Squamation and ecology of thelodonts

Thelodonts are an enigmatic group of Paleozoic jawless vertebrates that have been well studied from taxonomical, biostratigraphic and paleogeographic points of view, although our knowledge of their ecology and mode of life is still scant. Their bodies were covered by micrometric scales whose morphology, histology and the developmental process are extremely similar to those of extant sharks. Based on these similarities and on the well-recognized relationship between squamation and ecology in sharks, here we explore the ecological diversity and lifestyles of thelodonts. For this we use classic morphometrics and discriminant analysis to characterize the squamation patterns of a significant number of extant shark species whose ecology is well known. Multivariate analyses have defined a characteristic squamation pattern for each ecological group, thus establishing a comparative framework for inferring lifestyles in thelodonts. We then use this information to study the squamation of the currently described 147 species of thelodonts, known from both articulated and disarticulated remains. Discriminant analysis has allowed recognizing squamation patterns comparable to those of sharks and links them to specific ecological groups. Our results suggest a remarkable ecological diversity in thelodonts. A large number of them were probably demersal species inhabiting hard substrates, within caves and crevices in rocky environments or reefs, taking advantage of the flexibility provided by their micromeric squamations. Contrary to classical interpretations, only few thelodonts were placed among demersal species inhabiting sandy and muddy substrates. Schooling species with defensive scales against ectoparasites could be also abundant suggesting that social interactions and pressure of ectoparasites were present in vertebrates as early the Silurian. The presence of species showing scales suggestive of low to moderate speed and a lifestyle presumably associated with open water environments indicates adaptation of thelodonts to deep water habitats. Scale morphology suggests that some other thelodonts were strong-swimming pelagic species, most of them radiating during the Early Devonian in association with the Nekton Revolution

Patterns of ecological diversification in thelodonts

Here we explore the spatial, temporal and phylogenetic patterns of ecological diversification for the entire clade of thelodonts, one of the earliest groups of vertebrates and longest lasting of the Palaeozoic agnathans in the fossil record. Parsimony and maximum-likelihood methods are used to reconstruct ancestral states of their geographical distributions, habitats and lifestyles. Our results support the concept that thelodonts originated during the Middle?-Late Ordovician probably in marine open waters of Laurasia, with a demersal lifestyle on hard substrates being the ancestral condition for the whole clade. Later, thelodonts underwent a complex ecological diversification and palaeobiogeographical history, comparable in many aspects to those of some major groups of living fishes. Different modes of life evolved repeatedly and a wide range of habitats were colonized by distinct groups, including deep waters and brackish marine and/or freshwater environments. Diadromous strategies presumably appeared on nine different occasions. The palaeobiogeographical history of thelodonts reveals significant differences in the dispersal potential of some major groups. Dispersal of thelodontiforms entailed displacements over long distances and the crossing of deep-water biogeographical barriers, whereas those of furcacaudiforms were always limited to areas interconnected by shallow platforms. We propose that the evolution of pelagic larval stages in thelodontiforms might explain this biogeographical pattern and could satisfactorily account for the greater evolutionary success of this group

The evolution of gigantism in active marine predators

A novel hypothesis to better understand the evolution of gigantism in active marine predators and the diversity of body sizes, feeding strategies and thermophysiologies of extinct and living aquatic vertebrates is proposed. Recent works suggest that some aspects of animal energetics can act as constraining factors for body size. Given that mass-specific metabolic rate decreases with body mass, the body size of active predators should be limited by the high metabolic demand of this feeding strategy. In this context, we propose that shifts towards higher metabolic levels can enable the same activity and feeding strategy to be maintained at bigger body sizes, offering a satisfactory explanation for the evolution of gigantism in active predators, including a vast quantity of fossil taxa. Therefore, assessing the metabolic ceilings of living aquatic vertebrates and the thermoregulatory strategies of certain key extinct groups is now crucial to define the energetic limits of predation and provide quantitative support for this model

Ecomorphological inferences in early vertebrates: Reconstructing Dunkleosteus terrelli (Arthrodira, Placodermi) caudal fin from palaeoecological data

Our knowledge about the body morphology of many extinct early vertebrates is very limited, especially in regard to their post-thoracic region. The prompt disarticulation of the dermo-skeletal elements due to taphonomic processes and the lack of a well-ossified endoskeleton in a large number of groups hinder the preservation of complete specimens. Previous reconstructions of most early vertebrates known from partial remains have been wholly based on phylogenetically closely related taxa. However, body design of fishes is determined, to a large extent, by their swimming mode and feeding niche, making it possible to recognise different morphological traits that have evolved several times in non-closely related groups with similar lifestyles. Based on this well-known ecomorphological correlation, here we propose a useful comparative framework established on extant taxa for predicting some anatomical aspects in extinct aquatic vertebrates from palaeoecological data and vice versa. For this, we have assessed the relationship between the locomotory patterns and the morphological variability of the caudal region in extant sharks by means of geometric morphometrics and allometric regression analysis. Multivariate analyses reveal a strong morphological convergence in non-closely related shark species that share similar modes of life, enabling the characterization of the caudal fin morphology of different ecological subgroups. In addition, interspecific positive allometry, affecting mainly the caudal fin span, has been detected. This phenomenon seems to be stronger in sharks with more pelagic habits, supporting its role as a compensation mechanism for the loss of hydrodynamic lift associated with the increase in body size, as previously suggested for many other living and extinct aquatic vertebrates. The quantification of shape change per unit size in each ecological subgroup has allowed us to establish a basis for inferring not only qualitative aspects of the caudal fin morphology of extinct early vertebrates but also to predict absolute values of other variables such as the fin span or the hypocercal and heterocercal angles. The application of this ecomorphological approach to the specific case of Dunkleosteus terrelli has led to a new reconstruction of this emblematic placoderm. Our proposal suggests a caudal fin with a well-developed ventral lobe, narrow peduncle and wide span, in contrast to classical reconstructions founded on the phylogenetic proximity with much smaller placoderms known from complete specimens. Interestingly, this prediction gains support with the recent discovery of fin distal elements (ceratotrichia) in a well preserved D. terrelli, which suggests a possible greater morphological variability in placoderm caudal fins than previously thought

Network dynamics of eukaryotic LTR retroelements beyond phylogenetic trees

<p>Abstract</p> <p>Background</p> <p>Sequencing projects have allowed diverse retroviruses and LTR retrotransposons from different eukaryotic organisms to be characterized. It is known that retroviruses and other retro-transcribing viruses evolve from LTR retrotransposons and that this whole system clusters into five families: <it>Ty3/Gypsy, Retroviridae, Ty1/Copia, Bel/Pao </it>and <it>Caulimoviridae</it>. Phylogenetic analyses usually show that these split into multiple distinct lineages but what is yet to be understood is how deep evolution occurred in this system.</p> <p>Results</p> <p>We combined phylogenetic and graph analyses to investigate the history of LTR retroelements both as a tree and as a network. We used 268 non-redundant LTR retroelements, many of them introduced for the first time in this work, to elucidate all possible LTR retroelement phylogenetic patterns. These were superimposed over the tree of eukaryotes to investigate the dynamics of the system, at distinct evolutionary times. Next, we investigated phenotypic features such as duplication and variability of amino acid motifs, and several differences in genomic ORF organization. Using this information we characterized eight reticulate evolution markers to construct phenotypic network models.</p> <p>Conclusion</p> <p>The evolutionary history of LTR retroelements can be traced as a time-evolving network that depends on phylogenetic patterns, epigenetic host-factors and phenotypic plasticity. The <it>Ty1/Copia </it>and the <it>Ty3/Gypsy </it>families represent the oldest patterns in this network that we found mimics eukaryotic macroevolution. The emergence of the <it>Bel/Pao, Retroviridae </it>and <it>Caulimoviridae </it>families in this network can be related with distinct inflations of the <it>Ty3/Gypsy </it>family, at distinct evolutionary times. This suggests that <it>Ty3/Gypsy </it>ancestors diversified much more than their <it>Ty1/Copia </it>counterparts, at distinct geological eras. Consistent with the principle of preferential attachment, the connectivities among phenotypic markers, taken as network-represented combinations, are power-law distributed. This evidences an inflationary mode of evolution where the system diversity; 1) expands continuously alternating vertical and gradual processes of phylogenetic divergence with episodes of modular, saltatory and reticulate evolution; 2) is governed by the intrinsic capability of distinct LTR retroelement host-communities to self-organize their phenotypes according to emergent laws characteristic of complex systems.</p> <p>Reviewers</p> <p>This article was reviewed by Eugene V. Koonin, Eric Bapteste, and Enmanuelle Lerat (nominated by King Jordan)</p

Biomechanics of <i>Machaeracanthus</i> pectoral fin spines provide evidence for distinctive spine function and lifestyle among early chondrichthyans

Acanthodians are a major group of Paleaozoic jawed vertebrates that constitute a paraphyletic assemblage of stem-chondrichthyans (Brazeau and Friedman, 2015). Representatives of this group are characterized, among other traits, by the presence of bony spines in front of all paired and median fins except the caudal (Denison, 1979), which has given rise to their colloquial name of 'spiny sharks'. The occurrence of pectoral fin spines is recognized as a potential gnathostome synapomorphy (Miller et al., 2003) or symplesiomorphy (Coates, 2003), being also present in other major groups of Paleaozoic jawed vertebrates, including placoderms (Young, 2010), 'non-acanthodian' chondrichthyans (Miller et al., 2003), and osteichthyans (Zhu et al., 1999). However, this trait was independently lost in the later evolutionary history of these lineages and is absent in most living representatives (Coates, 2003; Miller et al., 2003), with the exception of catfishes (Siluriformes), that acquired pectoral fin spines as an evolutionary reversion (Price et al., 2015). As a consequence, the paucity of living analogsue precludes deriving functional interpretations of those structures and the role that they fulfilled in life remains unclear, despite this having the potential to enrich our understanding on the ecologies and lifestyles of groups of early jawed vertebrates. Machaeracanthus constitutes a genus of acanthodians that ranged from the Late Silurian to the Middle Devonian, which is known from fin spines, scales, and a few endoskeletal remains (Burrow et al., 2010; Botella et al., 2012). The spines of this genus differ from the fin spines of all other acanthodians and sharks in presenting a marked cross-sectional asymmetry and a totally enclosed central canal, which is usually open along the proximal end of the trailing edge in other taxa (Burrow et al., 2010). The description of wear patterns at the tips of pectoral fin spines of Machaeracanthus and their peculiar arrangement in pairs has led some authors to propose that these elements could have been used as 'snow-shoes' to lay on and prevent sinking into the substrate below or even to propel itself along the bottom (Südkamp and Burrow, 2007). Here, we test this hypothesis through beam theory analyses and provide evidence that the biomechanical properties of Machaeracanthus pectoral fin spines are compatible with this interpretation, thus shedding light on the diversity of the functions of these intriguing anatomical structures and the lifestyles of some of the earliest jawed vertebrates

Lonchidion derenzii sp. nov., a new lonchidiid shark (Chondriychtyes, Hybodontiforms) from the Late Triassic of Spain with remarks on lonchidiid enameloid

Lonchidiidae Herman, 1977, represents one of the most diverse and controversial families of Hybodontiformes, the sister group of Neoselachii (i.e., modern sharks, skates, and rays). It was initially erected as a monogeneric family including only Lonchidion Estes, 1964, a genus of small euryhaline hybodonts from the Mesozoic. Recently, Cappetta (2012) recognized up to eight genera within the family: Baharyodon, Diplolonchidion, Vectiselachos, Hylaeobatis, Isanodus, Parvodus,Lissodus, andLonchidion, although the content of the family is still under discussion (see, e.g., Rees, 2008; Khamha et al., 2016). Major discrepancies concern the phylogenetic relationships between Lonchidion and Lissodus and the taxonomic status of the latter. Thus, based on the general similarity of their teeth,Duffin (1985, 2001) considered Lonchidion as a junior synonym of Lissodus. Subsequently, Rees and Underwood (2002) restored Lonchidion as a valid genus, closely related to Lissodus, within the family Lonchidiidae (togetherwith Vectiselachos, Parvodus, andHylaeobatis). This interpretation has been followed by several authors (e.g., Fischer, 2008; Cappetta, 2012; Johns et al., 2014). In contrast, Rees (2008) considered Lonchidion and Lissodus not so closely related to each other, excluding Lissodus from Lonchidiidae. The majority of Lonchidion species has been described on the basis of disarticulated teeth, and complete or partial articulated skeletons have been known only recently from juvenile specimens, assigned to Lonchidion sp., from the inland lacustrine Konservat- Lagerst¿atten outcrop of Las Hoyas (Lower Cretaceous, Spain) (Soler-Gij on et al., 2016). Currently, the stratigraphic distribution of the ranges from the Middle-Upper Triassic (Fischer et al., 2011; Johns et al., 2014) to the Upper Cretaceous (Estes, 1964). In the present study, we describe a new species assigned to Lonchidiidae, Lonchidion derenzii, sp. nov., based on distinctive isolated teeth from the Upper Triassic (Carnian) of Spain, representing the earliest well-documented occurrence of the genus in Europe

Bioluminescent-like squamation in the galeomorph shark Apristurus ampliceps (Chondrichthyes: Elasmobranchii)

Galeomorph sharks constitute the most taxonomically and ecologically diverse superorder of living selachians. Despite comprising several typically deep-water taxa, no bioluminescent species have been reported in this group so far. Interestingly, the study of shark squamation has been revealed in recent years to be a good proxy for inferring some ecological aspects of poorly known species. In particular, the high morphological specificity of the dermal denticles and the squamation patterns of all currently-known bioluminescent sharks could constitute a potential tool for predicting bioluminescence in both fossil and living taxa. Following this idea, we provide the first evidence supporting the possible existence of bioluminescence among galeomorph sharks by means of the quantitative study of Apristurus ampliceps squamation pattern. Classical morphometric analysis and multivariate statistical procedures have allowed us to determine that A. ampliceps squamation, composed mainly of bristle-shaped dermal denticles, is highly convergent with that of the bioluminescent shark Etmopterus spinax. The ecology of A. ampliceps, being a species that exclusively inhabits aphotic waters, is in agreement with such a morphofunctional interpretation, but finding photophores is imperative to confirm this prediction

Use of nursery areas by the extinct megatooth shark Otodus megalodon (Chondrichthyes: Lamniformes)

Nursery areas are fundamental for the success of many marine species, particularly for large, slow-growing taxa with low fecundity and high age of maturity. Here, we examine the population size-class structure of the extinct gigantic shark Otodus megalodon in a newly described middle Miocene locality from Northeastern Spain, as well as in eight previously known formations (Temblor, Calvert, Pisco, Gatún, Chucunaque, Bahía Inglesa, Yorktown and Bone Valley). In all cases, body lengths of all individuals were inferred from dental parameters and the size-class structure was estimated from kernel probability density functions and Gaussian mixture models. Our analyses support the presence of five potential nurseries ranging from the Langhian (middle Miocene) to the Zanclean (Pliocene), with higher densities of individuals with estimated body lengths within the typical range of neonates and young juveniles. These results reveal, for the first time, that nursery areas were commonly used by O. megalodon over large temporal and spatial scales, reducing early mortality and playing a key role in maintaining viable adult populations. Ultimately, the presumed reliance of O. megalodon on the presence of suitable nursery grounds might have also been determinant in the demise of this iconic top predatory shark