Using the whole body as a sucker: Combining respiration and feeding with an attached lifestyle in hill stream loaches (Balitoridae,Cypriniformes)

Small fishes living in fast‐flowing rivers face a harsh environment as they can easily be swept away by the rapid currents. To survive such circumstances, teleosts evolved a wide variety of attachment mechanisms, based on friction, negative pressure or both. Balitorinae (Balitoridae, Cypriniformes) are exceptional in using their whole body as an adhesive apparatus. We investigated the morphological adaptations of Balitorinae by studying the osteology and myology of four species (Beaufortia leveretti, Sewellia lineolata, Pseudogastromyzon myersi, and Gastromyzon punctulatus) using clearing and staining, serial cross‐sections and CT‐scanning. A kinematic analysis was performed to study the respiration and feeding mechanisms and to identify key structures in these mechanisms. Our research showed that the whole body of Balitorinae acts as a suction disc, with friction‐enhancing structures (unculi) on the thickened anterior rays of the paired fins. The abruptly rising head profile, supported by the extremely enlarged lacrimal bone and the flat ventral body surface facilitate effective substrate attachment. During attachment, the pelvic girdle is pulled anterodorsally, suggesting the formation of a negative pressure underneath the body. Detachment by water inflow underneath the body is prevented by three mechanisms. 1) Barbels control the water inflow by detachment and reattachment to the substrate. 2) Most water present underneath the body is removed during inspiration. 3) Excess water is regularly removed by movements of the posterior pectoral fin rays. The balitorine body is thus modified as such that it allows effective attachment, while not impairing respiration. Comparison with other teleosts living in similar environments shows that most species use more locally concentrated modifications of the paired fins and/or the mouth for attachment. The high diversity in teleostean adhesive apparatuses and associated myological modifications suggest a substantial functional convergent evolution, without necessarily highly convergent anatomical adaptations. J. Morphol. 275:1066–1079, 2014. © 2014 Wiley Periodicals, Inc.     

Revealing the mechanisms of the rostral shift of pelvic fins among teleost fishes

In teleost fishes, the position of the pelvic fins shift during evolution; this positional shift seems to have diversified their locomotion and feeding behavior, thereby expanding the habitats of these fishes. Thus, such a positional shift of the pelvic fins is one of the significant features of teleost fishes from evolutionary, embryological, and taxonomic viewpoints, but no studies to date have investigated the mechanism for the rostral shift of the pelvic fins from the anal region in teleosts. Examining the fate of the prospective pelvic fin cells of the zebrafish Danio rerio and the Nile tilapia Oreochromis niloticus embryos demonstrates that the prospective pelvic fin cells are originally located near the anus, as seen in tetrapods, but their position shifts with respect to the body trunk after its protrusion from the yolk surface. In this article, we highlight such recent findings and discuss the mechanisms of pelvic fin evolution among teleost fishes.     

The origins of adipose fins: an analysis of homoplasy and the serial homology of vertebrate appendages

Adipose fins are appendages found on the dorsal midline between the dorsal and caudal fins in more than 6000 living species of teleost fishes. It has been consistently argued that adipose fins evolved once and have been lost repeatedly across teleosts owing to limited function. Here, we demonstrate that adipose fins originated repeatedly by using phylogenetic and anatomical evidence. This suggests that adipose fins are adaptive, although their function remains undetermined. To test for generalities in the evolution of form in de novo vertebrate fins, we studied the skeletal anatomy of adipose fins across 620 species belonging to 186 genera and 55 families. Adipose fins have repeatedly evolved endoskeletal plates, anterior dermal spines and fin rays. The repeated evolution of fin rays in adipose fins suggests that these fins can evolve new tissue types and increased structural complexity by expressing fin-associated developmental modules in these new territories. Patterns of skeletal elaboration differ between the various occurrences of adipose fins and challenge prevailing hypotheses for vertebrate fin origin. Adipose fins represent a powerful and, thus far, barely studied model for exploring the evolution of vertebrate limbs and the roles of adaptation and generative biases in morphological evolution.     

Allometric growth of the trunk leads to the rostral shift of the pelvic fin in teleost fishes

The pelvic fin position among teleost fishes has shifted rostrally during evolution, resulting in diversification of both behavior and habitat. We explored the developmental basis for the rostral shift in pelvic fin position in teleost fishes using zebrafish (abdominal pelvic fins) and Nile tilapia (thoracic pelvic fins). Cell fate mapping experiments revealed that changes in the distribution of lateral plate mesodermal cells accompany the trunk-tail protrusion. Presumptive pelvic fin cells are originally located at the body wall adjacent to the anterior limit of hoxc10a expression in the spinal cord, and their position shifts rostrally as the trunk grows. We then showed that the differences in pelvic fin position between zebrafish and Nile tilapia were not due to changes in expression or function of gdf11. We also found that hox-independent motoneurons located above the pelvic fins innervate into the pelvic musculature. Our results suggest that there is a common mechanism among teleosts and tetrapods that controls paired appendage positioning via gdf11, but in teleost fishes the position of prospective pelvic fin cells on the yolk surface shifts as the trunk grows. In addition, teleost motoneurons, which lack lateral motor columns, innervate the pelvic fins in a manner independent of the rostral-caudal patterns of hox expression in the spinal cord.     

Axial elongation in fishes: using morphological approaches to elucidate developmental mechanisms in studying body shape

One of the most notable features in looking across fishes is their diversity of body shape and size. Extant actinopterygian fishes range in shape from nearly spheroidal in pufferfishes to extremely elongate in snipe eels with nearly every shape in-between. One extreme along the body-shape continuum is a highly elongate form, which has evolved multiple times independently in Actinopterygii. Thus, comparison of these separate (independent) radiations provides a unique opportunity for examining the anatomical traits underlying elongation as well as the similarities and differences in the evolutionary pathways followed. Body elongation generally evolves via an increase in region-specific vertebral number, although certain lineages elongate via an increase in vertebral length. In this study, we describe how anatomical characters related to feeding and locomotion are correlated with elongation of the body across Actinopterygii. In addition to modifications of the postcranial axial skeleton, elongation in fishes is often accompanied by an increase in head length, loss of the pelvic fins, reduction of the pectoral fins, and expansion of the median fins. Based on anatomical studies and on recent studies of developmental control of the body axis in different species, we hypothesize how an axial trait might change at the genetic level. Overall, we discuss the evolution of body elongation in fishes in light of an understanding of the underlying anatomical modifications, developmental control, ecology, and locomotion.     

Fins,limbs, and tails: outgrowths and axial patterning in vertebrate evolution

Current phylogenies show that paired fins and limbs are unique to jawed vertebrates and their immediate ancestry. Such fins evolved first as a single pair extending from an anterior location, and later stabilized as two pairs at pectoral and pelvic levels. Fin number, identity, and position are therefore key issues in vertebrate developmental evolution. Localization of the AP levels at which developmental signals initiate outgrowth from the body wall may be determined by Hox gene expression patterns along the lateral plate mesoderm. This regionalization appears to be regulated independently of that in the paraxial mesoderm and axial skeleton. When combined with current hypotheses of Hox gene phylogenetic and functional diversity, these data suggest a new model of fin/limb developmental evolution. This coordinates body wall regions of outgrowth with primitive boundaries established in the gut, as well as the fundamental nonequivalence of pectoral and pelvic structures. BioEssays 20 :371–381, 1998. © 1998 John Wiley & Sons Inc.     

Phylogeny of the snailfishes (Teleostei: Liparidae) based on molecular and morphological data

Liparidae (snailfishes) is one of the most diverse and abundant fish families in polar and deep-sea habitats. However, the evolution of this family is poorly known because of the rarity of many species and difficulties in scoring morphological characters. We perform phylogenetic analyses of Liparidae using sequences from two mtDNA genes, 16S (585 bp) and cytochrome b (426 bp), and 84 morphological characters from 24 species of Liparidae and 4 species of Cyclopteridae (outgroup). The present study confirms earlier hypotheses that the shallow-water genera, such as Liparis and Crystallichthys, occupy basal positions and that deep-water genera, such as Careproctus, Elassodiscus, Rhinoliparis, Paraliparis, Rhodichthys and Psednos, are increasingly derived. The later two genera form a terminal clade which does not include Paraliparis. The topology shows that the family has undergone a reductive type of evolution, with a gradual loss of characters (e.g. sucking disc/pelvic fins, pseudobranchial filaments, skin spinules). Nectoliparis, which had previously been placed either as the basal most genus or among the most derived genera, are found to occupy the most basal position among the taxa analyzed. This result indicates that the sucking disc has been lost at least twice during the evolution of the Liparidae. The basal position of Nectoliparis is supported by its plesiomorphic otolith morphology, whereas an advanced overgrown otolith ostium, unique among teleosts, is found to be apomorphic for a clade containing the derived genera: Paraliparis, Psednos, Rhinoliparis and Rhodichthys. We also identify the presence of probable nuclear inserts of mitochondrial DNA (Numts) in three species of Careproctus and in Elassodiscus caudatus.     

Comparative morphology and osteology of pelvic fin‐derived midline suckers in lumpfishes,snailfishes and gobies

Some fishes use modified body structures – including pelvic fins – to produce suction to facilitate stability in turbulent environments. This study compares the morphology and osteology of the pelvic suckers of representative lumpfishes (Cyclopteridae), snailfishes (Liparidae) and gobies (Gobiidae). In all species studied the midline sucker (pelvic suctorial organ [PSO]) is formed from the pelvic girdle and fin rays I and 5 of the pelvic fins, comprised of similar osteological elements to those found in the pelvic girdle and pelvic fin rays although the morphology of the bony elements is species‐specific. Pelvic suctorial organs in those fishes that lack pelvic girdles are therefore homologous to pelvic girdles. The phenotypic diversity seen in so few species indicates that many sucker morphologies have arisen, origination depending on the concerted development of muscular, skeletal, nervous, and skin body tissues. The structure of the soft rays of the pelvic fins in the liparids and cyclopterids is unusual and indicative of unconventional developmental patterning of fin ray halves and of evolution in the underlying mechanisms responsible for the development of midline suckers.     

The evolution of paired fins

Summary The Archipterygium is Gegenbaur’s most lasting contribution to the study of vertebrate limb evolution. This transformational hypothesis of gill arches to limb girdles, rays to fins, and proposal of a vertebrate fin-limb groundplan, is generally treated as a flawed alternative to the more widely accepted lateral fin-fold hypothesis of vertebrate limb evolution. When compared to the phylogenetic distribution and diversity of fins and limbs, both hypotheses fail. Dermal skeletal lateral folds, spines and keels originate repeatedly in vertebrate evolution, but paired fins with girdles originate at pectoral level and are anteroposteriorly restricted. Pelvic fins emerge later in phylogeny; pectoral and pelvic appendages primitively differ. Endoskeletal girdles never exhibit characteristics of gill arches. The emergent sequence of paired fin evolution depends upon phylogenetic hypotheses within which extant agnathan interrelationships are uncertain; positions of jawless fossil fish along the gnathostome stem are insecure; the fossil data set is patchy. However, certain features of the data set are robust. This has prompted a reconsideration of Gegenbaur’s hypothesized arch-girdle relationship, and an iterative homology between scapulocoracoid and extrabranchial cartilages is suggested. No transformation of arch to girdle is necessarily implied, but some signal of developmental relatedness is predicted.     

Jaw structures and movements in higher teleostean fishes

All of the diverse jaw structures in higher teleosts appear to be modifications of a single basal type and are treated as such. Only some of the principal variants are discussed. Though the two jaws act as a coordinated unit during feeding, their movements are different. The upper and lower jaws are discussed separately. In the upper jaw the principal concern is with the various types of premaxillary protrusion and with the secondary development in some groups of a rocking premaxilla. For the lower jaw most of the account is devoted to the repeated differentiation of movements in its anterior and posterior sections. The paper concludes with comments on the jaw apparatus as a functional unit and its evolution in higher teleosts.     

The pelvic girdle and fin in certain Indian hill stream fishes

This paper deals with the functional morphology of the pelvic girdle and fins in various genera of hill stream cyprinid and sisorid fishes. The pelvic plate of Pseudecheneis shows the greatest modification; it is unusually large and reaches the coracoids of the pectoral arch in front.
The elaborate working of the pelvic muscles and their function in bringing about effective adhesion by the pelvic fins is described in detail. The formation of a new muscle, M. pars retractor ischii of the M. mesioventralis, is reported in Garra and Psilorhynchus (Cyprinidae) and in Glyptothorax and Pseudecheneis (Sisoridae). In Pseudecheneis , the complete separation of this muscle from the M. mesioventral, and modification of the M. protractor ischii, are discussed in relation to the crawling habit of the genus. The appearance of the M. arrector pel vicalis ventralis in Glyptothorax and Pseudecheneis among sisorids has been associated with the adhesive function of the outer ray.     

Development of the paired fins in the paddlefish, Polyodon spathula

In Polyodon spathula, the pectoral fin radials, with the exception of the metapterygium, are derived from the decomposition of a single continuous cartilage fin plate that is continuous with the scapulocoracoid. This cartilage sheet develops two interior splits to form three precursor pieces, and these decompose in a predictable way to generate the propterygium and radials. The metapterygium is an extension of the scapulocoracoid that segments off of it during early development. To our knowledge, this has not been reported for acipenserids or other basal actinopterygians. In teleosts, the proximal radials also develop from the "break up" of an initially continuous paddle-like sheet of cartilage along the posterior edge of the scapulocoracoid, and in Polypterus and sharks a similar pattern holds. Thus, the pattern observed in Polyodon may represent the basal developmental condition for the gnathostome pectoral fin. The process underlying development of the superficially similar cartilages of the pelvic and pectoral fins is different. In the pectoral fin, the metapterygium is segmented off of the scapulocoracoid and other radials form from the decomposition of the cartilage plate. In contrast, individual rod-like basipterygial elements form in a close one-to-one correspondence with the middle radials of the pelvic fin, but later fuse to form an anterior element that is branched in appearance. To evaluate further claims of similarity among the pectoral and pelvic fin elements of various fishes, the course of the development of these structures must be observed. The pectoral fin and girdle in Polyodon ossifies in a different sequence than that proposed as ancestral (and highly conserved) for actinopterygians: the supracleithrum ossifies significantly before the cleithrum. The later ossification of the cleithrum in Polyodon may be related to the primary use of the caudal fin vs. the pectoral fins in their locomotion.     

Synchronized swimming: coordination of pelvic and pectoral fins during augmented punting by the freshwater stingray Potamotrygon orbignyi

Benthic animals live at the juncture of fluid and solid environments, an interface that shapes many aspects of their behavior, including their means of locomotion. Aquatic walking and similar substrate-dependent forms of underwater propulsion have evolved multiple times in benthic invertebrate and vertebrate taxa, including batoid elasmobranchs. Skates (Rajidae) use the pelvic fins to punt across the substrate, keeping the pectoral fin disc still. Other batoids combine pelvic fin motions with pectoral fin undulation in augmented punting, but the coordination of these two modes has not been described. In this study of an augmented punter, the freshwater stingray Potamotrygon orbignyi, we demonstrate the synchrony of pelvic and pectoral fin cycles. The punt begins as the pelvic fins, held in an anterior position, are planted into the substrate and used to push the body forward. Meanwhile, a wave of pectoral fin undulation begins, increasing to maximum height just before the cycle's halfway point, when the pelvic fins reach their furthest posterior extension. The pectoral fin wave subsides as the pelvic fins return to their starting position for subsequent punts. Despite definitive links between pectoral and pelvic fin activity, we find no significant relationship between pectoral fin kinematics (frequency, wave height, and wave speed) and punt performance. However, slip calculations indicate that pectoral undulation can produce thrust and augment punting. Pelvic fin kinematics (frequency and duty factor) have significant effects, suggesting that while both sets of fins contribute to thrust generation, the pelvic fins likely determine punt performance.     

Developmental constraints on fin diversity

The fish fin is a breathtaking repository full of evolutionary diversity, novelty, and convergence. Over 500 million years, the adaptation to novel habitats has provided landscapes of fin diversity. Although comparative anatomy of evolutionarily divergent patterns over centuries has highlighted the fundamental architectures and evolutionary trends of fins, including convergent evolution, the developmental constraints on fin evolution, which bias the evolutionary trajectories of fin morphology, largely remain elusive. Here, we review the evolutionary history, developmental mechanisms, and evolutionary underpinnings of paired fins, illuminating possible developmental constraints on fin evolution. Our compilation of anatomical and genetic knowledge of fin development sheds light on the canalized and the unpredictable aspects of fin shape in evolution. Leveraged by an arsenal of genomic and genetic tools within the working arena of spectacular fin diversity, evolutionary developmental biology embarks on the establishment of conceptual framework for developmental constraints, previously enigmatic properties of evolution.     

Solitary chemosensory cells — taste,common chemical sense or what?

Summary Secondary solitary chemosensory cells (SCCs) occur scattered within the epidermis of lampreys, teleosts and ranid tadpoles. Counts in representative telost species revealed that SCC's outnumber chemosensory cells organized in taste buds. Therefore, SCCs may be considered the structural substrate of a basic and probably important vertebrate chemosense. However, detailed information on structure, innervation and function is only available from specialized fins in a few teleost species, where SCCs are sufficiently concentrated. The foremost research model has been the anterior dorsal fin (ADF) in rocklings, which contains millions of SCCs but no other specialized chemosensory elements. It has been shown that these ADF-SCCs are innervated from the recurrent facial nerve. Electrophysiological recordings revealed that there is virtually no overlap in stimulus spectrum between the ADF-SCCs and pelvic fin taste buds; SCC responses could only be triggered by dilutions of heterospecific fish body mucus. Results of behavioural experiments indicate that fish mucus is indeed a relevant stimulus. Therefore it is hypothesized that the biological role of the ADF-SCCs is predator avoidance rather than search for food. Whether these findings are valid for rockings only, or can be generalized for the scattered SCC systems in more than 20000 species of fish and in some amphibians, remains an open question. Further investigations on the function and biological roles of the SCC chemosense will be crucially important to improve our understanding of sensory perception and its evolution in aquatic vertebrates.     

Vertebrate vitellogenin gene duplication in relation to the "3R hypothesis": correlation to the pelagic egg and the oceanic radiation of teleosts

The spiny ray-finned teleost fishes (Acanthomorpha) are the most successful group of vertebrates in terms of species diversity. Their meteoric radiation and speciation in the oceans during the late Cretaceous and Eocene epoch is unprecedented in vertebrate history, occurring in one third of the time for similar diversity to appear in the birds and mammals. The success of marine teleosts is even more remarkable considering their long freshwater ancestry, since it implies solving major physiological challenges when freely broadcasting their eggs in the hyper-osmotic conditions of seawater. Most extant marine teleosts spawn highly hydrated pelagic eggs, due to differential proteolysis of vitellogenin (Vtg)-derived yolk proteins. The maturational degradation of Vtg involves depolymerization of mainly the lipovitellin heavy chain (LvH) of one form of Vtg to generate a large pool of free amino acids (FAA 150-200 mM). This organic osmolyte pool drives hydration of the ooctye while still protected within the maternal ovary. In the present contribution, we have used Bayesian analysis to examine the evolution of vertebrate Vtg genes in relation to the "3R hypothesis" of whole genome duplication (WGD) and the functional end points of LvH degradation during oocyte maturation. We find that teleost Vtgs have experienced a post-R3 lineage-specific gene duplication to form paralogous clusters that correlate to the pelagic and benthic character of the eggs. Neo-functionalization allowed one paralogue to be proteolyzed to FAA driving hydration of the maturing oocytes, which pre-adapts them to the marine environment and causes them to float. The timing of these events matches the appearance of the Acanthomorpha in the fossil record. We discuss the significance of these adaptations in relation to ancestral physiological features, and propose that the neo-functionalization of duplicated Vtg genes was a key event in the evolution and success of the teleosts in the oceanic environment.     

The Biological Origin of Linguistic Diversity

In contrast with animal communication systems, diversity is characteristic of almost every aspect of human language. Languages variously employ tones, clicks, or manual signs to signal differences in meaning; some languages lack the noun-verb distinction (e.g., Straits Salish), whereas others have a proliferation of fine-grained syntactic categories (e.g., Tzeltal); and some languages do without morphology (e.g., Mandarin), while others pack a whole sentence into a single word (e.g., Cayuga). A challenge for evolutionary biology is to reconcile the diversity of languages with the high degree of biological uniformity of their speakers. Here, we model processes of language change and geographical dispersion and find a consistent pressure for flexible learning, irrespective of the language being spoken. This pressure arises because flexible learners can best cope with the observed high rates of linguistic change associated with divergent cultural evolution following human migration. Thus, rather than genetic adaptations for specific aspects of language, such as recursion, the coevolution of genes and fast-changing linguistic structure provides the biological basis for linguistic diversity. Only biological adaptations for flexible learning combined with cultural evolution can explain how each child has the potential to learn any human language.     

Shh and forebrain evolution in the blind cavefish Astyanax mexicanus

The blind cavefish and its surface counterpart of the teleost species Astyanax mexicanus constitute an excellent model to study the evolution of morphological features. During adaptation to their lives in perpetual darkness, the cave population has lost eyes (and pigmentation), but has gained several constructive traits. Recently, the demonstration that an increase in Shh (Sonic Hedgehog) midline signalling was indirectly responsible for the loss of eyes in cavefish led to new ways to search for possible modifications in the forebrain of these cavefish, as this anterior-most region of the vertebrate central nervous system develops under close control of the powerful Shh morphogen. In this review, we summarize the recent progress in the understanding of forebrain and eye modifications in cavefish. These include major changes in cell death, cell proliferation and cell migration in various parts of the forebrain when compared with their surface counterparts with eyes. The outcome of these modifications, in terms of neuronal circuitry, morphological and behavioral adaptations are discussed.