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Cartilaginous Fishes (Chondrichthyes)

Cartilaginous Fishes (Chondrichthyes)

Cartilaginous fi shes ()

Matthew P. Heinickea,*, Gavin J. P. Naylorb, and dorsoventrally P attened and benthic in habit. Although S. Blair Hedgesa early chondrichthyans included many freshwater forms, aDepartment of , 208 Mueller Laboratory, Pennsylvania living species are overwhelmingly marine in distribution, State University, University Park, PA 16802-5301, USA; bSchool excluding a few and rays and some of Computational Biology, Dirac Science Library, Florida State freshwater stingrays. Here, we review the relationships University, Tallahassee, FL 32306, USA of the subclasses, orders, and families of cartilaginous *To whom correspondence should be addressed ([email protected]) A shes. Additionally, molecular divergence times of these groups are estimated from publicly available sequence data and presented. Abstract 7 e record of Chondrichthyes has been consid- ered excellent, based largely on rich deposits of dental Sharks, rays, , and relatives (Class Chondrichthyes) material (6). 7 e cartilaginous of Chondrich- comprise an important component of living thyes fossilizes poorly; therefore, skeletal fossil mater- diversity, with two subclasses, 18 orders, ~55 families, and ial is much rarer ( 7). 7 e earliest assigned to ~1200 species. Recent morphological studies have sup- Chondrichthyes are from the (444–416 Ma) (8). ported a position for rays deeply nested within sharks. Fossils become more common in the (416–359 Molecular analyses, however, support a basal divergence Ma), including many representatives of extinct groups. between rays and sharks. New molecular timing analyses Based on these fossils, the Subclasses and presented here suggest that the earliest divergences in are estimated to have diverged by 410 Chondrichthyes occurred deep in the , 460–300 Ma (8). Fossil evidence for modern representatives of million ago (Ma), and that most living families origi- these subclasses—Suborder Chimaeroidei (chimaeras) nated before the end of the (66 Ma). If accurate, and Infraclass (sharks and rays)—does not these dates imply large ghost ranges in the fossil record for occur until the Mesozoic (251–66 Ma) (9, 10). Living many chondrichthyan groups. orders and families can be identiA ed from the (200–146 Ma) onward, with fossil evidence of most fam- Living members of the Subclasses Holocephali (chimae- ilies before the end of the Mesozoic (7, 10). ras, including ratA shes, spookA shes, and rabbitA shes, ~43 sp.) and Elasmobranchii (sharks, rays, skates, saw- A shes, and guitarA shes, ~1125 sp.) together comprise the extant representatives of the Class Chondrichthyes (car- tilaginous A shes) (1). Holocephali includes only a single living order with three families (1, 2). Elasmobranchs are more diverse, with ~17 orders and ~52 families (there is some disagreement in ordinal and familial lim- its, especially among rays) (1, 3–5). Chondrichthyans can be diB erentiated from their closest living relatives, (bony ), by possession of a skel- eton of prismatic and internal fertilization via modiA ed male pelvic A ns (claspers). Other characters common to the group are possession of placoid (- like) scales and, in many lineages, a heterocercal tail A n. While most sharks and chimaeras have a generally cylindrical “A shlike” body form (Fig. 1), some sharks and Fig. 1 A Great White ( ) from near all batoids (rays, skates, sawA shes, and guitarA shes) are Isla Guadalupe, Mexico. Credit: T. Goss.

M. P. Heinicke, G. J. P. Naylor, and S. B. Hedges. Cartilaginous A shes (Chondrichthyes). Pp. 320–327 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009).

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Carcharhinidae 44 42 Triakidae-1 40 35 Triakidae-2 Leptochariidae 22 21 25

Proscylliidae 16 Scyliorhinidae-1 Scyliorhinidae-2 Alopiidae 39 Megachasmidae 13 33 Odontaspididae 31 Pseudocarchariidae 29 36 Cetorhinidae 20 32 Carchariidae 7 45 38 Stegosomatidae 5 19 Brachaeluridae 27 14 Orectolobidae Orectolobiformes Heterodontidae Heterodontiformes Heterodontiformes Oxynotidae 28 3

23

Centrophoridae 12 Squatinidae 9 18

Echinorhinidae Squalimorphii Galeomorphii Pristiophoridae Squatiniformes

4 Echinorhiniformes Notorynchidae 43

15 Hexanchidae Pristiophoriformes Chlamydoselachidae (continued on next page) O S D C P Tr J K Pg PALEOZOIC MESOZOIC CZ 400 300 200 100 0 Million years ago

Fig. 2 Continues

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(continued on previous page) Myliobatidae 34 Gymnuridae Dasyatidae-1 2 Dasyatidae-2 30 Hexatrygonidae Plesiobatidae 11 Rhinidae 41 10 Rhynchobatidae 24 Rhiniformes 1 Pristidae

Rhinobatidae Rhynchobatiformes Pristiformes 8

Torpedinidae Rhinobatiformes

26 Platyrhiniformes -2 6 Narcinidae-1

Rajidae Torpediniformes

Rhinochimaeridae 37 17 Callorhinchidae Holocephali Chimaeriformes O S D C P Tr J K Pg PALEOZOIC MESOZOIC CZ 400 300 200 100 0 Million years ago Fig. 2 A timetree of cartilaginous fi shes (Chondrichthyes). for paraphyletic and/or polyphyletic groups are as follows: Divergence times are from Table 1. Galeomorphii, Triakidae-1 (Mustelus), Triakidae-2 (), Scyliorhinidae-1 Squalimorphii, and Batoidea comprise the Subclass (Pentanchinae), Scyliorhinidae-2 (Scyliorhininae), Dasyatidae-1 Elasmobranchii. Abbreviations: C (), CZ (), (), Dasyatidae-2 (), Narcinidae-1 (Narcininae), D (Devonian), J (Jurassic), K (Cretaceous), O (), and Narcinidae-2 (Narkinae). P (), Pg (Paleogene), S (Silurian), and Tr (). Codes

Division of living cartilaginous A shes into Elasmo- compressed (Pristiophoriformes) and angel branchii and Holocephali is strongly supported by sharks (Squatiniformes) (15). 7 ese in turn group morphological analyses, as is uniting these groups to with the Orders Squaliformes, Hexanchiformes, and form Chondrichthyes (6, 9, 11). Within Holocephali, it Echinorhiniformes in the Hypnosqualean clade. 7 e is believed that and Chimaeridae Orders Lamniformes, Carcharhiniformes, Orectolob- form a group to the exclusion of Callorhinchidae ( 12). iformes, and Heterodontiformes are grouped as Galea (3, 7 e relationships of the more species-rich elasmo- 4). Minor modiA cations to Shirai’s original 1992 hypoth- branchs are more contentious. Early studies suggested esis of elasmobranch interrelationships were made by de a basal split between sharks and rays (13, 14). In 1992, Carvalho in 1996 (4). 7 is hypothesis remains the con- Shirai published an extensive and inP uential analysis sensus from morphological data. of morphological variation among sharks and rays Because the monophyly of Chondrichthyes and recip- in which he proposed a “Hypnosqualean hypothesis” rocal monophyly of Elasmobranchii and Holocephali wherein the batoids fall together with the dorsoventrally have not been controversial and are supported by

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Table 1. Divergence times (Ma) and their confi dence/credibility intervals (CI) among cartilaginous fi shes (Chondrichthyes), based on analyses presented here.

Timetree Estimates Node Time This study (a) This study (b) This study (c) Time CI Time CI Time CI

1 471 471 494–434 486 495–463 436 482–411 2 393 393 431–354 440 471–403 357 402–319 3 350 350 392–309 419 452–380 273 319–235 4 327 327 372–283 392 431–345 256 304–214 5 318 318 359–279 374 414–330 258 301–222 6 291 291 333–250 308 368–248 308 357–262 7 289 289 329–252 344 386–300 234 276–201 8 281 281 324–241 – – 294 344–249 9 276 276 323–232 329 385–265 219 269–178 10 274 274 318–235 – – 285 334–240 11 265 265 307–227 283 341–228 273 321–228 12 263 263 311–220 312 370–247 207 256–165 13 259 259 297–226 304 346–262 220 260–190 14 237 237 287–186 280 338–215 – – 15 236 236 295–183 285 353–202 – – 16 226 226 261–195 269 310–228 189 227–166 17 220 220 320–125 248 351–128 – – 18 214 214 269–163 252 324–176 – – 19 195 195 249–139 231 296–160 – – 20 185 185 224–148 222 270–175 – – 21 179 179 210–153 213 251–177 155 194–124 22 173 173 204–149 205 242–171 141 179–111 23 170 170 218–128 190 268–121 142 188–106 24 159 159 219–105 – – 169 233–110 25 153 153 183–127 183 222–147 114 156–77 26 145 145 205–98 – – 154 215–101 27 142 142 201–84 169 243–97 – – 28 135 135 184–93 154 229–91 108 155–73 29 126 126 160–104 167 217–125 120 154–102 30 124 124 159–98 – – 127 166–99 31 122 122 155–100 140 193–93 – – 32 122 122 154–101 122 167–100 117 150–100 33 119 119 151–97 120 172–74 117 151–98 34 111 111 139–97 115 148–100 115 149–98 35 110 110 133–96 112 140–96 – – 36 109 109 142–83 93.4 139–59 109 142–86 37 107 107 182–51 – – 123 197–65 38 106 106 162–60 127 196–69 – – 39 104 104 139–73 103 157–58 – –

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Table 1. Continued

Timetree Estimates Node Time This study (a) This study (b) This study (c) Time CI Time CI Time CI

40 98.6 98.6 118–90 99 123–90 107 139–90 41 92.4 92.4 150–47 – – 99.6 164–49 42 91.6 91.6 111–77 91 116–73 94.8 127–73 43 79.7 79.7 150–29 98.6 185–34 – – 44 72.1 72.1 94–53 70.9 97–50 – – 45 53.1 53.1 97–23 64.6 119–27 – –

Note: Node times for the timetree are from the combined analysis of RAG1, 12S, and 16S alignments [shown with CI in column (a)]. Columns (b) and (c) present estimates from RAG1 and 12S/16S analyses, respectively.

numerous morphological characters, molecular stud- determined the relationships among the families of ies have not been designed to speciA cally address these guitarA shes (Rhinidae, Rhynchobatidae), thornback rays relationships. However, recent molecular studies that (Platyrhinidae), or panrays (Zanobatidae). Based on ana- have included a broad enough sample of taxa to draw lysis of mitochondrial 12S ribosomal RNA (rRNA) gene conclusions have supported the monophyly of these sequences available in GenBank, however, it appears that groups (16, 17). 7 e interrelationships among the holo- Rhinidae and Rhyncobatidae form a sawA sh/guitarA sh cephalan families have not yet been addressed with group with Pristidae and Rhinobatidae, while the pos- molecular data. However, one mitochondrial gene study, ition of thornback rays remains unresolved (results not using several holocephalan species as outgroups, has shown). suggested that Rhinochimaeridae is embedded within Molecular studies of shark orders and families have Chimaeridae (18). led to a somewhat better understanding of relation- Most molecular studies have focused on elasmobranch ships. 7 e two major groups of sharks, galeomorphs and interrelationships. Studies in the early to mid-1990s squalimorphs, are supported in most molecular stud- included too few taxa or sites to infer strong conclusions ies (7, 17, 18, 22, 23, 25). Although morphologically part (19–21). Since 2003, elasmobranch relationships have of Galeomorphii, the horn sharks (Heterodontiformes) been inferred with more comprehensive data sets of both are in a basal position in molecular phylogenies, and nuclear and mitochondrial data, including most orders cluster with both Squalimorphii and Galeomorphii, and families (7, 17, 18, 22, 23). 7 ese studies consistently depending on the data set. Within the Galeomorphii, (but weakly) reject the Hypnosqualea hypothesis, and the orders Lamniformes and Carcharhiniformes are instead suggest a basal divergence between sharks and generally recovered as closest relatives (7, 18, 23). In batoids. Within the batoids, skates (Rajiformes) appear the Squalimorphii, Squatiniformes (angel sharks), and basal, followed by electric rays (Torpediniformes), then Echinorhiniformes (bramble sharks) are close relatives, sawA shes and guitarA shes (Pristiformes, Rhinoba- while cow sharks (Hexanchiformes) are outside all other tiformes), with stingrays (including butterP y, eagle, and squalimorph orders (7, 17, 18, 22, 23, 25). At the family manta rays; Myliobatiformes) being the most derived level, the nominal groups Scyliorhinidae and Triakidae (7, 17, 21, 24). In these studies, most of the batoid orders are estimated to be paraphyletic (26, 27) while the pos- were represented by only one or a few families, but ition of the hammerhead sharks is seen to fall within there are numerous myliobatiform families. Analyses the Carcharhinidae. Accordingly, they are not con- including these families have not found signiA cantly sidered a distinct family herein (24). Carchariidae and supported relationships, although it appears that the Odontaspididae (oJ en considered a single family) form butterP y rays and manta/eagle rays (Gymnuridae and divergent branches in Lamniformes (7, 28). 7 e interfa- Myliobatidae) form a group (24). No studies have yet milial relationships of Squaliformes remain unexplored.

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Until now, no timing analyses have been performed taxa are not presented in the timetree. A total of 14 min- at or above the family level using molecular sequence imum (min.) and three maximum (max.) fossil con- data. Martin et al. (29) calculated the rate of evolution in straints used to calibrate the timetree were obtained from sharks for cytochrome b sequences, but did not use this the literature (7, 8, 10, 34). 7 ese include the divergence rate to infer times of divergence among diB erent fam- of from other Squaliformes (min. 89 ilies. Batoid divergence times have been calculated, but Ma); the divergence of Squatinidae and Echinorhinidae only within families (30, 31). However, divergence times (min. 151 Ma); the divergence of Hexanchidae and of higher chondrichthyan taxa have been inferred using Chlamydoselachidae (min. 176 Ma); the divergence of immunological distances (32). 7 ese data suggest a very Triakidae and Carcharhinidae (min. 89 Ma); the diver- old divergence between sharks and batoids (392 Ma), and gence of Scyliorhinidae and other Carcharhiniformes show divergences among sharks beginning 300 Ma. (min. 165 Ma); the divergence of Carchariidae and Because there is no study reporting molecular diver- Lamnidae (min. 100 Ma); the divergence of Parascyllidae gence times of chondrichthyan families, we report herein and other Orectolobiformes (min. 100 Ma); the diver- the results of an analysis using published sequence gence of Heterodontidae and other sharks (min. 176 Ma); data employing methodology described elsewhere (33). the divergence of Dasyatidae and Myliobatidae (min. Sequence data were obtained from the most comprehen- 100 Ma); the divergence of Rajidae and other batoids sive available studies, using the nuclear protein-coding (min. 176 Ma); the divergence of sharks and batoids RAG1 gene and the mitochondrial 12S and 16S rRNA (min. 190 Ma); the divergence of elasmobranchs and genes (7, 18, 26). Additional 12S and 16S sequences of holocephalans (min. 410 Ma, max. 495 Ma); the diver- 15 batoid families were included from GenBank, as gence of and amphibians (min. 340 Ma, max. only Rajidae and Urolophidae were included in the 370 Ma); and the divergence of actinopterygians and study of Douady et al. (18). Together these data encom- sarcopterygians (min. 435 Ma, max. 495 Ma). pass a patchwork of sequences for 53 of 55 families of Times of divergence obtained from the separate RAG1 Chondrichthyes, excluding only Zanobatidae (panrays) and 12S/16S analyses diB er markedly for most com- and Rhincodontidae (). We note that while parisons. Of the nodes shared between these two ana- 53 of 55 families are represented, relatively few families lyses, only the estimates for nodes within Batoidea and are represented by all three genes, as a consequence of Lamniformes, and among derived carcharhiniform fam- concatenating the data from three diB erent studies with ilies (Carcharhinidae, Hemigaleidae, Triakidae), show few overlapping taxa. In total, eight batoid families are noteworthy temporal concordance. In general the RAG1- represented only by 12S sequences, and 15 shark fam- based estimates are much older than those based on ilies by only RAG1 sequences, while 17 families include 12S/16S sequences (Table 1). In some cases, the discrep- all data and the remaining 13 families include data for ancy in age estimates is quite large. For example, RAG1 two genes. Tree topology was based on the studies that data result in times more than 100 million years older reported the sequences, although branches that are not than 12S and 16S data for divergences among the major resolved or conP ict among these and other published chondrichthyan groups (chimaeras, batoids, galeomorph molecular phylogenies were collapsed to polytomies for sharks, and squalimorph sharks). 7 is may be caused by the A nal timetree (Fig. 2). 7 ese polytomies mainly aB ect the large amount of branch length variation in the RAG1 Squaliformes and the batoid orders, as molecular stud- data set (7), while the 12S and 16S data have relatively less ies including squaliform families have very short, poorly variation (18). Time estimates from the combined ana- supported internal branches, and relationships within lysis, discussed later, are generally between values from batoid orders are similarly poorly supported (7, 17, 22, the individual analyses. Conclusions based on the com- 24). An analysis of batoid 12S sequences used in the bined analysis must be tempered by the knowledge that timetree did not A nd any signiA cantly supported rela- not all genes are present for all taxa (i.e., a large amount tionships within batoid orders (results not shown). of missing data) and the large diB erences in times of For the timetree, a combined analysis of all data deep branches obtained with RAG1 as compared to 12S was used. Analyses were also performed for the sep- and 16S data. arate RAG1 and 12S/16S data sets (Table 1). An amni- Notwithstanding the discrepancies in age esti- ote (Homo), amphibian (Xenopus), actinopterygian mates among genes, the timetree (Fig. 2) suggests that (Danio), cyclostome (Petromyzon), and echinoderm holocephalans and elasmobranchs diverged in the (Strongylocentrotus) were used as outgroups, but these Ordovician, 471 (494–434) Ma. Fossil evidence indicates

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that these subclasses had diverged by at least 410 Ma (8). been the early sites of diversiA cation within batoids and 7 e living families of Holocephali apparently diverged in inshore sharks. 7 e timetree (Fig. 2) is compatible with the Mesozoic (251–66 Ma). 7 e divergence of sharks and previous interpretations of shark evolution based on the batoids is inferred to have occurred in the Devonian, 393 fossil record, including a major radiation of neoselachian (431–354) Ma. 7 is date is more than 100 million years sharks in the Jurassic and Cretaceous (200–66 Ma), pos- older than the A rst appearance of neoselachian elasmo- sibly related to a parallel radiation of prey, actinoptery- branchs in the fossil record, and over 200 million years gian A shes (37). In order to better understand the factors older than unambiguous evidence of modern orders leading to diversiA cation in Chondrichthyes, additional (10). If these estimates are accurate, one must infer fossil (especially skeletal) and paleogeographic data a large ghost range in the fossil record for early diver- will be needed to complement the emerging molecu- gences within modern elasmobranchs. Times obtained lar phylogenetic data. In addition, more comprehensive with only 12S and 16S data are substantially younger, at molecular data, including nuclear gene loci that exhibit 357 (402–319) Ma, but still suggests a large ghost range. more uniform rates of evolution among lineages, are Our analyses of the presented molecular data suggest needed to resolve poorly known parts of the chondrich- that ordinal divergences were largely completed by the thyan tree and to estimate better-constrained times of beginning of the Triassic, 251 Ma (whether considering divergence. the combined, RAG1, or 12S/16S analyses) and that living families diverged throughout the Mesozoic, but espe- cially during the Cretaceous (146–66 Ma). With the pos- Acknowledgments sible exceptions of Ginglymostomatidae (nurse sharks) Support was provided by grants from the U.S. National and Stegostomatidae (), all elasmobranch Science Foundation (NSF) to G.J.P.N. and from NSF and families are estimated to have appeared by the end of the the National Aeronautics and Space Administration Cretaceous. (NASA Astrobiology Institute) to S.B.H. Because of these apparent ancient divergences, oceanic habits of chondrichthyans, and large diB erences in time estimates depending upon analysis used, it is di1 cult References to infer the biogeographic history of the living families. 1. L. J. V. Compagno, D. A. Didier, G. H. Burgess, inSharks, Most chondrichthyan families today are cosmopolitan Rays, and Chimaeras, the Status of the Chondrichthyan in distribution, or found in widely divergent (i.e., separ- , S. L. Fowler et al., Eds. (IUCN/SSC Shark Specialist ate ocean basins) areas of suitable habitat. For the many Group, Gland, 2005), pp. 4–11. families with pelagic or deep-sea distributions, it may 2. D. A. Didier, in Biology of Sharks and their Relatives, J. C. Carrier, J. A. Musick, M. R. Heithaus, Eds. (CRC Press, be impossible to infer biogeographic history due to the Boca Raton, 2004), pp. 115–138. worldwide of their habitats. Extensive plate tec- 3. S. Shirai, in Interrelationships of Fishes, M. L. J. Stiassny, tonic activity has contributed to substantial changes in L. R. Parenti, G. D. Johnson, Eds. (Academic Press, San ocean basins since the divergence of most families of Diego, 1996), pp. 9–34. Chondrichthyes. Although all ocean P oor is geologic- 4. M. R. de Carvalho, in Interrelationships of Fishes, ally young (Mesozoic and Cenozoic), oceans diB er in M. L. J. Stiassny, L. R. Parenti, G. D. Johnson, Eds. age when considered as bodies of water (aquatic habitat). (Academic Press, San Diego, 1996), pp. 35–62. For example, the Atlantic is relatively young (~150 Ma) 5. J. 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