Fossil fishes from china provide first evidence of dermal pelvic girdles in osteichthyans

Background

The pectoral and pelvic girdles support paired fins and limbs, and have transformed significantly in the diversification of gnathostomes or jawed vertebrates (including osteichthyans, chondrichthyans, acanthodians and placoderms). For instance, changes in the pectoral and pelvic girdles accompanied the transition of fins to limbs as some osteichthyans (a clade that contains the vast majority of vertebrates – bony fishes and tetrapods) ventured from aquatic to terrestrial environments. The fossil record shows that the pectoral girdles of early osteichthyans (e.g., Lophosteus, Andreolepis, Psarolepis and Guiyu) retained part of the primitive gnathostome pectoral girdle condition with spines and/or other dermal components. However, very little is known about the condition of the pelvic girdle in the earliest osteichthyans. Living osteichthyans, like chondrichthyans (cartilaginous fishes), have exclusively endoskeletal pelvic girdles, while dermal pelvic girdle components (plates and/or spines) have so far been found only in some extinct placoderms and acanthodians. Consequently, whether the pectoral and pelvic girdles are primitively similar in osteichthyans cannot be adequately evaluated, and phylogeny-based inferences regarding the primitive pelvic girdle condition in osteichthyans cannot be tested against available fossil evidence.

Methodology/Principal Findings

Here we report the first discovery of spine-bearing dermal pelvic girdles in early osteichthyans, based on a new articulated specimen of Guiyu oneiros from the Late Ludlow (Silurian) Kuanti Formation, Yunnan, as well as a re-examination of the previously described holotype. We also describe disarticulated pelvic girdles of Psarolepis romeri from the Lochkovian (Early Devonian) Xitun Formation, Yunnan, which resemble the previously reported pectoral girdles in having integrated dermal and endoskeletal components with polybasal fin articulation.

Conclusions/Significance

The new findings reveal hitherto unknown similarity in pectoral and pelvic girdles among early osteichthyans, and provide critical information for studying the evolution of pelvic girdles in osteichthyans and other gnathostomes.     

Number and arrangement of extraocular muscles in primitive gnathostomes: evidence from extinct placoderm fishes

Exceptional braincase preservation in some Devonian placoderm fishes permits interpretation of muscles and cranial nerves controlling eye movement. Placoderms are the only jawed vertebrates with anterior/posterior obliques as in the jawless lamprey, but with the same function as the superior/inferior obliques of other gnathostomes. Evidence of up to seven extraocular muscles suggests that this may be the primitive number for jawed vertebrates. Two muscles innervated by cranial nerve 6 suggest homologies with lampreys and tetrapods. If the extra muscle acquired by gnathostomes was the internal rectus, Devonian fossils show that it had a similar insertion above and behind the eyestalk in both placoderms and basal osteichthyans.     

The metamorphosis of visual systems in the sea lamprey

The life cycle of the sea lamprey, Petromyzon marinus, includes two metamorphoses. At the end of a period spent as a blind larva, buried in the mud of streams, a first metamorphosis prepares it to migrate downstream to the sea or a lake for its growth phase. Then, following a second metamorphosis, it migrates upstream as a sexually mature adult to spawn and die. The downstream migrants have a visual system based upon rhodopsin and vitamin A₁, whereas that of the upstream migrants is based upon porphyropsin and vitamin A₂. The livers contain vitamin A₁ at all stages. The sea lamprey therefore exhibits a metamorphosis of visual systems, like those observed earlier among amphibia. The presence of porphyropsin in this member of the most primitive living group of vertebrates, as in fishes and amphibia, supports the notion that porphyropsin may have been the primitive vertebrate visual pigment. Its association with fresh water existence throughout this range of organisms also is consistent with the view that the vertebrate stock originated in fresh water. The observation that in the life cycle of the lamprey rhodopsin precedes porphyropsin is not at variance with the idea that porphyropsin is the more primitive pigment, since this change is part of the second metamorphosis, marking the return to the original environment. The observation that in lampreys, fishes, and amphibia, porphyropsin maintains the same general association with fresh water, and rhodopsin with marine and terrestrial habit, suggests that a single genetic mechanism may govern this association throughout this wide span of organisms.     

The characters of Palaeozoic jawed vertebrates

Newly discovered fossils from the Silurian and Devonian periods are beginning to challenge embedded perceptions about the origin and early diversification of jawed vertebrates (gnathostomes). Nevertheless, an explicit cladistic framework for the relationships of these fossils relative to the principal crown lineages of the jawed vertebrates (osteichthyans: bony fishes and tetrapods; chondrichthyans: sharks, batoids, and chimaeras) remains elusive. We critically review the systematics and character distributions of early gnathostomes and provide a clearly stated hierarchy of synapomorphies covering the jaw‐bearing stem gnathostomes and osteichthyan and chondrichthyan stem groups. We show that character lists, designed to support the monophyly of putative groups, tend to overstate their strength and lack cladistic corroboration. By contrast, synapomorphic hierarchies are more open to refutation and must explicitly confront conflicting evidence. Our proposed synapomorphy scheme is used to evaluate the status of the problematic fossil groups Acanthodii and Placodermi, and suggest profitable avenues for future research. We interpret placoderms as a paraphyletic array of stem‐group gnathostomes, and suggest what we regard as two equally plausible placements of acanthodians: exclusively on the chondrichthyan stem, or distributed on both the chondrichthyan and osteichthyan stems. © 2014 The Authors. Zoological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London     

Lamprey as an evo-devo model: lessons from comparative embryology and molecular phylogenetics

Lamprey, the living jawless vertebrate, has been regarded as one of the most primitive groups of vertebrates. The evolutionary phylogenetic position of the lamprey promises to provide hints about the origin of the vertebrate genome as well as the origin of the body plan, a part of which may be written in the genome. Since the lamprey split from the gnathostome lineage early in the history of vertebrates, the shared developmental mechanisms in lampreys and gnathostomes can be regarded as possessed by the hypothetical common ancestor of these animals, whereas the gnathostome-specific developmental mechanisms that are absent from lampreys indicate that they are relatively new, added to the developmental program only after the split of gnathostomes. Thus, the sequential establishment of the gnathostome body plan is inherently related to the history of genomic duplication events. In this review, recent molecular developmental and evolutionary molecular research on the living lampreys are summarized and discussed, taking vertebrate comparative morphology and embryology into consideration.     

Abbreviation of larval development and extension of brood care as key features of the evolution of freshwater Decapoda

The transition from marine to freshwater habitats is one of the major steps in the evolution of life. In the decapod crustaceans, four groups have colonized fresh water at different geological times since the Triassic, the freshwater shrimps, freshwater crayfish, freshwater crabs and freshwater anomurans. Some families have even colonized terrestrial habitats via the freshwater route or directly via the sea shore. Since none of these taxa has ever reinvaded its environment of origin the Decapoda appear particularly suitable to investigate life‐history adaptations to fresh water. Evolutionary comparison of marine, freshwater and terrestrial decapods suggests that the reduction of egg number, abbreviation of larval development, extension of brood care and lecithotrophy of the first posthatching life stages are key adaptations to fresh water. Marine decapods usually have high numbers of small eggs and develop through a prolonged planktonic larval cycle, whereas the production of small numbers of large eggs, direct development and extended brood care until the juvenile stage is the rule in freshwater crayfish, primary freshwater crabs and aeglid anomurans. The amphidromous freshwater shrimp and freshwater crab species and all terrestrial decapods that invaded land via the sea shore have retained ocean‐type planktonic development. Abbreviation of larval development and extension of brood care are interpreted as adaptations to the particularly strong variations of hydrodynamic parameters, physico‐chemical factors and phytoplankton availability in freshwater habitats. These life‐history changes increase fitness of the offspring and are obviously favoured by natural selection, explaining their multiple origins in fresh water. There is no evidence for their early evolution in the marine ancestors of the extant freshwater groups and a preadaptive role for the conquest of fresh water. The costs of the shift from relative r‐ to K‐strategy in freshwater decapods are traded‐off against fecundity, future reproduction and growth of females and perhaps against size of species but not against longevity of species. Direct development and extension of brood care is associated with the reduction of dispersal and gene flow among populations, which may explain the high degree of speciation and endemism in directly developing freshwater decapods. Direct development and extended brood care also favour the evolution of social systems, which in freshwater decapods range from simple subsocial organization to eusociality. Hermaphroditism and parthenogenesis, which have evolved in some terrestrial crayfish burrowers and invasive open water crayfish, respectively, may enable populations to adapt to restrictive or new environments by spatio‐temporal alteration of their socio‐ecological characteristics. Under conditions of rapid habitat loss, environmental pollution and global warming, the reduced dispersal ability of direct developers may turn into a severe disadvantage, posing a higher threat of extinction to freshwater crayfish, primary freshwater crabs, aeglids and landlocked freshwater shrimps as compared to amphidromous freshwater shrimps and secondary freshwater crabs.     

Homology of the Fifth Epibranchial and Accessory Elements of the Ceratobranchials among Gnathostomes: Insights from the Development of Ostariophysans

Epibranchials are among the main dorsal elements of the gill basket in jawed vertebrates (Gnathostomata). Among extant fishes, chondrichthyans most resemble the putative ancestral condition as all branchial arches possess every serially homologous piece. In osteichthyans, a primitive rod-like epibranchial 5, articulated to ceratobranchial 5, is absent. Instead, epibranchial 5 of many actinopterygians is here identified as an accessory element attached to ceratobranchial 4. Differences in shape and attachment of epibranchial 5 in chondrichthyans and actinopterygians raised suspicions about their homology, prompting us to conduct a detailed study of the morphology and development of the branchial basket of three ostariophysans (Prochilodus argenteus, Characiformes; Lophiosilurus alexandri and Pseudoplatystoma corruscans, Siluriformes). Results were interpreted within a phylogenetic context of major gnathostome lineages. Developmental series strongly suggest that the so-called epibranchial 5 of actinopterygians does not belong to the epal series because it shares the same chondroblastic layer with ceratobranchial 4 and its ontogenetic emergence is considerably late. This neomorphic structure is called accessory element of ceratobranchial 4. Its distribution among gnathostomes indicates it is a teleost synapomorphy, occurring homoplastically in Polypteriformes, whereas the loss of the true epibranchial 5 is an osteichthyan synapomorphy. The origin of the accessory element of ceratobranchial 4 appears to have occurred twice in osteichthyans, but it may have a single origin; in this case, the accessory element of ceratobranchial 4 would represent a remnant of a series of elements distally attached to ceratobranchials 1–4, a condition totally or partially retained in basal actinopterygians. Situations wherein a structure is lost while a similar neomorphic element is present may lead to erroneous homology assessments; these can be avoided by detailed morphological and ontogenetic investigations interpreted in the light of well-supported phylogenetic hypotheses.     

Proposed habitats of early tetrapods: gills, kidneys, and the water-land transition

Recent finds of early tetrapods have established that the most primitive form, Acanthostega, retained internal gills and other fish-like features; this has led to the conclusion that it was a primarily aquatic animal. Other Late Devonian tetrapods, such as lchthyostega and Tulerpeton, provide no evidence of internal gills, but have also been interpreted as inhabiting an aquatic environment. The probable aquatic habits of a diversity of Devonian tetrapods has led to the suggestion that the entire early tetrapod radiation may have been an aquatic one, with terrestriality having evolved in later forms. However, consideration of the physiology of living amphibious vertebrates suggests that this scenario is unlikely. The use of the gills for the excretion of carbon dioxide and ammonia appears to be a fundamental feature of all primarily aquatic vertebrates. No living fish loses its internal gills, even if it excretes a significant portion of its nitrogenous waste as urea via the kidney in the water. Gills are simply too valuable to be lost by an aquatic animal, even in those air-breathing fishes that no longer use the gills for oxygen uptake. We suggest that the apparent loss of the gills in tetrapods more derived than Acanthostega signals their descent from a more terrestrial phase in tetrapod evolution, following the primary assumption by the kidney of the excretion of nitrogenous wastes. Without this new role of the kidney, loss of the gills would have been impossible. With this new kidney role, loss of the gills may have been advantageous in reducing desiccation on land.     

痕迹化石在识别东濮凹陷古近纪河口湾环境和下切谷中的作用

河口湾砂岩储层,在下切谷型油气勘探类型中极具潜在经济价值,因而引起众多沉积环境研究者的关注。河口湾是河水、海水相互作用的场所,具明显的三重沉积结构,即在河口湾内侧,河流淡水沉积具主导;在河口湾外侧,则以潮汐或波浪等海水水流沉积占优;而河口湾的中央地带,是海水和淡水汇合区,表现出咸水水体和低能环境的沉积特征。东濮凹陷沙河街组四段,低位期形成的下切谷和高位期转变成河口湾的过程,由沉积柱子中的海水生物痕迹、咸水生物痕迹及淡水生物痕迹记录下来,这些适应于不同水体的造迹生物所留下的痕迹,弥补了这一地区缺乏标志性实体化石带来的认识障碍,为识别其沉积环境真面目找到了新途径。由Cylindricum-Scoyenia为代表的淡水痕迹化石组合,以Tigillites和喜盐植物根迹为代表的咸水生物痕迹和以Thalassinoides,Teichichnus为代表的海水生物痕迹,在东濮凹陷沙河街组四段钻取的岩芯中多次出现,证实了那里河口湾沉积的三重结构和下切谷的存在。     

Otx1 gene-controlled morphogenesis of the horizontal semicircular canal and the origin of the gnathostome characteristics

SUMMARY The horizontal semicircular canal of the inner ear is a unique feature of gnathostomes and is predated by the two vertical semicircular canals, which are already present in lampreys and some fossil, armored jawless vertebrates regarded as close relatives of gnathostomes. Inactivation in mice of the orthodenticle -related gene Otx1 results in the absence of this structure. In bony fishes and tetrapods (osteichthyans), this gene belongs to a small multigene family comprising at least two orthology classes, Otx1 and Otx2 . We report that, as in the mouse, xenopus and zebrafish, Otx1- and Otx2 -related genes are present in a chondrichthyan, the dogfish Scyliorhinus canicula , with an Otx1 expression domain in the otocyst very similar to those observed in osteichthyans. A strong correlation is thus observed in extant vertebrates between the distribution of the horizontal semicircular canal and the presence of an Otx1 ortholog expressed in the inner ear, which supports the hypothesis that the absence of this characteristic in Otx1 ^-/- mice may correspond to an atavism. The same conclusion applies to two other gnathostome-specific characteristics also deleted in Otx1 ^-/- mice, the utriculosaccular duct and the ciliary process. Together with functional analyses of Otx1 and Otx2 genes in mice and comparative analyses of the Otx gene families characterized in chordates, these discoveries lead to the hypothesis that some of the anatomic characteristics of gnathostomes have appeared quite suddenly and almost simultaneously in vertebrate evolution, possibly as a consequence of gene functional diversifications following duplications of an ancestral chordate gene.     

Cardiac septation in heart development and evolution

The heart is one of the vital organs and is functionalized for blood circulation from its early development. Some vertebrates have altered their living environment from aquatic to terrestrial life over the course of evolution and obtained circulatory systems well adapted to their lifestyles. The morphology of the heart has been changed together with the acquisition of a sophisticated respiratory organ, the lung. Adaptation to a terrestrial environment requires the coordination of heart and lung development due to the intake of oxygen from the air and the production of the large amount of energy needed for terrestrial life. Therefore, vertebrates developed pulmonary circulation and a septated heart (four-chambered heart) with venous and arterial blood completely separated. In this review, we summarize how vertebrates change the structures and functions of their circulatory systems according to environmental changes.     

Has the importance of the amniote egg been overstated?

The evolution of the amniote egg is commonly regarded as an important milestone in the history of the vertebrates, an innovation that completed the transition from aquatic to fully terrestrial existence by permitting eggs to be laid away from standing water. This view derives ultimately from the recapitulationist theories of Haeckel, and rests on the assumption that extant frogs and salamanders are good models for the reproductive habits of early tetrapods and the ancestors of the amniotes. It also assumes that it is more difficult to lay eggs on land than in water, and that the amniote egg is an adaptation to the physical rigours that eggs encounter in terrestrial environments. Taken together, these assumptions comprise what may be termed the 'Haeckelian framework' for the origin of vertebrate terrestriality. Several independent lines of evidence suggest that the assumptions of the Haeckelian framework are false. There appear to be no theoretical reasons to assume that the evolution of terrestrial egg-laying was difficult, or required a structure as elaborate as the amniote egg. The physical conditions eggs encounter in the terrestrial environments where they are actually laid are quite mild. Land may in fact be an easier place to lay eggs than water. In addition, analysis of the distribution of key reproductive character states among vertebrates provides no evidence that the 'typical amphibian' reproductive mode is primitive for tetrapods. Amniotes are as likely as frogs or salamanders to retain primitive reproductive character states.     

Fossilized ontogenies: the contribution of placoderm ontogeny to our understanding of the evolution of early gnathostomes

Placoderms, representing phylogenetically more inclusive jawed vertebrates and successive sister taxa to crown‐group gnathostomes, are critical to our understanding of character evolution within the crown‐group (chondrichthyans + osteichthyans), including developmental characters. Early ontogenetic stages of placoderms are generally poorly known, although some exceptional faunas preserve both embryonic (e.g. from the Gogo Formation, Western Australia) and post‐embryonic individuals (the Miguasha Formation, Canada; Lode Formation, Latvia; Merriganowry Formation, Gogo Formation, Australia). Information provided by these ontogenies is relevant to questions of placoderm taxonomy and phylogeny, but also to broader questions pertinent to vertebrate evolution as a whole, for example, evolution of bone development, evolution of the axial skeleton and evolution of reproduction.     

A novel sperm adaptation to evolutionary constraints on reproduction: Pre‐ejaculatory sperm activation in the beach spawning capelin (Osmeridae)

Reproduction of external fertilizing vertebrates is typically constrained to either fresh or salt water, not both. For all studied amphibians and fishes, this constraint includes immotile sperm that are activated after ejaculation only by the specific chemistry of the fertilizing medium in which the species evolved (fresh, brackish, or salt water). No amphibians can reproduce in the sea. Although diadromous fishes may migrate between salt and fresh water, they are shackled to their natal environment for spawning in part because of sperm activation. Here, we report for the first time among all documented external fertilizing vertebrates, that in the absence of any external media, sperm are motile at ejaculation in a marine spawning fish (Osmeridae, capelin, Mallotus villosus). To illuminate why, we evaluated sperm behavior at different salinities in M. villosus as well as the related freshwater spawning anadromous rainbow smelt (Osmerus mordax). Surprisingly, sperm performance was superior in fresh water for both species. M. villosus spend their entire life at sea but our results show that their sperm are deactivated by sea water, suggesting a freshwater ancestry. By circumventing constraining water chemistry, we interpret the unique pre‐ejaculatory sperm activation in this species as a novel adaptation that enables fertilization in the marine environment. These findings also contribute to understanding the persistence of anadromy, despite great energetic costs to adult fishes.     

Scales and Dermal Skeletal Histology of an Early Bony Fish Psarolepis romeri and Their Bearing on the Evolution of Rhombic Scales and Hard Tissues

Recent discoveries of early bony fishes from the Silurian and earliest Devonian of South China (e.g. Psarolepis, Achoania, Meemannia, Styloichthys and Guiyu) have been crucial in understanding the origin and early diversification of the osteichthyans (bony fishes and tetrapods). All these early fishes, except Guiyu, have their dermal skeletal surface punctured by relatively large pore openings. However, among these early fishes little is known about scale morphology and dermal skeletal histology. Here we report new data about the scales and dermal skeletal histology of Psarolepis romeri, a taxon with important implications for studying the phylogeny of early gnathostomes and early osteichthyans. Seven subtypes of rhombic scales with similar histological composition and surface sculpture are referred to Psarolepis romeri. They are generally thick and show a faint antero-dorsal process and a broad peg-and-socket structure. In contrast to previously reported rhombic scales of osteichthyans, these scales bear a neck between crown and base as in acanthodian scales. Histologically, the crown is composed of several generations of odontodes and an irregular canal system connecting cylindrical pore cavities. Younger odontodes are deposited on older ones both superpositionally and areally. The bony tissues forming the keel of the scale are shown to be lamellar bone with plywood-like structure, whereas the other parts of the base are composed of pseudo-lamellar bone with parallel collagen fibers. The unique tissue combination in the keel (i.e., extrinsic Sharpey''s fibers orthogonal to the intrinsic orthogonal sets of collagen fibers) has rarely been reported in the keel of other rhombic scales. The new data provide insights into the early evolution of rhombic (ganoid and cosmoid) scales in osteichthyans, and add to our knowledge of hard tissues of early vertebrates.     

Salinity influences the distribution of marine snakes: implications for evolutionary transitions to marine life

Secondary transitions from terrestrial to marine life provide remarkable examples of evolutionary change. Although the maintenance of osmotic balance poses a major challenge to secondarily marine vertebrates, its potential role during evolutionary transitions has not been assessed. In the current study, we investigate the role of oceanic salinity as a proximate physiological challenge for snakes during the phylogenetic transition from the land to the sea. Large‐scale biogeographical analyses using the four extant lineages of marine snakes suggest that salinity constrains their current distribution, especially in groups thought to resemble early transitional forms between the land and the sea. Analyses at the species‐level suggest that a more efficient salt‐secreting gland allows a species to exploit more saline, and hence larger, oceanic areas. Salinity also emerged as the strongest predictor of sea snake richness. Snake species richness was negatively correlated with mean annual salinity, but positively correlated with monthly variation in salinity. We infer that all four independent transitions from terrestrial to marine life in snakes may have occurred in the Indonesian Basin, where salinity is low and seasonally variable. More generally, osmoregulatory challenges may have influenced the evolutionary history and ecological traits of other secondarily marine vertebrates (turtles, birds and mammals) and may affect the impact of climate change on marine vertebrates.     

Freshwater or marine origin of the vertebrates?

1. Paleontological data indicate that the earliest recognizable vertebrate remains, bone fragments of Upper Cambrian and Lower Ordovician heterostracan fishes, were deposited in a marine situation. 2. Since these earliest fossils are sporadic in occurrence, from atypical marine deposits and since they only represent the full grown adult stage, the possibility of a freshwater developmental stage or estuarine habitat cannot be excluded. 3. The hagfishes, supposedly the most primitive of living vertebrates, are exclusively marine and possess an osmoregulatory strategy (monovalent ion levels nearly identical with sea-water with little capability of regulation) that is consonant with a strictly marine evolutionary history. Possibly, but less parsimoniously, this strategy and habitat could be secondarily derived. 4. The hagfish has a glomerular kidney, renal sodium reabsorption and branchial pumps for the uptake of sodium and chloride which are indicative, but not unequivocally diagnostic, of a freshwater ancestry. 5. A scenario in which the earliest vertebrate was anadromous, breeding in fresh water and migrating to the sea, is consistent with the paleontological data and with the physiology and life history of living 'primitive' fishes. It also leads to more coherent explanations for the origin of bone and for the evolution of vertebrate special senses than do alternative marine scenarios.