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100 Million Years of Shark Macroevolution

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100 Million Years of Shark Macroevolution Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 2001 100 million years of shark macroevolution A morphometric dive into tooth shape diversity MOHAMAD BAZZI ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 ISBN 978-91-513-1108-1 UPPSALA urn:nbn:se:uu:diva-429934 2021 Dissertation presented at Uppsala University to be publicly examined in Ekmansalen, Evolutionsbiologiskt centrum, Norbyvägen 14, Uppsala, Monday, 1 March 2021 at 13:15 for the degree of Doctor of Philosophy. The examination will be conducted in English. Faculty examiner: Associate Professor Dr. Matt Friedman (University of Michigan). Abstract Bazzi, M. 2021. 100 million years of shark macroevolution. A morphometric dive into tooth shape diversity. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 2001. 55 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-1108-1. Few vertebrate clades exhibit the evolutionary longevity and versatility of sharks, which constitute nearly half of all current chondrichthyan biodiversity and represent an ecological diversity of mid-to-apex trophic-level predators in both marine and freshwater environments. The rich fossil record of shark teeth from Mesozoic and Cenozoic rocks also makes the group amenable to large-scale quantitative analyses. This thesis reconstructs the morphological tooth disparity of dominant lamniform (Mackerel sharks) and carcharhiniform (Ground sharks) clades over the last 100 million years. The relative diversity of these major lineages is strongly skewed, with lamniforms, including the famous White shark, making up less than 3% of the total species richness, whereas carcharhiniforms, such as Tiger sharks, comprise over 290 described species. Paradoxically, this long-recognized disproportionate representation was reversed in the distant geological past. Indeed, the fossil record shows that lamniforms accounted for nearly all of the documented shark diversity during the final stages of the Late Cretaceous — the terminal time interval of the ‘Age of Dinosaurs’, which ended 66 million years ago. The causes of this radical diversity turnover are debated, with recent research suggesting that competition and/or climate change drove major shifts in shark evolution. Perhaps more surprisingly, most analyses of diversity dynamics of sharks centre largely on taxonomic data, thus omitting more direct proxies of ecology, such as morphological diversity, or disparity. To mitigate this shortfall, I adopt a Procrustes framework combined with phylogenetic comparative and multivariate statistics to shed light on the deep-time morphological evolution of sharks. My work indicates that the end-Cretaceous mass extinction initiated a sustained evolutionary turnover in ecological dominance between lamniforms and carcharhiniforms. More specifically, the morphospace of these clades, indicate a selective extinction at the K/Pg Boundary affecting ‘large-bodied’ anacoracid lamniform sharks, whereas triakid carcharhiniforms proliferated in the extinction aftermath, perhaps as a response to new prey sources. Overall, my thesis suggests that the modern shark assemblages are the synergistic result of feeding ecology (including dietary niche breadth) and environmental shifts in global sea levels and temperature acting over the last 100 million years. Keywords: Sharks, Macroevolution, Extinction recovery dynamics, Geometric Morphometrics, Morphospace-Disparity Framework, Teeth Mohamad Bazzi, Department of Organismal Biology, Evolution and Developmental Biology, Norbyv 18 A, Uppsala University, SE-75236 Uppsala, Sweden. © Mohamad Bazzi 2021 ISSN 1651-6214 ISBN 978-91-513-1108-1 urn:nbn:se:uu:diva-429934 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-429934) To my family List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Bazzi, M., Kear, B. P., Blom, H., Ahlberg, P. E. & Campione, N. E. (2018). Static dental disparity and morphological turnover in sharks across the end-Cretaceous mass extinction. Current Biology, 28(16), 2607-2615. II Bazzi, M., Campione, N. E., Kear, B. P., Blom, H. & Ahlberg, P. E. The extinction and survival of sharks across the end-creta- ceous mass extinction. III Bazzi, M., Campione, N. E., Kear, B. P. & Ahlberg, P. E. Feed- ing ecology has shaped the evolution of sharks. IV Bazzi, M., Kear, B. & Siversson, M. Southern higher-latitude lamniform sharks track mid-Cretaceous environmental change. Additionally, the following papers was prepared during the course of the PhD, but is not included in this thesis. I Conte, G. L., Fanti, F., Trevisani, E., Guaschi, P., Barbieri, R. & Bazzi, M. (2019). Reassessment of a large lamniform shark from the Upper Cretaceous (Santonian) of Italy. Cretaceous Research, 99, 156-168. II Zhu, Y., Giles, S., Young, G., Hu, Y., Zhu, M., Bazzi, M., Ahl- berg, P. E. & Lu, J. (2021). Endocast and bony labyrinth of a Devonian ‘placoderm’ challenges stem gnathostome phylogeny Current Biology. III Kear, B. P., Bazzi, M., Campione, N. E., Madzia, D., Lindgren, J., Sachs, S. & Lee, M. Polar plesiosaurs elucidate environmen- tal interplay in marine reptile evolution. Reprints were made with permission from the respective publishers. Contents Introduction ..................................................................................................... 9 Survey of the field .................................................................................... 13 A ‘taxon-free’ approach ........................................................................... 14 Comparing sister taxa ............................................................................... 15 Tooth morphology and diet ...................................................................... 18 The Procrustes paradigm .......................................................................... 20 Data acquisition ................................................................................... 21 Definitions of morphological disparity .................................................... 23 Disparity metrics .................................................................................. 24 Temporal strategies .............................................................................. 25 Assumptions ............................................................................................. 26 Research Aims .............................................................................................. 27 Summary of results ....................................................................................... 28 Mass extinction and its impact on sharks (Papers I and II) ................. 28 A swim through the Cenozoic (Paper III) ............................................ 31 The Mackerel Shark Rises (Paper IV) ................................................. 34 Limitations ........................................................................................... 36 Conclusions and future prospects ................................................................. 38 Svensk sammanfattning ................................................................................ 40 42 ............................................................................................ ﻣﻠﺨﺺ ﺑﺎﻟﻠﻐﺔ ﺍﻟﻌﺮﺑﻴﺔ Acknowledgments......................................................................................... 44 References ..................................................................................................... 46 Abbreviations k number of dimensions of the object or of the configuration p number of landmarks n number of objects or observations PCA principal component analysis dP partial Procrustes distance Be bending energy matrix GPA generalised Procrustes analysis TPS Thin-Plate Splines Introduction Biodiversity is unevenly partitioned across the Tree of Life (Raup et al., 1973; Slowinski and Guyer, 1993; Mooers and Heard, 1997). For example, in the marine realm, actinopterygian fishes reign supreme, with > 33.000 extant spe- cies, outnumbering the combined diversity of cartilaginous fishes, jawless fishes, lobe-finned fishes, and marine tetrapods (Nelson, Grande and Wilson, 2016). This imbalance in richness distribution also persists at lower taxonomic levels (e.g., acanthomorphs comprise at least half of actinopterygian fish di- versity) (Near et al., 2013). We observe a similar trend of richness asymme- tries between clades in the fossil record, and it is, therefore, one of the most pervasive patterns in organismal biology (Benton, 2015; Scholl and Wiens, 2016; Wiens, 2017). Prevailing evolutionary hypotheses suggests that clades will achieve higher richness either because 1) they have had more time to evolve (i.e., they are older) or 2) as an outcome related to faster rates of net diversification (i.e., speciation minus extinction over time) (reviewed in Wiens, 2017) (but also see: McPeek and Brown, 2007; Ricklefs, 2007). Yet, on a larger phylogenetic-scale the analytical support for variation in diver- sification rates, generally surpass that of clade ages, as an explanation, for the dramatic difference in species richness between clades (Scholl and Wiens, 2016; Wiens, 2017). Underlying factors, such as trait variability (e.g., mor- phology, ecology) and species interactions (e.g., competition), are consecu- tively invoked to explain rate difference among clades (Wiens, 2017). Perti- nently, such factors are considered key components of the ecological
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