Ancient DNA re-opens the question of the phylogenetic position of the Sardinian pika Prolagus sardus (Wagner, 1829), an extinct lagomorph.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
21 08 2023
Historique:
received: 18 03 2023
accepted: 16 08 2023
medline: 23 8 2023
pubmed: 22 8 2023
entrez: 21 8 2023
Statut: epublish

Résumé

Palaeogenomics is contributing to refine our understanding of many major evolutionary events at an unprecedented resolution, with relevant impacts in several fields, including phylogenetics of extinct species. Few extant and extinct animal species from Mediterranean regions have been characterised at the DNA level thus far. The Sardinian pika, Prolagus sardus (Wagner, 1829), was an iconic lagomorph species that populated Sardinia and Corsica and became extinct during the Holocene. There is a certain scientific debate on the phylogenetic assignment of the extinct genus Prolagus to the family Ochotonidae (one of the only two extant families of the order Lagomorpha) or to a separated family Prolagidae, or to the subfamily Prolaginae within the family Ochotonidae. In this study, we successfully reconstructed a portion of the mitogenome of a Sardinian pika dated to the Neolithic period and recovered from the Cabaddaris cave, an archaeological site in Sardinia. Our calibrated phylogeny may support the hypothesis that the genus Prolagus is an independent sister group to the family Ochotonidae that diverged from the Ochotona genus lineage about 30 million years ago. These results may contribute to refine the phylogenetic interpretation of the morphological peculiarities of the Prolagus genus already described by palaeontological studies.

Identifiants

pubmed: 37604894
doi: 10.1038/s41598-023-40746-w
pii: 10.1038/s41598-023-40746-w
pmc: PMC10442435
doi:

Substances chimiques

DNA, Ancient 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

13635

Informations de copyright

© 2023. Springer Nature Limited.

Références

Miller, W. et al. Sequencing the nuclear genome of the extinct woolly mammoth. Nature 456, 387–390 (2008).
pubmed: 19020620
Soubrier, J. et al. Early cave art and ancient DNA record the origin of European bison. Nat. Commun. 7, 13158 (2016).
pubmed: 27754477 pmcid: 5071849
Ciucani, M. M. et al. Old wild wolves: Ancient DNA survey unveils population dynamics in Late Pleistocene and Holocene Italian remains. PeerJ 2019, e6424 (2019).
Ciucani, M. M. et al. Evolutionary history of the extinct Sardinian dhole. Curr. Biol. 31, 5571-5579.e6 (2021).
pubmed: 34655517
Hempel, E. et al. Identifying the true number of specimens of the extinct blue antelope (Hippotragus leucophaeus). Sci. Rep. 11, 2100 (2021).
pubmed: 33483538 pmcid: 7822880
Hempel, E. et al. Blue turns to grey - Palaeogenomic insights into the evolutionary history and extinction of the blue antelope (Hippotragus leucophaeus). Mol. Biol. Evol. 39, msac241 (2022).
pubmed: 36322483 pmcid: 9750129
Angelici, F. M. et al. The Sicilian Wolf: Genetic identity of a recently extinct insular population. Zool. Sci. 36, 189–197 (2019).
Koupadi, K. et al. Population dynamics in Italian canids between the late pleistocene and bronze age. Genes (Basel) 11, 1429 (2020).
Hekkala, E. et al. Paleogenomics illuminates the evolutionary history of the extinct Holocene “horned” crocodile of Madagascar, Voay robustus. Commun. Biol. 4, 505 (2021).
pubmed: 33907305 pmcid: 8079395
Hu, J. et al. Ancient mitochondrial genomes from Chinese cave hyenas provide insights into the evolutionary history of the genus Crocuta. Proc. R. Soc. B Biol. Sci. 288, 20202934 (2021).
Molodtseva, A. S. et al. Phylogeography of ancient and modern brown bears from eastern Eurasia. Biol. J. Linn. Soc. 135, 722–733 (2022).
Baleka, S. et al. Revisiting proboscidean phylogeny and evolution through total evidence and palaeogenetic analyses including Notiomastodon ancient DNA. iScience 25, 103559 (2022).
pubmed: 34988402
Lalueza-Fox, C. et al. Molecular dating of caprines using ancient DNA sequences of Myotragus balearicus, an extinct endemic Balearic mammal. BMC Evol. Biol. 5, 70 (2005).
pubmed: 16332256 pmcid: 1325260
Bover, P. et al. Ancient DNA from an extinct Mediterranean micromammal—Hypnomys morpheus (Rodentia: Gliridae)—Provides insight into the biogeographic history of insular dormice. J. Zool. Syst. Evol. Res. 58, 427–438 (2020).
Torres-Roig, E. et al. Origin, extinction and ancient DNA of a new fossil insular viper: Molecular clues of overseas immigration. Zool. J. Linn. Soc. 192, 144–168 (2021).
Psonis, N. et al. Mitochondrial sequences of the extinct Cypriot pygmy hippopotamus confirm its phylogenetic placement. Zool. J. Linn. Soc. 196, 979–989 (2022).
Wagner, R. Über den zahnbau der gattung Lagomys. Isis von Oken 22, 1132–1141 (1829).
Forsyth Major, C. I. I. X. On fossil and recent lagomorpha. Trans. Linn. Soc. Lond. 2nd Ser. Zool. 7, 433–520 (1899).
Dawson, M. R. Osteology of Prolagus sardus, a Quaternary Ochotonid (Mammalia, Lagomorpha). Palaeovertebrata 2, 157–190 (1969).
López Martínez, N. Paleobiogeographical history of Prolagus, an European Ochotonid (Lagomorpha). Lynx 32, 215–231 (2001).
Lopez Martinez, N. Cladistique et paleontologie; application a la phylogenie des Ochotonides europeens (Lagomorpha, Mammalia). Bull. Soc. Geol. Fr. S7-XX, 821–830 (1978).
Tobien, H. Zur Gebißstruktur, Systematik und Evolution der Genera Piezodus, Prolagus und Ptychoprolagus (Lagomorpha, Mammalia) aus einigen Vorkommen im jüngeren Tertiär Mittel-und Westeuropas. Notizblatt des Hess. Landesamtes für Bodenforsch. zu Wiesbad. 103, 103–186 (1975).
Gureev, A. Fauna SSSR. Mlekopitayushchie (Fauna of the USSR: Mammals), vol. 3, no. 10: Zaitseobraznye (Lagomorpha) (Lagomorphs). (Nauka, 1964).
Gureev, A. A. & Erbajeva, M. A. On the Diagnostics of deciduous teeth in fossil lagomorphs. Paleontol. Zh. 3, 152–153 (1975).
Averianov, A. O. Lagomorphs (mammalia) from the pleistocene of Eurasia. Paleontol. J. 35, 191–199 (2001).
Erbajeva, M. A. Cenozoic pikas (Taxonomy, Systematics, Phylogeny). (Nauka, 1988).
Erbajeva, M. A. The ochotonids of Eurasia: Biochronology and taxonomic diversity. Biol. Bull. 43, 729–735 (2016).
Hoffmann, R. & Smith, A. Order Lagomorpha. in Mammal species of the world: A taxonomic and geographic reference (eds. Wilson, D. & Reeder, D.) (The Johns Hopkins University Press, 2005).
Angelone, C., Prieto, J. & Gross, M. Complement to the study of the pikas (Lagomorpha, Ochotonidae) from the Middle Miocene of Gratkorn, Austria. Palaeobiodiv. Palaeoenviron. 94, 125–134 (2014).
Laplana, C. et al. How far into Europe did pikas (lagomorpha: Ochotonidae) go during the Pleistocene? New evidence from central iberia. PLoS ONE 10, e0140513 (2015).
pubmed: 26535576 pmcid: 4633061
Viret, T. Sur une microévolution du type orthogénétique chez les Lagomorphes européens. Colloq. Intern. C.N.R.S. 175–179 (1950).
López-Martínez, N. & Thaler, L. Biogéographie, évolution et complements à la systématique du groupe d’Ochotonidés Piezodus-Prolagus dans le cénozoïque d’Europe Sud-Occidentale. Bull. Soc. Géol. Fr. 850–866 (1975).
Mazza, P. Prolagus apricenicus and Prolagus imperialis: two new Ochotonids (Lagomorpha, Mammalia) of the Gargano (Southern Italy). Boll. Soc. Paleontol. Ital. 26, 233–243 (1987).
Mazza, P. & Zafonte, F. Phyletic and ecologic considerations on the Gargano (Southern Italy) Prolagus (Ochotonidae, Lagomorpha, Mammalia). Boll. Soc. Paleontol. Ital. 26, 221–231 (1987).
Angelone, C., Čermák, S. & Kotsakis, T. The most ancient lagomorphs of Sardinia: An overview. Geobios 48, 287–296 (2015).
Angelone, C., Moncunill-Solé, B. & Kotsakis, T. Fossil Lagomorpha (Mammalia) of Italy: Systematics and biochronology. Riv. Ital. Paleontol. Stratigr. 126, 157–187 (2020).
Vigne, J.-D. Les mammifères post-glaciaires de Corse - étude archéozoologique. in XXVII supplément à Gallia Préhistoire 1–25 (Centre national de la recherche scientifique, 1988).
Vigne, J.-D. peuplement paléolithique des îles: Le debat s’ouvre en Sardaigne. Les Nouv. d’Archéologie 35, 39–42 (1989).
Vigne, J.-D. Zooarchaeology and the biogeographical history of the mammals of Corsica and Sardinia since the last ice age. Mamm. Rev. 22, 87–96 (1992).
Zoboli, D. & Caddeo, G. A. Articulated skeletons of Prolagus sardus (Mammalia, Lagomorpha) from the quaternary of grotta del campanaccio (Santadi, south-western Sardinia). Boll. Soc. Paleontol. Ital. 55, 81–83 (2016).
Zoboli, D., Pala, A., Pirellas, A. & Pillola, G. L. Pleistocene mammals from Sa Cona Cave (Teulada, south-western Sardinia, Italy). J. Mediterr. Earth Sci. 11, 15–29 (2019).
Zoboli, D. & Pillola, G. L. Quaternary mammal fauna from “Surconis”, Bolotana (Sardinia, Italy). Boll. Soc. Paleontol. Ital. 55, 193–203 (2016).
Zoboli, D. & Pillola, G. L. Upper pleistocene mammal assemblage from SU Concali Quarry (Samatzai, Southern Sardinia, Italy). Riv. Ital. Paleontol. Stratigr. 123, 243–254 (2017).
Zoboli, D., Zedda, M., Pillola, G. L. & Palombo, M. R. Does a relationship exist between palaeopathologies and insularity ? A case study of some bones of Prolagus sardus (Wagner, 1829) from Sardinia (Italy). Alp. Mediterr. Quat. 31, 75–86 (2018).
Malatesta, A. Cynotherium sardous Studiati. An extinct canid from the pleistocene of Sardinia. Mem. Istituto Ital. Paleontol. Um. 1, 1–72 (1970).
Lyras, G. & Van Der Geer, A. Adaptations of the Pleistocene island canid Cynotherium sardous (Sardinia, Italy) for hunting small prey. Cranium 23, 51–60 (2006).
Carenti, G. & Wilkens, B. L. colonizzazione fenicia e punica e il suo influsso sulla fauna sarda. Sardinia Corsica Balear. Antiq. 4, 173–186 (2006).
Valenzuela, A., Torres-Roig, E., Zoboli, D., Pillola, G. L. & Alcover, J. A. Asynchronous ecological upheavals on the Western Mediterranean islands: New insights on the extinction of their autochthonous small mammals. Holocene 32, 137–146 (2022).
Angelone, C. Systematic revision of genus Prolagus (Lagomorpha, Mammalia) in Italy and in Western Mediterranean islands: new systematic tools, biochronology and palaeogeography (Università Roma Tre, 2005).
Palombo, M. R. Biochronology of the Plio-Pleistocene terrestrial mammals of Sardinia: the state of the art. Hell. J. Geosci. 41, 47–66 (2006).
Angelone, C., Tuveri, C., Arca, M., López Martínez, N. & Kotsakis, T. Evolution of Prolagus sardus (Ochotonidae, Lagomorpha) in the Quaternary of Sardinia Island (Italy). Quat. Int. 182, 109–115 (2008).
Hofreiter, M. et al. The future of ancient DNA: Technical advances and conceptual shifts. BioEssays 37, 284–293 (2015).
pubmed: 25413709
Fontani, F. et al. First bronze age human mitogenomes from Calabria (Grotta della Monaca, Southern Italy). Genes (Basel) 12, 636 (2021).
pubmed: 33922908
Orlando, L. et al. Ancient DNA analysis reveals woolly rhino evolutionary relationships. Mol. Phylogenet. Evol. 28, 485–499 (2003).
pubmed: 12927133
Hofreiter, M. et al. Progress in forensic bone DNA analysis: Lessons learned from ancient DNA. Forensic Sci. Int. Genet. 54, 102538 (2021).
pubmed: 34265517
Alves, P. C. & Hacklander, K. Lagomorph Species: Geographical Distribution and Conservation Status. in Lagomorph Biology: Evolution, Ecology, and Conservation (eds. Alves, P. C., Ferrand, N. & Hacklander, K.) 395–405 (Springer-Verlag, 2008).
Fontanesi, L. et al. LaGomiCs - lagomorph genomics consortium: An international collaborative effort for sequencing the genomes of an entire mammalian order. J. Hered. 107, 295–308 (2016).
pubmed: 26921276 pmcid: 4888434
Melo-Ferreira, J. & Alves, P. C. Systematics of Lagomorphs. In Lagomorphs: Pikas, Rabbits, and Hares of the World 9–12 (John Hopkins University Press, 2018).
dos Reis, M. et al. Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc. R. Soc. B Biol. Sci. 279, 3491–3500 (2012).
Goswami, A. A dating success story: Genomes and fossils converge on placental mammal origins. EvoDevo 3, 18 (2012).
pubmed: 22883371 pmcid: 3472198
Lanier, H. C. & Olson, L. E. Inferring divergence times within pikas (Ochotona spp.) using mtDNA and relaxed molecular dating techniques. Mol. Phylogenet. Evol. 53, 1–12 (2009).
pubmed: 19501176
Ruedas, L. A., Mora, J. M. & Lanier, H. C. Evolution of lagomorphs. In Lagomorphs: Pikas, Rabbits, and Hares of the World 4–8 (John Hopkins University Press, 2018).
Asher, R. J. et al. Stem lagomorpha and the antiquity of glires. Science 307, 1091–1094 (2005).
pubmed: 15718468
Li, C., Meng, J. & Wang, Y. Dawsonolagus antiquus, A primitive lagomorph from the eocene arshanto formation, Nei Mongol, China. Bull. Carnegie Museum Nat. Hist. 39, 97–110 (2007).
Rose, K. D. et al. Early Eocene lagomorph (Mammalia) from Western India and the early diversification of Lagomorpha. Proc. R. Soc. B Biol. Sci. 275, 1203–1208 (2008).
Erbajeva, M., Flynn, L. J. & Alexeeva, N. Late Cenozoic Asian Ochotonidae: Taxonomic diversity, chronological distribution and biostratigraphy. Quat. Int. 355, 18–23 (2015).
Erbajeva, M. A., Mead, J. I., Alexeeva, N. V., Angelone, C. & Swift, S. L. Taxonomic diversity of Late Cenozoic Asian and North American ochotonids (an overview). Palaeontol. Electron. 14, 27 (2011).
López-Martinez, N. Evolution de la lignée d’Ochotonidés Piezadus-Prolagus dans le Cénozoïque d’Europe Sud-Occidentale (Univ. Sci. Tech. Languedoc, 1974).
López-Martínez, N. Revisión sistemática y bioestratigráfica de los lagomorfos (Mammalia) del Terciario y Cuaternario de España. Zaragoza. Memorias del Mus. Paleontológico la Univ. Zaragoza 343 (1989).
Lissovsky, A. A. Taxonomic revision of pika Ochotona (Lagomorpha, Mammalia) at the species level. Mammalia 78, 199–216 (2014).
Liu, S. J. et al. The phylogeny of the Anderson’s White-bellied Rat (Niviventer andersoni) based on complete mitochondrial genomes. Ecol. Evol. 12, e8663 (2022).
pubmed: 35261750 pmcid: 8890005
Bronstein, O., Kroh, A. & Haring, E. Mind the gap! the mitochondrial control region and its power as a phylogenetic marker in echinoids. BMC Evol. Biol. 18, 80 (2018).
pubmed: 29848319 pmcid: 5977486
Longin, R. New method of collagen extraction for radiocarbon dating. Nature 230, 241–242 (1971).
pubmed: 4926713
Beaumont, W., Beverly, R., Southon, J. & Taylor, R. E. Bone preparation at the KCCAMS laboratory. Nucl. Instrum. Methods Phys. Res. Sect. B Beam. Interact. Mater. Atoms. 268, 906–909 (2010).
Reimer, P. et al. The IntCal20 Northern Hemisphere radiocarbon age calibration curve (0–55 cal kBP). Radiocarbon 62, 725–757 (2020).
Cooper, A. & Poinar, H. N. Ancient DNA: Do it right or not at all. Science 289, 1139 (2000).
pubmed: 10970224
Cilli, E. Archaeogenetics, in Encyclopedia of Archaeology, 2nd ed. (eds. Nikita, E. & Rehren, T. H.) (Elsevier, 2023).
Llamas, B. et al. From the field to the laboratory: Controlling DNA contamination in human ancient DNA research in the high-throughput sequencing era. STAR Sci. Technol. Archaeol. Res. 3, 1–14 (2017).
Dabney, J. et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl. Acad. Sci. 110, 15758–15763 (2013).
pubmed: 24019490 pmcid: 3785785
Cilli, E. et al. A multifaceted approach towards investigating childbirth deaths in double burials: Anthropology, paleopathology and ancient DNA. J. Archaeol. Sci. 122, 105219 (2020).
Damgaard, P. B. et al. Improving access to endogenous DNA in ancient bones and teeth. Sci. Rep. 5, 11184 (2015).
pubmed: 26081994 pmcid: 4472031
Maricic, T., Whitten, M. & Pääbo, S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS ONE 5, e14004 (2010).
pubmed: 21103372 pmcid: 2982832
Kapp, J. D., Green, R. E. & Shapiro, B. A fast and efficient single-stranded genomic library preparation method optimized for ancient DNA. J. Hered. 112, 241–249 (2021).
pubmed: 33768239 pmcid: 8141684
Wingett, S. W. & Andrews, S. FastQ screen: A tool for multi-genome mapping and quality control. F1000Research 7, 1338 (2018).
pubmed: 30254741 pmcid: 6124377
Schubert, M. et al. Characterization of ancient and modern genomes by SNP detection and phylogenomic and metagenomic analysis using PALEOMIX. Nat. Protoc. 9, 1056–1082 (2014).
pubmed: 24722405
Peltzer, A. et al. EAGER: Efficient ancient genome reconstruction. Genome Biol. 17, 60 (2016).
pubmed: 27036623 pmcid: 4815194
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168 pmcid: 2705234
Jónsson, H., Ginolhac, A., Schubert, M., Johnson, P. L. F. & Orlando, L. mapDamage2.0: Fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29, 1682–1684 (2013).
pubmed: 23613487 pmcid: 3694634
Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24–26 (2011).
pubmed: 21221095 pmcid: 3346182
Conant, G. C. & Wolfe, K. H. GenomeVx: Simple web-based creation of editable circular chromosome maps. Bioinformatics 24, 861–862 (2008).
pubmed: 18227121
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547 (2018).
pubmed: 29722887 pmcid: 5967553
Matthee, C. A., Van Vuuren, B. J., Bell, D. & Robinson, T. J. A molecular supermatrix of the rabbits and hares (Leporidae) allows for the identification of five intercontinental exchanges during the Miocene. Syst. Biol. 53, 433–447 (2004).
pubmed: 15503672
Kozlov, A. M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. RAxML-NG: A fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35, 4453–4455 (2019).
pubmed: 31070718 pmcid: 6821337
Jukes, T. H. & Cantor, C. Evolution of Protein Molecules. In Mammalian Protein Metabolism. 21–132 (Academic Press, 1969).
Bouckaert, R. et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 15, e1006650 (2019).
pubmed: 30958812 pmcid: 6472827
Heled, J. & Drummond, A. J. Calibrated tree priors for relaxed phylogenetics and divergence time estimation. Syst. Biol. 61, 138–149 (2012).
pubmed: 21856631
Ge, D. et al. Did the expansion of C4 plants drive extinction and massive range contraction of micromammals? Inferences from food preference and historical biogeography of pikas. Palaeogeogr. Palaeoclimatol. Palaeoecol. 326–328, 160–171 (2012).
Tamura, K. et al. Estimating divergence times in large molecular phylogenies. Proc. Natl. Acad. Sci. U. S. A. 109, 19333–19338 (2012).
pubmed: 23129628 pmcid: 3511068
Tamura, K., Tao, Q. & Kumar, S. Theoretical foundation of the reltime method for estimating divergence times from variable evolutionary rates. Mol. Biol. Evol. 35, 1770–1782 (2018).
pubmed: 29893954 pmcid: 5995221
Tao, Q., Tamura, K., Mello, B. & Kumar, S. Reliable confidence intervals for reltime estimates of evolutionary divergence times. Mol. Biol. Evol. 37, 280–290 (2020).
pubmed: 31638157
Gradstein, F. M., Ogg, J. G., Smith, A. G., Bleeker, W. & Lourens, L. J. A new geologic time scale, with special reference to precambrian and neogene. Episodes 27, 83–100 (2004).

Auteurs

Valerio Joe Utzeri (VJ)

Department of Agricultural and Food Sciences, Division of Animal Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy. va.joe6@gmail.com.

Elisabetta Cilli (E)

Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, 48121, Ravenna, Italy. elisabetta.cilli@unibo.it.

Francesco Fontani (F)

Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, 48121, Ravenna, Italy.

Daniel Zoboli (D)

Department of Chemical and Geological Sciences, University of Cagliari, Cittadella Universitaria SS 554, 09042, Monserrato, Italy.

Massimiliano Orsini (M)

Laboratory of Microbial Ecology, Istituto Zooprofilattico Sperimentale delle Venezie, Viale dell'università 10, 35120, Legnaro, Italy.

Anisa Ribani (A)

Department of Agricultural and Food Sciences, Division of Animal Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy.

Adriana Latorre (A)

Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, 48121, Ravenna, Italy.

Andrey A Lissovsky (AA)

A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Moscow, Russia.

Gian Luigi Pillola (GL)

Department of Chemical and Geological Sciences, University of Cagliari, Cittadella Universitaria SS 554, 09042, Monserrato, Italy.

Samuele Bovo (S)

Department of Agricultural and Food Sciences, Division of Animal Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy.

Giorgio Gruppioni (G)

Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, 48121, Ravenna, Italy.

Donata Luiselli (D)

Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, 48121, Ravenna, Italy.

Luca Fontanesi (L)

Department of Agricultural and Food Sciences, Division of Animal Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy. luca.fontanesi@unibo.it.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH