Geometric morphometric analysis of caudal fin shapes in lamniform sharks (Chondrichthyes: Elasmobranchii) and its evolutionary implications Phillip C. Sternes a and Kenshu Shimadaa, b aDepartment
of Biological Sciences, DePaul University, 2325 North Clifton Avenue, Chicago, Illinois 60614, USA,
[email protected] bDepartment of Environmental Science and Studies, DePaul University, 1110 West Belden Avenue, Chicago, Illinois 60614, USA,
[email protected]
Abstract.—Lamniformes is a small order of sharks consisting of only 15 extant species but a highly diverse group, including a wide interspecific variation range in their caudal fin shape. A previous study has suggested that caudal fins of lamniforms can be grouped into two types. Type 1 fins have a high aspect ratio and high heterocercal angles, characterized by Cetorhinidae and Lamnidae. Type 2 fins are those with a moderate heterocercal angle and a moderate to well-developed subterminal lobe and are found in Mitsukurinidae, Odontaspididae, Pseudocarchariidae, Megachasmidae, and Alopiidae where an exceptionally elongate alopiid tails representing an extreme end of Type 2 spectrum. Based on nonembryonic specimens housed in various museums, we quantitatively examined the caudal fin shape of all 15 species using a principal component analysis. Whereas Type 2 is generally regarded as a plesiomorphic condition in Lamniformes, our analysis clearly shows two evolutionary pathways emerging from Type 2, one representing the Alopiidae clade and another the Type 1 clade. What is particularly intriguing is the sequence of taxa within each clade. In the Alopiidae clade, the plot for A. superciliosus is situated closest to the center of the Type 2 cluster, suggesting the species is less derived compared to A. pelagicus and A. vulpinus. In the Type 1 clade, Cetorhinidae is placed closest to the Type 2 taxa, followed successively by Lamna and ‘Isurus + Carcharodon.’ These specific taxonomic sequences based purely on the caudal fin morphology broadly agree with their evolutionary sequences predicted by molecular-based phylogeny.
Results Our PCA gave three principal components (Table 1). PC1 explains 81.05% of the overall variation in shape among species. PC2 and PC3 explained 17.57% and 1.38%, respectively. PCs 1 and 2 explained most of the variation whereas PC3 explained a minimal amount (Table 1). The PCA plot shows the placement of each of lamniform caudal fin. Three groups of sharks are present and interestingly these groups are similar to their phylogenetic relationships. The thresher sharks (Alopiidae) are located in the lower left corner of the plot. The middle of the plot has Mitsukurinidae, Odontaspididae, Pseudocarchariidae, Megachasmidae. The far right of the plot has Lamnidae. Cetorhinidae falls in between the middle plot and the far right plot.
FIGURE 1. Phylogenetic trees of Lamniformes. A, Phylogenetic tree proposed by Shimada (2005) based on morphological characters. B, Phylogenetic tree proposed by Naylor et al. (2012) based strictly on molecular data.
TABLE 1. Percent explained for relative warps.
Introduction Lamniformes is a small order of sharks consisting of only 15 species, but they display large morphological variation (Ebert et al., 2013). This wide variation has resulted in several competing hypotheses on their phylogenetic relationships based on exclusively on morphology as compared to those based on molecular data. Compagno (1990), Shirai (1996), and Shimada (2005) have all proposed phylogenetic tree based on morphology with Shimada (2005) being the most recent. Whereas the Shimada’s (2005) morphology tree has many unresolved relationships Naylor et al.’s molecular tree shows a distinct evolutionary history (Figure 1). Such differences include the placement of Carcharias taurus in relation with other sand tiger sharks and Alopias superciliosus in relation with other thresher sharks. Using a landmark based geometric morphometric analysis, we survey the caudal fin morphology of each lamniform species, and examine the evolutionary pattern through character mapping of the tail morphology using both morphology-based and molecular-based phylogenetic tress.
Within Lamniformes, Thomson and Simanek (1977) recognized two types of caudal fins (Type 1 and Type 2). Type 1 fins are characterized by their high aspect ratio and high heterocercal angles observed in Lamnidae and Cetorhinidae. Functionally, these fins are associated with high swimming speeds or efficient slow cruising speeds (Thomson and Simanek, 1977). For instance, the lamnid shark Isurus oxyrhinchus is considered the fastest swimming shark in the ocean whereas Cetorhinus maximus lacks speed but it migrates thousands of kilometers (Ebert et al., 2013). Type 2 fins are recognized by their moderate heterocercal angle and a moderate to well-developed subterminal lobe and are found in Mitsukurinidae, Odontaspididae, Pseudocarchariidae, Megachasmidae (Thomson and Simanek, 1977). Type 2 fins are known for increased maneuverability and slower swimming speeds. Alopiidae also have a Type 2 fin but the upper lobe is far more extended for its functional specialization (Aalbers et al., 2010). Previous studies (Shimada, 2005; Kim et al., 2013) have used the caudal fin for phylogenetic studies of Lamniformes. Our PCA shows some trends and relationships that are seen in molecular based studies including Naylor et al. (2012). For example, the Type 1 fin is considered to be more specialized and derived belonging to Lamnidae. In our plot, lamnid sharks are located far to the right and distinctively separate from other sharks. The other families of sharks possess the Type 2 fin and form their own distinct group located in the center of the plot. This pattern of morphology is congruent with the molecular based phylogeny (Fig. 1B). Interestingly, Cetorhinidae is placed directly in the middle of the Type 1 and Type 2 fins in our PCA plot which is similar to the evolutionary trend seen in Naylor et al. (2012). Lastly, Alopiidae sharks form their own cluster but they are still considered Type 2. Furthermore, Alopiidae sharks in our PCA show similar trends to those in the molecular tree. Specifically, A. superciliosus is considered to be less derived in the molecular-based tree, and in our plot, A. superciliosus is situated closest to the to the rest of the Type 2 fin sharks. This implies the possible evolutionary path of the specialization of the Type 2 fins seen in Alopiidae.
Conclusion Despite being a small order of sharks, Lamniformes is among if not the most diverse order of sharks. Thus, phylogenetic trees based on morphology differ with those based on molecular data. Our Principal Component Analysis on one morphological feature, the caudal fin, showed patterns similar to that of a molecular based phylogeny. Future studies using geometric morphometrics on the entire shark body may reveal similar or possibly different results than the ones presented here.
FIGURE 2. Type 1 and Type 2 lamniform fins. Adapted from Thomson and Simanek (1977).
Materials and Methods The 15 species of lamniform sharks were obtained from the following institutions: Bernice P. Bishop Museum (BPBM), Honolulu, USA; Field Museum of Natural History (FMNH), Chicago, USA ; Natural History Museum of Los Angeles (LACM), California, USA; Museum of Comparative Zoology (MCZ), Harvard University, Cambridge, Massachusetts, USA; Scripps Institution of Oceanography (SIO), University of California at San Diego, La Jolla, USA; Florida Museum of Natural History, University of Florida (UF), Gainesville, USA; Museum of Zoology, University of Michigan (UMMZ), Ann Arbor, USA; and United States National Museum (USNM; Smithsonian Institution), Washington, D.C., USA. Specimens include BPBM 9334 (Odontaspis ferox), FMNH 117473 (Alopias pelagicus), FMNH 117474 (Pseudocarcharias kamoharai) , MCZ 436 (Carcharias taurus), MCZ 54113 (Cetorhinus maximus), SIO 064-804 (Alopias vulpinus), SIO 07-46 (Mitsukurina owstoni), SIO 07-53 (Megachasma pelagios), UMMZ 60412 (Lamna nasus), USNM 201915 (Lamna ditropis), USNM 201731 (Isurus oxyrinchus), UF 160174 (Isurus paucas), UF 178509 (Alopias superciliosus), LACM 43804 (Carcharodon carcharias), and HUMZ 110959 (Odontaspis noronhai). One representative of each species of Lamniformes was used for a Principal Component Analysis (PCA). The caudal fin of each shark was flattened and a transparency was placed over the fin for it to be traced. Each tracing was photographed from a 1 m height to be uploaded into the tpsutil232. Landmarks were plotted using tpsdig232, and these landmarks included (1) upper origin (2) posterior tip (3) ventral tip (4) lower origin (Figure 3). After the four landmarks were placed on each of the 15 species a PCA was carried out using MorphoJ.
Discussion
Acknowledgements We thank the following individuals who were involved in the acquisition, loan, or transportation of examined specimens: A. Y. Suzumoto (BPBM): M. A. Rogers, K. Swagel, M. W. Westneat, P. Willink (FMNH); K. Nakaya (HUMZ); J. A. Seigel (LACM); K. E. Hartel, A. Williston (MCZ); C. Klepadlo, P. A. Hastings, H. J. Walker (SIO); L. M. Page, R. H. Robins (UF); D. W. Nelson (UMMZ); J. Finan, L. Palmer, S. Raredon, S. Smith; E. Wilbur, D. Pitassy, and J. T. Williams (USNM); M. Miya (Natural History Museum and Institute, Chiba, Japan), S. J. Arceneaux, R. L. Humphreys, Jr. (Pacific Island Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration); S. R. Van Sommeran (Pelagic Shark Research Foundation, Capitola, California): B. L. Beatty (New York College of Osteopathic Medicine); and J. L. CastilloGeniz (Instituto National de la Pesca, Baja California, México). Special thanks to K. Gray, B. Karl, J. Hickey, P. Myefski, A. Nicholas, L. Wansk(Children’s Memorial Hospital, Chicago, Illinois) for assisting with CT scanning and X-ray shooting of examined specimens.
Literature Cited
FIGURE 3. Illustration of four landmarks placed around the caudal fin of Lamniformes. Four landmarks include (1) upper origin (2) posterior tip (3) ventral tip (4) lower origin. Drawing of lamniform caudal fin adapted from Ebert et al. (2013).
FIGURE 4. PCA of preserved lamniform caudal fins. Illustrations of caudal fins adapted from Ebert et al. (2013).
Aalbers, S. A., D. Bernal, and C. A. Sepulveda. 2010. The functional role of the caudal fin in the feeding ecology of the common thresher shark Alopias vulpinus. Journal of Fish Biology 76:1863–1868. Compagno, L. J. V. 1990. Relationships of the megamouth shark, Megachasma pelagios (Lamniformes: Megachasmidae), with comments on its feeding habits. NOAA Technical Report NMFS 90:357–379. Ebert, D. A., S. Fowler, L. Compagno, and M. Dando. 2013. Sharks of the World: A fully illustrated guide. Wild Nature Press, Plymouth, New Hampshire, 528 pp. Klingenberg, C. P. 2011. MorpoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11:353–357. Naylor, G. J. P., J. N. Caira, K. Jensen, K. A. M. Rosana, N. Straube, and C. Lakner. 2012. Elasmobranch phylogeny: a mitochondrial estimate based on 595 species; pp. 31–56 in J. C. Carrier, J. A. Musick, M. R. Heithaus (eds.) Biology of Sharks and Their Relatives Second Edition. CRC Press, Boca Raton, Florida. Rohlf, F. J. 2015. The tps series of software. Hystrix, the Italian Journal of Mammalogy. 26:9–12. Shimada, K. 2005. Phylogeny of lamniform sharks (Chondrichthyes: Elasmobranchii) and the contribution of dental characters to lamniform systematics. Paleontological Research 9:55–72. Shirai, S. 1996. Phylogenetic interrelationships of neoselachians (Chondrichthyes: Euselachii); pp. 9–34 in M. L. J. Stiassny, L. R. Parenti, G. D. Johnson (eds.), Interrelationships of Fishes, Academic Press, New York. Thomson, K. S., and D. E. Simanek. 1977. Body form and locomotion in sharks. American Zoology 17:343–354.
