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Phylogeny of Lamniform Sharks Based on Whole Mitochondrial Genome Sequences

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Phylogeny of Lamniform Sharks Based on Whole Mitochondrial Genome Sequences Iowa State University Capstones, Theses and Retrospective Theses and Dissertations Dissertations 1-1-2003 Phylogeny of lamniform sharks based on whole mitochondrial genome sequences Toni Laura Ferrara Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/rtd Recommended Citation Ferrara, Toni Laura, "Phylogeny of lamniform sharks based on whole mitochondrial genome sequences" (2003). Retrospective Theses and Dissertations. 19960. https://lib.dr.iastate.edu/rtd/19960 This Thesis is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Retrospective Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Phylogeny of lamniform sharks based on whole mitochondrial genome sequences by Toni Laura Ferrara A thesis submitted to the graduate faculty in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE Major: Zoology Program of Study Committee: Gavin Naylor, Major Professor Dean Adams Bonnie Bowen Jonathan Wendel Iowa State University Ames, Iowa 2003 11 Graduate College Iowa State University This is to certify that the master's thesis of Toni Laura Ferrara has met the thesis requirements of Iowa State University Signatures have been redacted for privacy 111 TABLE OF CONTENTS GENERAL INTRODUCTION 1 LITERATL:jRE REVIEW 2 CHAPTER ONE: THE BIOLOGY OF LAMNIFORM SHARKS 2 CHAPTER TWO: LAMNIFORM SYSTEMATICS AND PHYLOGENY 49 CHAPTER THREE: THE FOSSIL RECORD OF LAMNIFORMES 76 CHAPTER FOUR: MITOCHONDRIAL GENOMES, TAXON SAMPLING AND PHYLOGENY 96 CHAPTER FIVE: A PHYLOGENY OF LAMNIFORM SHARKS BASED ON WHOLE MITOCHONDRIAL GENOME SEQUENCES 115 CHAPTER SIX: A TANDEM DUPLICATION IN THE MITOCHONDRIAL GENOME OF THE GOBLIN SHARK MITSUKURINA OWSTONI 147 GENERAL CONCLUSIONS 153 RErERENCES 154 ACKNOWLEDGEMENTS 180 APPENDIX 181 1 GENERAL INTRODUCTION The order Lamniformes comprises 15 living species of sharks organized into seven families. The diversity among these species is impressive. Within the Lamniformes are the notorious predator, the great white shark (Carcharodon carcharias), and two species of harmless filter-feeding sharks, the megamouth (Megachasma pelagios) and the basking shark (Cetorhinus maximus). The remarkable discovery of the megamouth shark in 1976 renewed interest in the phylogenetic relationships among lamniform sharks. Morphology-based analyses of lamniform phylogeny have produced conflicting results (Maisey, 1985; Compagno, 1990; Shirai 1992, 1996; De Carvalho, 1996). Subsequent molecular-based analyses of this group were also unable to discern their phylogeny (Morrissey et al., 1997; Martin and Naylor, 1997; Naylor et al., 1997; Martin et al., 2002; Martin and Burg, 2002; Lopez et al., MS). Although lamniform teeth are abundant in the fossil record, these have proved of limited use in revealing relationships among living species. The aim of this thesis is to attempt to resolve lamniform phylogeny using entire mitochondrial genome sequences from all living taxa. As there are only 15 living species of lamniform sharks, this group represents an excellent opportunity to test the idea that complete taxon sampling combined with large datasets (such as entire mitochondrial genome sequences) can improve phylogenetic reconstruction. Thesis Organization This thesis is written in an alternative format. It includes an extensive literature review, that is divided into four chapters: Chapter One is an overview of the biology of lamniform sharks; Chapter Two examines lamniform systematics; Chapter Three covers the fossil record of these sharks; and Chapter Four discusses the utility of mitchondrial genes and genomes in phylogenetic analysis. Chapters Five and Six present the results of this study and are written in manuscript format. A general conclusion summarizing the contents of all six Chapters is included, followed by a final list of references combined for all Chapters. Compete mitochondrial genome sequences for all 15 species of lamniform sharks are listed in the Appendix in GENBANK format. 2 LITERATURE REVIEW CHAPTER ONE: THE BIOLOGY OF LAMNIFORM SHARKS Introduction The order Lamniformes comprises 15 living species of sharks organized into seven families. The diversity among these species is impressive. Within the Lamniformes is the notorious predator, the great white shark (Carcharodon carcharias), and two species of harmless filter-feeding sharks, the megamouth (Megachasma pelagios) and the basking shark (Cetorhinus maximus). Individual lamniforms also exhibit an array of biological adaptations unique among cartilaginous fishes. For example, the sand tiger shark Carcharias taurus, a common inhabitant of many public aquaria, was the first shark in which the unusual reproductive behavior of uterine cannibalism was documented (Bass et al., 1975). Thresher sharks (Alopias spp.) have enormously long and asymmetrical tails that make up about half the shark's total body length. Endothermy, a rare adaptation among fishes, has been described for several species of lamniform sharks. Also included in the order are poorly studied species such as the crocodile shark (Pseudocarcharias kamoharai) and the bizarre deep-sea goblin shark (Mitsukurina owstoni). This Chapter provides an introduction to the unique adaptations exhibited by lamniform species as well as an overall guide to their biology. Subsequent chapters include detailed information on the fossil record of the group, and the systematics and evolutionary relationships among taxa. A list of sharks is presented (for a key to species, see Chapter Two) as a guide to recognized species within the Lamniformes and as an outline for the Chapter, since species are also discussed in the order listed. Adaptations such as filter-feeding, endothermy and reproduction are discussed separately. List of families and species in the order Lamniformes Order Lamniformes Compagno,1973 Family Megachasmidae Taylor et a1.,1983 Megamouth shark, one species in one genus: Genus Megachasma Taylor et al., 1983 Species M. pelagios Taylor et al., 1983 3 Family Cetorhinidae Gill, 1862 Basking shark, one species in one genus: Genus Cetorhinus Blainville, 1816 Species C. maximus (Gunnerus, 1765) Family Mitsukurinidae Jordan, 1898 Goblin shark, one species in one genus: Genus Mitsukurina Jordan, 1898 Species M. owstoni Jordan, 1898 Family Pseudocarchariidae Compagno,1973 Crocodile shark, one species in one genus: Genus Pseudocarcharias Cadenat, 1963 Species P. kamoharai (Matsubara, 1936) Family Qdontaspididae Muller and Henle,1839 Sand tiger sharks, three species in two genera: Genus Carcharias Rafinesque, 1810 Species C. taurus Rafinesque, 1810 Genus Odontaspis Agassiz, 1838 Species O. ferox (Risso, 1810) O. noronhai Maul, 1955 Family Alopiidae Bonaparte, 1838 Thresher sharks, three species in one genus: Genus Alopias Rafinesque, 1810 Species A. vulpinus (Bonnaterre, 1788) A. pelagicus Nakamura, 1935 A. superciliosus Lowe, 1839 Family Lamnidae Muller and Henle,1838 Mackerel sharks, five species in three genera: 4 Genus Lamna Cuvier, 1817 (porbeagle and salmon shark) Species L. nasus (Bonnaterre, 1788) L. ditropis Hubbs and Follett, 1947 Genus Isurus Rafinesque, 1809 (mako sharks) Species 1. oxyrinchus Rafinesque, 1809 1.paucus Guitart Manday, 1966 Genus Carcharodon Smith, 1838 (great white shark) Species: C. carcharias (Linnaeus, 1758) Family Megachasmidae In November, 1976, the crew of a research vessel operating off the coast of Oahu, Hawaii, was stunned when they found a large, bizarre shark caught in their gear. Realizing the uniqueness of such a creature the crew kept the shark (despite complications imposed by its large size) and made it available for scientific study. The shark, a 4.46m male, weighing 750kg, was determined not only to be a new species of shark, but to represent a new genus and family belonging to the order Lamniformes (see Chapter Two for diagnostic features). The shark was dubbed "megamouth shark" by the press and the animal was formally named Megachasma pelagios, from the Greek "megachasma" for "large opening", and "pelagios" meaning "of the open sea" (Taylor et al., 1983). The remarkable discovery of this large, previously unknown and bizarre species of shark has been likened in importance to the 1938 capture of the coelacanth (Berra, 1997). The unusual nature of the animal makes this find even more impressive; Megachasma pelagios is believed to be a filter- feeder, one of only three species of sharks to possess such a feeding mechanism (Taylor et al., 1983). The following section details current information on the biology of Megachasma pelagios. A discussion of filter-feeding in this animal as compared to other filter-feeding sharks (including the lamniform, Cetorhinus maximus) is presented elsewhere in this Chapter. Since its discovery in 1976, less than 20 specimens of Megachasma pelagios have been documented. Almost all of these have been males caught in the Pacific Ocean (Hawaii, California, Japan, Philippines, Indonesia) (Amorim et. al, 2000). One specimen (a male) was caught off Western Australia, making it the first specimen captured in the Indian Ocean (Berra and Hutchins, 1990). Although Megachasma was then unknown from the Atlantic Ocean, Berra and Hutchins (1991) believed the shark should inhabit these waters. This statement was based on previous studies of the 5 other two known species of large
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