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Phenotypic Changes Across a Geographic Gradient: The Case of Three Sympatric Dolphin Species

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Abstract

Phenotypic changes in the mammalian mandible can occur at different spatial and temporal scales. We investigated mandibular size and shape variation in three extant closely related dolphins (Cetacea, Odontoceti): Tursiops truncatus, Stenella coeruleoalba and Delphinus delphis in order to test the hypothesis that similar phenotypic changes occur across the same geographical gradient. Our data included 219 specimens representative of the following geographic locations: the Mediterranean Sea, the eastern north Atlantic and the North Sea. Each mandibula was photographed laterally and spatial positioning of eight homologous 2D landmarks was recorded. After applying generalised Procrustes analysis (GPA), intraspecific variation was first investigated between sexes and among populations to allow further pooling of samples. Size and shape differences among populations and species were investigated through multivariate ordination techniques (PCA), Procrustes ANOVA and allometric analyses. In all three species, Mediterranean populations clearly differed in mandible shape from the extra-Mediterranean ones. Among the three, the direction of geographic phenotypic changes was significantly similar in the striped and common dolphin, while the bottlenose dolphin was the most divergent species, differing both in size and allometric trajectory. Shape variation of the two former species highlighted a morphological convergence in the Atlantic, and a phenotypic divergence in the Mediterranean. Shape differences among the three dolphin species were interpreted in the light of different prey preferences, feeding strategies and habitat partitioning to avoid direct competition.

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References

  • Adams, D. C., & Collyer, M. L. (2009). A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution, 63(5), 1143–1154. doi:10.1111/j.1558-5646.2009.00649.x.

    Article  PubMed  Google Scholar 

  • Adams, D. C., & Nistri, A. (2010). Ontogenetic convergence and evolution of foot morphology in European Cave Salamanders (Family: Plethodontidae). BMC Evolutionary Biology, 10(216), 1–10. doi:10.1186/1471-2148-10-216.

    Google Scholar 

  • Adams, D. C., & Otárola-Castillo, E. (2013). Geomorph: An R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4, 393–399. doi:10.1111/2041-210X.12035.

    Article  Google Scholar 

  • Adams, D. C., & Rohlf, F. J. (2000). Ecological character displacement in plethodon: Biomechanical differences found from a geometric morphometric study. Proceedings of National Academy of Sciences of the United States of America, 97(8), 4106–4111. doi:10.1073/pnas.97.8.4106.

    Article  CAS  Google Scholar 

  • Adams, D. C., Rohlf, F. J., & Slice, D. E. (2013). A field comes of age: Geometric morphometrics in the 21st Century. Hystrix, The Italian Journal of Mammalogy. doi:10.4404/hystrix-24.1-6283.

    Google Scholar 

  • Amaral, A. R., Jackson, J. A., Möller, L. M., Beheregaray, L. B., & Coelho, M. M. (2012). Species tree of a recent radiation: The subfamily delphininae (Cetacea, Mammalia). Molecular Phylogenetics and Evolution, 64(1), 243–253. doi:10.1016/j.ympev.2012.04.004.

    Article  PubMed  Google Scholar 

  • Amaral, A. R., Sequeira, M., & Coelho, M. M. (2007). A first approach to the usefulness of Cytochrome c Oxidase I barcodes in the identification of closely related Delphinid Cetacean Species. Marine and Freshwater Research, 58(6), 505–510. doi:10.1071/MF07050.

    Article  CAS  Google Scholar 

  • Anderson, P. S. L., Renaud, S., & Rayfield, E. J. (2014). Adaptive plasticity in the mouse mandible. BMC Evolutionary Biology, 14(1), 85. doi:10.1186/1471-2148-14-85.

    Article  PubMed  PubMed Central  Google Scholar 

  • Atchley, W. R., & Hall, B. K. (1991). A model for development and evolution of complex morphological structures. Biological Reviews, 66, 101–157.

    Article  CAS  PubMed  Google Scholar 

  • Barroso, C., Cranford, T. W., & Berta, A. (2012). Shape analysis of odontocete mandibles: Functional and evolutionary implications. Journal of Morphology, 273(9), 1021–1030. doi:10.1002/jmor.20040.

    Article  PubMed  Google Scholar 

  • Bearzi, G., Fortuna, C. M., & Reeves, R. R. (2009). Ecology and conservation of common bottlenose Dolphins Tursiops truncatus in the Mediterranean Sea. Mammal Review, 39(2), 92–123. doi:10.1111/j.1365-2907.2008.00133.x.

    Article  Google Scholar 

  • Bearzi, G., Politi, E., Agazzi, S., Bruno, S., Costa, M., & Bonizzoni, S. (2005). Occurrence and present status of coastal Dolphins (Delphinus delphis and Tursiops truncatus) in the Eastern Ionian Sea. Aquatic Conservation: Marine and Freshwater Ecosystems, 15(3), 243–257. doi:10.1002/aqc.667.

    Article  Google Scholar 

  • Bearzi, G., Reeves, R. R., di Sciara, G. N., Politi, E., Cañadas, A., Frantzis, A., & Mussi, B. (2003). Ecology, status and conservation of short-beaked common Dolphins Delphinus delphis in the Mediterranean Sea. Mammal Review, 33(3), 224–252. doi:10.1046/j.1365-2907.2003.00032.x.

    Article  Google Scholar 

  • Bearzi, M. (2005). Dolphin sympatric ecology. Marine Biology Research, 1(3), 165–175. doi:10.1080/17451000510019132.

    Article  Google Scholar 

  • Bell, C. H., Kemper, C. M., & Conran, J. G. (2002). Common dolphins (Delphinus delphis) in Southern Australia: A morphometric study. Australian Mammalogy, 24, 1–10.

    Article  Google Scholar 

  • Bianchi, C. N., & Morri, C. (2000). Marine biodiversity of the Mediterranean Sea: Situation, problems and prospects for future research. Marine Pollution Bulletin, 40(5), 367–376. doi:10.1016/S0025-326X(00)00027-8.

    Article  CAS  Google Scholar 

  • Blanco, C., Raga, J. A., & Salomón, O. (2001). Diet of the bottlenose dolphin (Tursiops truncatus) in the Western Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom, 81, 1053–1058. doi:10.1017/S0025315401005057.

    Article  Google Scholar 

  • Bourret, V. J. R., Macé, M. R. J. M., & Crouau-Roy, B. (2007). Genetic variation and population structure of Western Mediterranean and Northern Atlantic Stenella coeruleoalba populations inferred from Microsatellite Data. Journal of the Marine Biological Association of the United Kingdom, 87, 265–269. doi:10.1017/S0025315407054859.

    Article  CAS  Google Scholar 

  • Cagnolaro, L., & Cozzi, B., di Sciara, G. N. & Podestà M. (2015). Cetacea. Fauna d’Italia Vol. XLIX. Mammalia IV. Bologna: Calderini.

    Google Scholar 

  • Castillo, D. L., del, M., Viglino, D. A., Flores, & Cappozzo, H. L. (2017). Skull ontogeny and modularity in two species of Lagenorhynchus: Morphological and ecological implications. Journal of Morphology, 278(2), 203–214. doi:10.1002/jmor.20629.

    Article  PubMed  Google Scholar 

  • Cimmaruta, R., Bondanelli, P., & Nascetti, G. (2005). Genetic structure and environmental heterogeneity in the European Hake (Merluccius Merluccius). Molecular Ecology 14 (8), 2577–2591. doi:10.1111/j.1365-294X.2005.02595.x.

    Article  CAS  PubMed  Google Scholar 

  • Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F., Aguzzi, J., Ballesteros, E., et al. (2010). The biodiversity of the Mediterranean Sea: Estimates, patterns, and threats. PLoS ONE, 5(8), e11842. doi:10.1371/journal.pone.0011842.

    Article  PubMed  PubMed Central  Google Scholar 

  • Collyer, M. L., & Adams, D. C. (2013).Phenotypic trajectory analysis: Comparison of shape change patterns in evolution and ecology linear shape change associated with a continuous variable. Hystrix, the Italian Journal of Mammalogy, 24(1), 75–83. doi:10.4404/hystrix-24.1-6298.

    Google Scholar 

  • Collyer, M. L., Sekora, D. J., & Adams, D. C. (2015). A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity, 115(4), 357–365. doi:10.1038/hdy.2014.75.

    Article  CAS  PubMed  Google Scholar 

  • Committee for Taxonomy. (2016). Committee on Taxonomy. List of Marine Species and Sub Species. Society for Marine Mammology. https://www.marinemammalscience.org/.

  • Danovaro, R., & Pusceddu, A. (2007). Ecomanagement of biodiversity and ecosystem functioning in the Mediterranean Sea: Concerns and strategies. Chemistry and Ecology, 23(5), 347–360. doi:10.1080/02757540701653384.

    Article  Google Scholar 

  • de Francesco, M. C., & Loy, A. 2016. Intra- and interspecific interactions as proximate determinants of sexual dimorphism and allometric trajectories in the bottlenose Dolphin Tursiops Truncatus. PLoS ONE. doi:10.1371/journal.pone.0164287.

    Google Scholar 

  • Duran, S., Palacin, C., Becerro, M. A., Turon, X., & Giribet, G. 2004. Genetic diversity and population structure of the commercially Harvested Sea Urchin Paracentrotus lividus (Echinodermata, Echinoidea). Molecular Ecology, 13(11), 3317–3328.

    Article  CAS  PubMed  Google Scholar 

  • Figueirido, B., Palmqvist, P., & Pérez-Claros, J. A. (2009). Ecomorphological correlates of craniodental variation in bears and paleobiological implications for extinct taxa: An approach based on geometric morphometrics. Journal of Zoology, 277, 70–80. doi:10.1111/j.1469-7998.2008.00511.x.

    Article  Google Scholar 

  • Frantzis, A., & Herzing, D. L. (2002). Mixed-species associations of striped dolphins (Stenella coeruleoalba), short-beaked common dolphins (Delphinus delphis), and Risso’s Dolphins (Grampus Griseus) in the Gulf of Corinth (Greece, Mediterranean Sea). Aquatic Mammals, 28(2), 188–197.

    Google Scholar 

  • Garcia-Castellanos, D., Estrada, F., Jiménez-Munt, I., Gorini, C., Fernàndez, M., Vergés, J., & De Vicente, R. 2009. Catastrophic flood of the Mediterranean after the Messinian Salinity Crisis. Nature, 462 (7274), 778–781. 10.1038/nature08555.

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Martinez, J., Barrio, E., Raga, J. A., & Latorre, A. (1995). Mitochondrial DNA variability of striped dolphins (Stenella coeruleoalba) in the Spanish Mediterranean Waters.. Science, 11(2), 183–199. doi:10.1111/j.1748-7692.1995.tb00517.x.

    Google Scholar 

  • Garcia-Martinez, J., Moya, A., Raga, J. A., & Latorre, A. (1999). Genetic differentiation in the striped dolphin Stenella coeruleoalba from European Waters according to Mirochondrial DNA (mtDNA) restriction analysis. Molecular Ecology, 8, 1069–1073.

    Article  CAS  PubMed  Google Scholar 

  • Gaspari, S., Azzellino, A., Airoldi, S., & Hoelzel, A. R. (2007). Social Kin Associations and genetic structuring of striped dolphin populations (Stenella coeruleoalba) in the Mediterranean Sea. Molecular Ecology, 16(14), 2922–2933. doi:10.1111/j.1365-294X.2007.03295.x.

    Article  PubMed  Google Scholar 

  • Guidarelli, G., Nicolosi, P., Fusco, G., de Francesco, M. C., & Loy, A. (2014). Morphological variation and modularity in the mandible of three Mediterranean dolphins. Italian Journal of Zoology, 81(3), 354–367.

    Article  CAS  Google Scholar 

  • Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological Statistics Software Package for Education and Data Analysis Vol 4. Palaeontolia Electronica .

  • Hanken, J., & Hall, B. K. (1993). Mechanisms of Skull diversity and evolution. The Skull, 3, 1–36.

    Article  Google Scholar 

  • Heyning, J. E., & Perrin, W. F. (1994). Evidence for two species of common dolphins (Genus Delphinus) from the Eastern North Pacific. Natural History Museum of Los Angeles County, Contributions in Science. http://www.nhm.org/site/sites/default/files/pdf/contrib_science/CS442.pdf.

  • Johnston, C., & Berta, A. (2011). Comparative anatomy and evolutionary history of suction feeding in Cetaceans. Marine Mammal Science, 27(3), 493–513. doi:10.1111/j.1748-7692.2010.00420.x.

    Article  Google Scholar 

  • Kingston, S. E., Adams, L. D., & Rosel, P. E. (2009). Testing mitochondrial sequences and anonymous nuclear markers for phylogeny reconstruction in a rapidly radiating group: Molecular systematics of the Delphininae (Cetacea: Odontoceti: Delphinidae). BMC Evolutionary Biology, 9, 245. doi:10.1186/1471-2148-9-245.

    Article  PubMed  PubMed Central  Google Scholar 

  • Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357. doi:10.1111/j.1755-0998.2010.02924.x.

    Article  PubMed  Google Scholar 

  • Klingenberg, C. P., Mebus, K., & Auffray, J. (2003). Developmental integration in a complex morphological structure: How distinct are the modules in the mouse mandible? Evolution and Development, 5(5), 522–531. doi:10.1046/j.1525-142X.2003.03057.x.

    Article  PubMed  Google Scholar 

  • Krijgsman, W., Hilgen, F. J., Raffi, I., Sierro, F. J., & Wilson, D. S. (1999). Chronology, causes and progression of the messinian salinity crisis. Nature, 400(6745), 652–655. 10.1038/23231.

    Article  CAS  Google Scholar 

  • Lahaye, V., Bustamante, P., Dabin, W., Van Canneyt, O., Dhermain, F., Cesarini, C., Pierce, G. J., & Caurant, F. (2006). New insights from age determination on toxic element accumulation in striped and bottlenose dolphins from Atlantic and Mediterranean Waters. Marine Pollution Bulletin, 52(10), 1219–1230. doi:10.1016/j.marpolbul.2006.02.020.

    Article  CAS  PubMed  Google Scholar 

  • Loy, A., Tamburelli, A., Carlini, R., & Slice, D. E. (2011). Craniometric Variation of some mediterranean and atlantic populations of Stenella coeruleoalba (Mammalia, Delphinidae): A three-dimensional geometric morphometric analysis. Marine Mammal Science, 27(2), E65–E78. doi:10.1111/j.1748-7692.2010.00431.x.

    Article  Google Scholar 

  • McGowen, M. R. (2011). Toward the resolution of an explosive radiation-a multilocus phylogeny of oceanic dolphins (Delphinidae). Molecular Phylogenetics and Evolution, 60(3), 345–357. doi:10.1016/j.ympev.2011.05.003.

    Article  PubMed  Google Scholar 

  • McGowen, M. R., Spaulding, M., & Gatesy, J. 2009. Divergence date estimation and a comprehensive molecular tree of extant cetaceans. Molecular Phylogenetics and Evolution, 53(3), 891–906. doi:10.1016/j.ympev.2009.08.018.

    Article  CAS  PubMed  Google Scholar 

  • Mead, J. G., & Fordyce, R. E. (2009). The therian skull : A Lexicon with emphasis on the Odontocetes. Smithsonian Contributions to Zoology, 627, 1–249. doi:10.5479/si.00810282.627.

    Article  Google Scholar 

  • Meloro, C. (2011). Feeding habits of Plio-Pleistocene large carnivores as revealed by the mandibular geometry. Journal of Vertebrate Paleontology, 31(2), 428–446. doi:10.1080/02724634.2011.550357.

    Article  Google Scholar 

  • Meloro, C., Caceres, N. C., Carotenuto, F., Sponchiado, J., Melo, G. L., Passaro, F., & Raia, P. (2015a). Chewing on the trees: Constraints and adaptation in the evolution of the primate mandible. Evolution, 69(7), 1690–1700. doi:10.1111/evo.12694.

    Article  PubMed  Google Scholar 

  • Meloro, C., Cáceres, N., Carotenuto, F., Passaro, F., Sponchiado, J., Melo, G. L., & Raia, P. (2014). Ecogeographical variation in skull shape of Capuchin Monkeys. Journal of Biogeography, 41(3), 501–512. doi:10.1111/jbi.12203.

    Article  Google Scholar 

  • Meloro, C., Guidarelli, G., Colangelo, P., Ciucci, P., & Loy, A. (2017). Mandible Size and Shape in Extant Ursidae (Carnivora, Mammalia): A Tool for Taxonomy and Ecogeography. Journal of Zoological Systematics and Evolutionary Research. Hoboken: Wiley.

    Google Scholar 

  • Meloro, C., Hudson, A., & Rook, L. (2015b). Feeding habits of extant and fossil canids as determined by their skull geometry. Journal of Zoology, 295(3), 178–188. doi:10.1111/jzo.12196.

    Article  Google Scholar 

  • Meloro, C., & O’Higgins, P. (2011). Ecological adaptations of mandibular form in fissiped carnivora. Journal of Mammalian Evolution, 18(3), 185–200. doi:10.1007/s10914-011-9156-z.

    Article  Google Scholar 

  • Meloro, C., Raia, P., Carotenuto, F., & Cobb, S. N. (2011). Phylogenetic signal, function and integration in the subunits of the carnivoran mandible. Evolutionary Biology, 38(4), 465–475. doi:10.1007/s11692-011-9135-6.

    Article  Google Scholar 

  • Meloro, C., Raia, P., Piras, P., Barbera, C., & O’Higgins, P. (2008). The Shape of the mandibular corpus in large fissiped carnivores : Allometry, function and phylogeny. Zoological Journal of the Linnean Society, 154, 832–845.

    Article  Google Scholar 

  • Meotti, C., & Podestà, M. (1997). Stomach contents of striped dolphins, Stenella coeruleoalba (Meyen, 1833) from the Western Ligurian Sea (Cetacea, Delphinidae). Atti Della Societa Italiana Di Scienze Naturali E Del Museo Civico Di Storia Naturale Di Milano, 137, 5–15.

    Google Scholar 

  • Monteiro, L. R., & Nogueira, M. R. (2010). Adaptive radiations, ecological specialization, and the evolutionary integration of complex morphological structures. Evolution: International Journal of Organic Evolution, 64(3), 724–744. doi:10.1111/j.1558-5646.2009.00857.x.

    Article  Google Scholar 

  • Murphy, S., Herman, J. S., Pierce, G. J., Rogan, E., & Kitchener, A. C. (2006). Taxonomic status and geographical cranial variation of common dolphins (Delphinus) in the Eastern North Atlantic. Marine Mammal Science, 22(3), 573–599. doi:10.1111/j.1748-7692.2006.00037.x.

    Article  Google Scholar 

  • Naciri, M., Lemaire, C., Borsa, P., & Bonhomme, F. (1999). Genetic Study of the Atlantic/Mediterranean transition in sea bass (Dicentrarchus Labrax). Journal of Heredity, 90(6), 591–596. doi:10.1093/jhered/90.6.591.

    Article  Google Scholar 

  • Natoli, A., Birkun, A., Aguilar, A., Lopez, A., & Hoelzel, A. R. 2005. Habitat structure and the dispersal of male and female bottlenose Dolphins (Tursiops truncatus). Proceedings of The Royal Society—Biological Sciences 272(1569), 1217–1226. doi:10.1098/rspb.2005.3076.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Natoli, A., Cañadas, A., Vaquero, C., Politi, E., Fernandez-Navarro, P., & Hoelzel, A. R. (2008). Conservation genetics of the short-beaked common dolphin (Delphinus delphis) in the Mediterranean Sea and in the Eastern North Atlantic Ocean. Conservation Genetics, 9(6), 1479–1487. doi:10.1007/s10592-007-9481-1.

    Article  Google Scholar 

  • Nicolosi, P. 2011. Variabilità Intraspecifica in Delfino Comune, Delphinus delphis Linnaeus, 1758. L’utilizzo Della Morfometria Geometrica Bi- E Tridimensionale Come Strumento Diagnostico E Conoscitivo. Campobasso, CB: University of Molise.

    Google Scholar 

  • Nummela, S., Kosove, J. E., Lancaster, T. E., & Thewissen, J. G. M. (2004). Lateral mandibular wall thickness in Tursiops truncatus: Variation due to sex and age. Marine Mammal Science, 20(3), 491–497. doi:10.1111/j.1748-7692.2004.tb01174.x.

    Article  Google Scholar 

  • Otero, M. D. M., & Conigliaro, M. (2012). Marine mammals and Sea Turtles of the Mediterranean and Black Seas. Gland and Malaga: IUCN.

    Google Scholar 

  • Patarnello, T., Volckaert, F. A. M. J., & Castilho, R. (2007). Pillars of hercules: Is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology, 16(21), 4426–4444. doi:10.1111/j.1365-294X.2007.03477.x.

    Article  PubMed  Google Scholar 

  • Pérez-Losada, M., Guerra, A., & Carvalho, G. R. (2002). Extensive population subdivision of the Cuttlefish Sepia Officinalis (Mollusca: Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity, 89, 417–424. http://www.nature.com/hdy/journal/v89/n6/abs/6800160a.html.

  • Perrin, W. F. 1975. Variation of spotted and spinner porpoise (Genus Stenella) in the Eastern Pacific and Hawaii Vol 21. La jolla, CA: Scripps Institution of Oceanography.

  • Perrin, W. F. (1984). Patterns of geographical variation in small Cetaceans. Acta Zoologica Fennica, 172(1956), 137–140.

    Google Scholar 

  • Perrin, W. F., Rosel, P. E., & Cipriano, F. (2013). How to contend with paraphyly in the taxonomy of the Delphinine Cetaceans? Marine Mammal Science, 29(4), 567–588. doi:10.1111/mms.12051.

    CAS  Google Scholar 

  • Piras, P., Maiorino, L., Raia, P., Marcolini, F., Salvi, D., Vignoli, L., & Kotsakis, T. (2010). Functional and phylogenetic constraints in Rhinocerotinae Craniodental Morphology. Evolutionary Ecology Research, 12(8), 897–928.

    Google Scholar 

  • Piras, P., Maiorino, L., Teresi, L., Meloro, C., Lucci, F., Kotsakis, T., & Raia, P. (2013). Bite of the cats: Relationships between functional integration and mechanical performance as revealed by mandible geometry. Systematic Biology, 62(6), 878–900. doi:10.1093/sysbio/syt053.

    Article  PubMed  Google Scholar 

  • Pusineri, C., Magnin, V., Meynier, L., Spitz, J., Hassani, S., & Ridoux, V. (2007). Food and feeding ecology of the common dolphin (Delphinus delphis) in the Oceanic Northeast Atlantic and comparison with its diet in Neritic Areas. Marine Mammal Science, 23(1), 30–47. doi:10.1111/j.1748-7692.2006.00088.x.

    Article  Google Scholar 

  • Quesada, H., Beynon, C. M., & Skibinski, D. O. (1995). A Mitochondrial DNA Discontinuity in the Mussel Mytilus Galloprovincialis Lmk: Pleistocene vicariance biogeography and secondary intergradation. Molecular Biology and Evolution, 12(3): 521–524. http://mbe.oxfordjournals.org/cgi/content/long/12/3/521.

  • R Studio. (n.d.) [Program]. 0.98.1103 Version. Boston: RStudio Inc 2009–2014.

  • Raia, P. (2004). Morphological correlates of tough food consumption in Large Land Carnivores. Italian Journal of Zoology, 71(1), 45–50.

    Article  Google Scholar 

  • Raia, P., Carotenuto, F., Meloro, C., Piras, P., & Pushkina, D. (2010). The shape of contention: Adaptation, history, and contingency. Ungulate Mandibles. Evolution, 64(5), 1489–1503. doi:10.1111/j.1558-5646.2009.00921.x.

    PubMed  Google Scholar 

  • Rohlf, F. J. (2003). tpsDig2 Version 2.26. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.

    Google Scholar 

  • Rohlf, F. J., & Slice, D. E. (1990). Extensions of the procrustes method for the Optimal Superimposition of Landmarks. Systematic Biology, 39(1), 40–59. doi:10.2307/2992207.

    Google Scholar 

  • Santos, M. B. (1998). Feeding ecology of harbour porpoises, common and bottlenose dolphins and sperm whales in the Northeast Atlantic. PhD Thesis, p. 284.

  • Santos, M. B., Pierce, G. J., Reid, R. J., Patterson, I. A. P., Ross, H. M., & Mente, E. (2001). Contents of bottlenose dolphins (Tursiops truncatus) in Scottish Waters. Journal of the Marine Biological Association of the United Kingdom, 81(5), 873–878. doi:10.1017/S0025315401004714.

    Article  Google Scholar 

  • Santos, M. B., Pierce, G. J., Ross, H. M., Reid, R. J., & Wilson, B. (1994). Diets of small cetaceans from the Scottish Coast. International Council for the Exploration of the Sea (Marina Mammal Committee) CM 1994/N: p. 16.

  • Silva, M. A. (1999). Diet of common dolphins, Delphinus delphis, off the Portuguese Continental Coast. Journal of the Marine Biological Association of the United Kingdom, 79, 531–540.

    Article  Google Scholar 

  • Slater, G. J., Price, S. A., Santini, F., & Alfaro, M. E. (2010). Diversity versus disparity and the radiation of modern cetaceans. Proceedings of The Royal Society—Biological Sciences, 277(May), 3097–3104. doi:10.1098/rspb.2010.0408.

    Article  PubMed  PubMed Central  Google Scholar 

  • Slice, D. E. (2001). Landmark coordinates aligned by procrustes analysis do not lie in kendall’s shape space. Systematic Biology, 50(1), 141–149. doi:10.1080/106351501750107594.

    Article  CAS  PubMed  Google Scholar 

  • Spitz, J., Richard, E., Meynier, L., Pusineri, C., & Ridoux, V. (2006a). Dietary plasticity of the oceanic striped Dolphin, Stenella coeruleoalba, in the Neritic Waters of the Bay of Biscay. Journal of Sea Research, 55(4), 309–320. doi:10.1016/j.seares.2006.02.001.

    Article  Google Scholar 

  • Spitz, J., Rousseau, Y., & Ridoux, V. (2006b). Diet overlap between harbour porpoise and bottlenose Dolphin: An argument in favour of interference competition for food? Estuarine. Coastal and Shelf Science, 70(1–2), 259–270.

    Article  Google Scholar 

  • Steeman, M. E., Hebsgaard, M. B., Fordyce, R. E., Ho, S. Y. W., Rabosky, D. L., Nielsen, R., Rahbek, C., Glenner, H., Sørensen, M. V., & Willerslev, E. (2009). Radiation of extant cetaceans driven by restructuring of the oceans. Systematic Biology, 58(6), 573–585. doi:10.1093/sysbio/syp060.

    Article  PubMed  PubMed Central  Google Scholar 

  • Valsecchi, E., Amos, W., Raga, J. A., Podestà, M., & Sherwin, W. (2004). The effects of inbreeding on mortality during a morbillivirus outbreak in the Mediterranean Striped Dolphin (Stenella coeruleoalba). Animal Conservation, 7(2), 139–146. doi:10.1017/S1367943004001325.

    Article  Google Scholar 

  • van Heteren, A. H. (2009). Cave bears and their closest living relatives : A 3D geometric morphometrical approach to the functional morphology of the Cave Bear. Acta Carsologica Slovaca, 47(1), 33–46.

    Google Scholar 

  • van Heteren, A. H., MacLarnon, A., Soligo, C., & Rae, T. C. (2016). Functional morphology of the Cave Bear (Ursus Spelaeus) Mandible: A 3D geometric morphometric analysis. Quaternary International, 16(1), 299–314. doi:10.1016/j.quaint.2013.10.056.

    Google Scholar 

  • Wang, J. Y., Chou, L.-S., & White, B. N. (2000). Osteological differences between two sympatric forms of bottlenose Dolphins (Genus Tursiops) in Chinese Waters. Journal of Zoology, 252(2), 147–162. doi:10.1017/S0952836900009894.

    Article  Google Scholar 

  • Werth, A. J. (2000). A Kinematic Study of suction feeding and associated behavior in the long-finned Pilot Whale, Globicephala Melas (Traill). Marine Mammal Science, 16(2), 299–314. doi:10.1111/j.1748-7692.2000.tb00926.x.

    Article  Google Scholar 

  • Westgate, A. J. (2007). Geographic variation in cranial morphology of short-beaked common dolphins (Delphinus delphis) from the North Atlantic. Journal of Mammalogy, 88(3), 678–688. doi:10.1644/06-MAMM-A-177R.1.

    Article  Google Scholar 

  • Wilson, B., Thompson, P. M., & Hammond, P. S. (1997). Habitat use by bottlenose dolphins: Seasonal distribution and stratified movement patterns in the Moray Firth, Scotland. Journal of Applied Ecology, 34, 1365–1374.

    Article  Google Scholar 

  • Wurtz, M., & Marrale, D. (1993). Food of striped dolphin, Stenella coeruleoalba, in the Ligurian Sea. Journal of the Marine Biological Association of the United Kingdom, 73, 571–578.

    Article  Google Scholar 

  • Zelditch, Miriam, Leah, Donald L, Swiderski, & David Sheets, H. (2012). Geometric morphometrics for biologists: A primer. Cambridge: Academic Press.

    Google Scholar 

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Acknowledgements

The authors warmly thank the curators of the following institutions for providing access to the collections and to museum facilities: Museo Civico di Storia Naturale, Milano; Museo Civico di Storia Naturale “G. Doria”, Genova; Museo Civico di Zoologia, Roma; Museo di Storia Naturale, Calci; Museo Zoologico, Università di Firenze; Accademia dei Fisiocritici di Siena; Muséum National d’Histoire Naturelle, Paris; Naturalis Biodiversity Center, Leiden; Royal Belgian Institute of Natural Sciences, Bruxelles; Zoological Museum, University of Copenhagen; National History Museum of Scotland, Edinburgh; University of Haifa, Israel; Natural History Museum, Tel Aviv University; Aquário Vasco da Gama, Lisboa; Museu Nacional de História Natural e da Ciência, Lisboa; Naturhistoriska riksmuseet, Stockholm; Zoological Museum, Barcelona. This research received financial support from the University of Molise and through SYNTHESYS funding (Grant Agreement No. 226506) within the European Union’s Seventh Framework Programme.

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Authors and Affiliations

  1. Environmetrics Lab, Dipartimento di Bioscienze e Territorio, Università del Molise, Contrada Fonte Lappone s.n., 86090, Pesche, IS, Italy

    Giulia Guidarelli, Maria Carla de Francesco & Anna Loy

  2. CNR - Institute for Ecosystem Study, Largo Tonolli 50, 28922, Verbania Pallanza, VB, Italy

    Paolo Colangelo

  3. Museo di Zoologia, Università degli Studi di Padova, Via Jappelli 1/a, 35121, Padova,, Italy

    Paola Nicolosi

  4. Research Centre in Evolutionary Anthropology and Palaeoecology, School of Natural Sciences and Psychology, Liverpool John Moores University, Byrom Street, Liverpool, L3 3AF, UK

    Carlo Meloro

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  1. Giulia Guidarelli
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  2. Paolo Colangelo
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  3. Maria Carla de Francesco
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  4. Paola Nicolosi
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  5. Carlo Meloro
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  6. Anna Loy
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Correspondence to Giulia Guidarelli or Carlo Meloro.

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Guidarelli, G., Colangelo, P., de Francesco, M.C. et al. Phenotypic Changes Across a Geographic Gradient: The Case of Three Sympatric Dolphin Species. Evol Biol 45, 113–125 (2018). https://doi.org/10.1007/s11692-017-9435-6

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