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100 million years of shark macroevolution: A morphometric dive into tooth shape diversity
Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för organismbiologi, Evolution och utvecklingsbiologi. Uppsala University.ORCID-id: 0000-0002-9495-0781
2021 (Engelska)Doktorsavhandling, sammanläggning (Övrigt vetenskapligt)
Abstract [en]

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.

Ort, förlag, år, upplaga, sidor
Uppsala: Acta Universitatis Upsaliensis, 2021. , s. 55
Serie
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2001
Nyckelord [en]
Sharks, Macroevolution, Extinction recovery dynamics, Geometric Morphometrics, Morphospace-Disparity Framework, Teeth
Nationell ämneskategori
Evolutionsbiologi
Forskningsämne
Biologi med inriktning mot evolutionär organismbiologi
Identifikatorer
URN: urn:nbn:se:uu:diva-429934ISBN: 978-91-513-1108-1 (tryckt)OAI: oai:DiVA.org:uu-429934DiVA, id: diva2:1514605
Disputation
2021-03-01, Ekmansalen, Evolutionsbiologiskt centrum, Norbyvägen 14, Uppsala, 13:15 (Engelska)
Opponent
Handledare
Forskningsfinansiär
WallenbergstiftelsernaTillgänglig från: 2021-02-08 Skapad: 2021-01-06 Senast uppdaterad: 2021-03-04
Delarbeten
1. Static Dental Disparity and Morphological Turnover in Sharks across the End-Cretaceous Mass Extinction
Öppna denna publikation i ny flik eller fönster >>Static Dental Disparity and Morphological Turnover in Sharks across the End-Cretaceous Mass Extinction
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2018 (Engelska)Ingår i: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 28, nr 16, s. 2607-2615Artikel i tidskrift (Refereegranskat) Published
Abstract [en]

The Cretaceous-Palaeogene (K-Pg) mass extinction profoundly altered vertebrate ecosystems and prompted the radiation of many extant clades [1, 2]. Sharks (Selachimorpha) were one of the few larger-bodied marine predators that survived the K-Pg event and are represented by an almost-continuous dental fossil record. However, the precise dynamics of their transition through this interval remain uncertain [3]. Here, we apply 2D geometric morphometrics to reconstruct global and regional dental morphospace variation among Lamniformes (Mackerel sharks) and Carch-arhiniformes (Ground sharks). These clades are prevalent predators in today's oceans, and were geographically widespread during the late Cretaceous-early Palaeogene. Our results reveal a decoupling of morphological disparity and taxonomic richness. Indeed, shark disparity was nearly static across the K-Pg extinction, in contrast to abrupt declines among other higher-trophic-level marine predators [4, 5]. Nevertheless, specific patterns indicate that an asymmetric extinction occurred among lamniforms possessing lowcrowned/triangular teeth and that a subsequent proliferation of carcharhiniforms with similar tooth morphologies took place during the early Paleocene. This compositional shift in post-Mesozoic shark lineages hints at a profound and persistent K-Pg signature evident in the heterogeneity of modern shark communities. Moreover, such wholesale lineage turnover coincided with the loss of many cephalopod [6] and pelagic amniote [5] groups, as well as the explosive radiation of middle trophic-level teleost fishes [1]. We hypothesize that a combination of prey availability and post-extinction trophic cascades favored extant shark antecedents and laid the foundation for their extensive diversification later in the Cenozoic [7-10].

Ort, förlag, år, upplaga, sidor
CELL PRESS, 2018
Nationell ämneskategori
Evolutionsbiologi
Identifikatorer
urn:nbn:se:uu:diva-363937 (URN)10.1016/j.cub.2018.05.093 (DOI)000442111300030 ()30078565 (PubMedID)
Forskningsfinansiär
Knut och Alice Wallenbergs StiftelseKungliga Vetenskapsakademien, GS2017-0018
Tillgänglig från: 2018-10-23 Skapad: 2018-10-23 Senast uppdaterad: 2021-01-06Bibliografiskt granskad
2. The extinction and survival of sharks across the end-Cretaceous mass extinction
Öppna denna publikation i ny flik eller fönster >>The extinction and survival of sharks across the end-Cretaceous mass extinction
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(Engelska)Ingår i: Artikel i tidskrift (Refereegranskat) Submitted
Nyckelord
Selachimorpha, Macroevolution, Extinction recovery dynamics, Geometric Morphometrics, Morphospace-Disparity Framework
Nationell ämneskategori
Evolutionsbiologi
Identifikatorer
urn:nbn:se:uu:diva-429931 (URN)
Forskningsfinansiär
Wallenbergstiftelserna
Tillgänglig från: 2021-01-06 Skapad: 2021-01-06 Senast uppdaterad: 2021-01-07
3. Feeding ecology has shaped the evolution of modern sharks
Öppna denna publikation i ny flik eller fönster >>Feeding ecology has shaped the evolution of modern sharks
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2021 (Engelska)Ingår i: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 31, nr 23, s. 5138-5148.e4Artikel i tidskrift (Refereegranskat) Published
Abstract [en]

Sharks are iconic predators in today’s oceans, yet their modern diversity has ancient origins. In particular, present hypotheses suggest that a combination of mass extinction, global climate change, and competition has regulated the community structure of dominant mackerel (Lamniformes) and ground (Carcharhiniformes) sharks over the last 66 million years. However, while these scenarios advocate an interplay of major abiotic and biotic events, the precise drivers remain obscure. Here, we focus on the role of feeding ecology using a geometric morphometric analysis of 3,837 fossil and extant shark teeth. Our results reveal that morphological segregation rather than competition has characterized lamniform and carcharhiniform evolution. Moreover, although lamniforms suffered a long-term disparity decline potentially linked to dietary “specialization,” their recent disparity rivals that of “generalist” carcharhiniforms. We further confirm that low eustatic sea levels impacted lamniform disparity across the end-Cretaceous mass extinction. Adaptations to changing prey availability and the proliferation of coral reef habitats during the Paleogene also likely facilitated carcharhiniform dispersals and cladogenesis, underpinning their current taxonomic dominance. Ultimately, we posit that trophic partitioning and resource utilization shaped past shark ecology and represent critical determinants for their future species survivorship.

Ort, förlag, år, upplaga, sidor
Cell Press, 2021
Nationell ämneskategori
Evolutionsbiologi Ekologi Multidisciplinär geovetenskap
Identifikatorer
urn:nbn:se:uu:diva-429932 (URN)10.1016/j.cub.2021.09.028 (DOI)000729217200002 ()34614390 (PubMedID)
Forskningsfinansiär
Knut och Alice Wallenbergs StiftelseAustralian Research CouncilVetenskapsrådet, 2020-3423
Tillgänglig från: 2021-01-06 Skapad: 2021-01-06 Senast uppdaterad: 2024-01-15Bibliografiskt granskad
4. Southern higher-latitude lamniform sharks track mid-Cretaceous environmental change
Öppna denna publikation i ny flik eller fönster >>Southern higher-latitude lamniform sharks track mid-Cretaceous environmental change
2022 (Engelska)Ingår i: Gondwana Research, ISSN 1342-937X, E-ISSN 1878-0571, Vol. 103, s. 362-370Artikel i tidskrift (Refereegranskat) Published
Abstract [en]

The mid-Cretaceous (Albian and Cenomanian, 113–93.9 Myr) marked a transformative interval of shark evolution during which lamniforms (mackerel sharks) diversified as dominant marine predators. Yet, their radiation dynamics relative to major biotic turnovers delimiting the Albian–Cenomanian and Cenomanian–Turonian boundaries are incompletely understood. Here, we use the high-resolution dental fossil record of lamniforms to track changing morphological disparity and tooth size through a succession of mid-Cretaceous shark assemblages from higher-palaeolatitude (up to ∼ 58°S) settings in Australia. Our geometric morphometric analyses and evolutionary model fitting reveal stable disparity throughout the late Albian–late Cenomanian. By contrast, lamniform disparity increased in the early Turonian, which might reflect local habitat differences and/or intraspecific variability through heterodonty. Nevertheless, clade-specific partial disparity increases are evident among small-bodied carchariids, and couple with a trend towards larger teeth as a proxy for body-size in coeval anacoracids. We correlate these signals with recovery after the Oceanic Anoxic Event 2, which severely disrupted latest Cenomanian marine ecosystems and apparently instigated disjunct responses in shark communities occupying epeiric versus outer neritic environments.

Ort, förlag, år, upplaga, sidor
Elsevier, 2022
Nyckelord
Lamniformes, Albian–Cenomanian, Cenomanian–Turonian, Australia, Geometric morphometrics, Oceanic Anoxic Event 2
Nationell ämneskategori
Evolutionsbiologi
Identifikatorer
urn:nbn:se:uu:diva-429933 (URN)10.1016/j.gr.2021.10.012 (DOI)000802182800003 ()
Tillgänglig från: 2021-01-06 Skapad: 2021-01-06 Senast uppdaterad: 2024-07-02Bibliografiskt granskad

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