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1.  Evidence for hearing loss in amblyopsid cavefishes 
Biology Letters  2013;9(3):20130104.
The constant darkness of caves and other subterranean habitats imposes sensory constraints that offer a unique opportunity to examine evolution of sensory modalities. Hearing in cavefishes has not been well explored, and here we show that cavefishes in the family Amblyopsidae are not only blind but have also lost a significant portion of their hearing range. Our results showed that cave and surface amblyopsids shared the same audiogram profile at low frequencies but only surface amblyopsids were able to hear frequencies higher than 800 Hz and up to 2 kHz. We measured ambient noise in aquatic cave and surface habitats and found high intensity peaks near 1 kHz for streams underground, suggesting no adaptive advantage in hearing in those frequencies. In addition, cave amblyopsids had lower hair cell densities compared with their surface relative. These traits may have evolved in response to the loud high-frequency background noise found in subterranean pools and streams. This study represents the first report of auditory regression in a subterranean organism.
PMCID: PMC3645044  PMID: 23536444
auditory; evolution; fish; subterranean
2.  A New Approach for the Determination of Ammonite and Nautilid Habitats 
PLoS ONE  2014;9(1):e87479.
Externally shelled cephalopods were important elements in open marine habitats throughout Earth history. Paleotemperatures calculated on the basis of the oxygen isotope composition of their shells can provide insights into ancient marine systems as well as the ecology of this important group of organisms. In some sedimentary deposits, however, the aragonitic shell of the ammonite or nautilid is poorly or not preserved at all, while the calcitic structures belonging to the jaws are present. This study tests for the first time if the calcitic jaw structures in fossil cephalopods can be used as a proxy for paleotemperature. We first analyzed the calcitic structures on the jaws of Recent Nautilus and compared the calculated temperatures of precipitation with those from the aragonitic shell in the same individuals. Our results indicate that the jaws of Recent Nautilus are secreted in isotopic equilibrium, and the calculated temperatures approximately match those of the shell. We then extended our study to ammonites from the Upper Cretaceous (Campanian) Pierre Shale of the U.S. Western Interior and the age-equivalent Mooreville Chalk of the Gulf Coastal Plain. In the Pierre Shale, jaws occur in situ inside the body chambers of well-preserved Baculites while in the Mooreville Chalk, the jaw elements appear as isolated occurrences in the sediment and the aragonitic shell material is not preserved. For the Pierre Shale specimens, the calculated temperatures of well-preserved jaw material match those of well-preserved shell material in the same individual. Analyses of the jaw elements in the Mooreville Chalk permit a comparison of the paleotemperatures between the two sites, and show that the Western Interior is warmer than the Gulf Coast at that time. In summary, our data indicate that the calcitic jaw elements of cephalopods can provide a reliable geochemical archive of the habitat of fossil forms.
PMCID: PMC3903699  PMID: 24475295
3.  Development of the Acoustically Evoked Behavioral Response in Larval Plainfin Midshipman Fish, Porichthys notatus 
PLoS ONE  2013;8(12):e82182.
The ontogeny of hearing in fishes has become a major interest among bioacoustics researchers studying fish behavior and sensory ecology. Most fish begin to detect acoustic stimuli during the larval stage which can be important for navigation, predator avoidance and settlement, however relatively little is known about the hearing capabilities of larval fishes. We characterized the acoustically evoked behavioral response (AEBR) in the plainfin midshipman fish, Porichthys notatus, and used this innate startle-like response to characterize this species' auditory capability during larval development. Age and size of larval midshipman were highly correlated (r2 = 0.92). The AEBR was first observed in larvae at 1.4 cm TL. At a size ≥1.8 cm TL, all larvae responded to a broadband stimulus of 154 dB re1 µPa or −15.2 dB re 1 g (z-axis). Lowest AEBR thresholds were 140–150 dB re 1 µPa or −33 to −23 dB re 1 g for frequencies below 225 Hz. Larval fish with size ranges of 1.9–2.4 cm TL had significantly lower best evoked frequencies than the other tested size groups. We also investigated the development of the lateral line organ and its function in mediating the AEBR. The lateral line organ is likely involved in mediating the AEBR but not necessary to evoke the startle-like response. The midshipman auditory and lateral line systems are functional during early development when the larvae are in the nest and the auditory system appears to have similar tuning characteristics throughout all life history stages.
PMCID: PMC3858275  PMID: 24340003
4.  Oral Region Homologies in Paleozoic Crinoids and Other Plesiomorphic Pentaradial Echinoderms 
PLoS ONE  2013;8(11):e77989.
The phylogenetic relationships between major groups of plesiomorphic pentaradial echinoderms, the Paleozoic crinoids, blastozoans, and edrioasteroids, are poorly understood because of a lack of widely recognized homologies. Here, we present newly recognized oral region homologies, based on the Universal Elemental Homology model for skeletal plates, in a wide range of fossil taxa. The oral region of echinoderms is mainly composed of the axial, or ambulacral, skeleton, which apparently evolved more slowly than the extraxial skeleton that forms the majority of the body. Recent phylogenetic hypotheses have focused on characters of the extraxial skeleton, which may have evolved too rapidly to preserve obvious homologies across all these groups. The axial skeleton conserved homologous suites of characters shared between various edrioasteroids and specific blastozoans, and between other blastozoans and crinoids. Although individual plates can be inferred as homologous, no directly overlapping suites of characters are shared between edrioasteroids and crinoids. Six different systems of mouth (peristome) plate organization (Peristomial Border Systems) are defined. These include four different systems based on the arrangement of the interradially-positioned oral plates and their peristomial cover plates, where PBS A1 occurs only in plesiomorphic edrioasteroids, PBS A2 occurs in plesiomorphic edrioasteroids and blastozoans, and PBS A3 and PBS A4 occur in blastozoans and crinoids. The other two systems have radially-positioned uniserial oral frame plates in construction of the mouth frame. PBS B1 has both orals and uniserial oral frame plates and occurs in edrioasterid and possibly edrioblastoid edrioasteroids, whereas PBS B2 has exclusively uniserial oral frame plates and is found in isorophid edrioasteroids and imbricate and gogiid blastozoans. These different types of mouth frame construction offer potential synapomorphies to aid in parsimony-based phylogenetics for exploring branching order among stem groups on the echinoderm tree of life.
PMCID: PMC3823914  PMID: 24244284
5.  By the Teeth of Their Skin, Cavefish Find Their Way 
Current biology : CB  2012;22(16):R629-R630.
PMCID: PMC3427538  PMID: 22917507
6.  Comparative Anatomy of the Bony Labyrinth (Inner Ear) of Placental Mammals 
PLoS ONE  2013;8(6):e66624.
Variation is a naturally occurring phenomenon that is observable at all levels of morphology, from anatomical variations of DNA molecules to gross variations between whole organisms. The structure of the otic region is no exception. The present paper documents the broad morphological diversity exhibited by the inner ear region of placental mammals using digital endocasts constructed from high-resolution X-ray computed tomography (CT). Descriptions cover the major placental clades, and linear, angular, and volumetric dimensions are reported.
Principal Findings
The size of the labyrinth is correlated to the overall body mass of individuals, such that large bodied mammals have absolutely larger labyrinths. The ratio between the average arc radius of curvature of the three semicircular canals and body mass of aquatic species is substantially lower than the ratios of related terrestrial taxa, and the volume percentage of the vestibular apparatus of aquatic mammals tends to be less than that calculated for terrestrial species. Aspects of the bony labyrinth are phylogenetically informative, including vestibular reduction in Cetacea, a tall cochlear spiral in caviomorph rodents, a low position of the plane of the lateral semicircular canal compared to the posterior canal in Cetacea and Carnivora, and a low cochlear aspect ratio in Primatomorpha.
The morphological descriptions that are presented add a broad baseline of anatomy of the inner ear across many placental mammal clades, for many of which the structure of the bony labyrinth is largely unknown. The data included here complement the growing body of literature on the physiological and phylogenetic significance of bony labyrinth structures in mammals, and they serve as a source of data for future studies on the evolution and function of the vertebrate ear.
PMCID: PMC3689836  PMID: 23805251
7.  The Nervous Systems of Basally Branching Nemertea (Palaeonemertea) 
PLoS ONE  2013;8(6):e66137.
In recent years, a lot of studies have been published dealing with the anatomy of the nervous system in different spiralian species. The only nemertean species investigated in this context probably shows derived characters and thus the conditions found there are not useful in inferring the relationship between nemerteans and other spiralian taxa. Ingroup relationships within Nemertea are still unclear, but there is some agreement that the palaeonemerteans form a basal, paraphyletic grade. Thus, palaeonemertean species are likely the most informative when comparing with other invertebrate groups. We therefore analyzed the nervous system of several palaeonemertean species by combining histology and immunostaining. 3D reconstructions based on the aligned slices were performed to get an overall impression of the central nervous system, and immunohistochemistry was chosen to reveal fine structures and to be able to compare the data with recently published results. The insights presented here permit a first attempt to reconstruct the primary organization of the nemertean nervous system. This comparative analysis allows substantiating homology hypotheses for nerves of the peripheral nervous system. This study also provides evidence that the nemertean brain primarily consists of two lobes connected by a strong ventral commissure and one to several dorsal commissures. During nemertean evolution, the brain underwent continuous compartmentalization into a pair of dorsal and ventral lobes interconnected by commissures and lateral tracts. Given that this conclusion can be corroborated by cladistic analyses, nemerteans should share a common ancestor with spiralians that primarily have a simple brain consisting of paired medullary, frontally commissurized and reinforced cords. Such an organization resembles the situation found in presumably basally branching annelids or mollusks.
PMCID: PMC3681988  PMID: 23785478
8.  Aerial Jumping in the Trinidadian Guppy (Poecilia reticulata) 
PLoS ONE  2013;8(4):e61617.
Many fishes are able to jump out of the water and launch themselves into the air. Such behavior has been connected with prey capture, migration and predator avoidance. We found that jumping behavior of the guppy Poecilia reticulata is not associated with any of the above. The fish jump spontaneously, without being triggered by overt sensory cues, is not migratory and does not attempt to capture aerial food items. Here, we use high speed video imaging to analyze the kinematics of the jumping behavior P. reticulata. Fish jump from a still position by slowly backing up while using its pectoral fins, followed by strong body trusts which lead to launching into the air several body lengths. The liftoff phase of the jump is fast and fish will continue with whole body thrusts and tail beats, even when out of the water. This behavior occurs when fish are in a group or in isolation. Geography has had substantial effects on guppy evolution, with waterfalls reducing gene flow and constraining dispersal. We suggest that jumping has evolved in guppies as a behavioral phenotype for dispersal.
PMCID: PMC3629028  PMID: 23613883
9.  An Integrated Transcriptome-Wide Analysis of Cave and Surface Dwelling Astyanax mexicanus 
PLoS ONE  2013;8(2):e55659.
Numerous organisms around the globe have successfully adapted to subterranean environments. A powerful system in which to study cave adaptation is the freshwater characin fish, Astyanax mexicanus. Prior studies in this system have established a genetic basis for the evolution of numerous regressive traits, most notably vision and pigmentation reduction. However, identification of the precise genetic alterations that underlie these morphological changes has been delayed by limited genetic and genomic resources. To address this, we performed a transcriptome analysis of cave and surface dwelling Astyanax morphs using Roche/454 pyrosequencing technology. Through this approach, we obtained 576,197 Pachón cavefish-specific reads and 438,978 surface fish-specific reads. Using this dataset, we assembled transcriptomes of cave and surface fish separately, as well as an integrated transcriptome that combined 1,499,568 reads from both morphotypes. The integrated assembly was the most successful approach, yielding 22,596 high quality contiguous sequences comprising a total transcriptome length of 21,363,556 bp. Sequence identities were obtained through exhaustive blast searches, revealing an adult transcriptome represented by highly diverse Gene Ontology (GO) terms. Our dataset facilitated rapid identification of sequence polymorphisms between morphotypes. These data, along with positional information collected from the Danio rerio genome, revealed several syntenic regions between Astyanax and Danio. We demonstrated the utility of this positional information through a QTL analysis of albinism in a surface x Pachón cave F2 pedigree, using 65 polymorphic markers identified from our integrated assembly. We also adapted our dataset for an RNA-seq study, revealing many genes responsible for visual system maintenance in surface fish, whose expression was not detected in adult Pachón cavefish. Conversely, several metabolism-related genes expressed in cavefish were not detected in surface fish. This resource will enable powerful genetic and genomic analyses in the future that will better clarify the heritable genetic changes governing adaptation to the cave environment.
PMCID: PMC3566029  PMID: 23405189
10.  The Giant Cretaceous Coelacanth (Actinistia, Sarcopterygii) Megalocoelacanthus dobiei Schwimmer, Stewart & Williams, 1994, and Its Bearing on Latimerioidei Interrelationships 
PLoS ONE  2012;7(11):e49911.
We present a redescription of Megalocoelacanthus dobiei, a giant fossil coelacanth from Upper Cretaceous strata of North America. Megalocoelacanthus has been previously described on the basis of composite material that consisted of isolated elements. Consequently, many aspects of its anatomy have remained unknown as well as its phylogenetic relationships with other coelacanths. Previous studies have suggested that Megalocoelacanthus is closer to Latimeria and Macropoma than to Mawsonia. However, this assumption was based only on the overall similarity of few anatomical features, rather than on a phylogenetic character analysis. A new, and outstandingly preserved specimen from the Niobrara Formation in Kansas allows the detailed description of the skull of Megalocoelacanthus and elucidation of its phylogenetic relationships with other coelacanths. Although strongly flattened, the skull and jaws are well preserved and show many derived features that are shared with Latimeriidae such as Latimeria, Macropoma and Libys. Notably, the parietonasal shield is narrow and flanked by very large, continuous vacuities forming the supraorbital sensory line canal. Such an unusual morphology is also known in Libys. Some other features of Megalocoelacanthus, such as its large size and the absence of teeth are shared with the mawsoniid genera Mawsonia and Axelrodichthys. Our cladistic analysis supports the sister-group relationship of Megalocoelacanthus and Libys within Latimeriidae. This topology suggests that toothless, large-sized coelacanths evolved independently in both Latimeriidae and Mawsoniidae during the Mesozoic. Based on previous topologies and on ours, we then review the high-level taxonomy of Latimerioidei and propose new systematic phylogenetic definitions.
PMCID: PMC3507921  PMID: 23209614
11.  Torosaurus Is Not Triceratops: Ontogeny in Chasmosaurine Ceratopsids as a Case Study in Dinosaur Taxonomy 
PLoS ONE  2012;7(2):e32623.
In horned dinosaurs, taxonomy is complicated by the fact that the cranial ornament that distinguishes species changes with age. Based on this observation, it has been proposed that the genera Triceratops and Torosaurus are in fact synonymous, with specimens identified as Torosaurus representing the adult form of Triceratops. The hypothesis of synonymy makes three testable predictions: 1) the species in question should have similar geographic and stratigraphic distributions, 2) specimens assigned to Torosaurus should be more mature than those assigned to Triceratops, and 3) intermediates should exist that combine features of Triceratops and Torosaurus. The first condition appears to be met, but it remains unclear whether the other predictions are borne out by the fossil evidence.
Methodology/Principal Findings
We assessed the relative maturity of Torosaurus and Triceratops specimens by coding skulls for characters that vary with maturity, and then using a clustering analysis to arrange them into a growth series. We found that a well-defined sequence of changes exists in horned dinosaurs: development of cranial ornament occurs in juveniles, followed by fusion of the skull roof in subadults, and finally, the epoccipitals, epijugals, and rostral fuse to the skull in adults. Using this scheme, we identified mature and immature individuals of both Torosaurus and Triceratops. Furthermore, we describe the ventral depressions on the frill of Triceratops, and show that they differ in shape and position from the parietal fenestrae of Torosaurus. Thus, we conclude that these structures are not intermediates between the solid frill of Triceratops and the fenestrated frill of Torosaurus.
Torosaurus is a distinct genus of horned dinosaur, not the adult of Triceratops. Our method provides a framework for assessing the hypothesis of synonymy through ontogeny in the fossil record.
PMCID: PMC3290593  PMID: 22393425
12.  Characterization of Synaptically Connected Nuclei in a Potential Sensorimotor Feedback Pathway in the Zebra Finch Song System 
PLoS ONE  2012;7(2):e32178.
Birdsong is a learned behavior that is controlled by a group of identified nuclei, known collectively as the song system. The cortical nucleus HVC (used as a proper name) is a focal point of many investigations as it is necessary for song production, song learning, and receives selective auditory information. HVC receives input from several sources including the cortical area MMAN (medial magnocellular nucleus of the nidopallium). The MMAN to HVC connection is particularly interesting as it provides potential sensorimotor feedback to HVC. To begin to understand the role of this connection, we investigated the physiological relation between MMAN and HVC activity with simultaneous multiunit extracellular recordings from these two nuclei in urethane anesthetized zebra finches. As previously reported, we found similar timing in spontaneous bursts of activity in MMAN and HVC. Like HVC, MMAN responds to auditory playback of the bird's own song (BOS), but had little response to reversed BOS or conspecific song. Stimulation of MMAN resulted in evoked activity in HVC, indicating functional excitation from MMAN to HVC. However, inactivation of MMAN resulted in no consistent change in auditory responses in HVC. Taken together, these results indicate that MMAN provides functional excitatory input to HVC but does not provide significant auditory input to HVC in anesthetized animals. We hypothesize that MMAN may play a role in motor reinforcement or coordination, or may provide modulatory input to the song system about the internal state of the animal as it receives input from the hypothalamus.
PMCID: PMC3285214  PMID: 22384172
13.  Life History of Rhamphorhynchus Inferred from Bone Histology and the Diversity of Pterosaurian Growth Strategies 
PLoS ONE  2012;7(2):e31392.
Rhamphorhynchus from the Solnhofen Limestones is the most prevalent long tailed pterosaur with a debated life history. Whereas morphological studies suggested a slow crocodile-like growth strategy and superprecocial volant hatchlings, the only histological study hitherto conducted on Rhamphorhynchus concluded a relatively high growth rate for the genus. These controversial conclusions can be tested by a bone histological survey of an ontogenetic series of Rhamphorhynchus.
Methodology/Principal Findings
Our results suggest that Bennett's second size category does not reflect real ontogenetic stage. Significant body size differences of histologically as well as morphologically adult specimens suggest developmental plasticity. Contrasting the ‘superprecocial hatchling’ hypothesis, the dominance of fibrolamellar bone in early juveniles implies that hatchlings sustained high growth rate, however only up to the attainment of 30–50% and 7–20% of adult wingspan and body mass, respectively. The early fast growth phase was followed by a prolonged, slow-growth phase indicated by parallel-fibred bone deposition and lines of arrested growth in the cortex, a transition which has also been observed in Pterodaustro. An external fundamental system is absent in all investigated specimens, but due to the restricted sample size, neither determinate nor indeterminate growth could be confirmed in Rhamphorhynchus.
The initial rapid growth phase early in Rhamphorhynchus ontogeny supports the non-volant nature of its hatchlings, and refutes the widely accepted ‘superprecocial hatchling’ hypothesis. We suggest the onset of powered flight, and not of reproduction as the cause of the transition from the fast growth phase to a prolonged slower growth phase. Rapidly growing early juveniles may have been attended by their parents, or could have been independent precocial, but non-volant arboreal creatures until attaining a certain somatic maturity to get airborne. This study adds to the understanding on the diversity of pterosaurian growth strategies.
PMCID: PMC3280310  PMID: 22355361
14.  Cretaceous Small Scavengers: Feeding Traces in Tetrapod Bones from Patagonia, Argentina 
PLoS ONE  2012;7(1):e29841.
Ecological relationships among fossil vertebrate groups are interpreted based on evidence of modification features and paleopathologies on fossil bones. Here we describe an ichnological assemblage composed of trace fossils on reptile bones, mainly sphenodontids, crocodyliforms and maniraptoran theropods. They all come from La Buitrera, an early Late Cretaceous locality in the Candeleros Formation of northwestern Patagonia, Argentina. This locality is significant because of the abundance of small to medium-sized vertebrates. The abundant ichnological record includes traces on bones, most of them attributable to tetrapods. These latter traces include tooth marks that provde evidence of feeding activities made during the sub-aerial exposure of tetrapod carcasses. Other traces are attributable to arthropods or roots. The totality of evidence provides an uncommon insight into paleoecological aspects of a Late Cretaceous southern ecosystem.
PMCID: PMC3253797  PMID: 22253800
15.  Fish Geometry and Electric Organ Discharge Determine Functional Organization of the Electrosensory Epithelium 
PLoS ONE  2011;6(11):e27470.
Active electroreception in Gymnotus omarorum is a sensory modality that perceives the changes that nearby objects cause in a self generated electric field. The field is emitted as repetitive stereotyped pulses that stimulate skin electroreceptors. Differently from mormyriformes electric fish, gymnotiformes have an electric organ distributed along a large portion of the body, which fires sequentially. As a consequence shape and amplitude of both, the electric field generated and the image of objects, change during the electric pulse. To study how G. omarorum constructs a perceptual representation, we developed a computational model that allows the determination of the self-generated field and the electric image. We verify and use the model as a tool to explore image formation in diverse experimental circumstances. We show how the electric images of objects change in shape as a function of time and position, relative to the fish's body. We propose a theoretical framework about the organization of the different perceptive tasks made by electroreception: 1) At the head region, where the electrosensory mosaic presents an electric fovea, the field polarizing nearby objects is coherent and collimated. This favors the high resolution sampling of images of small objects and perception of electric color. Besides, the high sensitivity of the fovea allows the detection and tracking of large faraway objects in rostral regions. 2) In the trunk and tail region a multiplicity of sources illuminate different regions of the object, allowing the characterization of the shape and position of a large object. In this region, electroreceptors are of a unique type and capacitive detection should be based in the pattern of the afferents response. 3) Far from the fish, active electroreception is not possible but the collimated field is suitable to be used for electrocommunication and detection of large objects at the sides and caudally.
PMCID: PMC3214058  PMID: 22096578
16.  Sabretoothed Carnivores and the Killing of Large Prey 
PLoS ONE  2011;6(10):e24971.
Sabre-like canines clearly have the potential to inflict grievous wounds leading to massive blood loss and rapid death. Hypotheses concerning sabretooth killing modes include attack to soft parts such as the belly or throat, where biting deep is essential to generate strikes reaching major blood vessels. Sabretoothed carnivorans are widely interpreted as hunters of larger and more powerful prey than that of their present-day nonsabretoothed relatives. However, the precise functional advantage of the sabretooth bite, particularly in relation to prey size, is unknown. Here, we present a new point-to-point bite model and show that, for sabretooths, depth of the killing bite decreases dramatically with increasing prey size. The extended gape of sabretooths only results in considerable increase in bite depth when biting into prey with a radius of less than ∼10 cm. For sabretooths, this size-reversed functional advantage suggests predation on species within a similar size range to those attacked by present-day carnivorans, rather than “megaherbivores” as previously believed. The development of the sabretooth condition appears to represent a shift in function and killing behaviour, rather than one in predator-prey relations. Furthermore, our results demonstrate how sabretoothed carnivorans are likely to have evolved along a functionally continuous trajectory: beginning as an extension of a jaw-powered killing bite, as adopted by present-day pantherine cats, followed by neck-powered biting and thereafter shifting to neck-powered shear-biting. We anticipate this new insight to be a starting point for detailed study of the evolution of pathways that encompass extreme specialisation, for example, understanding how neck-powered biting shifts into shear-biting and its significance for predator-prey interactions. We also expect that our model for point-to-point biting and bite depth estimations will yield new insights into the behaviours of a broad range of extinct predators including therocephalians (gorgonopsian + cynodont, sabretoothed mammal-like reptiles), sauropterygians (marine reptiles) and theropod dinosaurs.
PMCID: PMC3198467  PMID: 22039403
17.  Evolution of a behavioral shift mediated by superficial neuromasts helps cavefish find food in darkness 
Current biology : CB  2010;20(18):1631-1636.
How cave animals adapt to life in darkness is a poorly understood aspect of evolutionary biology [1]. Here we identify a behavioral shift and its morphological basis in Astyanax mexicanus, a teleost with a sighted surface dwelling form (surface fish) and various blind cave dwelling forms (cavefish) [2–4]. Vibration attraction behavior (VAB) is the ability of fish to swim toward the source of a water disturbance in darkness. VAB was typically seen in cavefish, rarely in surface fish, and advantageous for feeding success in the dark. The potential for showing VAB has a genetic component and is linked to the mechanosensory function of the lateral line. VAB was evoked by vibration stimuli peaking at 35 Hz, blocked by lateral line inhibitors, appeared after developmental increases in superficial neuromast (SN) number and size [5–7], and was significantly reduced by bilateral ablation of SN. We conclude that VAB and SN enhancement co-evolved to compensate for loss of vision and help blind cavefish find food in darkness.
PMCID: PMC2946428  PMID: 20705469
18.  A New Paleozoic Symmoriiformes (Chondrichthyes) from the Late Carboniferous of Kansas (USA) and Cladistic Analysis of Early Chondrichthyans 
PLoS ONE  2011;6(9):e24938.
The relationships of cartilaginous fishes are discussed in the light of well preserved three-dimensional Paleozoic specimens. There is no consensus to date on the interrelationship of Paleozoic chondrichthyans, although three main phylogenetic hypotheses exist in the current literature: 1. the Paleozoic shark-like chondrichthyans, such as the Symmoriiformes, are grouped along with the modern sharks (neoselachians) into a clade which is sister group of holocephalans; 2. the Symmoriiformes are related to holocephalans, whereas the other Paleozoic shark-like chondrichthyans are related to neoselachians; 3. many Paleozoic shark-like chondrichthyans, such as the Symmoriiformes, are stem chondrichthyans, whereas stem and crown holocephalans are sister group to the stem and crown neoselachians in a crown-chondrichthyan clade. This third hypothesis was proposed recently, based mainly on dental characters.
Methodology/Principal Findings
On the basis of two well preserved chondrichthyan neurocrania from the Late Carboniferous of Kansas, USA, we describe here a new species of Symmoriiformes, Kawichthys moodiei gen. et sp. nov., which was investigated by means of computerized X-ray synchrotron microtomography. We present a new phylogenetic analysis based on neurocranial characters, which supports the third hypothesis and corroborates the hypothesis that crown-group chondrichthyans (Holocephali+Neoselachii) form a tightly-knit group within the chondrichthyan total group, by providing additional, non dental characters.
Our results highlight the importance of new well preserved Paleozoic fossils and new techniques of observation, and suggest that a new look at the synapomorphies of the crown-group chondrichthyans would be worthwhile in terms of understanding the adaptive significance of phylogenetically important characters.
PMCID: PMC3181253  PMID: 21980367
19.  Ontogeny of the Alligator Cartilago Transiliens and Its Significance for Sauropsid Jaw Muscle Evolution 
PLoS ONE  2011;6(9):e24935.
The cartilago transiliens is a fibrocartilaginous structure within the jaw muscles of crocodylians. The cartilago transiliens slides between the pterygoid buttress and coronoid region of the lower jaw and connects two muscles historically identified as m. pseudotemporalis superficialis and m. intramandibularis. However, the position of cartilago transiliens, and its anatomical similarities to tendon organs suggest the structure may be a sesamoid linking a single muscle. Incompressible sesamoids often form inside tendons that wrap around bone. However, such structures rarely ossify in reptiles and have thus far received scant attention. We tested the hypothesis that the cartilago transiliens is a sesamoid developed within in one muscle by investigating its structure in an ontogenetic series of Alligator mississippiensis using dissection, 3D imaging, and polarizing and standard light microscopy. In all animals studied, the cartilago transiliens receives collagen fibers and tendon insertions from its two main muscular attachments. However, whereas collagen fibers were continuous within the cartilaginous nodule of younger animals, such continuity decreased in older animals, where the fibrocartilaginous core grew to displace the fibrous region. Whereas several neighboring muscles attached to the fibrous capsule in older individuals, only two muscles had significant contributions to the structure in young animals. Our results indicate that the cartilago transiliens is likely a sesamoid formed within a single muscle (i.e., m. pseudotemporalis superficialis) as it wraps around the pterygoid buttress. This tendon organ is ubiquitous among fossil crocodyliforms indicating it is a relatively ancient, conserved structure associated with the development of the large pterygoid flanges in this clade. Finally, these findings indicate that similar tendon organs exist among potentially homologous muscle groups in birds and turtles, thus impacting inferences of jaw muscle homology and evolution in sauropsids in general.
PMCID: PMC3174982  PMID: 21949795
20.  Detection of Interaural Time Differences in the Alligator 
The auditory systems of birds and mammals use timing information from each ear to detect interaural time difference (ITD). To determine whether the Jeffress-type algorithms that underlie sensitivity to ITD in birds are an evolutionarily stable strategy, we recorded from the auditory nuclei of crocodilians, who are the sister group to the birds. In alligators, precisely timed spikes in the first-order nucleus magnocellularis (NM) encode the timing of sounds, and NM neurons project to neurons in the nucleus laminaris (NL) that detect interaural time differences. In vivo recordings from NL neurons show that the arrival time of phase-locked spikes differs between the ipsilateral and contralateral inputs. When this disparity is nullified by their best ITD, the neurons respond maximally. Thus NL neurons act as coincidence detectors. A biologically detailed model of NL with alligator parameters discriminated ITDs up to 1 kHz. The range of best ITDs represented in NL was much larger than in birds, however, and extended from 0 to 1000 μs contralateral, with a median ITD of 450 μs. Thus, crocodilians and birds employ similar algorithms for ITD detection, although crocodilians have larger heads.
PMCID: PMC3170862  PMID: 19553438
21.  Variation, Variability, and the Origin of the Avian Endocranium: Insights from the Anatomy of Alioramus altai (Theropoda: Tyrannosauroidea) 
PLoS ONE  2011;6(8):e23393.
The internal braincase anatomy of the holotype of Alioramus altai, a relatively small-bodied tyrannosauroid from the Late Cretaceous of Mongolia, was studied using high-resolution computed tomography. A number of derived characters strengthen the diagnosis of this taxon as both a tyrannosauroid and a unique, new species (e.g., endocranial position of the gasserian ganglion, internal ramification of the facial nerve). Also present are features intermediate between the basal theropod and avialan conditions that optimize as the ancestral condition for Coelurosauria—a diverse group of derived theropods that includes modern birds. The expression of several primitive theropod features as derived character states within Tyrannosauroidea establishes previously unrecognized evolutionary complexity and morphological plasticity at the base of Coelurosauria. It also demonstrates the critical role heterochrony may have played in driving patterns of endocranial variability within the group and potentially reveals stages in the evolution of neuroanatomical development that could not be inferred based solely on developmental observations of the major archosaurian crown clades. We discuss the integration of paleontology with variability studies, especially as applied to the nature of morphological transformations along the phylogenetically long branches that tend to separate the crown clades of major vertebrate groups.
PMCID: PMC3154410  PMID: 21853125
22.  So Small, So Loud: Extremely High Sound Pressure Level from a Pygmy Aquatic Insect (Corixidae, Micronectinae) 
PLoS ONE  2011;6(6):e21089.
To communicate at long range, animals have to produce intense but intelligible signals. This task might be difficult to achieve due to mechanical constraints, in particular relating to body size. Whilst the acoustic behaviour of large marine and terrestrial animals has been thoroughly studied, very little is known about the sound produced by small arthropods living in freshwater habitats. Here we analyse for the first time the calling song produced by the male of a small insect, the water boatman Micronecta scholtzi. The song is made of three distinct parts differing in their temporal and amplitude parameters, but not in their frequency content. Sound is produced at 78.9 (63.6–82.2) SPL rms re 2.10−5 Pa with a peak at 99.2 (85.7–104.6) SPL re 2.10−5 Pa estimated at a distance of one metre. This energy output is significant considering the small size of the insect. When scaled to body length and compared to 227 other acoustic species, the acoustic energy produced by M. scholtzi appears as an extreme value, outperforming marine and terrestrial mammal vocalisations. Such an extreme display may be interpreted as an exaggerated secondary sexual trait resulting from a runaway sexual selection without predation pressure.
PMCID: PMC3115974  PMID: 21698252
23.  Investigating Behaviour and Population Dynamics of Striped Marlin (Kajikia audax) from the Southwest Pacific Ocean with Satellite Tags 
PLoS ONE  2011;6(6):e21087.
Behaviour and distribution of striped marlin within the southwest Pacific Ocean were investigated using electronic tagging data collected from 2005–2008. A continuous-time correlated random-walk Kalman filter was used to integrate double-tagging data exhibiting variable error structures into movement trajectories composed of regular time-steps. This state-space trajectory integration approach improved longitude and latitude error distributions by 38.5 km and 22.2 km respectively. Using these trajectories as inputs, a behavioural classification model was developed to infer when, and where, ‘transiting’ and ‘area-restricted’ (ARB) pseudo-behavioural states occurred. ARB tended to occur at shallower depths (108±49 m) than did transiting behaviours (127±57 m). A 16 day post-release period of diminished ARB activity suggests that patterns of behaviour were affected by the capture and/or tagging events, implying that tagged animals may exhibit atypical behaviour upon release. The striped marlin in this study dove deeper and spent greater time at ≥200 m depth than those in the central and eastern Pacific Ocean. As marlin reached tropical latitudes (20–21°S) they consistently reversed directions, increased swimming speed and shifted to transiting behaviour. Reversals in the tropics also coincided with increases in swimming depth, including increased time ≥250 m. Our research provides enhanced understanding of the behavioural ecology of striped marlin. This has implications for the effectiveness of spatially explicit population models and we demonstrate the need to consider geographic variation when standardizing CPUE by depth, and provide data to inform natural and recreational fishing mortality parameters.
PMCID: PMC3114854  PMID: 21695132
24.  Ontogenetic Development of Weberian Ossicles and Hearing Abilities in the African Bullhead Catfish 
PLoS ONE  2011;6(4):e18511.
The Weberian apparatus of otophysine fishes facilitates sound transmission from the swimbladder to the inner ear to increase hearing sensitivity. It has been of great interest to biologists since the 19th century. No studies, however, are available on the development of the Weberian ossicles and its effect on the development of hearing in catfishes.
Methodology/Principal Findings
We investigated the development of the Weberian apparatus and auditory sensitivity in the catfish Lophiobagrus cyclurus. Specimens from 11.3 mm to 85.5 mm in standard length were studied. Morphology was assessed using sectioning, histology, and X-ray computed tomography, along with 3D reconstruction. Hearing thresholds were measured utilizing the auditory evoked potentials recording technique. Weberian ossicles and interossicular ligaments were fully developed in all stages investigated except in the smallest size group. In the smallest catfish, the intercalarium and the interossicular ligaments were still missing and the tripus was not yet fully developed. Smallest juveniles revealed lowest auditory sensitivity and were unable to detect frequencies higher than 2 or 3 kHz; sensitivity increased in larger specimens by up to 40 dB, and frequency detection up to 6 kHz. In the size groups capable of perceiving frequencies up to 6 kHz, larger individuals had better hearing abilities at low frequencies (0.05–2 kHz), whereas smaller individuals showed better hearing at the highest frequencies (4–6 kHz).
Our data indicate that the ability of otophysine fish to detect sounds at low levels and high frequencies largely depends on the development of the Weberian apparatus. A significant increase in auditory sensitivity was observed as soon as all Weberian ossicles and interossicular ligaments are present and the chain for transmitting sounds from the swimbladder to the inner ear is complete. This contrasts with findings in another otophysine, the zebrafish, where no threshold changes have been observed.
PMCID: PMC3075255  PMID: 21533262
25.  Tactical Release of a Sexually-Selected Pheromone in a Swordtail Fish 
PLoS ONE  2011;6(2):e16994.
Chemical communication plays a critical role in sexual selection and speciation in fishes; however, it is generally assumed that most fish pheromones are passively released since most fishes lack specialized scent glands or scent-marking behavior. Swordtails (genus Xiphophorus) are widely used in studies of female mate choice, and female response to male chemical cues is important to sexual selection, reproductive isolation, and hybridization. However, it is unclear whether females are attending to passively produced cues, or to pheromones produced in the context of communication.
Methodology/Principal Findings
We used fluorescein dye injections to visualize pulsed urine release in male sheepshead swordtails, Xiphophorus birchmanni. Simultaneous-choice assays of mating preference showed that females attend to species- and sex-specific chemical cues emitted in male urine. Males urinated more frequently in the presence and proximity of an audience (conspecific females). In the wild, males preferentially courted upstream of females, facilitating transmission of pheromone cues.
Males in a teleost fish have evolved sophisticated temporal and spatial control of pheromone release, comparable to that found in terrestrial animals. Pheromones are released specifically in a communicative context, and the timing and positioning of release favors efficient signal transmission.
PMCID: PMC3037275  PMID: 21339807

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