The rise of pelagic sharks and adaptive evolution of pectoral fin morphology during the Cretaceous

The emergence and subsequent evolution of pectoral fins is a key point in vertebrate evolution, as pectoral fins are dominant control surfaces for locomotion in extant fishes.1Coates M. The evolution of paired fins.Theory Biosci. 2003; 122: 266-287Crossref Scopus (91) Google Scholar,2Webb P.W. Locomotor patterns in the evolution of Actinopterygian fishes.Am. Zool. 1982; 22: 329-342Crossref Scopus (224) Google Scholar,3Fish F.E. Lauder G.V. Control surfaces of aquatic vertebrates: active and passive design and function.J. Exp. Biol. 2017; 220: 4351-4363Crossref PubMed Scopus (58) Google Scholar However, major gaps remain in our understanding of the diversity and evolution of pectoral fins among cartilaginous fishes (Chondrichthyes), a group with an evolutionary history spanning over 400 million years with current selachians (modern sharks) appearing about 200 million years ago.4Compagno L.J.V. Alternative life-history strategies of cartilaginous fishes in time and space.Environ. Biol. Fishes. 1990; 28: 33-75Crossref Scopus (294) Google Scholar,5Grogan E.D. Lund R. Greenfest-Allen E. The origin and early relationships of early chondrichthyans.in: Carrier J.C. Musick J.A. Heithaus M.R. Biology of Sharks and Their Relatives. Second Edition. CRC Press, 2012: 3-30Crossref Google Scholar,6Maisey J.G. What is an 'elasmobranch'? the impact of paleontology in understanding elasmobranch phylogeny and evolution.J. Fish. Biol. 2012; 80: 918-951Crossref PubMed Scopus (0) Google Scholar Modern sharks are a charismatic group of vertebrates often thought to be predators roaming the open ocean and coastal areas, but most extant species occupy the seafloor.4Compagno L.J.V. Alternative life-history strategies of cartilaginous fishes in time and space.Environ. Biol. Fishes. 1990; 28: 33-75Crossref Scopus (294) Google Scholar Here we use an integrative approach to understand what facilitated the expansion to the pelagic realm and what morphological changes accompanied this shift. On the basis of comparative analyses in the framework of a time-calibrated molecular phylogeny,7Stein R.W. Mull C.G. Kuhn T.S. Aschliman N.C. Davidson L.N.K. Joy J.B. Smith G.J. Dulvy N.K. Mooers A.O. Global priorities for conserving the evolutionary history of sharks, rays and chimaeras.Nat. Ecol. Evol. 2018; 2: 288-298Crossref PubMed Scopus (185) Google Scholar we show that modern sharks expanded to the pelagic realm no later than the Early Cretaceous (Barremian). The pattern of pectoral fin aspect ratios across selachians is congruent with adaptive evolution, and we identify an increase of the subclade disparity of aspect ratio at a time when sea surface temperatures were at their highest.8Scotese C.R. Song H. Mills B.J. van der Meer D.G. Phanerozoic paleotemperatures: the earth's changing climate during the last 540 million years.Earth Sci. Rev. 2021; 215103503Crossref Scopus (271) Google Scholar The expansion to open ocean habitats likely involved extended bouts of sustained fast swimming, which led to the selection for efficient movement via higher aspect ratio pectoral fins. Swimming performance was likely enhanced in pelagic sharks during this time due to the elevated temperatures in the sea, highlighting that shark evolution has been greatly impacted by climate change.