brandt), Siberian (Acipenser baerii Brandt), and Amur (Acipenser schrenckii Brandt) sturgeons using the method of polyacrylamide gel electrophoresis. A group of fractions, which is presumably the product of a polyallelic duplicated MY-1* locus, is recorded among the general pool of proteins. Data from densitometric analysis makes it possible to put forward a hypothesis about an eight-gene determination of this system of proteins. The highest heterogeneity and polymorphism was revealed in the Russian sturgeon. Analysis of the genotype distribution in samples of the studied species allowed us to make an assumption that the genetic structure of spawning sturgeon stocks is significantly metamorphosed under the influence of anthropogenic and natural factors.     

Morphology and fine structure of Acipenser persicus (Acipenseridae, Chondrostei) spermatozoon: Inter-species comparison in Acipenseriformes

This study describes morphology and fine structure of the Persian sturgeon (Acipenser persicus) (Acipenseridae, Chondrostei) spermatozoon. The results show that the spermatozoon of A. persicus is differentiated into an elongated head (length: mean±SD: 7.1±0.5μm) with an acrosome (length: 1.2±0.2μm), a cylindrical midpiece (length: 1.8±0.5μm), a flagellum (length: 50.3±5.9μm) and a total length of 59.2±6.2μm. Ten posterolateral projections (PLPs) arise from the posterior edge of the acrosome and there were 3 endonuclear canals that traversed the nucleus from the acrosomal end to the basal nuclear fossa region. Three to six mitochondria were in peripheral midpiece and the proximal and distal centrioles were located near to "implantation fossa" and basement of the flagellum. The axoneme has a typical eukaryotic structure composed of 9 peripheral microtubules and a central pair of single microtubule surrounded by the plasma membrane. Lateral fins were observed along the flagellum. The fins started and ended at 0.5-1μm from midpiece and at 4-6μm from the end of flagellum. There were significant differences in the size of almost all measured morphological parameters between males and flagellar, midpiece and nucleus characters were more isolated parameters that can be considered for detecting inter-individual variations. This study showed that sperm morphology and fine structure are similar among sturgeon species, but the dimensions of the parameters may differ.     

Brain lipid biochemistry of the sturgeons Acipenseridae]

Brain lipids of 4 species of sturgeons-Acipenser güldenst?dti, A. stellatus, A. ruthenus and Huso huso-have been investigated. In whole brain homogenates the content of the basic phospholipid families, their fatty acid composition as well as the content of glycosphingolipids-gangliosides, cerebrosides and sulfatides were studied. The quantitative relations between different molecular ganglioside fractions and their fatty acid composition, as well as the relative content of hydroxycerebrosides and cerebrosides with normal fatty acids were determined. The brain lipids of Acipenseridae were compared to previously obtained data on the brain of Elasmobranch and Teleost fishes. The brain lipid pattern of the four sturgeon species is very similar, but it differs greatly from that of Elasmobranch and of Teleostean brain, being in some respect more like the type of bony fish brain, in others the kind of brain of sharks and rays, and frequently considerably differing from both these types. The conspicous peculiarity in the content and molecular characteristics of the brain lipids of Acipenseridae compels us to agree with the opinion expressed by the late A.N. Belozerski and his coworkers [26, 27], based on a detailed study of fish DNA nucleotides, that the Ganoid fish are to be regarded as an independent class.     

Formation and structure of egg envelopes in Russian sturgeon Acipenser gueldenstaedtii (Acipenseriformes: Acipenseridae)

The covering of the eggs in Russian sturgeon Acipenser gueldenstaedtii consists of three envelopes (the vitelline envelope, chorion and extrachorion) and is equipped with multiple micropyles. The most proximal to the oocyte is the vitelline envelope that consists of four layers of filamentous and trabecular material. The structural components of this envelope are synthesized by the oocyte (primary envelope). The chorion encloses the vitelline envelope. The extrachorion covers the external surface of the egg. Examination of the arrangement of layers that comprise the egg envelopes together with the ultrastructure of follicular cells revealed that the chorion and extrachorion are secondary envelopes. They are secreted by follicular cells and are built of homogeneous material. During formation of egg envelopes, the follicular cells gradually diversify into three morphologically different populations: 1) cells covering the animal oocyte region (cuboid), (2) main body cells (cylindrical) and (3) micropylar cells. The apical surfaces of follicular cells from the first two populations form processes that remain connected with the oocyte plasma membrane by means of gap junctions. Micropylar cells are located at the animal region of the oocyte. Their apical parts bear projections that form a barrier to the deposition of materials for egg envelopes, resulting in the formation of the micropylar canal.     

Biological peculiarities of the industrially bred juvenile Russian sturgeon Acipenser gueldenstaedtii (Acipenseridae, Acipenseriformes) in the Don

We discuss results of the investigation into biological peculiarities of the juvenile Russian sturgeon (Acipenser gueldenstaedtii) from the Aksay-Don Sturgeon Hatchery living in a natural riverine environment and migrating seaward. We supply data on the growth rate, geographic distribution, behavior and the feeding manner of the juvenile Russian sturgeon in the Don. We have estimated the survival rate of the industrially bred juvenile Russian sturgeon living in a natural environment. Apart from the nutritive base in the river and the predation pressure, we found that ecologically and physiologically determined biological characteristics mostly influence the survival rate in the juvenile Russian sturgeon released into the Don. The findings allow estimation of artificial propagation of the Russian sturgeon in the Azov Sea basin.     

Formation of populations of Acipenseridae sturgeons in the Volga-Caspian basin

Analysis of dynamics of commercial catches and the state of populations of Russian sturgeon Acipenser gueldenstaedtii, starred sturgeon A. stellatus, and great sturgeon A. huso (Huso huso) in the Caspian Sea is presented. In the retrospective, the role of natural and artificial reproduction in formation of populations of Acipenseridae sturgeons is considered. The main principles of rational organization of practical activity for preservation and restoration of populations of Acipenseridae sturgeons are formulated.     

The historical biogeography of sturgeons (Osteichthyes: Acipenseridae): a synthesis of phylogenetics, palaeontology and palaeogeography

Abstract. The historical biogeography of sturgeons is explored using information from palaeogeography, palaeontology and phylogenetic interrelationships. The integration of information from these diverse sources indicates that sturgeons reached a wide Laurasian distribution in the Cretaceous and Tertiary by freshwater and coastal dispersal routes across land connections and along newly forming continental margins. The fossil record also suggests a considerable degree of morphological stasis and also supports an estuarine habit, and perhaps diadromy, as an old and conserved life history trait. While a ‘centre of origin’ for sturgeons remains elusive, phylogenetic relationships indicate that diversification appears to have been associated with fragmentation of biota, and of landmasses and basins, by late Tertiary geological and climatic phenomena, such as orogeny and unequal glaciation over North America, the desiccation of central Asia and alteration of its drainages, and the formation of discrete Ponto-Caspian basins by the fragmentation of the Paratethys. Amphi-oceanic distributions of certain species (Acipenser medirostris Ayres) and sister taxa (e.g. A. oxyrhynchus Mitchill and A. sturio L.) are explained by coastal dispersal and subsequent vicariance by geological (sea-floor spreading and development of new continental margins) and climatic (Pliocene cooling) changes during the Tertiary. An hypothesis is developed for the relationships of the North American sturgeons and their potential relationships with the Siberian sturgeon A. baeri. Late Tertiary climatic and geological phenomena are hypothesized as mediators of vicariance and subsequent diversification of these acipenserids. It appears that although acipenserids are a geologically old group, the historical biogeography of surviving lineages is best explained by more recent geological and climatic changes.     

Complete mitochondrial genome sequence and phylogenetic position of the Amu Darya sturgeon,Pseudoscaphirhynchus kaufmanni (Acipenseriformes: Acipenseridae)

In this study, we successfully assembled the complete mitochondrial genome of the Amu Darya sturgeon Pseudoscaphirhynchus kaufmanni. Based on this mitochondrial genome and previously published mitochondrial genomes of members of the Acipenseridae family, we assessed the phylogenetic position of P. kaufmanni using maximum likelihood and Bayesian inference for phylogeny reconstruction. The resultant phylogenetic trees were well-resolved, with congruence between different phylogenetic methods. This robust phylogenetic analysis elucidated the relationship among the four acipenserid genera and strongly supported the division of the family into three main clades. Evaluation of molecular phylogeny using maximum likelihood and Bayesian analysis led to the following conclusions: (a) the most basal position within the Acipenseridae remains in the clade containing Acipenser oxyrinchus and Acipenser sturio; (b) the genus Scaphirhynchus belongs to the Atlantic clade and is a sister group of the remaining species of the clade; and (c) the close relationship between P. kaufmanni and Acipenser stellatus is well supported.     

Phylogenetic relationships of the North American sturgeons (order Acipenseriformes) based on mitochondrial DNA sequences

The evolutionary relationships of the extant species within the order Acipenseriformes are not well understood. Nucleotide sequences of four mitochondrial genes (12S rRNA, COII, tRNA(Phe), and tRNA(Asp) genes) in North American sturgeon and paddlefish were examined to reconstruct a phylogeny. Analysis of the combined gene sequences suggests a basal placement of the paddlefish with regard to the sturgeons. Nucleotide sequences of all four genes for the three Scaphirhynchus species were identical. The position of Scaphirhynchus based on our data was uncertain. Within the genus Acipenser, the two Acipenser oxyrinchus subspecies were very similar in sequence and found to be basal to the remaining Acipenser species examined. Based on our data, Acipenser transmontanus and Acipenser medirostris were sister taxa, as were Acipenser fulvescens and Acipenser brevirostrum. Comparison of our results with hypotheses of sturgeon relationships proposed by previous authors is presented. The sequence data presented here are phylogenetically useful and provide a solid foundation of genetic information for the North American Acipenseriformes that can be expanded to include Eurasian species to provide a global picture of sturgeon evolution.     

Systematics of the Deropristiidae Cable & Hunninen, 1942 (Trematoda) and biogeographical associations with sturgeons (Osteichthyes: Acipenseridae)

The 11 nominal species of the Deropristiidae, belonging to the genera Deropristis (three species), Pristicola (one species), Skrjabinopsolus (five species) and Cestrahelmins (two species) were re-evaluated for a phylogenetic and biogeographical analysis of the group. Skrjabinopsolus elongatus (Madhavi, 1974) (= S. indicus Gupta & Ahmad, 1976, S. kurotchkini Parukhin, 1976), S. sanyaensis Shen, 1990, Deropristis paurosoma Wang, 1989 and Cestrahelmins Fischthal, 1957, do not belong to the Deropristiidae. The genus Opisthodiplomonorchis Madhavi, 1974 is resurrected for its type-species, O. elongatus (= S. elongatus), and D. paurosoma is also transferred to this genus. Species of Opisthodiplomonorchis occur in polynemid fishes of the Indo-Pacific. Five nominal species thus comprise the Deropristiidae, i.e. S. armatus Ivanov in Ivanov and Mrygin, 1937, S. manteri (Cable, 1952), D. hispida (Abildgaard, 1819), D. inflata (Molin, 1859) and P. sturionis (Little, 1930), which corresponds to the original composition of the family. A comparison of Skrjabinopsolus from acipenserids in North America and Europe revealed variability in morphological characters considered diagnostic in the past (body size and position of the ovary and testes). Based on the morphology and biology, the two species of Skrjabinopsolus can be considered incipient species. A phylogenetic analysis of the redefined Deropristiidae indicates that Deropristis and Pristicola may form a monophyletic group with Skrjabinopsolus as the sister taxon. The biogeography of the Deropristiidae suggests an origin and distribution associated with the formation of the North Atlantic basin. Freshwater and marine/estuarine origins for the family are equally parsimonious possibilities. A freshwater origin can be traced at least to Cretaceous Laurasia followed by a drift-vicariance separation and subsequent association with North Atlantic drainages. Support for a marine ancestry of the Deropristiidae is indicated by the biogeography of its sister taxa (outgroups in this study) and of its hosts, and is also consistent with an Atlantic origin. The deropristiids evidently originated and speciated within the Acipenseridae in the Atlantic region, with a host switch into Atlantic Anguilla spp.     

Anatomy and early development of the pectoral girdle,fin, and fin spine of sturgeons (Actinopterygii: Acipenseridae)

Acipenseriformes hold an important place in the evolutionary history of bony fishes. Given their phylogenetic position as extant basal Actinopterygii, it is generally held that a thorough understanding of their morphology will greatly contribute to the knowledge of the evolutionary history and the origin of diversity for the major osteichthyan clades. To this end, we examined comparative developmental series from the pectoral girdle in Acipenser fulvescens, A. medirostris, A. transmontanus, and Scaphirhynchus albus to document, describe, and compare ontogenetic and allometric differences in the pectoral girdle. We find, not surprisingly, broad congruence between taxa in the basic pattern of development of the dermal and chondral elements of the pectoral girdle. However, we also find clear differences in the details of structure and development among the species examined in the dermal elements, including the clavicle, cleithrum, supracleithrum, posttemporal, and pectoral‐fin spine. We also find differences in the internal fin elements such as the distal radials as well as in the number of fin rays and their association with the propterygium. Further, there are clear ontogenetic differences during development of the dermal and chondral elements in these species and allometric variation in the pectoral‐fin spine. The characters highlighted provide a suite of elements for further examination in studies of the phylogeny of sturgeons. Determining the distribution of these characters in other sturgeons may aid in further resolution of phylogenetic relationships, and these data highlight the role that ontogenetic and comparative developmental studies provide in systematics. J. Morphol. 276:241–260, 2015. © 2014 Wiley Periodicals, Inc.     

Development of the muscles associated with the mandibular and hyoid arches in the Siberian sturgeon,Acipenser baerii (Acipenseriformes: Acipenseridae)

The skeleton of the jaws and neurocranium of sturgeons (Acipenseridae) are connected only through the hyoid arch. This arrangement allows considerable protrusion and retraction of the jaws and is highly specialized among ray‐finned fishes (Actinopterygii). To better understand the unique morphology and the evolution of the jaw apparatus in Acipenseridae, we investigated the development of the muscles of the mandibular and hyoid arches of the Siberian sturgeon, Acipenser baerii. We used a combination of antibody staining and formalin‐induced fluorescence of tissues imaged with confocal microscopy and subsequent three‐dimensional reconstruction. These data were analyzed to address the identity of previously controversial and newly discovered muscle portions. Our results indicate that the anlagen of the muscles in A. baerii develop similarly to those of other actinopterygians, although they differ by not differentiating into distinct muscles. This is exemplified by the subpartitioning of the m. adductor mandibulae as well as the massive m. protractor hyomandibulae, for which we found a previously undescribed portion in each. The importance of paedomorphosis for the evolution of Acipenseriformes has been discussed before and our results indicate that the muscles of the mandibular and the hyoid may be another example for heterochronic evolution.     

Development of the skull and pectoral girdle in Siberian sturgeon,Acipenser baerii,and Russian sturgeon,Acipenser gueldenstaedtii (Acipenseriformes: Acipenseridae)

The head is considered the major novelty of the vertebrates and directly linked to their evolutionary success. Its form and development as well as its function, for example in feeding, is of major interest for evolutionary biologists. In this study, we describe the skeletal development of the cranium and pectoral girdle in Siberian (Acipenser baerii ) and Russian sturgeon (A. gueldenstaedtii ), two species that are commonly farmed in aquaculture and increasingly important in developmental studies. This study comprises the development of the neuro‐, viscero‐ and dermatocranium and the dermal and chondral components of the pectoral girdle, from first condensation of chondrocytes in prehatchlings to the early juvenile stage and reveals a clear pattern in formation. The otic capsules, the parachordal cartilages, and the trabeculae cranii are the first centers of chondrification, at 8.4mm TL. These are followed by the mandibular, then the hyoid, and later the branchial arches. Teeth form early on the dentary, dermopalatine, and palatopterygoid, and then appear later in the buccal cavity as dorsal and ventral toothplates. With ongoing chondrification in the neurocranium a capsule around the brain and a strong rostrum are formed. Dermal ossifications start to form before closure of the dorsal neurocranial fenestrae. Perichondral ossification of cartilage bones occurs much later in ontogeny. Our results contribute data bearing on the homology of elements such as the lateral rostral canal bone that we regard homologous to the antorbital of other actinopterygians based on its sequence of formation, position and form. We further raise doubts on the homology of the posterior ceratobranchial among Actinopteri based on the formation of the hyoid arch elements. We also investigate the basibranchials and the closely associated unidentified gill‐arch elements and show that they are not homologous. J. Morphol. 278:418–442, 2017. © 2017 Wiley Periodicals, Inc.