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A Supermatrix Analysis of Genomic, Morphological, and Paleontological Data from Crown Cetacea

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A Supermatrix Analysis of Genomic, Morphological, and Paleontological Data from Crown Cetacea UC Riverside UC Riverside Previously Published Works Title A supermatrix analysis of genomic, morphological, and paleontological data from crown Cetacea Permalink https://escholarship.org/uc/item/5qp747jj Journal BMC Evolutionary Biology, 11(1) ISSN 1471-2148 Authors Geisler, Jonathan H McGowen, Michael R Yang, Guang et al. Publication Date 2011-04-25 DOI http://dx.doi.org/10.1186/1471-2148-11-112 Supplemental Material https://escholarship.org/uc/item/5qp747jj#supplemental Peer reviewed eScholarship.org Powered by the California Digital Library University of California Geisler et al. BMC Evolutionary Biology 2011, 11:112 http://www.biomedcentral.com/1471-2148/11/112 RESEARCHARTICLE Open Access A supermatrix analysis of genomic, morphological, and paleontological data from crown Cetacea Jonathan H Geisler1*, Michael R McGowen2,3, Guang Yang4 and John Gatesy2 Abstract Background: Cetacea (dolphins, porpoises, and whales) is a clade of aquatic species that includes the most massive, deepest diving, and largest brained mammals. Understanding the temporal pattern of diversification in the group as well as the evolution of cetacean anatomy and behavior requires a robust and well-resolved phylogenetic hypothesis. Although a large body of molecular data has accumulated over the past 20 years, DNA sequences of cetaceans have not been directly integrated with the rich, cetacean fossil record to reconcile discrepancies among molecular and morphological characters. Results: We combined new nuclear DNA sequences, including segments of six genes (~2800 basepairs) from the functionally extinct Yangtze River dolphin, with an expanded morphological matrix and published genomic data. Diverse analyses of these data resolved the relationships of 74 taxa that represent all extant families and 11 extinct families of Cetacea. The resulting supermatrix (61,155 characters) and its sub-partitions were analyzed using parsimony methods. Bayesian and maximum likelihood (ML) searches were conducted on the molecular partition, and a molecular scaffold obtained from these searches was used to constrain a parsimony search of the morphological partition. Based on analysis of the supermatrix and model-based analyses of the molecular partition, we found overwhelming support for 15 extant clades. When extinct taxa are included, we recovered trees that are significantly correlated with the fossil record. These trees were used to reconstruct the timing of cetacean diversification and the evolution of characters shared by “river dolphins,” a non-monophyletic set of species according to all of our phylogenetic analyses. Conclusions: The parsimony analysis of the supermatrix and the analysis of morphology constrained to fit the ML/ Bayesian molecular tree yielded broadly congruent phylogenetic hypotheses. In trees from both analyses, all Oligocene taxa included in our study fell outside crown Mysticeti and crown Odontoceti, suggesting that these two clades radiated in the late Oligocene or later, contra some recent molecular clock studies. Our trees also imply that many character states shared by river dolphins evolved in their oceanic ancestors, contradicting the hypothesis that these characters are convergent adaptations to fluvial habitats. Background the amount of molecular data published on cetaceans It has been 12 years since the publication of Messenger has increased by more than two orders of magnitude, and McGuire [1], the first major effort to develop a phy- the number of relevant morphological characters has logenetic hypothesis for crown Cetacea (Neoceti) based increased ~50%, while advances in computer applica- on a combined phylogenetic analysis of morphological tions and analytical methods now enable large-scale and molecular characters (Figure 1A). Since that time, phylogenetic analyses that could not be completed in 1998. Although the Messenger and McGuire [1] study was groundbreaking, some of their morphological char- * Correspondence: [email protected] 1Department of Anatomy, New York College of Osteopathic Medicine, New acters and observations have been disputed [2]. In addi- York Institute of Technology, Northern Boulevard, Old Westbury, NY,11568, tion, the only extinct cetacean included in their study USA was a composite outgroup taxon, Archaeoceti, despite Full list of author information is available at the end of the article © 2011 Geisler et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Geisler et al. BMC Evolutionary Biology 2011, 11:112 Page 2 of 33 http://www.biomedcentral.com/1471-2148/11/112 Delphinidae Delphinidae Phocoenidae Phocoenidae Phocoenidae Monodontidae 4 Monodontidae Monodontidae Delphinidae 3 Iniidae 3 Iniidae Iniidae 5 5 3 5 Pontoporiidae 6 7 Pontoporiidae Pontoporiidae 2 Lipotidae Lipotidae 1 Lipotidae 1 1 Ziphiidae Ziphiidae Platanistidae 8 Ziphiidae Platanistidae Platanistidae Physeteridae Physeteridae Physeteridae Kogiidae Kogiidae Kogiidae A) Messenger and McGuire 1998 B) Price et al. 2005 C) McGowen et al. 2009 P: morphology+3 mt genes MRP: 201 source trees P: 45 nu genes+mt genome+SINEs+morphology Delphinidae Iniidae Delphinidae Pontoporiidae Phocoenidae 9 Phocoenidae Monodontidae Lipotidae Monodontidae 3 4 Iniidae Platanistidae Iniidae 3 5 Delphinidae 3 2 7 Pontoporiidae Pontoporiidae Lipotidae 1 Phocoenidae 2 Lipotidae 1 Platanistidae Monodontidae Platanistidae Ziphiidae Ziphiidae Physeteridae Physeteridae Physeteridae Kogiidae Kogiidae Kogiidae Ziphiidae D) Heyning 1989, 1997 E) Barnes 1990 F) Muizon 1987, 1988, 1991 P: morphology None: morphology None: morphology Physeteridae Iniidae Delphinidae 5 Pontoporiidae 9 Lipotidae Kogiidae Lipotidae 3 Platanistidae Ziphiidae 2 Pontoporiidae Delphinidae 2 1 Platanistidae Delphinidae Phocoenidae 4 Monodontidae Ziphiidae Pontoporiidae Physeteridae Physeteridae Kogiidae Platanistidae Ziphiidae Kogiidae G) Fordyce 1994 H) Geisler and Sanders 2003 I) Lambert 2005 P: morphology P: morphology P: morphology Phocoenidae Phocoenidae Phocoenidae Monodontidae Monodontidae Monodontidae Delphinidae 4 Delphinidae 4 Delphinidae 3 Iniidae Iniidae Iniidae 5 5 3 5 3 2 7 Pontoporiidae Pontoporiidae Pontoporiidae Lipotidae 6 Lipotidae 1 Lipotidae 1 Platanistidae 1 Ziphiidae Ziphiidae 8 Ziphiidae Platanistidae Platanistidae Physeteridae Physeteridae Physeteridae Kogiidae Kogiidae Kogiidae J) Yang and Zhou 1999 K) Cassens et al. 2000 L) Cassens et al. 2000 NJ: 1 mt gene - *odontocete paraphyly NJ: 2 nu+3 mt genes ML: 2 nu+3 mt genes Phocoenidae Delphinidae Delphinidae Monodontidae Phocoenidae Phocoenidae 4 Delphinidae 4 Monodontidae Monodontidae Iniidae Iniidae 3 Iniidae 5 5 3 5 3 Pontoporiidae Pontoporiidae 6 Pontoporiidae Lipotidae 6 Lipotidae Lipotidae Physeteridae 1 Ziphiidae 1 Ziphiidae Kogiidae Platanistidae Platanistidae Ziphiidae Physeteridae Physeteridae 8 Platanistidae Kogiidae Kogiidae M) Cassens et al. 2000 N) Hamilton et al. 2001 O) Nikaido et al. 2001 P: 2 nu+3 mt genes ML, P: 3 mt genes P: SINEs Figure 1 Previous hypotheses that position extant river dolphins, including Pontoporia, relative to other living odontocete lineages. Continued in Figure 2. Topologies based on combined analysis of morphology and molecules (A-C), morphology (D-I), and molecules (J-O) are shown. River dolphin lineages are colored red, and other branches are blue. Groupings that are commonly replicated in the various trees are labeled 1-9. For each topology, the following are shown: authors, date of publication, mode of analysis (P = parsimony, ML = maximum likelihood, NJ = neighbor joining distance, Bayes = Bayesian analysis, MRP = matrix representation with parsimony supertree, none = tree constructed manually), and data examined (morphology, mitochondrial [mt] genes, nuclear [nu] genes, mt genomes, source trees = published topologies used as input for MRP, SINEs = insertions of short interspersed nu elements). In the analysis of Yang and Zhou [12], Odontoceti was not supported as monophyletic (J). Geisler et al. BMC Evolutionary Biology 2011, 11:112 Page 3 of 33 http://www.biomedcentral.com/1471-2148/11/112 Phocoenidae Delphinidae Phocoenidae Monodontidae Monodontidae Monodontidae Delphinidae Delphinidae 3 4 Phocoenidae 3 Iniidae 5 5 Iniidae Iniidae 2 7 Pontoporiidae 6 7 Pontoporiidae 5 3 Pontoporiidae Lipotidae Lipotidae 1 1 6 Lipotidae Platanistidae Ziphiidae Ziphiidae Platanistidae Ziphiidae Physeteridae Physeteridae Platanistidae Kogiidae P) Nikaido et al. 2001 Q) Yang et al. 2002 R) Yan et al. 2005 ML: 12 nu genes ML, P, NJ: 1 mt gene Bayes, P: mt genome (AAs) Phocoenidae Phocoenidae Phocoenidae Monodontidae Monodontidae Monodontidae Delphinidae Delphinidae Delphinidae 3 Iniidae 3 Iniidae 3 Iniidae 5 5 5 7 Pontoporiidae 7 Pontoporiidae 2 7 Pontoporiidae 1 2 Lipotidae Lipotidae Lipotidae 1 1 8 Ziphiidae Platanistidae Platanistidae Platanistidae Ziphiidae Ziphiidae Physeteridae Physeteridae Physeteridae Kogiidae Kogiidae Kogiidae S) Yan et al. 2005 T) May-Collado and Agnarsson 2006 U) Agnarsson and May-Collado 2008 Bayes, ML: mt genome Bayes: 1 mt gene Bayes: 1 mt gene Phocoenidae Phocoenidae Phocoenidae Monodontidae Monodontidae Monodontidae Delphinidae Delphinidae 33 Delphinidae Iniidae Iniidae 3 5 5 Iniidae Pontoporiidae 5 667 Pontoporiidae 7 Pontoporiidae Lipotidae Lipotidae 6 7 1 1 Lipotidae Ziphiidae Ziphiidae 1 Platanistidae Platanistidae
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