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1.  Development and Evolution of the Muscles of the Pelvic Fin 
PLoS Biology  2011;9(10):e1001168.
Locomotor strategies in terrestrial tetrapods have evolved from the utilisation of sinusoidal contractions of axial musculature, evident in ancestral fish species, to the reliance on powerful and complex limb muscles to provide propulsive force. Within tetrapods, a hindlimb-dominant locomotor strategy predominates, and its evolution is considered critical for the evident success of the tetrapod transition onto land. Here, we determine the developmental mechanisms of pelvic fin muscle formation in living fish species at critical points within the vertebrate phylogeny and reveal a stepwise modification from a primitive to a more derived mode of pelvic fin muscle formation. A distinct process generates pelvic fin muscle in bony fishes that incorporates both primitive and derived characteristics of vertebrate appendicular muscle formation. We propose that the adoption of the fully derived mode of hindlimb muscle formation from this bimodal character state is an evolutionary innovation that was critical to the success of the tetrapod transition.
Author Summary
The transition of vertebrates from water to land is a fundamental step in the evolution of terrestrial life. Innovations that were critical to this transition were the evolution of a weight bearing pelvis, hindlimbs and their associated musculature, and the development of the “rear wheel drive” strategy that predominates in terrestrial locomotion. The fossil record can reveal how the skeletal framework of the load-bearing limbs of tetrapods (animals descended from fish) has evolved, but as soft tissues are rarely preserved within the fossil record, it can shed little light on how the accompanying dramatic alterations of the limb musculature arose developmentally. To examine this question we determined the mechanisms that generate fin muscles within larvae of living species representing several clades of fish across the vertebrate phylogeny. Using this comparative approach and a novel somite transplantation technique in zebrafish, we determine that the pelvic fin muscles of bony fish are generated by a bimodal mechanism that has features of limb/fin muscle formation in tetrapods and primitive cartilaginous fish. Using these data, we propose a unifying evolutionary hypothesis on the origins of the muscle of the paired fins and limbs, and speculate that the adoption of tetrapod mode of hindlimb muscle formation was also an evolutionary innovation critical to the success of the tetrapod transition.
PMCID: PMC3186808  PMID: 21990962
2.  Fossil Fishes from China Provide First Evidence of Dermal Pelvic Girdles in Osteichthyans 
PLoS ONE  2012;7(4):e35103.
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.
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.
PMCID: PMC3318012  PMID: 22509388
3.  Comparative pelvic development of the axolotl (Ambystoma mexicanum) and the Australian lungfish (Neoceratodus forsteri): conservation and innovation across the fish-tetrapod transition 
EvoDevo  2013;4:3.
The fish-tetrapod transition was one of the major events in vertebrate evolution and was enabled by many morphological changes. Although the transformation of paired fish fins into tetrapod limbs has been a major topic of study in recent years, both from paleontological and comparative developmental perspectives, the interest has focused almost exclusively on the distal part of the appendage and in particular the origin of digits. Relatively little attention has been paid to the transformation of the pelvic girdle from a small unipartite structure to a large tripartite weight-bearing structure, allowing tetrapods to rely mostly on their hindlimbs for locomotion. In order to understand how the ischium and the ilium evolved and how the acetabulum was reoriented during this transition, growth series of the Australian lungfish Neoceratodus forsteri and the Mexican axolotl Ambystoma mexicanum were cleared and stained for cartilage and bone and immunostained for skeletal muscles. In order to understand the myological developmental data, hypotheses about the homologies of pelvic muscles in adults of Latimeria, Neoceratodus and Necturus were formulated based on descriptions from the literature of the coelacanth (Latimeria), the Australian Lungfish (Neoceratodus) and a salamander (Necturus).
In the axolotl and the lungfish, the chondrification of the pelvic girdle starts at the acetabula and progresses anteriorly in the lungfish and anteriorly and posteriorly in the salamander. The ilium develops by extending dorsally to meet and connect to the sacral rib in the axolotl. Homologous muscles develop in the same order with the hypaxial musculature developing first, followed by the deep, then the superficial pelvic musculature.
Development of the pelvic endoskeleton and musculature is very similar in Neoceratodus and Ambystoma. If the acetabulum is seen as being a fixed landmark, the evolution of the ischium only required pubic pre-chondrogenic cells to migrate posteriorly. It is hypothesized that the iliac process or ridge present in most tetrapodomorph fish is the precursor to the tetrapod ilium and that its evolution mimicked its development in modern salamanders.
PMCID: PMC3651358  PMID: 23342976
Fish-tetrapod transition; Pelvic girdle; Heterochrony; Extant phylogenetic bracketing method; Evolutionary novelty; Muscle development
4.  Ancestry of motor innervation to pectoral fin and forelimb 
Nature Communications  2010;1(4):1-8.
Motor innervation to the tetrapod forelimb and fish pectoral fin is assumed to share a conserved spinal cord origin, despite major structural and functional innovations of the appendage during the vertebrate water-to-land transition. In this paper, we present anatomical and embryological evidence showing that pectoral motoneurons also originate in the hindbrain among ray-finned fish. New and previous data for lobe-finned fish, a group that includes tetrapods, and more basal cartilaginous fish showed pectoral innervation that was consistent with a hindbrain-spinal origin of motoneurons. Together, these findings support a hindbrain–spinal phenotype as the ancestral vertebrate condition that originated as a postural adaptation for pectoral control of head orientation. A phylogenetic analysis indicated that Hox gene modules were shared in fish and tetrapod pectoral systems. We propose that evolutionary shifts in Hox gene expression along the body axis provided a transcriptional mechanism allowing eventual decoupling of pectoral motoneurons from the hindbrain much like their target appendage gained independence from the head.
It was previously thought that the nerves in the pectoral fin of fish came solely from the spinal cord. Here, motoneurons in ray-finned fish are shown to also originate from the hindbrain, demonstrating that innervation was from both the hindbrain and the spinal cord in ancesteral vertebrates.
PMCID: PMC2963806  PMID: 20975699
5.  First description of a musculoskeletal linkage in an adipose fin: innovations for active control in a primitively passive appendage 
Adipose fins are enigmatic appendages found between the dorsal and caudal fins of some teleostean fishes. Long thought to be vestigial, degenerate second dorsal fins, remnants of the primitive gnathostome condition, adipose fins have since been recognized as novel morphologies. Unique among the fins of extant fishes, adipose fins have uniformly been described as passive structures, with no associated musculature. Here we provide the first description of a musculoskeletal linkage in an adipose fin, identified in the sun catfish Horabagrus brachysoma. Modified supracarinalis posterior muscles insert from the dorsal midline anterior to the adipose fin by tendons onto the fin base. An additional pair of posterior adipose-fin muscles also inserts upon the fin base and lay posterolateral to the fin, superficial to the axial muscle. This musculoskeletal linkage is an evolutionary innovation, a novel mechanism for controlling adipose-fin movement. These muscles appear to exemplify two approaches by which fins evolve to be actively controlled. We hypothesize that the anterior muscles arose through co-option of an existing fin linkage, while the posterior muscles originated as de novo fin muscles. These findings present adipose fins as a rich system within which to explore the evolution of novel vertebrate appendages.
PMCID: PMC3574436  PMID: 23135670
adipose fin; evolutionary innovation; swimming; catfish
6.  Stem sarcopterygians have primitive polybasal fin articulation 
Biology Letters  2009;5(3):372-375.
Among osteichthyans, basal actinopterygian fishes (e.g. paddlefish and bowfins) have paired fins with three endoskeletal components (pro-, meso- and metapterygia) articulating with polybasal shoulder girdles, while sarcopterygian fishes (lungfish, coelacanths and relatives) have paired fins with one endoskeletal component (metapterygium) articulating with monobasal shoulder girdles. In the fin–limb transition, the origin of the sarcopterygian paired fins triggered new possibilities of fin articulation and movement, and established the proximal segments (stylopod and zeugopod) of the presumptive tetrapod limb. Several authors have stated that the monobasal paired fins in sarcopterygians evolved from a primitive polybasal condition. However, the fossil record has been silent on whether and when the inferred transition took place. Here we describe three-dimensionally preserved shoulder girdles of two stem sarcopterygians (Psarolepis and Achoania) from the Lower Devonian of Yunnan, which demonstrate that stem sarcopterygians have polybasal pectoral fin articulation as in basal actinopterygians. This finding provides a phylogenetic and temporal constraint for studying the origin of the stylopod, which must have originated within the stem sarcopterygian lineage through the loss of the propterygium and mesopterygium.
PMCID: PMC2679918  PMID: 19324642
sarcopterygians; fin–limb transition; stylopod; shoulder girdle; polybasal fin articulation
7.  Conservation and Divergence of Regulatory Strategies at Hox Loci and the Origin of Tetrapod Digits 
PLoS Biology  2014;12(1):e1001773.
During development, expression of the Hoxa and Hoxd genes in zebrafish fins and mouse limbs are regulated via a conserved chromatin structure. However, zebrafish lack certain regulatory elements required to produce digits, revealing that radials—the fin's bony elements—are likely not homologous to tetrapod digits.
The evolution of tetrapod limbs from fish fins enabled the conquest of land by vertebrates and thus represents a key step in evolution. Despite the use of comparative gene expression analyses, critical aspects of this transformation remain controversial, in particular the origin of digits. Hoxa and Hoxd genes are essential for the specification of the different limb segments and their functional abrogation leads to large truncations of the appendages. Here we show that the selective transcription of mouse Hoxa genes in proximal and distal limbs is related to a bimodal higher order chromatin structure, similar to that reported for Hoxd genes, thus revealing a generic regulatory strategy implemented by both gene clusters during limb development. We found the same bimodal chromatin architecture in fish embryos, indicating that the regulatory mechanism used to pattern tetrapod limbs may predate the divergence between fish and tetrapods. However, when assessed in mice, both fish regulatory landscapes triggered transcription in proximal rather than distal limb territories, supporting an evolutionary scenario whereby digits arose as tetrapod novelties through genetic retrofitting of preexisting regulatory landscapes. We discuss the possibility to consider regulatory circuitries, rather than expression patterns, as essential parameters to define evolutionary synapomorphies.
Author Summary
Our upper limbs differ from fish fins, notably by their subdivision into arm and hand regions, which are separated by a complex articulation, the wrist. The development of this anatomy is associated with two distinct waves of expression of the Hoxa and Hoxd genes during development. Would such a shared expression pattern be sufficient to infer homology between fish fins and mouse limbs? We investigated this question here, looking at whether the two phases of Hox gene transcription that are observed during tetrapod limb development also occur during zebrafish fin development. We find the answer is “not quite.” For although the mechanisms that regulate the expression of Hoxa and Hoxd are comparable between zebrafish fins and mouse limbs, when the genomic regions that regulate Hox gene expression in fish fins are introduced into transgenic mice, they trigger Hox gene expression in only the proximal limb segment (the segment nearest the body) and not in the presumptive digits. We conclude that although fish have the Hox regulatory toolkit to produce digits, this potential is not utilized as it is in tetrapods, and as a result we propose that fin radials—the bony elements of fins—are not homologous to tetrapod digits.
PMCID: PMC3897358  PMID: 24465181
8.  A Marine Stem-Tetrapod from the Devonian of Western North America 
PLoS ONE  2012;7(3):e33683.
The origin of terrestrial vertebrates represents one of the major evolutionary and ecological transformations in the history of life, and the established timing and environment of this transition has recently come under scrutiny. The discovery and description of a well-preserved fossil sarcopterygian (fleshy-limbed vertebrate) from the Middle Devonian of Nevada helps to refine and question aspects of the temporal and anatomical framework that underpins the tetrapod condition. This new taxon, Tinirau clackae, demonstrates that substantial parallelism pervaded the early history of stem-tetrapods, raises additional questions about when digited sarcopterygians first evolved, and further documents that incipient stages of the terrestrial appendicular condition began when sarcopterygians still retained their median fins and occupied aquatic habitats.
PMCID: PMC3308997  PMID: 22448265
9.  Biphasic Hoxd Gene Expression in Shark Paired Fins Reveals an Ancient Origin of the Distal Limb Domain 
PLoS ONE  2007;2(8):e754.
The evolutionary transition of fins to limbs involved development of a new suite of distal skeletal structures, the digits. During tetrapod limb development, genes at the 5′ end of the HoxD cluster are expressed in two spatiotemporally distinct phases. In the first phase, Hoxd9-13 are activated sequentially and form nested domains along the anteroposterior axis of the limb. This initial phase patterns the limb from its proximal limit to the middle of the forearm. Later in development, a second wave of transcription results in 5′ HoxD gene expression along the distal end of the limb bud, which regulates formation of digits. Studies of zebrafish fins showed that the second phase of Hox expression does not occur, leading to the idea that the origin of digits was driven by addition of the distal Hox expression domain in the earliest tetrapods. Here we test this hypothesis by investigating Hoxd gene expression during paired fin development in the shark Scyliorhinus canicula, a member of the most basal lineage of jawed vertebrates. We report that at early stages, 5′Hoxd genes are expressed in anteroposteriorly nested patterns, consistent with the initial wave of Hoxd transcription in teleost and tetrapod paired appendages. Unexpectedly, a second phase of expression occurs at later stages of shark fin development, in which Hoxd12 and Hoxd13 are re-expressed along the distal margin of the fin buds. This second phase is similar to that observed in tetrapod limbs. The results indicate that a second, distal phase of Hoxd gene expression is not uniquely associated with tetrapod digit development, but is more likely a plesiomorphic condition present the common ancestor of chondrichthyans and osteichthyans. We propose that a temporal extension, rather than de novo activation, of Hoxd expression in the distal part of the fin may have led to the evolution of digits.
PMCID: PMC1937022  PMID: 17710153
10.  Tetrapod-like axial regionalization in an early ray-finned fish 
Tetrapods possess up to five morphologically distinct vertebral series: cervical, thoracic, lumbar, sacral and caudal. The evolution of axial regionalization has been linked to derived Hox expression patterns during development and the demands of weight-bearing and walking on land. These evolutionary and functional explanations are supported by an absence of similar traits in fishes, living and extinct. Here, I show that, Tarrasius problematicus, a marine ray-finned fish from the Mississippian (Early Carboniferous; 359–318 Ma) of Scotland, is the first non-tetrapod known to possess tetrapod-like axial regionalization. Tarrasius exhibits five vertebral regions, including a seven-vertebrae ‘cervical’ series and a reinforced ‘sacrum’ over the pelvic area. Most vertebrae possess processes for intervertebral contact similar to tetrapod zygapophyses. The fully aquatic Tarrasius evolved these morphologies alongside other traits convergent with early tetrapods, including a naked trunk, and a single median continuous fin. Regional modifications in Tarrasius probably facilitated pelagic swimming, rather than a terrestrial lifestyle or walking gait, presenting an alternative scenario for the evolution of such traits in tetrapods. Axial regionalization in Tarrasius could indicate tetrapod-like Hox expression patterns, possibly representing the primitive state for jawed vertebrates. Alternately, it could signal a weaker relationship, or even a complete disconnect, between Hox expression domains and vertebrate axial plans.
PMCID: PMC3385743  PMID: 22628471
axial patterning; neck; evolutionary development; biomechanics; sacrum; terrestriality
11.  Paedocypris, a new genus of Southeast Asian cyprinid fish with a remarkable sexual dimorphism, comprises the world's smallest vertebrate 
Paedocypris is a new genus of paedomorphic cyprinid fish from highly acidic blackwater peat swamps in Southeast Asia. It includes two new species, one of which (Paedocypris progenetica) appears to be the smallest fish and vertebrate known, with the smallest mature female measuring a mere 7.9 mm. Paedocypris has many ’larval’ features typically associated with paedomorphic fish (e.g. narrow frontals that leave the brain unprotected dorsally by bone and a precaudal larval-fin-fold), but, uniquely among fishes, males also possess highly modified pelvic fins with hypertrophied muscles and a keratinized pad in front of the pelvic girdle, which, we hypothesize, function together as a clasping or holding device, thereby suggesting an unusual reproductive mode. Unfortunately, habitat destruction jeopardizes the survival of these fishes and thus opportunities for further research.
PMCID: PMC1560243  PMID: 16627273
Paedocypris; Cyprinidae; peat swamps; smallest vertebrate; sexual dimorphism
12.  Visual ecology of the Australian lungfish (Neoceratodus forsteri) 
BMC Ecology  2008;8:21.
The transition from water to land was a key event in the evolution of vertebrates that occurred over a period of 15–20 million years towards the end of the Devonian. Tetrapods, including all land-living vertebrates, are thought to have evolved from lobe-finned (sarcopterygian) fish that developed adaptations for an amphibious existence. However, while many of the biomechanical and physiological modifications necessary to achieve this feat have been studied in detail, little is known about the sensory adaptations accompanying this transition. In this study, we investigated the visual system and visual ecology of the Australian lungfish Neoceratodus forsteri, which is the most primitive of all the lungfish and possibly the closest living relative to the ancestors of tetrapods.
Juvenile Neoceratodus have five spectrally distinct retinal visual pigments. A single type of rod photoreceptor contains a visual pigment with a wavelength of maximum absorbance (λmax) at 540 nm. Four spectrally distinct single cone photoreceptors contain visual pigments with λmax at 366 (UVS), 479 (SWS), 558 (MWS) and 623 nm (LWS). No double cones were found. Adult lungfish do not possess UVS cones and, unlike juveniles, have ocular media that prevent ultraviolet light from reaching the retina. Yellow ellipsoidal/paraboloidal pigments in the MWS cones and red oil droplets in the LWS cones narrow the spectral sensitivity functions of these photoreceptors and shift their peak sensitivity to 584 nm and 656 nm, respectively. Modelling of the effects of these intracellular spectral filters on the photoreceptor colour space of Neoceratodus suggests that they enhance their ability to discriminate objects, such as plants and other lungfishes, on the basis of colour.
The presence of a complex colour vision system based on multiple cone types and intracellular spectral filters in lungfishes suggests that many of the ocular characteristics seen in terrestrial or secondarily aquatic vertebrates, such as birds and turtles, may have evolved in shallow water prior to the transition onto land. Moreover, the benefits of spectral filters for colour discrimination apply equally to purely aquatic species as well as semi-aquatic and terrestrial animals. The visual system of the Australian lungfish resembles that of terrestrial vertebrates far more closely than that of other sarcopterygian fish. This supports the idea that lungfishes, and not the coelacanth, are the closest living relatives of the ancestors of tetrapods.
PMCID: PMC2639370  PMID: 19091135
13.  An antiarch placoderm shows that pelvic girdles arose at the root of jawed vertebrates 
Biology Letters  2012;8(3):453-456.
Almost all gnathostomes or jawed vertebrates (including osteichthyans, chondrichthyans, ‘acanthodians’ and most placoderms) possess paired pectoral and pelvic fins. To date, it has generally been believed that antiarch placoderms (extinct armoured jawed fishes from the Silurian–Devonian periods) lacked pelvic fins. The putative absence of pelvic fins is a key character bearing on the monophyly or paraphyly of placoderms. It also has far-reaching implications for studying the sequence of origin of pelvic girdles versus that of movable jaws in the course of vertebrate evolution. Parayunnanolepis xitunensis represents the only example of a primitive antiarch with extensive post-thoracic preservation, and its original description has been cited as confirming the primitive lack of pelvic fins in early antiarchs. Here, we present a revised description of Parayunnanolepis and offer the first unambiguous evidence for the presence of pelvic girdles in antiarchs. As antiarchs are placed at the base of the gnathostome radiation in several recent studies, our finding shows that all jawed vertebrates (including antiarch placoderms) primitively possess both pectoral and pelvic fins and that the pelvic fins did not arise within gnathostomes at a point subsequent to the origin of jaws.
PMCID: PMC3367742  PMID: 22219394
pelvic girdles; placoderms; antiarchs; jawed vertebrates; Devonian
14.  Analysis of the African coelacanth genome sheds light on tetrapod evolution 
Amemiya, Chris T. | Alföldi, Jessica | Lee, Alison P. | Fan, Shaohua | Philippe, Hervé | MacCallum, Iain | Braasch, Ingo | Manousaki, Tereza | Schneider, Igor | Rohner, Nicolas | Organ, Chris | Chalopin, Domitille | Smith, Jeramiah J. | Robinson, Mark | Dorrington, Rosemary A. | Gerdol, Marco | Aken, Bronwen | Biscotti, Maria Assunta | Barucca, Marco | Baurain, Denis | Berlin, Aaron M. | Blatch, Gregory L. | Buonocore, Francesco | Burmester, Thorsten | Campbell, Michael S. | Canapa, Adriana | Cannon, John P. | Christoffels, Alan | De Moro, Gianluca | Edkins, Adrienne L. | Fan, Lin | Fausto, Anna Maria | Feiner, Nathalie | Forconi, Mariko | Gamieldien, Junaid | Gnerre, Sante | Gnirke, Andreas | Goldstone, Jared V. | Haerty, Wilfried | Hahn, Mark E. | Hesse, Uljana | Hoffmann, Steve | Johnson, Jeremy | Karchner, Sibel I. | Kuraku, Shigehiro | Lara, Marcia | Levin, Joshua Z. | Litman, Gary W. | Mauceli, Evan | Miyake, Tsutomu | Mueller, M. Gail | Nelson, David R. | Nitsche, Anne | Olmo, Ettore | Ota, Tatsuya | Pallavicini, Alberto | Panji, Sumir | Picone, Barbara | Ponting, Chris P. | Prohaska, Sonja J. | Przybylski, Dariusz | Saha, Nil Ratan | Ravi, Vydianathan | Ribeiro, Filipe J. | Sauka-Spengler, Tatjana | Scapigliati, Giuseppe | Searle, Stephen M. J. | Sharpe, Ted | Simakov, Oleg | Stadler, Peter F. | Stegeman, John J. | Sumiyama, Kenta | Tabbaa, Diana | Tafer, Hakim | Turner-Maier, Jason | van Heusden, Peter | White, Simon | Williams, Louise | Yandell, Mark | Brinkmann, Henner | Volff, Jean-Nicolas | Tabin, Clifford J. | Shubin, Neil | Schartl, Manfred | Jaffe, David | Postlethwait, John H. | Venkatesh, Byrappa | Di Palma, Federica | Lander, Eric S. | Meyer, Axel | Lindblad-Toh, Kerstin
Nature  2013;496(7445):311-316.
It was a zoological sensation when a living specimen of the coelacanth was first discovered in 1938, as this lineage of lobe-finned fish was thought to have gone extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features . Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain, and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues demonstrate the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution.
PMCID: PMC3633110  PMID: 23598338
15.  Sequence and organization of coelacanth neurohypophysial hormone genes: Evolutionary history of the vertebrate neurohypophysial hormone gene locus 
The mammalian neurohypophysial hormones, vasopressin and oxytocin are involved in osmoregulation and uterine smooth muscle contraction respectively. All jawed vertebrates contain at least one homolog each of vasopressin and oxytocin whereas jawless vertebrates contain a single neurohypophysial hormone called vasotocin. The vasopressin homolog in non-mammalian vertebrates is vasotocin; and the oxytocin homolog is mesotocin in non-eutherian tetrapods, mesotocin and [Phe2]mesotocin in lungfishes, and isotocin in ray-finned fishes. The genes encoding vasopressin and oxytocin genes are closely linked in the human and rodent genomes in a tail-to-tail orientation. In contrast, their pufferfish homologs (vasotocin and isotocin) are located on the same strand of DNA with isotocin gene located upstream of vasotocin gene separated by five genes, suggesting that this locus has experienced rearrangements in either mammalian or ray-finned fish lineage, or in both lineages. The coelacanths occupy a unique phylogenetic position close to the divergence of the mammalian and ray-finned fish lineages.
We have sequenced a coelacanth (Latimeria menadoensis) BAC clone encompassing the neurohypophysial hormone genes and investigated the evolutionary history of the vertebrate neurohypophysial hormone gene locus within a comparative genomics framework. The coelacanth contains vasotocin and mesotocin genes like non-mammalian tetrapods. The coelacanth genes are present on the same strand of DNA with no intervening genes, with the vasotocin gene located upstream of the mesotocin gene. Nucleotide sequences of the second exons of the two genes are under purifying selection implying a regulatory function. We have also analyzed the neurohypophysial hormone gene locus in the genomes of opossum, chicken and Xenopus tropicalis. The opossum contains two tandem copies of vasopressin and mesotocin genes. The vasotocin and mesotocin genes in chicken and Xenopus, and the vasopressin and mesotocin genes in opossum are linked tail-to-head similar to their orthologs in coelacanth and unlike their homologs in human and rodents.
Our results indicate that the neurohypophysial hormone gene locus has experienced independent rearrangements in both placental mammals and teleost fishes. The coelacanth genome appears to be more stable than mammalian and teleost fish genomes. As such, it serves as a valuable outgroup for studying the evolution of mammalian and teleost fish genomes.
PMCID: PMC2315648  PMID: 18366747
16.  Trunk exoskeleton in teleosts is mesodermal in origin 
Nature Communications  2013;4:1639-.
The vertebrate mineralized skeleton is known to have first emerged as an exoskeleton that extensively covered the fossil jawless fish. The evolutionary origin of this exoskeleton has long been attributed to the emergence of the neural crest, but experimental evaluation for this is still poor. Here we determine the embryonic origin of scales and fin rays of medaka (teleost trunk exoskeletons) by applying long-term cell labelling methods, and demonstrate that both tissues are mesodermal in origin. Neural crest cells, however, fail to contribute to these tissues. This result suggests that the trunk neural crest has no skeletogenic capability in fish, instead highlighting the dominant role of the mesoderm in the evolution of the trunk skeleton. This further implies that the role of the neural crest in skeletogenesis has been predominant in the cephalic region from the early stage of vertebrate evolution.
Trunk exoskeleton elements of non-tetrapods such as scales and fin rays are believed to derive from the neural crest. Shimada and colleagues use long-term cell labelling methods to show that these elements are actually derived from the mesoderm.
PMCID: PMC3615485  PMID: 23535660
17.  Forelimb-hindlimb developmental timing changes across tetrapod phylogeny 
Tetrapods exhibit great diversity in limb structures among species and also between forelimbs and hindlimbs within species, diversity which frequently correlates with locomotor modes and life history. We aim to examine the potential relation of changes in developmental timing (heterochrony) to the origin of limb morphological diversity in an explicit comparative and quantitative framework. In particular, we studied the relative time sequence of development of the forelimbs versus the hindlimbs in 138 embryos of 14 tetrapod species spanning a diverse taxonomic, ecomorphological and life-history breadth. Whole-mounts and histological sections were used to code the appearance of 10 developmental events comprising landmarks of development from the early bud stage to late chondrogenesis in the forelimb and the corresponding serial homologues in the hindlimb.
An overall pattern of change across tetrapods can be discerned and appears to be relatively clade-specific. In the primitive condition, as seen in Chondrichthyes and Osteichthyes, the forelimb/pectoral fin develops earlier than the hindlimb/pelvic fin. This pattern is either retained or re-evolved in eulipotyphlan insectivores (= shrews, moles, hedgehogs, and solenodons) and taken to its extreme in marsupials. Although exceptions are known, the two anurans we examined reversed the pattern and displayed a significant advance in hindlimb development. All other species examined, including a bat with its greatly enlarged forelimbs modified as wings in the adult, showed near synchrony in the development of the fore and hindlimbs.
Major heterochronic changes in early limb development and chondrogenesis were absent within major clades except Lissamphibia, and their presence across vertebrate phylogeny are not easily correlated with adaptive phenomena related to morphological differences in the adult fore- and hindlimbs. The apparently conservative nature of this trait means that changes in chondrogenetic patterns may serve as useful phylogenetic characters at higher taxonomic levels in tetrapods. Our results highlight the more important role generally played by allometric heterochrony in this instance to shape adult morphology.
PMCID: PMC2194785  PMID: 17908305
18.  Evolution of the axial system in craniates: morphology and function of the perivertebral musculature 
The axial musculoskeletal system represents the plesiomorphic locomotor engine of the vertebrate body, playing a central role in locomotion. In craniates, the evolution of the postcranial skeleton is characterized by two major transformations. First, the axial skeleton became increasingly functionally and morphologically regionalized. Second, the axial-based locomotion plesiomorphic for craniates became progressively appendage-based with the evolution of extremities in tetrapods. These changes, together with the transition to land, caused increased complexity in the planes in which axial movements occur and moments act on the body and were accompanied by profound changes in axial muscle function. To increase our understanding of the evolutionary transformations of the structure and function of the perivertebral musculature, this review integrates recent anatomical and physiological data (e.g., muscle fiber types, activation patterns) with gross-anatomical and kinematic findings for pivotal craniate taxa. This information is mapped onto a phylogenetic hypothesis to infer the putative character set of the last common ancestor of the respective taxa and to conjecture patterns of locomotor and muscular evolution. The increasing anatomical and functional complexity in the muscular arrangement during craniate evolution is associated with changes in fiber angulation and fiber-type distribution, i.e., increasing obliqueness in fiber orientation and segregation of fatigue-resistant fibers in deeper muscle regions. The loss of superficial fatigue-resistant fibers may be related to the profound gross anatomical reorganization of the axial musculature during the tetrapod evolution. The plesiomorphic function of the axial musculature -mobilization- is retained in all craniates. Along with the evolution of limbs and the subsequent transition to land, axial muscles additionally function to globally stabilize the trunk against inertial and extrinsic limb muscle forces as well as gravitational forces. Associated with the evolution of sagittal mobility and a parasagittal limb posture, axial muscles in mammals also stabilize the trunk against sagittal components of extrinsic limb muscle action as well as the inertia of the body's center of mass. Thus, the axial system is central to the static and dynamic control of the body posture in all craniates and, in gnathostomes, additionally provides the foundation for the mechanical work of the appendicular system.
PMCID: PMC3041741  PMID: 21306656
19.  Eating without hands or tongue: specialization, elaboration and the evolution of prey processing mechanisms in cartilaginous fishes 
Biology Letters  2005;1(3):357-361.
The ability to separate edible from inedible portions of prey is integral to feeding. However, this is typically overlooked in favour of prey capture as a driving force in the evolution of vertebrate feeding mechanisms. In processing prey, cartilaginous fishes appear handicapped because they lack the pharyngeal jaws of most bony fishes and the muscular tongue and forelimbs of most tetrapods. We argue that the elaborate cranial muscles of some cartilaginous fishes allow complex prey processing in addition to their usual roles in prey capture. The ability to manipulate prey has evolved twice along different mechanical pathways. Batoid chondrichthyans (rays and relatives) use elaborate lower jaw muscles to process armored benthic prey, separating out energetically useless material. In contrast, megacarnivorous carcharhiniform and lamniform sharks use a diversity of upper jaw muscles to control the jaws while gouging, allowing for reduction of prey much larger than the gape. We suggest experimental methods to test these hypotheses empirically.
PMCID: PMC1617152  PMID: 17148206
Chondrichthyes; elasmobranch; feeding; functional morphology; asymmetry
20.  Prdm1 (Blimp-1) and the Expression of Fast and Slow Myosin Heavy Chain Isoforms during Avian Myogenesis In Vitro 
PLoS ONE  2010;5(4):e9951.
Multiple types of fast and slow skeletal muscle fibers form during early embryogenesis in vertebrates. In zebrafish, formation of the earliest slow myofibers in fin muscles requires expression of the zinc-finger transcriptional repressor Prdm1 (also known as Blimp1). To further understand how the role of Prdm1 in early myogenesis may vary through evolution and during development, we have now analyzed Prdm1 expression in the diverse types of myotubes that form in culture from somitic, embryonic, and fetal chicken myoblasts.
Principal Findings
In cultures of somitic, embryonic limb, and fetal limb chicken cells, we found that Prdm1 was expressed in all of the differentiated muscle cells that formed, including those that expressed only fast myosin heavy chain isoforms, as well as those that co-expressed both fast and slow myosin heavy chain isoforms. Prdm1 was also expressed in Pax7-positive myoblasts, as well as in non-myogenic cells in the cultures. Furthermore, though all differentiated cells in control somite cultures co-expressed fast and slow myosin heavy chains, antisense knockdown of Prdm1 expression inhibited the formation of these co-expressing cells in somite cultures.
In chicken myogenic cell cultures, Prdm1 was expressed in most Pax7-positive myoblasts and in all differentiated muscle cells, irrespective of the developmental stage of cell donor or the pattern of fast and slow myosin heavy chains expressed in the differentiated cells that were formed. Thus, Prdm1 was expressed in myogenic cells prior to terminal differentiation; and, after differentiation, Prdm1 expression was not limited to cells that expressed slow myosin heavy chain isoforms. In addition, Prdm1 appeared to be required for differentiation of the somitic myocytes, which are the earliest myocytes to form in the avian embryo.
PMCID: PMC2848592  PMID: 20376350
21.  Metabolic Expenditures of Lunge Feeding Rorquals Across Scale: Implications for the Evolution of Filter Feeding and the Limits to Maximum Body Size 
PLoS ONE  2012;7(9):e44854.
Bulk-filter feeding is an energetically efficient strategy for resource acquisition and assimilation, and facilitates the maintenance of extreme body size as exemplified by baleen whales (Mysticeti) and multiple lineages of bony and cartilaginous fishes. Among mysticetes, rorqual whales (Balaenopteridae) exhibit an intermittent ram filter feeding mode, lunge feeding, which requires the abandonment of body-streamlining in favor of a high-drag, mouth-open configuration aimed at engulfing a very large amount of prey-laden water. Particularly while lunge feeding on krill (the most widespread prey preference among rorquals), the effort required during engulfment involve short bouts of high-intensity muscle activity that demand high metabolic output. We used computational modeling together with morphological and kinematic data on humpback (Megaptera noveaangliae), fin (Balaenoptera physalus), blue (Balaenoptera musculus) and minke (Balaenoptera acutorostrata) whales to estimate engulfment power output in comparison with standard metrics of metabolic rate. The simulations reveal that engulfment metabolism increases across the full body size of the larger rorqual species to nearly 50 times the basal metabolic rate of terrestrial mammals of the same body mass. Moreover, they suggest that the metabolism of the largest body sizes runs with significant oxygen deficits during mouth opening, namely, 20% over maximum at the size of the largest blue whales, thus requiring significant contributions from anaerobic catabolism during a lunge and significant recovery after a lunge. Our analyses show that engulfment metabolism is also significantly lower for smaller adults, typically one-tenth to one-half . These results not only point to a physiological limit on maximum body size in this lineage, but also have major implications for the ontogeny of extant rorquals as well as the evolutionary pathways used by ancestral toothed whales to transition from hunting individual prey items to filter feeding on prey aggregations.
PMCID: PMC3443106  PMID: 23024769
22.  The mitochondrial phylogeny of an ancient lineage of ray-finned fishes (Polypteridae) with implications for the evolution of body elongation, pelvic fin loss, and craniofacial morphology in Osteichthyes 
The family Polypteridae, commonly known as "bichirs", is a lineage that diverged early in the evolutionary history of Actinopterygii (ray-finned fish), but has been the subject of far less evolutionary study than other members of that clade. Uncovering patterns of morphological change within Polypteridae provides an important opportunity to evaluate if the mechanisms underlying morphological evolution are shared among actinoptyerygians, and in fact, perhaps the entire osteichthyan (bony fish and tetrapods) tree of life. However, the greatest impediment to elucidating these patterns is the lack of a well-resolved, highly-supported phylogenetic tree of Polypteridae. In fact, the interrelationships of polypterid species have never been subject to molecular phylogenetic analysis. Here, we infer the first molecular phylogeny of bichirs, including all 12 recognized species and multiple subspecies using Bayesian analyses of 16S and cyt-b mtDNA. We use this mitochondrial phylogeny, ancestral state reconstruction, and geometric morphometrics to test whether patterns of morphological evolution, including the evolution of body elongation, pelvic fin reduction, and craniofacial morphology, are shared throughout the osteichthyan tree of life.
Our molecular phylogeny reveals 1) a basal divergence between Erpetoichthys and Polypterus, 2) polyphyly of P. endlicheri and P. palmas, and thus 3) the current taxonomy of Polypteridae masks its underlying genetic diversity. Ancestral state reconstructions suggest that pelvic fins were lost independently in Erpetoichthys, and unambiguously estimate multiple independent derivations of body elongation and shortening. Our mitochondrial phylogeny suggested species that have lower jaw protrusion and up-righted orbit are closely related to each other, indicating a single transformation of craniofacial morphology.
The mitochondrial phylogeny of polypterid fish provides a strongly-supported phylogenetic framework for future comparative evolutionary, physiological, ecological, and genetic analyses. Indeed, ancestral reconstruction and geometric morphometric analyses revealed that the patterns of morphological evolution in Polypteridae are similar to those seen in other osteichthyans, thus implying the underlying genetic and developmental mechanisms responsible for those patterns were established early in the evolutionary history of Osteichthyes. We propose developmental and genetic mechanisms to be tested under the light of this new phylogenetic framework.
PMCID: PMC2825197  PMID: 20100320
23.  Lake Malawi cichlid evolution along a benthic/limnetic axis 
Ecology and Evolution  2013;3(7):2262-2272.
Divergence along a benthic to limnetic habitat axis is ubiquitous in aquatic systems. However, this type of habitat divergence has largely been examined in low diversity, high latitude lake systems. In this study, we examined the importance of benthic and limnetic divergence within the incredibly species-rich radiation of Lake Malawi cichlid fishes. Using novel phylogenetic reconstructions, we provided a series of hypotheses regarding the evolutionary relationships among 24 benthic and limnetic species that suggests divergence along this axis has occurred multiple times within Lake Malawi cichlids. Because pectoral fin morphology is often associated with divergence along this habitat axis in other fish groups, we investigated divergence in pectoral fin muscles in these benthic and limnetic cichlid species. We showed that the eight pectoral fin muscles and fin area generally tended to evolve in a tightly correlated manner in the Lake Malawi cichlids. Additionally, we found that larger pectoral fin muscles are strongly associated with the independent evolution of the benthic feeding habit across this group of fish. Evolutionary specialization along a benthic/limnetic axis has occurred multiple times within this tropical lake radiation and has produced repeated convergent matching between exploitation of water column habitats and locomotory morphology.
PMCID: PMC3728963  PMID: 23919168
Adaptive radiation; African Great Lakes; aquatic locomotion; functional morphology; mbuna; utaka
24.  Hearing in the African lungfish (Protopterus annectens): pre-adaptation to pressure hearing in tetrapods? 
Biology Letters  2010;7(1):139-141.
Lungfishes are the closest living relatives of the tetrapods, and the ear of recent lungfishes resembles the tetrapod ear more than the ear of ray-finned fishes and is therefore of interest for understanding the evolution of hearing in the early tetrapods. The water-to-land transition resulted in major changes in the tetrapod ear associated with the detection of air-borne sound pressure, as evidenced by the late and independent origins of tympanic ears in all of the major tetrapod groups. To investigate lungfish pressure and vibration detection, we measured the sensitivity and frequency responses of five West African lungfish (Protopterus annectens) using brainstem potentials evoked by calibrated sound and vibration stimuli in air and water. We find that the lungfish ear has good low-frequency vibration sensitivity, like recent amphibians, but poor sensitivity to air-borne sound. The skull shows measurable vibrations above 100 Hz when stimulated by air-borne sound, but the ear is apparently insensitive at these frequencies, suggesting that the lungfish ear is neither adapted nor pre-adapted for aerial hearing. Thus, if the lungfish ear is a model of the ear of early tetrapods, their auditory sensitivity was limited to very low frequencies on land, mostly mediated by substrate-borne vibrations.
PMCID: PMC3030901  PMID: 20826468
lungfish; hearing; vibration; tetrapod; sound; evolution
25.  New regulators of vertebrate appendage regeneration 
Appendage regeneration is a complex and fascinating biological process exhibited in vertebrates by urodele amphibians and teleost fish. A current focus in the field is to identify new molecules that control formation and function of the regeneration blastema, a mass of proliferative mesenchyme that emerges after limb or fin amputation and serves as progenitor tissue for lost structures. Two studies published recently have illuminated new molecular regulators of blastemal proliferation. After amputation of a newt limb, the nerve sheath releases nAG, a blastemal mitogen that facilitates regeneration. In amputated zebrafish fins, regeneration is optimized through depletion of the microRNA miR-133, a mechanism that requires Fgf signaling. These discoveries establish research avenues that may impact the regenerative capacity of mammalian tissues.
PMCID: PMC2574633  PMID: 18644447

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