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Evolution of River Dolphins University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Publications, Agencies and Staff of the U.S. Department of Commerce U.S. Department of Commerce 3-7-2001 Evolution of river dolphins Healy Hamilton Susana Caballero Allen G. Collins Robert L. Brownell Jr. NOAA, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/usdeptcommercepub Part of the Environmental Sciences Commons Hamilton, Healy; Caballero, Susana; Collins, Allen G.; and Brownell, Robert L. Jr., "Evolution of river dolphins" (2001). Publications, Agencies and Staff of the U.S. Department of Commerce. 111. https://digitalcommons.unl.edu/usdeptcommercepub/111 This Article is brought to you for free and open access by the U.S. Department of Commerce at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Publications, Agencies and Staff of the U.S. Department of Commerce by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Proceedings: Biological Sciences, Vol. 268, No. 1466 (Mar. 7, 2001), pp. 549-556 B THE ROYAL doi 10.1098/rspb.2000.1385 92 SOCIETY Evolution of river dolphins Healy E{amiltonltsSusana Caballero2,Allen G. Coll;nsl and Robert L. BrownellJr3 lMuseumof Paleontologyand Department of IntegrativeBiology, University of California,Berkeley, CA 94720, USA 2FundacionSubarta, Carrara 24Foeste, no 3-110,Cali, Colombia 3SouthwestFisheries Science Center, PO Box 271,La jrolla, CA 92038, USA The world's river dolphins (Inia, Pontoporia,Lipotes and Platanista)are among the least known and most endangered of all cetaceans. The four extant genera inhabit geographically disjunct river systems and exhibit highly modified morphologies, leading many cetologists to regard river dolphins as an unnatural group. Numerous arrangements have been proposed for their phylogenetic relationships to one another and to other odontocete cetaceans. These alternative views strongly aXect the biogeographical and evolu- tionary implications raised by the important, although limited, fossil record of river dolphins. We present a hypothesis of river dolphin relationshipsbased on phylogenetic analysis of three mitochondrial genes for 29 cetacean species, concluding that the four genera representthree separate, ancient branches in odonto- cete evolution. Our molecular phylogeny correspondswell with the first fossil appearances of the primary lineages of modern odontocetes. Integrating relevant events inTertiary palaeoceanography,we develop a scenario for river dolphin evolution during the globally high sea levels of the Middle Miocene. We suggest that ancestorsof the four extant river dolphin lineages colonized the shallow epicontinental seas that inun- dated the Amazon, Parana, Yangtze and Indo-Gangetic river basins, subsequently remaining in these extensive waterways during their transition to freshwater with the Late Neogene trend of sea-level lowering. Keywords: Cetacea; fossil; phylogeny; Odontoceti; Miocene; epicontinental seas long, independent evolutionary histories. River dolphins 1. INTRODUCTION are highly modified taxa that have more autapomorphies Four genera of toothed cetaceans comprise the peculiar than shared characters useful for determining their and poorly known 'river dolphins'. Although several affiliations (Messenger 1994). Furthermore,river dolphin marine delphinids are commonly found in rivers quite far classifications have often assumed monophyly (Simpson upstream, river dolphins are morphologically and phylo- 1945; Kasuya 1973;Zhou 1982), although some characters genetically distinct from marine dolphins and most are used to unite river dolphins, such as an elongate rostrum restricted to freshwaterecosystems. Since the first sugges- and mandibular symphysis, may be primitive for odonto- tions of their affinities were advanced in the l9th century cete cetaceans. When exisiting taxa are few and so (Gray 1863; Flower 1867), the evolutionary relationship of distinctly modified that homologous characters are diffi- river dolphins to one another and to other odontocetes cult to detect, the fossil record of the group should play has remained controversial (Simpson 1945; Kasuya 1973; an important role in resolving taxonomic relationships Zhou 1982; Muizon 1984, 1988a; Fordyce & Barnes 1994; (Gauthier etal. 1988). Messenger 1994; Rice 1998). Despite diXering in detail, There are various fossil taxa related to extant genera, recent morphological systematic studies of modern and with the exception of Lipotes.Unfortunately, the record is fossil taxa ( Muizon 1988a,c, 1994; Heyning 1989; not yet complete enough to determine key character pola- Messenger & McGuire 1998) largely corroboratedearlier rities at intermediate stages. The fossil history of river views that each extant lineage is relatively ancient and dolphins has a long and confusing treatment in the that river dolphins comprise an unnatural group. Non- literature, with many fossils described as members of monophyly of river dolphins is consistent with their taxonomic groups no longer recognized; a comprehensive highly disjunct geographical distributions (figure 1): the re-examination is needed. A robust hypothesis of the Amazon river dolphin, Inia geoffrensis,and the La Plata relationships among extant lineages is critical for river dolphin, Pontoporiablainvillei, are found in South exploring the biogeographical and evolutionary implica- America; the Yangtze river dolphin, Lipotesvexillifer, and tions of river dolphin fossils. Indian river dolphin, Platanistagangetica, inhabit rivers on Higher-level molecular phylogenetic studies of ceta- opposite sides of continental Asia. Placing the four river ceans have primarily focused on the relationship between dolphin lineages within the evolutionary tree of cetaceans cetaceans and artiodactyls (Graur & Higgins 1994; can help resolve the confused state of odontocete beta Montelgard et al. 1997) and on the hypothesis of odonto- taxonomy (Heyning 1989; Fordyce et al. 1985; Fordyce & cete paraphyly (Milinkovitch et al. 1993; Hasegawa et al. Barnes 1994; figure 2) and refine our understanding of 1997; Messenger & McGuire 1998). River dolphins were odontocete evolution. discussed in Arnason & Gullberg's (1996) cytochrome b The difficulties of confronting river dolphin systematics phylogeny of cetaceans, which provided additional using morphological analyses may relate directly to their evidence for a distinct, though unresolved, position for Platanista.Two recent studies have specifically addressed river dolphin phylogeny using DNA sequence analysis. *Authorfor correspondence (heals(socrates.berkeley.edu). Yang & Zhou (1999) were the first to include all four Proc.R. Soc.Lond. B (2001)268, 54>556 :549 <) 2001 The Royal Society Received4 October 2000 Accepted24 October2000 8 broadlyapproachriver fromdolphinshas within beenin everytheto epicontinental sampleprimary bothlineage extensivelyseas of ofodontocete. the Middleand 550 H. Hamilton and others Evolutionofriverdolphins With problematicphylogenies, for which odontocetes {mboldtlana certainlyqualify, it maybe moreuseful to add taxa rather than to add characters(Hillis 1996;Graybeal 1998). Our :) Our objective is to reconstruct the evolutionary F history of river dolphins.We begin by presentinga I [ t hypothesis of the phylogeneticrelationships of extant < Inia river dolphinsbased on a multiplemitochondrial gene } geoffrensisJ phylogeny of 29 species of cetaceans. We consider l geoffrensif biogeographicaland stratigraphicalaspects of the fossil r ( z^/ recordof river dolphinsin relationto our phylogenetic ensis | hypothesis.Integrating the palaeontologicaldata with : knownevents inTertiary palaeoceanography, we conclude ,/- with a detailedscenario for the evolutionof the world's / Miocene. / 2. MATERIALAND METHODS Pontoporiablainvillei - Our data set is comprisedof the complete cytochromeb (1140bp),partial 12S (385bp), and partial 16S (530bp) mito- - - chondrialgenes, for 29 speciesbroadly representative of each primarylineage of odontocete.In additionto sequencesavail- able from previousstudies of cetacean molecularsystematics (Milinkovitchet al. 1994; Arnason & Gullberg1996; LeDuc et al. 1999),we sequencedeither the ribosomalgene fragments and/or the completecytochrome b for non-overlappingtaxa. In all, we generated 44 new sequences (GenBank accession numbersAF334482-AF334525). We analysedsequences of Inia of knownprovenance from Brazil,Peru and Bolivia,as well as Inia from GenBank (accessionnumber X92534; Arnason & Gullberg1996), in order to evaluatethe suggestionthat the Bolivian form, Inia geoXrensisboliviensis, is distinct from Inia geoXrensisgeoXrensis (da Silva 1994; Pilleri & Gihr 1977).The partial12S sequence for Lipotesvexillifer was not availablefor this analysis.The mysticeteoutgroup consists of four speciesfrom three families.The taxa in this study, with tissue source, scientificand common names, are listed at the archivedweb pages of the Universityof CaliforniaMuseum of Paleontology (www.ucmp.berkeley.edu/archdata/ HamiltonetalOl/river. html), as are the primersequences, gene sequences,and data set align- ments. Figure1. Geographicaldistribution of extant riverdolphins. Samples were obtained either by biopsy darting, from (a) IniageoXrensis humboldtiana inhabits the OrinocoRiver museumspecimens, or fromthe GeneticsTissue Archive, South- system.I.g. geoXrensis is found throughout the mainstem west FisheriesScience Center,LaJolla, CA, USA. DNA was AmazonRiver and its tributaries.I.g. boliviensisoccurs
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