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      Hematological convergence between Mesozoic marine reptiles (Sauropterygia) and extant aquatic amniotes elucidates diving adaptations in plesiosaurs

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          Abstract

          Plesiosaurs are a prominent group of Mesozoic marine reptiles, belonging to the more inclusive clades Pistosauroidea and Sauropterygia. In the Middle Triassic, the early pistosauroid ancestors of plesiosaurs left their ancestral coastal habitats and increasingly adapted to a life in the open ocean. This ecological shift was accompanied by profound changes in locomotion, sensory ecology and metabolism. However, investigations of physiological adaptations on the cellular level related to the pelagic lifestyle are lacking so far. Using vascular canal diameter, derived from osteohistological thin-sections, we show that inferred red blood cell size significantly increases in pistosauroids compared to more basal sauropterygians. This change appears to have occurred in conjunction with the dispersal to open marine environments, with cell size remaining consistently large in plesiosaurs. Enlarged red blood cells likely represent an adaptation of plesiosaurs repeated deep dives in the pelagic habitat and mirror conditions found in extant marine mammals and birds. Our results emphasize physiological aspects of adaptive convergence among fossil and extant marine amniotes and add to our current understanding of plesiosaur evolution.

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          Faunal turnover of marine tetrapods during the Jurassic-Cretaceous transition.

          Marine and terrestrial animals show a mosaic of lineage extinctions and diversifications during the Jurassic-Cretaceous transition. However, despite its potential importance in shaping animal evolution, few palaeontological studies have focussed on this interval and the possible climate and biotic drivers of its faunal turnover. In consequence evolutionary patterns in most groups are poorly understood. We use a new, large morphological dataset to examine patterns of lineage diversity and disparity (variety of form) in the marine tetrapod clade Plesiosauria, and compare these patterns with those of other organisms. Although seven plesiosaurian lineages have been hypothesised as crossing the Jurassic-Cretaceous boundary, our most parsimonious topology suggests the number was only three. The robust recovery of a novel group including most Cretaceous plesiosauroids (Xenopsaria, new clade) is instrumental in this result. Substantial plesiosaurian turnover occurred during the Jurassic-Cretaceous boundary interval, including the loss of substantial pliosaurid, and cryptoclidid diversity and disparity, followed by the radiation of Xenopsaria during the Early Cretaceous. Possible physical drivers of this turnover include climatic fluctuations that influenced oceanic productivity and diversity: Late Jurassic climates were characterised by widespread global monsoonal conditions and increased nutrient flux into the opening Atlantic-Tethys, resulting in eutrophication and a highly productive, but taxonomically depauperate, plankton. Latest Jurassic and Early Cretaceous climates were more arid, resulting in oligotrophic ocean conditions and high taxonomic diversity of radiolarians, calcareous nannoplankton and possibly ammonoids. However, the observation of discordant extinction patterns in other marine tetrapod groups such as ichthyosaurs and marine crocodylomorphs suggests that clade-specific factors may have been more important than overarching extrinsic drivers of faunal turnover during the Jurassic-Cretaceous boundary interval.
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            Cell size as a link between noncoding DNA and metabolic rate scaling.

            Accumulation of noncoding DNA and therefore genome size (C-value) may be under strong selection toward increase of body size accompanied by low metabolic costs. C-value directly affects cell size and specific metabolic rate indirectly. Body size can enlarge through increase of cell size and/or cell number, with small cells having higher metabolic rates. We argue that scaling exponents of interspecific allometries of metabolic rates are by-products of evolutionary diversification of C-values within narrow taxonomic groups, which underlines the participation of cell size and cell number in body size optimization. This optimization leads to an inverse relation between slopes of interspecific allometries of metabolic rates and C-value. To test this prediction we extracted literature data on basal metabolic rate (BMR), body mass, and C-value of mammals and birds representing six and eight orders, respectively. Analysis of covariance revealed significant heterogeneity of the allometric slopes of BMR and C-value in both mammals and birds. As we predicted, the correlation between allometric exponents of BMR and C-value was negative and statistically significant among mammalian and avian orders.
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              Vertebrate evolution. Evolutionary innovation and ecology in marine tetrapods from the Triassic to the Anthropocene.

              Many top consumers in today's oceans are marine tetrapods, a collection of lineages independently derived from terrestrial ancestors. The fossil record illuminates their transitions from land to sea, yet these initial invasions account for a small proportion of their evolutionary history. We review the history of marine invasions that drove major changes in anatomy, physiology, and ecology over more than 250 million years. Many innovations evolved convergently in multiple clades, whereas others are unique to individual lineages. The evolutionary arcs of these ecologically important clades are framed against the backdrop of mass extinctions and regime shifts in ocean ecosystems. Past and present human disruptions to marine tetrapods, with cascading impacts on marine ecosystems, underscore the need to link macroecology with evolutionary change.
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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ Inc. (San Diego, USA )
                2167-8359
                19 November 2019
                2019
                : 7
                : e8022
                Affiliations
                [1 ]Section Paleontology, Institute of Geosciences, University of Bonn , Bonn, Germany
                [2 ]Dinosaur Institute, Natural History Museum of Los Angeles County , Los Angeles, CA, USA
                [3 ]Institute of Anatomy, University of Bonn , Bonn, Germany
                [4 ]Department of General Zoology, Faculty of Biology, University of Duisburg-Essen , Essen, Germany
                Author information
                http://orcid.org/0000-0003-4981-4307
                http://orcid.org/0000-0002-1157-8604
                Article
                8022
                10.7717/peerj.8022
                6873879
                d0443c98-f6c1-42f6-99d8-b48e5fba880f
                © 2019 Fleischle et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 23 July 2019
                : 10 October 2019
                Funding
                Funded by: German Research Foundation
                Award ID: SA 469/47-1
                Funding was provided by the German Research Foundation (grant no. SA 469/47-1). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Evolutionary Studies
                Paleontology
                Histology

                plesiosauria,adaptive convergence,aquatic adaptation,sauropterygia,bone histology,erythrocytes,cell size,hematology

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