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TITLE: DNA analysis of a large collection of shark fins from a US retail shop: species composition, 1 global extent of trade and conservation - a Technical Report from the Monterey Bay Aquarium 2
AUTHORS: Stephen R. Palumbi,a,1 Kristin M. Robinson, a Kyle S. Van Houtan,b,c Salvador J. 3 Jorgensenb 4
AFFILIATIONS: a Department of Biology, Hopkins Marine Station, Stanford University, Pacific 5 Grove, California 93950 USA; b Monterey Bay Aquarium, Monterey, California 93940 USA; c 6 Nicholas School of the Environment, 450 Research Drive, Durham, North Carolina 27708 USA. 7
1 Send correspondence to: [email protected], [email protected] 8
KEY WORDS: Shark finning, wildlife trafficking, IUU fishing, elasmobranchs 9
RUNNING HEAD: Shark fin forensics 10
WORD COUNT: 7,324 11
No. REFERENCES: 22 12
No. FIGURES: 3 13
No. TABLES: 3 14
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ABSTRACT 19
We identified shark fins sampled across the entirety of a shark fin shop that had operated on the west 20 coast of the United States until 2014. From these specimens we obtained 963 species identifications 21 with Cytochrome oxidase (COI) sequencing and 1,720 identifications with control region (CR) 22 sequences. We found 36-39 distinct species with COI and 38-41 with CR. Of the species identified, 23 16-23 are currently listed as Endangered or Vulnerable on the IUCN Red List, an additional 2 are 24 considered data deficient, and 7 currently listed under CITES Appendix II. Of the 2.5 tonnes of fins 25 from this collection, we estimated 56-66% (CR or COI, respectively) come from CITES-listed species 26 or those the IUCN considers threatened or data deficient. Most of these species occur outside of the 27 United States EEZ, comprising a global set of species that is common in most fin surveys. The 28 principal target shark fishery in the United States (spiny dogfish; Squalus acanthias) has no fins in our 29 collection. Fins seen abundantly in our collection include pelagic species such as thresher, mako, 30 oceanic whitetip, silky, blue and hammerhead sharks, as in previous samples of the shark fin supply 31 chain. However, in addition, we see a large flood of blacktip, dusky, sandbar, and smalltail sharks that 32 are common in shallow coastal waters. This may indicate that the global market for shark fins takes 33 sharks from nearshore coastal zones, all over the world. Abundant species in the fin shop included 34 globally-distributed species such as scalloped hammerheads and shortfin mako sharks, but also 35 regionally-restricted species such as finetooth, blacknose, and Caribbean Reef sharks found only in the 36 western Atlantic or Caribbean. Specimens identified from rare species of particular conservation 37 concern included the wedgefish genus Rhyncobatus and the white shark. Both molecular markers 38 performed well in identifying most fins, achieving a similar degree of taxonomic certainty. The 39 universal primers for COI regularly amplified bacteria in wet fin samples, but the CR primers were 40 able to return shark sequences even from these degraded samples. However, the CR primers amplified 41 a second gene, likely a pseudogene, in some important and abundant species, and seriously 42 underestimated some species of high conversation concern such as the thresher sharks. 43
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INTRODUCTION 44
Shark fins comprise a lucrative, extensive global market that leads to the death of 70-100 million 45 sharks a year (Worm et al., 2013), largely for the use of fin collagen (ceratotrichia) in shark fin soup. 46 A recent study estimates that the majority of shark fin harvests are unsustainable, illegal, and that the 47 volume traded has dramatically increased over the last decade (Sadovy de Mitcheson et al., 2018). 48 Extensive capture of ocean-going sharks in long-line and net fisheries has led to the global collapse of 49 many shark species (Baum et al., 2003; Nicholas K. Dulvy et al., 2008). However, the extent of the 50 shark fin trade suggests that many other species are being similarly affected (Fields et al., 2018; 51 Steinke et al., 2017). Recent assessments furthermore indicate some coastal shark populations have 52 declined nearly 90% in the last 50 years (Martin et al., 2016). Efforts to monitor impacts from trade 53 have been impeded, in part, by the extensive processing of fin products. Though some fins are traded 54 with skin on, and with many morphological features intact, many are traded with most features 55 removed, defying easy morphological-based cataloging. 56
Molecular tools have been used extensively to discover the identity of shark fin products in 57 trade, particularly by testing fins in large wholesale markets (Clarke, Magnussen, Abercrombie, 58 McAllister, & Shivji, 2006). Such tests have shown the widespread occurrence of ocean going sharks 59 such as blue sharks, oceanic white tip sharks, thresher sharks, hammerhead sharks and mako sharks. 60 But coastal species have increasingly been observed. Recently, effort has shifted to tests of retail 61 outlets that likely integrate supply chains over months or years (Cardeñosa et al., 2018; Feitosa et al., 62 2018; Fields et al., 2018). For example, Fields et al. (2018) surveyed 92 retail markets in Hong Kong 63 in 2014-2015 and processed 3,800 samples with a small piece of the COI gene, identifying them to the 64 species level. They found 59 species and 17 other groups that could not be well identified. Cardeñosa 65 et al. (2018) extended this survey to a total of 9,200 samples between 2014-2016 with 80% 66 identification rate totaling 82 species or complexes. Feitosa et al. (2018) surveyed several retail fish 67 markets in northern Brazil from 2014-2016, and from government inspections obtained in 2007, 68 identifying 17 mostly regional and coastally-distributed species from 427 fins. In other cases, reliance 69 on relatively small data sets [n =72 in (Steinke et al., 2017)] may not show the complete spectrum of 70 commercial species. Another issue is that short DNA sequences can sometimes fail to differentiate 71 closely related species. The balance between large sample numbers and a gene region sufficient to 72 determine species identity has been difficult to achieve. Another opportunity is to compare retail 73 outlets in Asia – especially at the heart of the fin trade in Hong Kong – with retail outlets in other parts 74 of the world that have different local shark fisheries and consumer demand. 75
Here we test 1,720 fins collected from a retail outlet on the west coast of the US that was 76 shuttered after shark fin sales were banned. We use sequences of the mitochondrial control region 77 (Giles, Riginos, Naylor, & Ovenden, 2016), compared to published data sources, to estimate the 78 identity of fins on the basis of sequence similarity and phylogenetic placement. For a subset of 961 79 fins, we also sequenced a region of the COI gene, giving us a comparative data set to test the ability of 80 these two gene regions to deliver accurate identifications. Both data sets gave very similar results, 81 showing the existence of up to 41 species in this retail collection. Detailed comparisons suggest that in 82 some species some putative control region sequences are likely to be nuclear pseudogenes. In other 83 samples, bacterial contamination renders COI amplification impossible but CR data appear robust. 84
85
METHODS 86
Sample collection 87
These data are free and open to the public, and were collected from fins provided by Jenny Giles in a 88 collaborative research program involving Dr. Giles, Steve Palumbi, and Sal Jorgenson focused on 89 genetic identification of shark market products at the Monterey Bay Aquarium and Stanford 90
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University (Giles et al. submitted). The samples were derived from a larger collection of fins with a 91 range of physical conditions. Some fins occurred in a dried state, with skin attached (DR). Other dried 92 fins had their skin removed (DRR). Some fins were more processed –wet ceratotrichia from multiple 93 fins were pressed together in sheets (WC). Samples from disparate parts of each of these sheets were 94 punched out and individual ceratotrichia were processed. Representative fins from each separate box 95 or container were collected. 96
We used the IUCN Red List and CITES determinations to classify the conservation status of 97 the identified species. As per previous studies, we consider species listed as data deficient to be 98 threatened, as a central reason for being data poor is low population abundance, and most often when 99 data deficient species are eventually classified they become threatened (N K Dulvy et al., 2014; 100 Jenkins & Van Houtan, 2016). 101
DNA sequencing and alignment 102
DNA extractions were performed using NucleoSpin® Spin Columns (Macherey-Nagel). DNA was 103 amplified and sequenced using standard published methods. For COI amplifications, we used modified 104 Folmer COI primers [FishF1, FishF2, FishR1, FishR2 from (Ward, Zemlak, Innes, Last, & Hebert, 105 2005)], amplified with an extension temperature of 54°C, extension of 72°C, and denaturing of 94°C 106 for 60 seconds each. For the putative control region, 374-521 bp was amplified using the primers GwF 107 (5’-CTGCCCTTGGCTCCCAAAGC-3 )́ (Pardini et al., 2001) and 470r2 (5’-108 GCCATTAAAGGGAACTAGRGGA-3 )́, published in Giles et al. (2016). 109
Amplicons were treated with 0.75 units Exonuclease I and 1 unit Shrimp Alkaline Phosphatase (New 110 England Biolabs) per 8 microlitre of template, and were sequenced in one direction using the forward 111 PCR primer by Elim Biopharmaceuticals. Sequence data were aligned and ambiguities resolved 112 manually using CodonCodeAligner ver. 7.1.2 (CodonCode Corporation, Dedham, MA). Data sets of 113 cleaned sequences are in Appendix 1 (Master COI data file) and Appendix 2 (Master CR data file). 114
Constructing COI data base 115
All data used in analyses were derived from public data bases. We used the 1035 sequences of the COI 116 data base of Wong, Shivji, and Hanner (2009) to extract and download one or two individual COI 117 sequences from each of 75 shark species. We were unable to find a COI sequence of the large tooth 118 sawfish Pristis microdon, which appears in our Control Region data set (see below), although Pristis 119 zijsron is available (accession EU398989.1). Likewise, two recently described mitochondrial lineages 120 of the wedgefish genus Rhyncobatus (Giles et al., 2016) and the scoophead hammerhead Sphyra media 121 are available from control region sequences but not COI. Our final reference COI collection consists 122 of 177 sequences (sequences appended to Master COI data file, appendix 1). 123
Constructing the CR database 124
All data used in analyses were derived from public databases. We found 2876 sequences from 125 Genbank with mitochondrial control region sequences from Elasmobranchs (download Dec. 2017), 126 including 363 full mitochondrial genomes. From this set we chose one or two sequences from each 127 species. Because these were of variable length, we trimmed each sequence to the length between our 128 amplification primers (Giles et al., 2016). In addition, we collected representative control region 129 sequences from one representative product sample of each of the species that we found in our 130 Cytochrome oxidase survey. In total our reference data base has 122 sequences from 79 species 131 (sequences appended to Master CR data file, appendix 2). 132
BLAST searches 133
We compared all of our market COI sequences and CR sequences to the full NCBI BLAST data base 134 (in Jan 2018), and recorded the closest species match for each sample. Those species matches were 135
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added to the sequence sample name in FASTA format for ease in comparing phylogenetic and 136 sequence distance results. (see appendix 1 and 2) 137
Comparing COI sequences phylogenetically 138
We added 961 COI sequences from individual fin or fin products to the 177 sequences reference set 139 and aligned them using the MAFFT server (Katoh & Standley, 2013). We aligned sequences with 140 default conditions and created a Neighbor-joining phylogenetic tree using Jukes-Cantor sequence 141 evolutionary parameters with bootstrap branch reliability scores. We inspected the resulting tree for 142 clades containing conspecific sequences from Genbank and that contained market sequences 143 determined to be closest to those same species by BLAST. We thus combine a phylogenetic clade-144 based criterion with a sequence-distance BLAST criterion for assignment of COI sequences to species. 145 For crowded parts of the tree, particularly the genus Carcharhinus, we excluded all other sequences 146 and re-constructed the tree. 147
Comparing CR sequences phylogenetically 148
As a first step, we aligned all 1893 sequences plus 122 references using the MAFFT server. Because 149 control region sequences evolve so quickly, there were no conserved bases in the alignment on which 150 to build a well resolved tree. As a result, we constructed a UPGMA tree in MAFFT based on overall 151 genetic distances. This analysis identified four major clades, allowing us to split the data set. The first 152 clade included the lamnid sharks, and contained 423 sequences, including 346 sequences that 153 subsequently were determined to be pseudogenes. The Carcharhinus sharks consisted of 1044 154 sequences. The genus Spyrna contained 234 sequences, and finally, other Carchariniform sharks 155 consisted of 187 sequences. We re-aligned the sequences within these groups and rebuilt neighbor-156 joining trees with bootstrap support. As in the analysis of the COI data set, we compared the 157 sequences within defined clades on these phylogenetic trees to their closest BLAST match in our 158 reference database. We also cross referenced the closest BLAST match of the COI sequence from the 159 same fin in 816 cases for which we have both data sets. 160
Assigning names to sequences 161
We determined species names three ways. First, we determined the best match between each of our 162 control region sequences to available databases. Second, we determined the best match of our COI 163 sequences to these databases. Third, we examined the relationship among sequences in our collection 164 and public reference sequences phylogenetically, looking for clusters of sequences that form species 165 groups. Those species groups were defined by diagnostic bases, by statistical reliability of branches 166 (bootstrap percentages), or by simple clustering. The strongest species names were defined by high 167 confidence identification (>97% match for CR and >99% for COI) for both genes and high confidence 168 phylogenetic clustering. For some fins we only had one DNA sequence, and so we relied on high % 169 match for that sequence and phylogenetic clustering. 170
171
RESULTS 172
Below, we detail the results of the dual analyses on COI and control region sequences. Each set of 173 results steps through a set of phylogenetic trees that show the relationship of each sequence we 174 collected to a reference set of sequences from public databases. The large format, full resolution trees 175 are included as figures. 176
COI sequences 177
In total we identified 963 fins as coming from 36-41 species. The uncertainty in species numbers is 178 because certain pairs of species are difficult to distinguish with COI data and some species have 179 multiple clades. Table 1 presents the summary results from COI and the control region. Also shown in 180 this table are the sample sizes for each region, and the phylogenetic criteria used to assign species 181
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names to samples. The COI tree that we used is in a high definition pdf file in Figure 1A (all COI tree 182 w/ bootstraps). This figure can be expanded to examine any portion of the large, complex tree. 183
A taxonomic breakdown of the COI results shows that no market fins were derived from 184 dogfish (Squalus), catfish (Apristurus), carpet sharks (Nebrius), or Angel sharks (Squatina). Marketing 185 of dogfish fins is less likely because of their small size. However, dogfish make up the biggest shark 186 fishery in the U.S. and there have been calls for their fins to be exempted from state and national shark 187 fin bans. 188
Lamniform sharks 189
The lamnid market samples contain all three species of thresher sharks (Alopias), two species of mako 190 (Isurus), and the salmon shark (Lamna ditrops). COI clades have high bootstrap support (97%-99%) 191 across these species, except for A. superciliosus, the bigeye thresher, with bootstrap support of 55% 192 (Suppl. Fig 1A “all COI tree w bootstraps”). This species has the highest number of samples in our 193 COI data base (n=170), closely followed by Isurus onchyrhyncus, the shortfin mako shark (n=168). 194 DCA1-0004, which has a White Shark control region sequence is not in the COI data set. 195
Carcharhinoform sharks 196
Genus Carcharhinus. The largest number of congeneric species is in the genus Carcharhinus and is 197 reflected in the large number of market samples that cluster within this genus phylogenetically. Close 198 genetic ties among these species makes some identifications with COI difficult. However, there were a 199 number of cases where species formed well-supported clades in the bootstrap tree (Fig. 1B: 200 Carcharhinus COI tree w bootstraps). The Caribbean reef shark (C. perezii) is a common shark in the 201 Caribbean, and is represented here by a single COI sample in a clade defined by an 85% bootstrap. 202 Likewise, six sequences of C. leucas (bull shark) are defined by a 61% bootstrap value. This 203 Carcharhinus COI tree includes 14 other species clades with 41-93% bootstrap values and a total of 204 124 sequences (Table 1). 205
However, many other species of Carcharhinus are not well distinguishable by bootstrap 206 phylogenetic trees because they differ by few substitutions (Wong et al., 2009). In some cases, there 207 are diagnostic nucleotide substitutions that link sequences to certain species [(Wong et al., 2009), 208 Table 3]. For example, our bootstrap tree shows many market samples in a large undifferentiated set 209 representing reference sequences for C. falciformis, isodon, galapagensis and obscurus. Yet, C. 210 falciformis and C. isodon each have two diagnostic bases in the COI region, and C. galapagensis can 211 be distinguished from C. obscurus at two others. We used these diagnostic SNPs (listed in our Table 212 1) to provide species names and could then compare these names to the clades in the phylogenetic 213 analysis. As a result, a UPGMA tree shows a C. falciformis clade that corresponds largely to the 59 214 sequences that contain the C. falciformis diagnostic SNPs. Likewise, a C. isodon clade in the UPGMA 215 tree corresponds to the 15 sequences that show the diagnostic C. isodon SNPs. Diagnostic SNPs in 216 COI do not appear to exist to distinguish C. galapagensis and C. obscurus (Wong et al., 2009). 217 However, two SNPs define the COI clade that contains these two species and in our COI data set, we 218 observe 59 sequences. Another problematic species mixture is the sandbar and bignose sharks, C. 219 plumbeus and C. altimus. These cannot be distinguished by COI sequence alone and make up 17 220 sequences in our COI data base. For C. acronotus, we find two distinct sequence clades that BLAST to 221 this species at 96% or 100% identity (n=3, n=9, respectively). Whether the three sequences with lower 222 identity in a separate clade represent a different species will require further research. The widespread 223 blacktip reef shark (Carcharhinus limbatus) forms a UPGMA clade with 97 sequences. Less widely 224 distributed is the smalltail shark (C. porosus), found from the Gulf of Mexico to northern Brazil. 225 Despite its small size and restricted range, we found 33 sequences. 226
Hammerhead sharks 227
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The hammerhead clade within the Carcharhinoformes is represented in our data set by six of the eight 228 named species. The local endemic Sphyrna gilberti (Quattro, Driggers III, Grady, Ulrich, & MA, 229 2013) is missing, possibly because there is no recorded COI sequence. S. zygaena is also missing from 230 our COI data, although this species occurs in the CR data set. S. lewini occurs in three separate clades. 231 Clade I, with ten sequences of Sphyrna lewini appears outside the main Sphyrna clade in the bootstrap 232 phylogeny. This group contains sequences only 96% identical to a second clade of S. lewini that 233 occurs more deeply imbedded in the Sphyrna clade. These two intraspecific clades have the same COI 234 amino acid sequence and differ at only silent sites. This group is also 100% identical to a number of S. 235 lewini sequences on Genbank. The second lewini clade has the most hammerhead sequences in our 236 sample (n=56) and also has several voucher reference sequences on Genbank with 100% identity. 237 These two clades may represent different species, but we will count them together in our data 238 summary. 239
The third S. lewini clade has no Genbank or BOLD reference sequences. Our sequences that 240 fall into this clade have 11 CR sequences that BLAST to S. corona rather than to S. lewini. As a result, 241 this third clade, is probably S. corona. 242
Other Carcharhiniform sharks 243
Within the family Carcharhinidae, but outside the genus Carcharhinus, several genera have defined 244 clades and are found in our collection. These include the tiger shark (Galeocerdo cuvier, n=6), and 245 two species of lemon sharks (Negaprion, n=6). Rhizopriodon species (sharpnose sharks) are extremely 246 similar in their COI sequences and our phylogenetic approach cannot distinguish R. porosus from 247 terraenovae for these 27 sequences. By contrast, R. lalandii and R. acutus appear to have slightly 248 different COI sequences but do not appear in the COI data set. 249
Outside the family Carcharhinidae, there are market samples from a number of Carchariniform 250 sharks in different families. The school shark, Galeorhinus galeus occurs in a small clade of eight 251 samples. Batch BLAST searches originally identified our G. galeus sequences as coming from C. 252 dussumieri or C. obscurus. However, a manual recheck shows 99-100% identity with the Wong et al. 253 (2009) sequences of G. galeus. Two market sequences were included in the clade that included the 254 genus Mustelus. A manual BLAST shows this sample to be 100% identical to M. lunulatus. The other 255 sequence was named by BLAST as M. canis, and is 100% identical to other M. canis in Genbank. 256
Poor sequence reads 257
In addition to these 969 full length, high quality sequences, we obtained 149 sequences with poorer 258 read quality or shorter length. Phylogenetic analysis of these sequences using the same Genbank 259 reference libraries reveals a similar number and distribution of species as the higher quality sequences. 260 In particular, no species were seen in this set that had strong placement in species clades not included 261 in the previous analyses. Because these phylogenetic placements were in general more equivocal than 262 for the high quality sequence, we do not include them in our data summary. In addition, we produced 263 287 COI sequence reads that were such poor quality that they had lengths under 300 bp (n=144) or 264 between 300 and 500 bp (n=143). These sequences were not analyzed further. 265
Bacterial amplification of shark products 266
The final category of COI sequences is a set of 369 amplification products from fin samples that 267 BLAST to bacteria. Of these 244 are identified as Pseudomonas fluoresens, P. sp. or P. veronii (n=62, 268 174, 8 respectively). The rest are identified as generic bacteria, or in the genera Kangiella, 269 Oceanimonas, Ensifer, or Vibrio. Poor sequence quality reduced BLAST confidence in 97 sequences. 270 Most of these bacterial sequences (311 out of 369) are derived from wet ceratotrichia packaged to 271 allow rapid use in restaurants. 272
273
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CR Sequences 274
BLAST searches of our CR sequences on Genbank find a >95% match to publicly available data for 275 1,528 of our sequences. Embedded in that number are 1,496 sequences with a >97% match. Left 276 behind are 346 without a reputable >95% match. The largest part of that group is a set of sequences 277 that show a maximum of 77-80% match to any control region sequence in the publicly available 278 control region data for sharks. Below we suggest that these are pseudogenes and conduct a separate 279 analysis to ascertain their value in fin identification. 280
For each clade in each of the phylogenetic trees (see methods), we counted the number of fin 281 CR sequences for which there was the same closest species match for CR and COI (CR=COI), the 282 number for which the two sequences did not match (CR<>COI), the number of samples for which we 283 did not have COI sequence (No COI), and the number of reference sequences from the database. In 284 total, we counted 1888 CR sequences, of which 496 matched the COI sequence, 320 did not match, 285 and 1072 had no COI sequence. The breakdown of these sequence matches by species is in Table 2. 286
Genera outside major clades 287
There are no sequences in our CR data set from the dogfish Squalus, or any sequences in this family, a 288 conclusion that matches our COI data set. In the wedgefish genus Rhyncobatus, we find four species 289 with high bootstrap support (n=6,4,1,1 respectively). This genus is undergoing taxonomic revision 290 (e.g. Giles et al. 2016) and the names of two of these species are not yet determined. The two fins that 291 are identified in the genus Mustelus in the COI data set were not sequenced as part of the CR data set, 292 and this genus does not appear in any other sample. 293
Carcharhiniformes 294
The large number of insertions and deletions in the CR data set interferes with bootstrap analysis 295 because there are few conserved sequence positions that can be included. However, a bootstrap tree 296 shows distinct clades including sequences identified by Genbank samples as the blue shark Prionace 297 glauca (bootstrap 100%, n=72), Rhizoprionodon porosus (bootstrap 89%, n=25), Negaprion acutidens 298 and N. brevirostris (bootstrap 49%, N=5,54, resp.), Galeocerdo cuvier (bootstrap 100%, n=15), and 299 Triaenodon obesus (bootstrap 100%, n=3). (See Fig 2. “Other genera CR tree”). 300
In addition, there are a large number of sequences that cluster in the genus Carcharhinus. To 301 improve tree resolution, these were grouped separately into a separate sequence file trimmed to 475 302 bases to match reference sequences, and run in MAFFT to produce a large UPGMA tree (Fig. 3 303 Carcharhinus CR tree). This improved tree still shows poor bootstrap resolution among most 304 Carcharhinus CR sequences. Nevertheless, within this tree, a series of clades defines a large number 305 of species and sequences. We assign a species name to fin sequences based on their inclusion in 306 distinct sequence clades named by reference samples from Genbank. Further confidence in these 307 clades and assignments comes from evaluating these assignments based on whether the CR 308 identification matches the COI identification. In a few cases, no Genbank sequence exists, and we 309 assign clade names based on COI assignments from the same fins. The following summarizes these 310 results from the bottom to the top of the tree. 311
C. porosus, the blacktip shark, occurs in several large clades of similar sequences (ca. 99% 312 identical, n =107 total). C. limbatus is the most abundant species and occurs in two major clades (n 313 =132, 127 respectively). Two representative sequences from those two clades DCA1_0172 and 314 DCA1_0173 are 98.6% identical, differing at 4 transitions and 2 transversions. By contrast, C. isodon 315 has one small clade of sequences (n=28), highly similar to control regions from whole mitochondrial 316 genomes for this species. A group of 19 sequences cluster together but show highest BLAST hits in 317 the 96-97% identity range for a variety of Carcharhinus species. The COI sequences of five of these 318 also show similarity to a large number of different species, never the same as the best CR BLAST hit. 319 It is not possible to determine what species these 19 sequences derive from these data. 320
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For COI, C. plumbeus and C. altimus form a group that cannot be easily distinguished. 321 Although there are CR sequences for C. plumbeus in public data bases, there are currently no C. 322 altimus CR sequences. In our CR data set, C. plumbeus sequences make up a large clade (n=76). Two 323 of the sequences form a clade within this clade and have high affinity to COI C. altimus data (100%) 324 and lower affinity to C. plumbeus CR data (98-99%). Whether these two sequences represent C. 325 altimus (and the others represent C. plumbeus) will demand a series of positively identified individuals 326 sequenced for the control region. 327
A single sequence of C. brachyurus occurs in our data set, clusters well with the reference 328 sequence and has a COI sequence highly similar (100%) to C. brachyurus. In this clade is also a 329 subclade of C. brevipinna with 22 sequences. A large clade of sequences of C. obscurus occurs in 330 three subclades. Subclade 1 has four sequences with high similarity to the reference C. obscurus whole 331 mt genome. A second, large clade shows 98-99%% similarity to the first clade, with 109 sequences. A 332 third clade is a mixture of sequences with highest affinity to C. obscurus (n=16) or C. perezii (n=8). 333 One sequence in this third clade is 99% identical to C. perezii: this same fin has a 99% COI identity to 334 C. perezii. Whether this clade of 24 sequences actually represents C. perezii might require further 335 sampling. The species C. longimanus shows a single clade with 90 sequences, whereas C. 336 melanopterus occurs in a clade of 8. A clade of C. acronotus has 64 sequences, and C. leucas appears 337 with 18. The second most abundant species is C. falciformus (n=179) which occurs in a single clade in 338 our data set. 339
Last, there is a clade of 34 sequences that show no more than 94-96% identity to the closest 340 control region sequences in Genbank. Of the 12 fins with matching COI sequence, there is 100% 341 identity to C. amblyrhyncos in nine of them. (The three other fins have Alopias COI sequences.) There 342 is no C. amblyrhynchos CR sequence on Genbank, but we provisionally ascribe these 23 sequences to 343 C. amblyrhynchos based on their match to COI. 344
Hammerhead clade 345
The hammerhead group is represented by 234 sequences from the same species and clades as the COI 346 data set with the addition of four sequences from Sphyrna zygaena. Unlike the Carcharinids, bootstrap 347 values for hammerhead species assignments were high – ranging from 70-100% (Table 1). As in the 348 COI data set, there were two separate clades of control region sequences in S. lewini and a separate 349 clade for S. corona. There were 38 sequences of S. mokarran, two of which appeared in a related but 350 3-4% divergent clade. (Fig 4: Sphyrna CR tree). 351
Pseudogene sequences in Lamnid sharks 352
Our phylogenetic data and BLAST searches for the CR sequences show a virtual absence of Isurus or 353 A. pelagicus, despite the large occurrence of these taxa in the COI data set. Many CR sequences from 354 fins identified with COI in Isurus and Alopias are a poor match to vouchered CR sequences. For 355 example, sample DCA1-0745 has an Alopias pelagicus COI sequence (100% identical to 356 JN315429.1), but its CR sequence is only 75% identical to the control region sequence from the A. 357 pelagicus mtDNA genome sequence on Genbank (NC_022822.1). The closest match to the CR 358 sequence of DCA1-0745 is to a Lamnid shark in the genus Megachasma, at 77% identity. Overall, we 359 have 299 sequences that BLAST best to this genus at 77-81% identity. 360
To investigate this further, we generated a phylogenetic tree from control region sequences of 361 Lamnid species from Genbank including Isurus and Alopias (Fig. 5). Genbank sequences from full 362 mitochondrial genomes group together in this clade, along with sequences from other lamnid sharks 363 including two Isurus species, A. pelagicus and a large number of our market sequences from A. 364 superciliosus. (red labels in Figure 5). However, most of our market sample CR sequences from 365 lamnid sharks form a clade separate from the clade defined by vouchered whole mitochondrial 366 genomes. (upper, black labelled samples in Fig. 5). The other clade differs by about 20-24% and has 367
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no voucher sequences from full mitochondrial genomes. Instead it has exclusively sequences we 368 generated with our CR primers from market samples. These include most of our market sequences 369 from I. onchyrhyncus, I. paucus, and Alopias pelagicus samples. 370
One overall explanation for these data is that our control region primers typically amplify a 371 different, but related, gene region in Isurus and most Alopias sharks. Because there are no duplicate 372 control region sequences in the Alopias full mt genome, this duplicate, related gene region is likely to 373 be a mitochondrial pseudogene (e.g., Bensasson, Zhang, Hartl, & Hewitt, 2001). 374
Species differences show lower divergence among pseudogenes 375
The clade of sequences from validated mitochondrial genomes differ between species more than do 376 our amplified fragments from the other clade. For example, nucleotide divergence of I. paucus and I. 377 oxyrhincus is 8% for Genbank mitochondrial CR sequences: transversions outnumber transitions 19 to 378 12. Between the I. paucus and I. oxyrhinucs sequences we amplified in the other clade, we find only 379 1.5% divergence (4 transitions and 3 transversions) along with 18 insertion/deletions. High divergence 380 in the validated mitochondrial clade is expected given the generally higher rate of molecular evolution 381 in mtDNA (Avise, 2012). By comparison, COI sequences from these same two I. paucus and I. 382 oxyrhinucs individuals differed at 12% of 631 sites, including 58 transitions and 17 transversions, 383 suggesting that the lower sequence clade in Figure 6 is evolving much like other mtDNA genes. 384
True Lamnid mtDNA CR sequences in some species 385
The genus Isurus comprises a sizeable fraction of our COI data set, but there are only three sequences 386 from our CR data that BLAST highly and cluster phylogenetically to the available Isurus CR 387 sequences. Likewise, Alopias pelagicus is common in our COI data set but absent in the CR data set 388 despite a reference control region sequence from the complete mitochondrial genome of this species. 389 By contrast, we have 72 sequences of Alopias superciliosus that form a good clade with the control 390 region sequence from the mitochondrial genome of this species (lower clade in Figure 6). In addition 391 there are sequences from I. oxyrhincus (n =1), and I. paucus (n=2) in the clade of true CR sequences. 392
Two genes amplify from CR primers in some species 393
Multiple sequence products from individual fins can complicate identification. In our case, we 394 sometimes find sequences from different individuals of the same species in different clades: for 395 example, sequences from two I. oxyrhincus individuals identified as conspecifics by COI sequence 396 appear in different CR clades and differ by 21%. Likewise, phylogenetic trees of Alopias superciliosus 397 CR sequences from our fin sample suggest a mixture of valid control region sequences and pseudo-CR 398 data (Fig. 6, versus Fig. 7). Altogether, the phylogenetic tree shows 72 sequences of A. superciliosus 399 CR and 11 pseudoCR. The other two species, A. vulpinus and A. pelagicus have 1 and 7 pseudoCR 400 sequences, respectively. By contrast, Isurus oxyrhincus shows a large number of pseudoCR sequences 401 (296) and perhaps one true CR. The species I. paucus also is dominated by pseudoCR sequences 402 (n=9), with two valid CR. 403
Using pseudogenes in fin identifications 404
We can still use these pseudo-CR sequences in fin identification. First, we find fins that have been 405 identified as Isurus or Aolpias species by their COI sequences. Then we use the CR sequences from 406 these as references to identify species-specific clades of pseudo-CR sequences from other fins. 407 Effectively, this uses the COI identifications as a reference set of fins from which we derive species-408 specific pseudo-CR data sets. This assignment identifies 305 sequences from I. oxyrhincus, 9 from I. 409 paucus, 14 from A. superciliosus, and 8 from A. pelagicus (Fig. 7). These pseudogene numbers are in 410 addition to the numbers of valid CR sequences: I. oxyrhincus =1, I. paucus =2, A. superciliosus =72, 411 and A. pelagicus =0. However, an analysis of both data sets, (Fig. 8 see below), suggests caution in 412
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using CR sequences because species with these pseudogenes are seen in many fewer fins than 413 suggested by the COI data set. 414
Good CR amplifications for bacterial-laden samples 415
In our COI data set, 369 samples provided bacterial sequences. Of these, 284 amplified with our CR 416 primers, and 236 provided good CR sequence, demonstrating that these samples retained shark 417 mtDNA despite bacterial contamination. Most of these samples were from wet ceratotrichia 418 collections that had been stored at room temperature for weeks to months before processing. This 419 category of specimen is rare in shark fin samples. The species composition was similar to the 420 composition from the rest of the CR data set. Six samples BLASTed to Megachasma pelagios at low 421 similarity (80%), suggesting these were Lamnid sequences. Forty-eight sequences amplified the CR 422 region but did not return good sequence. 423
Comparison of CR and COI identities 424
In our data set of 1528 CR sequences with strong matches to Genbank, we also have COI data for 802. 425 Of these, 669 show a match between the species identities derived from the two different genes. 426 However, 133 show a high (>95%) match to a reference control region sequence but show a different 427 species match (also at high % identity) for COI. This mismatch calls into question these sequence 428 identifications. To resolve this, we re-sequenced a set of these mismatched samples for the 429 mitochondrial 16S gene or cytochrome b and found that the 16S species identity matches the COI 430 identity in about half the cases, and matches the CR identity in the other half. There are ten cases in 431 which a third species is discovered this way. As a result of the uncertainty that this causes in species 432 identifications, we have removed these sequences from our compilations. 433
Summary across all analyses 434
Table 2 compiles the species names derived from the CR data set, including cases where CR and COI 435 labels match, when they do not match, and when we do not have COI data. We then show the species 436 totals in Table 1, not including the cases where CR and COI sequences have high identity but do not 437 match. 438
Overall, we can identify 969 fin products by COI sequence as belonging to 38-41 species, 439 including 16-18 species of Carcharinus. We also identified 1,736 fins using control region sequences, 440 showing 41-43 species, including the vast majority of the species from the COI data set. Table 1 441 shows that the most common species are thresher sharks, mako sharks, hammerhead and blue sharks, 442 ocean species that have been seen widely in prior surveys of shark fin markets (e.g., Clarke et al., 443 2006). However, we also see a large number of samples and species of coastal requiem sharks in the 444 genus Carcharhinus, as well as a diverse collection of hammerheads in seven of eight named species. 445 The species targeted by the single biggest US shark fishery, spiny dogfish, does not appear among any 446 of our fin products. 447
The species list in our shop data sets (summarized in Table 1) include 14-20 vulnerable 448 species (IUCN Red list) and 3 endangered species. Six additional species the IUCN considers data 449 deficient, and 6 species are specifically regulated under CITES. Altogether, the vulnerable, 450 endangered and CITES species make up 36% of the species and 56% (CR) to 66% (COI) of the 451 individual fin products. Of the CITES listed species, only the whale shark, basking shark and 452 porbeagle (Lamna nasus) are not in our DNA sequence collection. 453
The Lamnid shark group and the hammerhead group have high fractions of vulnerable, 454 endangered or CITEs regulated species, and both have high frequency in our sample. Likewise, seven 455 of eight named hammerhead species are in our data set, including all five vulnerable, endangered or 456 CITES regulated species. Only the newly described endemic S. gilbert is not in our data set. 457
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Yet our data also show a wide variety of sharks that have not yet caught conservation 458 attention, including a number of Carcharhinus species. We see 16-18 species of Carcharhinus sharks 459 with an average number of individuals per species of 21 and 48 for COI and CR, respectively. These 460 include widely ranging sharks such as the blacktip (C. limbatus), sandbar (C. plumbeus) and dusky 461 sharks (C. obscurus). But we also see large numbers of more restricted species such as the shorttail 462 shark (C. porosus) which lives in muddy estuaries in the western Atlantic, the blacknose (C. 463 acronotus), inhabiting sandy habitats in the same regions, and the sharpnosed sharks (genus 464 Rhizopionodon) found in Atlantic or Caribbean waters. Coastal sharks such as these are in contrast to 465 the oceanic, pelagic sharks that have been the focus of a large shark fin fishery and large shark fin 466 concern. Our data confirm that the diversity of coastal sharks is also a target of active shark finning. 467
468
DISCUSSION 469
Our data show a large variety of sharks with great taxonomic diversity across the retail market sample. 470 The COI data set provides identification of 36-39 species of sharks, including 17-19 Carcharhinus 471 species, from 963 fin products. Likewise, the Control Region data set shows 38-41 species, including 472 the vast majority of the species from the COI data set. 473
These species represent a large fraction of the known endangered, vulnerable or data deficient 474 sharks in the world: more than 20 species in those categories occur in our data set. Moreover, 56-66% 475 of the fins in our data set derive from these categories of sharks, largely because of the preponderance 476 of thresher, mako and hammerhead sharks in the sample. 477
Our data bolster several recent retail market surveys that have also concluded that the shark fin 478 market is highly diverse and highly endangered (Cardeñosa et al., 2018; Feitosa et al., 2018; Fields et 479 al., 2018; Steinke et al., 2017). Steinke et al. (2017) found 20 species in 72 shark samples from 480 Vancouver, Canada. Fields et al. (2018) found 59 species and 17 higher taxonomic groups when they 481 monitored 3,952 samples from Hong Kong retail shops from 2014-2015. Similarly, Cardeñosa et al. 482 (2018) found 82 species and species complexes in Hong Kong among small fin discards in 2016. 483 Feitosa et al. (2018) found 17 predominantly nearshore species from 427 fin samples collected in 484 northeastern Brazil. In these cases, and the samples reported here, some similarities emerge. All 485 samples show a large number of endangered and threatened species. Thresher, hammerhead and mako 486 sharks are abundant (especially Alopias superciliosus, Sphyrna lewini, and Isurus oxyrhincus). 487 Abundant Carcharhinus samples include C. falciformis, C. limbatus, and C. longimanus, though there 488 is a wide variety of other Carcharhinus species – generally at low and variable abundance - in the 489 larger samples. 490
There are also some striking differences. The Alopias/Isurus group dominates the small 491 Steinke sample (Table 1). The Alopias/Isurus group is also abundant in our sample, dominated by A. 492 superciliosus and I. oxyrhincus. Yet in the Hong Kong shops sampled by Fields et al. (2018) and 493 Cardeñosa et al. (2018), this group is a minor component. By contrast, the Fields et al. (2018) and 494 Cardeñosa et al. (2018) samples are dominated by blue sharks, a single species in the Carcharhinidae 495 that makes up nearly half their samples. Blue sharks occur in our sample, and in Steinke et al. (2017), 496 at about 2-10%. Blue sharks also dominated the earlier sample of Clarke et al. (2006) from the Hong 497 Kong wholesale market, prompting Fields et al. (2018) to ask how blue sharks could maintain their 498 market presence at such a high level for so long. The relatively lower number of blue shark fins in 499 retail markets on the US west coast may partially answer this question if there is a strong regional 500 difference in market availability of this species. No blue sharks occur in the Brazil samples, which is 501 dominated by regional sharpnose and Carcharhinus species (Feitosa et al., 2018). 502
Comparison across genes and methods 503
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There is strong evidence from these data that the CR and COI generally produce data equivalently well 504 for most sharks, but that using CR primers specifically underestimates thresher shark abundance. The 505 number of shark fins in our COI data set for each species is highly correlated to the number of fins we 506 find with our CR primers (r2=0.91, Fig. 8). However there are two strong outliers. For both Alopias 507 superciliosus and A. pelagicus the number of fins observed with CR primers, even taking in to account 508 the fins identified with pseudo-gene CR sequences - falls far below the line relating COI and CR 509 results (Fig. 8). 510
These outliers are because Alopias fins defined by COI sequences frequently fail to show Alopias CR 511 sequences: 48 of the 208 Alopias fins with COI sequences have CR sequences with high identity to a 512 different species, all C. falciformis, C. obscurus, and C. longimanus (see Table 3). These CR 513 sequences are not Alopias pseudo-genes. Our hypothesis is that these CR identifications are incorrect, 514 and derive from failure of the CR primers to easily amplify Alopias CR regions, amplifying common 515 Carcharhinus species DNA as lab contaminants. 516
The lowest red point in Figure 8 represents very different identification rates for COI and CR for A. 517 pelagicus: COI data show 38 fins for this species out of a total of 963 fins, but we find only 8 out of 518 1736 CR sequences. Lab records show that failure rate of CR amplifications of fins that have a A. 519 pelagicus COI sequences is high. We searched for a possible explanation for this underrepresentation 520 and found that the reverse primer from (Giles et al., 2016) does not match A. pelagicus at four of 22 521 positions, making it a poor amplification tool (Fig. 9). The match to A. superciliosus is better: 21 of 22 522 bases match. But the 3’ end base, the most crucial one for the polymerase chain reaction, does not 523 match. This may make this primer less valuable for this species as well. 524
Conservation status 525
Our data confirm the strong abundance of endangered, vulnerable and CITES listed shark species in 526 retail fin markets. As in previous surveys, we find about half the fins come from species of 527 conservation concern. This consistency is particularly important because it spans very different types 528 of retail markets, in Hong Kong and the US west coast, imbedded in very different fisheries cultures 529 and retail markets. In particular, the US has made strong strides in recent years in regulating fisheries, 530 and returning overfished stocks to sustainability (Barner et al., 2015). Yet the shark markets in the US 531 and Hong Kong remain quite similar in the presence of protected species. This suggests that fisheries 532 policy improvements in the US have not penetrated the fin trade, and that highly regulated US 533 fisheries do not contribute much to the retail fin market. This suggestion is supported by lack of fins 534 from the biggest US shark fishery, spiny dogfish (squalus acanthias), both in the US west coast and 535 Hong Kong retail fin market (Cardeñosa et al., 2018; Feitosa et al., 2018; Fields et al., 2018; Steinke et 536 al., 2017). 537
There have been a series of other questions asked of the global shark fishery, notably about the 538 persistence of some abundant fins on the global market from the same species for over a decade 539 (Davidson, Krawchuk, & Dulvy, 2016; Fields et al., 2018). For example, blue sharks were a dominant 540 feature of the Hong Kong market as shown in (Clarke et al., 2006), and again a decade later 541 (Cardeñosa et al., 2018; Fields et al., 2018). Such dominance of a global market by a single species 542 might suggest higher sustainability for this species than thought originally. However, our data show 543 many fewer blue sharks, in contrast to nearly 50% of the samples being blue sharks in the Hong Kong 544 retail market (Cardeñosa et al., 2018; Fields et al., 2018), we show no more that 4% in our survey. 545 Likewise, bull sharks and sickle fin lemon sharks are at a much higher percentage in the Hong Kong 546 market than in the US west coast. By contrast, our data show a higher abundance of bigeye thresher 547 and the Atlantic smalltail sharks than seen in Hong Kong. These differences suggest that a single 548 market can provide an incomplete picture of the global trade and call for more coordinated fin testing 549 at high levels of sampling. 550
551
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ACKNOWLEDGMENTS 552 J. Giles provided assistance with data collection, technical issues, and laboratory supervision. 553 554 FUNDING 555 This research was supported through generous contributions to the Monterey Bay Aquarium. 556 557 COMPETING INTERESTS 558 The authors declare there are no competing interests. Stephen Palumbi is an employee of Stanford 559 University. Salvador Jorgensen and Kyle Van Houtan are employees of the Monterey Bay Aquarium. 560 561 AUTHOR CONTRIBUTIONS 562 SP oversaw data collection experiments, analyzed the data, contributed reagents/materials/analysis 563 tools, and prepared figures and tables. 564 565 KR collected data and performed lab work. 566 567 SP, SJ, KV, KR conceived and designed the experiments, authored or reviewed drafts of the paper, 568 and approved the final draft. 569 570 DATA AVAILABILITY 571 All data and supplemental files are available open-access via the Open Science Framework, available 572 at https://osf.io/9d65y/ and through the following DOI:10.17605/OSF.IO/9D65Y. 573 574 SUPLLEMENTAL INFORMATION 575 Supplemental information for this article can be found online. 576 577
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Table 1: COI and CR sequences identifications for this study, compared to recently published studies. 633
634
TAXON FAMILY GENUS SPECIES COMMON MBA MBA STIENKE FIELDS FEITOSA IUCN CITESGROUP NAME NAME NAME NAME COI CR COI COI COI STATUS STATUSthresher sharks Alopiidae Alopias pelagicus pelagic thresher shark 38 8 12 19 -- VU IIthresher sharks Alopiidae Alopias superciliosus bigeye thresher shark 170 95 8 37 -- VU IIthresher sharks Alopiidae Alopias vulpinus common thresher shark 1 1 1 2 -- VU IIlamnid sharks Lamnidae Isurus paucus longfin mako shark 12 11 3 4 -- VU --lamnid sharks Lamnidae Isurus oxyrinchus shortfin mako shark 168 306 8 133 -- VU --lamnid sharks Lamnidae Lamna ditropis salmon shark 1 1 3 17 -- LC --lamnid sharks Lamnidae Lamna nasus porbeagle shark -- 0 5 6 -- VU IIlamnid sharks Lamnidae Carcharodon carcharias white shark 0 1 -- -- -- VU IIground sharks Triakidae Mustelus canis dusky smooth-hound 1 -- -- 3 8 NT --ground sharks Triakidae Mustelus lunulatus sicklefin smooth-hound 1 -- 1 17 -- LC --ground sharks Triakidae Mustelus mustelus common smooth-hound -- -- -- 10 -- VU --ground sharks Triakidae Mustelus mosis Arabian smooth-hound -- -- -- 12 -- DD --ground sharks Triakidae Mustelus higmani smalleye smooth-hound 0 0 0 0 8 LC --requiem sharks Carcharhinidae Galeorhinus galeus school shark 8 -- -- 19 -- VU --requiem sharks Carcharhinidae Rhizoprionodon porosus/terraenovae Caribbean sharpnose shark 27 27 1 17 142 LC --requiem sharks Carcharhinidae Rhizoprionodon acutus milk shark -- -- 3 66 -- LC --requiem sharks Carcharhinidae Rhizoprionodon longurio Pacific sharpnose shark -- -- -- 7 -- DD --requiem sharks Carcharhinidae Rhizoprionodon lalandii Brazilian sharpnose shark 0 0 0 0 1 DD --carpet sharks Ginglymostomatidae Ginglymostoma cirratum nurse shark 0 0 0 0 14 DD --hammerheads Sphyrnidae Sphyrna zygaena smooth hammerhead 0 4 -- 165 -- VU IIhammerheads Sphyrnidae Sphyrna mokarran great hammerhead 10 38 2 41 40 EN IIhammerheads Sphyrnidae Sphyrna tiburo bonnethead 11 11 -- 3 12 LC --hammerheads Sphyrnidae Sphyrna corona scalloped bonnethead 11 6 -- 0.01 -- NT --hammerheads Sphyrnidae Sphyrna lewini clade 1 scalloped hammerhead 10 24 7 0 18 EN IIhammerheads Sphyrnidae Sphyrna lewini clade 2 scalloped hammerhead 56 92 -- 196 -- EN IIhammerheads Sphyrnidae Sphyrna media scoophead 4 5 -- 0.01 -- DD --hammerheads Sphyrnidae Sphyrna tudes smalleye hammerhead 20 38 -- 0.01 10 VU --requiem sharks Carcharhinidae Triaenodon obesus whitetip reef shark 4 2 -- 1 -- NT --requiem sharks Carcharhinidae Prionace glauca blue shark 42 72 7 1632 -- NT --requiem sharks Carcharhinidae Galeocerdo cuvier tiger shark 6 15 -- 16 12 NT --requiem sharks Carcharhinidae Negaprion acutidens sicklefin lemon shark 3 5 1 29 -- VU --requiem sharks Carcharhinidae Negaprion brevirostris lemon shark 3 54 -- 5 -- NT --ground sharks Hemigaleidae Hemipristis elongata snaggletooth shark -- 0 -- 5 -- VU --requiem sharks Carcharhinidae Lamiopsis temminckii broadfin shark -- 0 -- 4 -- EN --requiem sharks Carcharhinidae Carcharhinus amblyrhynchos grey reef shark 8 34 1 15 -- NT --requiem sharks Carcharhinidae Carcharhinus signatus night shark 1 1 -- 0 -- VU --requiem sharks Carcharhinidae Carcharhinus brevipinna spinner shark 12 22 1 55 -- NT --requiem sharks Carcharhinidae Carcharhinus brachyurus copper shark 1 1 -- 13 -- NT --requiem sharks Carcharhinidae Carcharhinus melanopterus I blacktip reef shark 4 8 -- 2 -- NT --requiem sharks Carcharhinidae Carcharhinus longimanus oceanic whitetip shark 26 64 -- 48 -- VU IIrequiem sharks Carcharhinidae Carcharhinus melanopterus II blacktip reef shark 3 0 -- 0 -- NT --requiem sharks Carcharhinidae Carcharhinus leucas bull shark 6 18 -- 87 17 NT --requiem sharks Carcharhinidae Carcharhinus perezii Caribbean reef shark 1 20 -- 0.01 -- NT --requiem sharks Carcharhinidae Carcharhinus falciformis silky shark 59 127 -- 483 11 NT IIrequiem sharks Carcharhinidae Carcharhinus isodon finetooth shark 15 18 -- 6 -- LC --requiem sharks Carcharhinidae Carcharhinus galapagensis=obscurus Galapagos/Dusky 59 87 1 42 -- VU --requiem sharks Carcharhinidae Carcharhinus acronotus blacknose shark 12 61 -- 9 68 NT --requiem sharks Carcharhinidae Carcharhinus plumbeus=altimus Sandbar/Bignose 19 72 -- 11 -- VU --requiem sharks Carcharhinidae Carcharhinus limbatus blacktip shark 97 254 1 219 9 NT --requiem sharks Carcharhinidae Carcharhinus porosus smalltail shark 33 105 -- 2 42 DD --requiem sharks Carcharhinidae Carcharhinus amboinensis pigeye shark -- -- -- 54 -- DD --requiem sharks Carcharhinidae Carcharhinus leiodon smoothtooth shark -- -- 2 -- -- VU --requiem sharks Carcharhinidae Carcharhinus dussumieri whitecheek shark -- -- -- 14 -- NT --requiem sharks Carcharhinidae Carcharhinus sorrah spot-tail shark -- -- -- 50 -- NT --requiem sharks Carcharhinidae Carcharhinus albimarginatus silvertip shark -- -- -- 5 -- VU --requiem sharks Carcharhinidae Carcharhinus macloti hardnose shark -- -- -- 6 -- NT --requiem sharks Carcharhinidae Isogomphodon oxyrhynchus daggernose shark 0 0 0 0 14 CR --requiem sharks Carcharhinidae -- -- -- 0 0 -- 114 -- NT --dogfishes Squalidae Squalus -- dogfishes -- -- -- 19 -- DD --dogfishes Squalidae Squalus brevirostris/megalops shortnose spurdog 0 0 0 0 1 DD --squaliform sharks Centrophoridae Deania profundorum arrowhead dogfish -- -- -- 4 -- LC --squaliform sharks Dalatiidae Dalatias licha kitefin shark -- -- -- 53 -- NT --chimaeras Callorhinchidae Callorhinchus -- elephantfish -- -- -- 27 -- LC --carpet sharks Hemiscylliidae Chiloscyllium -- bamboo sharks -- -- -- 21 -- NT --chimaeras Chimaeridae Hydrolagus -- chimaeras -- -- -- 14 -- LC --whale shark Rhincodontidae Rhincodon typus whale shark -- -- 4 -- -- EN IIwedgefishes Rhinidae Rhyncobatus [ Gulf species ] unk wedgefish -- 1 -- -- -- VU --wedgefishes Rhinidae Rhynchobatus laevis smoothnose wedgefish -- 4 -- -- -- VU --wedgefishes Rhinidae Rhynchobatus australiae whitespotted wedgefish -- 6 -- 26 -- VU --wedgefishes Rhinidae Rhynchobatus djiddensis giant guitarfish -- 1 -- -- -- VU ---- Mixed rare 17 rare species -- -- -- -- -- 26 -- -- --
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
16
Table 2: Comparison of best BLAST or phylogenetic identification for CR and COI gene sequences. 635 CR=COI represents the number of fins that showed the same identification for both genes. CR<>COI 636 represents fins with identifications that do not match. No COI represents fins for which there is no 637 COI sequence. Refs is the number of reference sequences from Genbank in the phylogeneytic clades 638 defining species. 639 640
641 642
Table2:CladeandBLASTidentificationofCRsequencescomparedtoCOI
Clade CR=COI CR<>COI NoCOItotalwithoutCR<>COI Refs Notes Taxontotals
Lamnid A.superciliosus 39 0 33 72 2A.pelagicus 0 0 0 0 1I.oxyrhincus 1 0 0 1 0I.paucus 0 0 2 2 3L.ditropis 1 0 0 1 1Carcharodoncarcharias 0 0 1 1 1 77
Hammerheads S.lewini 46 2 70 116 2S.tudes 19 0 19 38 2S.media 0 4 5 5 1 4alltudesS.tiburo 7 0 4 11 3 refsindiffcladeS.corona 0 10 6 6 1 10alllewiniS.mokarran 9 0 29 38 2S.zygaena 0 0 4 4 2 234
Charchariacea C.porosus 28 2 77 105 0C.limbatusclade1 20 0 112 132 0C.limbatusclade2 74 5 48 122 1 wrongref!C.isodon 11 10 7 18 6C.noname2 1 3 15 16 0C.plumbeus 14 4 58 72 4C.brachyurus 1 0 0 1 0C.brevipinna 12 0 10 22 2C.obscurusclade1 0 1 3 3 0C.obscurusclade2 51 25 33 84 2C.obscurusclade3 0 4 20 20 1 perezii?C.longimanus 26 26 38 64 2C.melanopterus 7 0 1 8 2C.acronotus 11 3 50 61 2C.falciformis 32 52 95 127 2C.noname1 0 2 0 0 3C.amblyrhyncus 23 0 11 34 0C.leucas 6 0 12 18 3 1044
439 153 763 1202 51 1355Rhyncobatus
Rhynchobatusaustraliae 0 0 6 6 3Rhynchobatuscf. 0 0 4 4 2RhynchobatusGulf 0 0 1 1 1RhynchobatusRedSea 0 0 1 1 1
OthergeneraP.glauca 13 0 59 72 1
Rhizopriodonporosus 23 0 2 25 1Rhizopriodonterraenovae 1 0 1 2 1
Negaprionbrevirostis 3 0 51 54 2Negaprionacutidens 3 0 2 5 2Triaenodonobesus 2 0 0 2 1Galeocerocuvier 5 0 10 15 2
Pseudogenesequences(BLASTtoMegamouth)I.oxyrinchus 135 161 296I.paucus 6 3 9A.superciliosus 3 8 2 13A.pelagicus 0 6 1 7A.vulpinus 0 1 0 1
PseudogenesequencesBLASTtoAlopiasA.pelagicus 1 1I.oxyrynchus 0 6 3 9 86%bootstrapA.superciliosus 3 0 0 3
PseudogenesequencesBLASTtoP.kamoharaiA.superciliosus 0 5 2 7
0Allpseudogenes 7 167 172 346 0 346
0496 167 1072 1568 68 1735 1389
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
17
Table 3: Fins with high fidelity COI sequence identifications (left column) that have different CR 643 identifications, mostly to three species of common Carcharhinus sharks. 644 645 646 647 648 649 650 651 652 653 654
Table3:FinswithhighfidelityCRidentificationsthathavedifferentCOIidentificationsIdentityofCRsequence:
COIidentity: Total C.falciformisCR C.longimanusCR C.obscurusCR otherAll 133 57 28 25 23
AlopiasCOI 48 15 16 17 0GaleocerdoCOI 8 1 2 2 3
Isurus 34 33 1 0 0Prionace 17 2 9 6 00ther 26 6 0 0 20
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
18
FIGURE LEGENDS 655
Figure 1A: All COI tree with bootstraps. All phylogenetic trees are expandable jpg files. Each shows 656 our market samples labeled as ‘DCA’ plus a sample number, followed by the best BLAST search of 657 the COI sequence from that sample, where available, then the best BLAST search of the CR sequence 658 from that sample. 659 660 Figure 1B: Carcharhinus COI tree with bootstraps. 661 662 Figure 2: Other genera CR tree 663 664 Figure 3: Carcharhinus CR tree 665 666 Figure 4: Sphyrna CR tree. 667 668 Figure 5: Unexpected amplification of pseudogenes. The figure shows phylogenetic relationships 669 among mitochondrial control region sequences (red labels) from Genbank and sequences from MBAq 670 fins derived from our control region primers (black labels). The top black-labelled cluster of sequences 671 from Alopias and Isurus species are 20-25% divergent from known mitochondrial sequences from the 672 same species. These black-labelled sequences are probably mitochondrial pseudogenes, sequences 673 originally from the mitochondria that were passed into the nucleus long ago and no longer function. 674 One exception is a set of Alopias superciliosus sequences from our data set that appear to be valid 675 control region sequences. 676 677 Figure 6: Lamnid CR sequence tree. Sequences that amplify with CR primer and that cluster with CR 678 sequences from whole mitochondrial genomes are shown in the lower clade, suggesting that these 679 sequences are from true Control Regions section of mtDNA. The upper clade, starting with 680 DCA_0857 are CR amplified sequences that are highly divergent, suggesting they are pseudogene 681 sequences. 682 683 Figure 7: Numerous sequences amplified with CR primers from lamnid sharks that form a clade 684 separate from the clade defined by vouchered whole mitochondrial genomes. These sequences have 685 only a best match of 70-80% match to M. pelagios or P. kamoharai or C. Taurus, and group together 686 with the putative pseudogene sequences in the upper clades of Figures 5 and 6. We use the species 687 identification of a subset of these fins based on COI to define species clades, and use membership of a 688 fin in one of these clades to assign the species name to that fin. For example, the first sequence at the 689 top of this tree (DCA1_0566) came from a fin with a COI sequence with a 99% match to A. pelagicus. 690 Another fin (DCA1_2250) is in this pseudo-CR sequence clade but has no COI sequence. We can use 691 the presence of DCA1_2250 in this clade as good evidence that it is a fin from A. pelagicus as well. 692
Figure 8: Good correlation between the number of fins seen for each species based on COI data (x-693 axis) compared to the control region (CR) data (y-axis). Two exceptions (red dots) are two species of 694 Alopias, which appear to be underestimated with CR primers compared to COI primers. 695
Figure 9: Mismatch between our reverse Control Region primer and the mitochondrial sequence of 696 Alopias pelagicus may explain the strong underestimate of this species in our CR data set. The reverse 697 CR primer is shown as the reverse complement of the synthesized reverse primer to correspond to the 698 published sequence. 699
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
12/28/2017 Phylo.io
https://mafft.cbrc.jp/alignment/server/spool/_phyloio.171229031330463.html 1/1
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404_DCA1_1333Carcharhinus_falciformis
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519_DCA1_1332Carcharhinus_melanopterus1053_ESHKC048-07_Carcharhinus_melanopterusQWX386_DCA1_1144Carcharhinus_falciformis783_DCA1_2514Prionace_glauca804_DCA1_1755Prionace_glauca806_DCA1_1754Prionace_glauca777_DCA1_0863Prionace_glauca774_DCA1_0611Prionace_glauca769_DCA1_0573Prionace_glauca799_DCA1_0787Prionace_glauca792_DCA1_0810Prionace_glauca786_DCA1_0688Prionace_glauca1129_ESHKC132-07_Carcharhinus_plumbeusQWX568_DCA1_2313Charcarhinus_altimus557_DCA1_0265Carcharhinus_plumbeus556_DCA1_0254Carcharhinus_plumbeus415_DCA1_1152Carcharhinus_falciformis1057_ESHKA006-07_Carcharhinus_obscurusQWX537_DCA1_0685Carcharhinus_obscurus535_DCA1_1357Carcharhinus_obscurus548_DCA1_0488Carcharhinus_obscurus326_DCA1_0746Carcharhinus_obscurus546_DCA1_0510Carcharhinus_obscurus314_DCA1_0795Carcharhinus_obscurus525_DCA1_0673Carcharhinus_obscurus308_DCA1_0532Carcharhinus_obscurus973_Carcharhinus_obscurus307_DCA1_0540Carcharhinus_obscurus304_DCA1_0534Carcharhinus_obscurus249_DCA1_0846Carcharhinus_galapagensis1043_ESHKC115-07_Carcharhinus_isodonQWX432_DCA1_1035Carcharhinus_isodon427_DCA1_1501Carcharhinus_isodon362_DCA1_1463Carcharhinus_acronotus212_DCA1_2729Carcharhinus_acronotus421_DCA1_1160Carcharhinus_falciformis247_DCA1_0554Carcharhinus_falciformis248_DCA1_0622Carcharhinus_falciformis398_DCA1_1150Carcharhinus_falciformis229_DCA1_0790Carcharhinus_falciformis420_DCA1_1390Carcharhinus_falciformis408_DCA1_1148Carcharhinus_falciformis238_DCA1_0785Carcharhinus_falciformis225_DCA1_0749Carcharhinus_falciformis231_DCA1_2694Carcharhinus_falciformis232_DCA1_2776Carcharhinus_falciformis223_DCA1_2793Carcharhinus_falciformis
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566_DCA1_1166Carcharhinus_porosus564_DCA1_1512Carcharhinus_porosus561_DCA1_1447Carcharhinus_porosus565_DCA1_1179Carcharhinus_porosus337_DCA1_2746Carcharhinus_porosus4545
4545
1093_ESHKD038-07_Negaprion_brevirostrisQWX1019_ESHKD031-07_Negaprion_brevirostrisQWX764_DCA1_1762Negaprion_brevirostris763_DCA1_0227Negaprion_brevirostris988_Negaprion_brevirostris761_DCA1_2311Negaprion_brevirostris6969
696969
762_DCA1_0475Negaprion_acutidens987_Negaprion_acutidens760_DCA1_0590Negaprion_acutides1085_ESHKD102-07_Negaprion_acutidensQWX1010_ESHKD101-07_Negaprion_acutidensQWX759_DCA1_0773Negaprion_acutidens8282
828282
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1097_EWTGS019-06_Galeocerdo_cuvierQWX1028_EWTGS016-06_Galeocerdo_cuvierQWX574_DCA1_1781Galeocerdo_cuvier573_DCA1_0660Galeocerdo_cuvier572_DCA1_0845Galeocerdo_cuvier571_DCA1_0291Galeocerdo_cuvier570_DCA1_0295Galeocerdo_cuvier980_Galeocerdo_cuvier569_DCA1_2816Galeocerdo_cuvier7979
797979797979
1116_ESHKA037-07_Carcharhinus_longimanusQWX1050_ESHKC167-07_Carcharhinus_longimanusQWX292_DCA1_0801Carcharhinus_longimanus283_DCA1_0545Carcharhinus_longimanus299_DCA1_0852Carcharhinus_longimanus296_DCA1_0889Carcharhinus_longimanus298_DCA1_0876Carcharhinus_longimanus511_DCA1_0659Carcharhinus_longimanus293_DCA1_0840Carcharhinus_longimanus508_DCA1_0686Carcharhinus_longimanus289_DCA1_0873Carcharhinus_longimanus514_DCA1_0639Carcharhinus_longimanus513_DCA1_0649Carcharhinus_longimanus297_DCA1_0606Carcharhinus_longimanus510_DCA1_1780Carcharhinus_longimanus509_DCA1_0665Carcharhinus_longimanus512_DCA1_0444Carcharhinus_longimanus300_DCA1_0723Carcharhinus_longimanus295_DCA1_0803Carcharhinus_longimanus294_DCA1_0722Carcharhinus_longimanus291_DCA1_0567Carcharhinus_longimanus290_DCA1_0580Carcharhinus_longimanus971_Carcharhinus_longimanus288_DCA1_0621Carcharhinus_longimanus287_DCA1_0613Carcharhinus_longimanus286_DCA1_0603Carcharhinus_longimanus285_DCA1_0592Carcharhinus_longimanus284_DCA1_0596Carcharhinus_longimanus282_DCA1_0578Carcharhinus_longimanus6363
6363636363636363636363636363636363636363636363636363
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3
3
1119_ESHKC051-07_Carcharhinus_melanopterusQWX1025_ESHKC083-07_Carcharhinus_cautusQWX515_DCA1_1180Carcharhinus_melanopterus972_Carcharhinus_melanopterus302_DCA1_0855Carcharhinus_melanopterus301_DCA1_0841Carcharhinus_melanopterus334_DCA1_2774Carcharhinus_porosus346_DCA1_2177Carcharhinus_porosus353_DCA1_1951Carcharhinus_porosus352_DCA1_2204Carcharhinus_porosus350_DCA1_1966Carcharhinus_porosus348_DCA1_2145Carcharhinus_porosus343_DCA1_1976Carcharhinus_porosus336_DCA1_2209Carcharhinus_porosus356_DCA1_2800Carcharhinus_porosus976_Carcharhinus_porosus345_DCA1_1012Carcharhinus_porosus567_DCA1_1338Carcharhinus_porosus347_DCA1_2824Carcharhinus_porosus563_DCA1_1036Carcharhinus_porosus349_DCA1_2808Carcharhinus_porosus560_DCA1_0312Carcharhinus_porosus562_DCA1_0302Carcharhinus_porosus344_DCA1_2649Carcharhinus_porosus342_DCA1_2777Carcharhinus_porosus341_DCA1_2736Carcharhinus_porosus340_DCA1_2732Carcharhinus_porosus351_DCA1_2819Carcharhinus_porosus355_DCA1_2737Carcharhinus_porosus354_DCA1_2735Carcharhinus_porosus339_DCA1_2810Carcharhinus_porosus338_DCA1_2779Carcharhinus_porosus333_DCA1_1454Carcharhinus_porosus1113_NOSMF038-08_Carcharhinus_leucasQWX1047_ESHKB023-07_Carcharhinus_leucasQWX257_DCA1_2790Carcharhinus_leucas256_DCA1_2792Carcharhinus_leucas969_Carcharhinus_leucas255_DCA1_2787Carcharhinus_leucas254_DCA1_2789Carcharhinus_leucas253_DCA1_2791Carcharhinus_leucas252_DCA1_2788Carcharhinus_leucas3131
313131313131311414141414141414141414141414141414141010101010101010101010101010
1141_ESHKC086-07_Carcharhinus_tilstoniQWX1077_ESHKC093-07_Carcharhinus_tilstoniQWX45464_DCA1_1358Carcharhinus_limbatus
468_DCA1_1306Carcharhinus_limbatus441_DCA1_1367Carcharhinus_limbatus447_DCA1_1411Carcharhinus_limbatus1115_NOSMF039-08_Carcharhinus_limbatusQWX1049_ESHKC004-07_Carcharhinus_limbatusQWX259_DCA1_1087Carcharhinus_limbatus507_DCA1_1295Carcharhinus_limbatus505_DCA1_1298Carcharhinus_limbatus504_DCA1_1373Carcharhinus_limbatus494_DCA1_1375Carcharhinus_limbatus488_DCA1_1300Carcharhinus_limbatus262_DCA1_0584Carcharhinus_limbatus482_DCA1_1356Carcharhinus_limbatus470_DCA1_1340Carcharhinus_limbatus469_DCA1_1372Carcharhinus_limbatus467_DCA1_1287Carcharhinus_limbatus463_DCA1_1067Carcharhinus_limbatus462_DCA1_1029Carcharhinus_limbatus277_DCA1_2657Carcharhinus_limbatus268_DCA1_0561Carcharhinus_limbatus970_Carcharhinus_limbatus263_DCA1_0547Carcharhinus_limbatus449_DCA1_1435Carcharhinus_limbatus448_DCA1_1748Carcharhinus_limbatus445_DCA1_2691Carcharhinus_limbatus444_DCA1_1342Carcharhinus_limbatus443_DCA1_1186Carcharhinus_limbatus442_DCA1_1486Carcharhinus_limbatus496_DCA1_1128Carcharhinus_limbatus495_DCA1_1105Carcharhinus_limbatus492_DCA1_1168Carcharhinus_limbatus491_DCA1_1033Carcharhinus_limbatus493_DCA1_1472Carcharhinus_limbatus489_DCA1_1482Carcharhinus_limbatus498_DCA1_1293Carcharhinus_limbatus478_DCA1_1414Carcharhinus_limbatus506_DCA1_1310Carcharhinus_limbatus497_DCA1_1403Carcharhinus_limbatus503_DCA1_1457Carcharhinus_limbatus501_DCA1_1441Carcharhinus_limbatus500_DCA1_1383Carcharhinus_limbatus502_DCA1_1444Carcharhinus_limbatus499_DCA1_1764Carcharhinus_limbatus481_DCA1_1778Carcharhinus_limbatus480_DCA1_1043Carcharhinus_limbatus456_DCA1_1420Carcharhinus_limbatus455_DCA1_1395Carcharhinus_limbatus454_DCA1_1126Carcharhinus_limbatus453_DCA1_1052Carcharhinus_limbatus452_DCA1_1011Carcharhinus_limbatus485_DCA1_1439Carcharhinus_limbatus484_DCA1_1122Carcharhinus_limbatus483_DCA1_1528Carcharhinus_limbatus477_DCA1_1460Carcharhinus_limbatus476_DCA1_1044Carcharhinus_limbatus473_DCA1_1485Carcharhinus_limbatus472_DCA1_1466Carcharhinus_limbatus471_DCA1_1165Carcharhinus_limbatus465_DCA1_1429Carcharhinus_limbatus450_DCA1_1385Carcharhinus_limbatus446_DCA1_0183Carcharhinus_limbatus439_DCA1_1493Carcharhinus_limbatus438_DCA1_0182Carcharhinus_limbatus437_DCA1_1453Carcharhinus_limbatus267_DCA1_0759Carcharhinus_limbatus479_DCA1_1331Carcharhinus_limbatus475_DCA1_1330Carcharhinus_limbatus474_DCA1_1322Carcharhinus_limbatus461_DCA1_1124Carcharhinus_limbatus460_DCA1_1091Carcharhinus_limbatus459_DCA1_1074Carcharhinus_limbatus458_DCA1_1045Carcharhinus_limbatus
280_DCA1_2207Carcharhinus_limbatus260_DCA1_2827Carcharhinus_limbatus261_DCA1_1973Carcharhinus_limbatus281_DCA1_1980Carcharhinus_limbatus278_DCA1_1945Carcharhinus_limbatus273_DCA1_1961Carcharhinus_limbatus272_DCA1_2682Carcharhinus_limbatus271_DCA1_2780Carcharhinus_limbatus270_DCA1_2744Carcharhinus_limbatus269_DCA1_2666Carcharhinus_limbatus264_DCA1_2669Carcharhinus_limbatus276_DCA1_2656Carcharhinus_limbatus275_DCA1_2782Carcharhinus_limbatus274_DCA1_2662Carcharhinus_limbatus279_DCA1_2813Carcharhinus_limbatus266_DCA1_2806Carcharhinus_limbatus265_DCA1_2679Carcharhinus_limbatus490_DCA1_0529Carcharhinus_limbatus451_DCA1_2678Carcharhinus_limbatus486_DCA1_1765Carcharhinus_limbatus487_DCA1_0530Carcharhinus_limbatus6060
606060606060606060606060606060606060
457_DCA1_1042Carcharhinus_limbatus
0
440_DCA1_1404Carcharhinus_limbatus258_DCA1_1077Carcharhinus_limbatus21
5
5
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Dessimoz Lab(../gotodessimozlab.html)
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
2/26/2018 Phylo.io
https://mafft.cbrc.jp/alignment/server/spool/_phyloio.18022705212877.html 1/2
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SVG (data:image/svg+xml;base64,
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Dessimoz Lab(../gotodessimozlab.html)
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
2/14/2018 Phylo.io
https://mafft.cbrc.jp/alignment/server/spool/_phyloio.180215025728187.html 1/1
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226_JN983463_1Mustelus_lunulatusWX
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Dessimoz Lab(../gotodessimozlab.html)
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
2/13/2018 Phylo.io
https://mafft.cbrc.jp/alignment/server/spool/_phyloio.18021404262509.html# 1/1
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SVG (data:image/svg+xml;base64,PHN2ZyB3aWR0aD0iODYxLjExMTE0NTAxOTUzMTIiIGhlaWdodD0iODUzLjMzMzM3NDAyMzQzNzUiIHZlcnNpb249IjEuM
Dessimoz Lab(../gotodessimozlab.html)
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
2/14/2018 Phylo.io
https://mafft.cbrc.jp/alignment/server/spool/_phyloio.18021502344066.html 1/1
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315_DCA1_2250_C_taurusCR_79_NoCOI_00_QWX
314_DCA1_0752_C_taurusCR_79_A_pelagicusCOI_100_QWX
312_DCA1_0745_M_pelagiosCR_77_A_pelagicusCOI_100_QWX
311_DCA1_0566_M_pelagiosCR_77_A_pelagicusCOI_99_QWX9392
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Dessimoz Lab(../gotodessimozlab.html)
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
Figure 8
R²=0.9086
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Numberoffinsidentifiedtoth
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specieswithCR
Number offinsidentified toaparticular specieswithCOI
allothergenera
genusAlopias
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint
Figure 9
.CC-BY 4.0 International licensecertified by peer review) is the author/funder. It is made available under aThe copyright holder for this preprint (which was notthis version posted October 5, 2018. . https://doi.org/10.1101/433847doi: bioRxiv preprint