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3-7-2001
Evolution of river dolphins
Healy Hamilton
Susana Caballero
Allen G. Collins
Robert Brownell, Jr.
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Proceedings: Biological Sciences, Vol. 268, No. 1466 (Mar. 7, 2001), pp. 549-556
B
92
doi
THE ROYAL
SOCIETY
10.1098/rspb.2000.1385
Evolution of river dolphins
Healy E{amiltonltsSusana Caballero2,Allen G. Coll;nsl and Robert L. BrownellJr3
CA94720, USA
of California,Berkeley,
Biology,University
of Integrative
andDepartment
lMuseumof Paleontology
24Foeste,no3-110,Cali,Colombia
Subarta,Carrara
2Fundacion
POBox 271,Lajrolla,CA92038, USA
FisheriesScienceCenter,
3Southwest
Lipotesand Platanista)are among the least known and most
The world's river dolphins (Inia,Pontoporia,
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 evolutionary 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 branchesin odontocete evolution. Our molecular phylogeny correspondswell with the first fossil appearancesof 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 inundated 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
1. INTRODUCTION
Four genera of toothed cetaceans comprise the peculiar
and poorly known 'river dolphins'. Although several
marine delphinids are commonly found in rivers quite far
upstream, river dolphins are morphologically and phylogenetically distinct from marine dolphins and most are
restricted to freshwaterecosystems. Since the first suggestions of their affinities were advanced in the l9th century
(Gray 1863; Flower 1867), the evolutionary relationship of
river dolphins to one another and to other odontocetes
has remained controversial (Simpson 1945; Kasuya 1973;
Zhou 1982; Muizon 1984, 1988a; Fordyce & Barnes 1994;
Messenger 1994; Rice 1998). Despite diXering in detail,
recent morphological systematic studies of modern and
fossil taxa (Muizon 1988a,c, 1994; Heyning 1989;
Messenger & McGuire 1998) largely corroboratedearlier
views that each extant lineage is relatively ancient and
that river dolphins comprise an unnatural group. Nonmonophyly of river dolphins is consistent with their
highly disjunct geographical distributions (figure 1): the
Amazon river dolphin, Inia geoffrensis,and the La Plata
river dolphin, Pontoporiablainvillei,are found in South
America; the Yangtze river dolphin, Lipotesvexillifer,and
Indian river dolphin, Platanistagangetica,inhabit rivers on
opposite sides of continental Asia. Placing the four river
dolphin lineages within the evolutionary tree of cetaceans
can help resolve the confused state of odontocete beta
taxonomy (Heyning 1989; Fordyce et al. 1985; Fordyce &
Barnes 1994; figure 2) and refine our understanding of
odontocete evolution.
The difficulties of confronting river dolphin systematics
using morphological analyses may relate directly to their
(heals(socrates.berkeley.edu).
*Authorforcorrespondence
Proc.R. Soc.Lond.B (2001)268, 54>556
24 October2000
4 October2000 Accepted
Received
long, independent evolutionary histories. River dolphins
are highly modified taxa that have more autapomorphies
than shared characters useful for determining their
affiliations (Messenger 1994). Furthermore,river dolphin
classifications have often assumed monophyly (Simpson
1945; Kasuya 1973;Zhou 1982), although some characters
used to unite river dolphins, such as an elongate rostrum
and mandibular symphysis, may be primitive for odontocete cetaceans. When exisiting taxa are few and so
distinctly modified that homologous characters are difficult to detect, the fossil record of the group should play
an important role in resolving taxonomic relationships
(Gauthier etal. 1988).
There are various fossil taxa related to extant genera,
Unfortunately,the record is
with the exception of Lipotes.
not yet complete enough to determine key character polarities at intermediate stages. The fossil history of river
dolphins has a long and confusing treatment in the
literature, with many fossils described as members of
taxonomic groups no longer recognized; a comprehensive
re-examination is needed. A robust hypothesis of the
relationships among extant lineages is critical for
exploring the biogeographical and evolutionary implications of river dolphin fossils.
Higher-level molecular phylogenetic studies of cetaceans have primarily focused on the relationshipbetween
cetaceans and artiodactyls (Graur & Higgins 1994;
Montelgard et al. 1997) and on the hypothesis of odontocete paraphyly (Milinkovitch et al. 1993; Hasegawa et al.
1997; Messenger & McGuire 1998). River dolphins were
discussed in Arnason & Gullberg's (1996) cytochrome b
phylogeny of cetaceans, which provided additional
evidence for a distinct, though unresolved, position for
Two recent studies have specifically addressed
Platanista.
river dolphin phylogeny using DNA sequence analysis.
Yang & Zhou (1999) were the first to include all four
:549
This article is a U.S. government work, and is not subject to copyright in the United States.
<) 2001 The Royal Society
broadly
approach
river from
dolphins
haswithin
been
in every
the
to epicontinental
sample
primary both
lineageextensively
seas of ofodontocete.
the Middle
and
8
550 H. Hamilton and others Evolution
ofriverdolphins
With problematicphylogenies,for which odontocetes
certainlyqualify,it maybe moreusefulto add taxa rather
{mboldtlana
than to add characters(Hillis 1996;Graybeal1998).Our
:)
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l
r
(
ensis
Inia
geoffrensisJ
geoffrensif
z^/
|
:
,/-
Miocene.
/
/
Our objective is to reconstruct the evolutionary
history of river dolphins.We begin by presentinga
hypothesisof the phylogeneticrelationshipsof extant
river dolphinsbased on a multiplemitochondrialgene
phylogeny of 29 species of cetaceans. We consider
biogeographicaland stratigraphicalaspectsof the fossil
recordof river dolphinsin relationto our phylogenetic
hypothesis.Integratingthe palaeontologicaldata with
knowneventsinTertiarypalaeoceanography,
we conclude
with a detailedscenariofor the evolutionof the world's
Pontoporiablainvillei
-
2. MATERIAL
ANDMETHODS
Our data set is comprisedof the completecytochromeb
(1140bp),partial 12S (385bp), and partial16S (530bp) mitochondrialgenes, for 29 speciesbroadlyrepresentative
of each
primarylineageof odontocete.In additionto sequencesavailable from previousstudiesof cetacean molecularsystematics
(Milinkovitchet al. 1994;Arnason& Gullberg1996;LeDuc
et al. 1999),we sequencedeitherthe ribosomalgene fragments
and/orthe completecytochromeb for non-overlapping
taxa. In
all, we generated 44 new sequences (GenBank accession
numbersAF334482-AF334525).
We analysedsequencesof Inia
of knownprovenancefromBrazil,Peruand Bolivia,as well as
Inia from GenBank(accessionnumberX92534; Arnason &
Gullberg1996), in order to evaluatethe suggestionthat the
Bolivian form, Inia geoXrensis
boliviensis,
is distinct from Inia
geoXrensis
geoXrensis
(da Silva 1994; Pilleri & Gihr 1977).The
partial12SsequenceforLipotes
vexillifer
was not availableforthis
analysis.The mysticeteoutgroupconsistsof four speciesfrom
three families.The taxa in this study, with tissue source,
scientificand commonnames,are listed at the archivedweb
pagesof the Universityof CaliforniaMuseumof Paleontology
(www.ucmp.
berkeley.edu/archdata/
HamiltonetalOl/river.
html),
as are the primersequences,gene sequences,and dataset alignments.
Figure1. Geographicaldistributionof extantriverdolphins.
Samples were obtained either by biopsy darting, from
(a) IniageoXrensis
humboldtiana
inhabitsthe OrinocoRiver
museumspecimens,or fromthe GeneticsTissueArchive,Southsystem.I.g.geoXrensis
is foundthroughoutthe mainstem
west FisheriesScienceCenter,LaJolla, CA, USA. DNA was
AmazonRiverand its tributaries.I.g.boliviensis
occursin the
extractedby standardphenol-chloroform/ethanol
precipitation
Amazontributariesof easternBolivia,geographicallyisolated
or with the QIAamp DNA extraction kit (Qiagen, Inc.,
by severalhundredkilometresof rapids.Pontoporia
blainvillei
is
restrictedto coastalSouthAtlanticwaters.(b) Lipotesvexillifer Valencia,CA, USA). After an initial 2 min denaturationat
94 °C, PCRconsistedof 35 cycles,30 s at 94 °C, 45 s at 48-52°C
is an extremelyendangeredriverdolphinthat occursonly in
the lowerand middlereachesof the YangtzeRiver.Platanista and 90s at 72°C. The productswere visualized,cleanedand
minorinhabitsthe IndusRiversystem.P. gangetica
is foundin
directlysequencedin both directionson an ABI 377 automated
the Ganges-Brahmaputra
Riversystem.
DNA sequencer(AppliedBiosystems,FosterCity, CA, USA).
Sequenceswereeditedwith Sequencherv. 3.0 sequenceanalysis
riverdolphintaxa in a molecularphylogeneticanalysis, software(GeneCodesCorporation,Ann Arbor,MI, USA) and
but their limiteddata set of only 307 base pairs (bp) of aligned manuallyin BioEdit4.7.8 (Tom Hall). Four sites of
the cytochromeb gene is insufficientto addressthe phylo- ambiguousalignmentin the 16Sgenewereexcluded.
All phylogenetic
analyseswerecarriedout usingPAUP4.0b3a
geny of deeplydivergingtaxa. In contrast,the molecular
phylogenyof Cassenset al. (2000) analysesfive genesfor (Swofford2000).Treesearcheswereconductedwith optimality
19 cetaceanspecies,both nuclearand mitochondrial,yet criteriaof parsimonyandmaximumlikelihood.Twentyreplicate
even this largedata set resultsin low bootstrapvaluesfor searchesweremadefor the maximum-likelihood
tree,assuming
key nodesin riverdolphinphylogeny,particularlyunder the HKY85modelof nucleotideevolution(Hasegawaetal. 1985)
(Ti:Tv)ratioof 6.0 anda gamma
the maximum-likelihood
criterionof molecularevolution. witha transitionto transversion
-
Proc.R. Soc.Lond.B (2001)
-
_
Pontoporiidae
Delphinidae
| _
|
Monodontidae
* Delphinidae
Monodontidae
Pontoporiidae
H. Hamiltonandothers 551
ofriverdolphins
Evolution
morphologyof extanttaxa
morphologywithfossil taxa
(e)
(c)
(a)
-
[
molecularsequences
|
Physeteridae
Platanistidae
Physeteridae
Ziphiidae
Physeteridae
Ziphiidae
Squalodontidaet
LX
r-{platanistid
Squalodelphidaet
t
Eurhinodelphidae
Lipotidae
Iniidae
_
_ _
_
Platanistidae
|
_
Physeteridae
SZiphudae
r
_
E
.
_
g
7
..
Imldae
Pontoporiidae
r
|
te
Phocoenidae
Phocoenidae
Delphinidae
Delphinidae
Physeteridae
(f)
Ziphiidae
l l
g
Pontoporiidae
Monodontidae |
Kentnodontidaet
l
Phocoenidae
_
I
=
Mysticeti
L
Physeteridae
Ziphiidae
Platanistidae
.
Lipotidae
Iniidae
|
Squalodelphidaet | '1
_
Platanistidae
Pontoporiidae
_
Iniidae
Lipotidae
_
Monodontidae
Phocoenidae
-
Pontoporiidae
-Monodontidae
-Phocoenidae
Delphinidae
.b}
Ziphiidae
| |
Lipotidae
Iniidae
Platanistidae
Delphinoidea
e
u
H
g
1
-r
Llpotldae
Iniidae
Figure2. Alternativehypothesesof odontocetephylogeny.Someendingshave been emendedto standardizetaxonomic
comparisons.(a) Muizon(1988a,1991), (b) Barnes(1990);(c) Heyning(1989), (d) Messenger& McGuire(1998); (e) Arnason
& Gullberg(1996), (G)Yang & Zhou (1999).
shapeparameterof 0.2.The assumedratioof Ti:Tvandthe shape porpoises,monodontidsand moderndolphins,essentially
rateswereestimatedunderthe
Muizon'sconceptof the InfraorderDelphinida(Muizon
of the distributionof substitution
criterionof likelihoodusing trees obtainedby both neighbour 1988a, 1991).In both analyses,beakedwhales compose
joining and unweightedparsimony.Parsimonysearches(with the sistergroupto Delphinida(Heyning1989). The data
riverdolphinsare the extant
1000 replicates)were carriedout with a range of differential indicatethat non-platanistid
of early lineagesthat divergedfrom the
weightingto assess the impact of these correctionson tree representatives
topology.Twobootstrapanalyseswereperformed,one with trees stem leading to Delphinoidea(porpoises,monodontids
found by neighbourjoining (with Jukes-Cantor corrected and dolphins), supporting their ranking as separate
distances)andonewithtreesobtainedusingweightedparsimony families. Our analysis suggestsInia and Pontoporiaare
Finally, monophyleticand together form the sister group of
countingsix timesas muchas transitions).
(transversions
Delphinoidea(Muizon 1984), and suggestsa distinction
supportindiceswere calculatedfor each node presentin the
weightedparsimonyanalysis(Bremer1988).
betweenthe Bolivianand Amazonformsof Inia. The two
3. RESULTS
The maximum-likelihoodtree and the consensusof
three most parsimonioustrees are largely congruent
(figure3). The Physeteridae,representedby Physeterand
Kogia,are basalodontocetesand do not forma cladewith
Ziphiidae,the beakedwhales,contradictingsomeclassifications (Fordyce1994;Muizon1991).The long-suspected
polyphylyof riverdolphinsis supportedby the mitochondrial sequencedata. In both trees,Platanistagangeticaand
Platanistaminor,representingPlatanistidae,are sister to
the remainingodontocetes,althoughbootstrapsupport
for this node is low. The remainingriver dolphintaxa
arranged
are paraphyletically
(Litotes,Inia and Pontoporia)
at the base of a well-supportedclade that also includes
Proc.R. Soc.Lond.B (2001)
analysesyield contradictinghypothesesfor the relationtree
shipswithinDelphinoidea.The maximum-likelihood
indicates that porpoises and marine dolphins form a
clade, while the weighted parsimony tree groups
porpoiseswith monodontids,a view recentlyadvanced
(Waddellet al. 2000).
4. DISCUSSION
The phylogenetic relationships of river dolphins
suggestedbyouranalysisallowsfora refinedunderstanding
of odontocetesystematicsand evolution,a long-elusive
goal. Just as the extensiveadaptationsinvolvedin the
transitionfrom land mammalto aquaticmammalhave
obscured cetacean origins, each primary odontocete
lineage exhibits a suite of highly derived characters
552 H. Hamiltonandothers Evolution
ofriverdolphins
(a)
(b)
Balaena mysticetus
Eschrichtiusrobustus
Balaenopteraphysalus
Megapteranovaeangliae
Physeter catodon
Kogia breviceps
Kogia simus
Plal;anistagangetica
Platanista minor
Berardiusbairdii
Tasmacetusshepardii
Ziphiuscavirostris
Mesoplodonbidens
Mesoplodoneuropaeus
Lipotes vexillifer
Pontopona blvinvillei
lnia geoffrensis boliviensis
Inia geoffrensis-GenBanl
Inia geoffrensis-Brazfl
Inia geoffrensis-Peru
Delphinapterusleucas
Monodonmonoceros
Neophocoenaphocoenoides
Phocoena phocoena
Lagenorhynchusalbirostris
Sousa chinensis
Steno bredanensis
Lagenorhynchusobscurus
Lissodelphisborealis
Orca orca
Pseudorca crassidens
Figure3. Optimaltreesunderthe criteriaof (a) maximumlikelihoodand (b) parsimony.The maximum-likelihood
treewas
obtainedby carryingout 20 replicateheuristicsearches,assumingthe HKY85modelof nucleotideevolutionwith a transitionto
transversionratioof 6.0 and a gammashapeparameterof 0.2. Bootstrapvalues (derivedfrom 1000replicatesof neighbourjoiningsearchesusingJukesWantorcorrecteddistances)are shownat the nodes.Valuesless than 50 are denotedby ' < '. The
tree to the rightis the consensusof threemostparsimonioustreesof length5416 foundwith 1000replicateheuristicsearches.
Transversions
wereweightedsix timesas heavilyas transitions.Aboveeach node are parsimonybootstrapvalues ( 1000
replicates)and Bremersupportindices,separatedby a verticalbar. The rangeof transitionto transversionweighting(fromequal
to ten times,as well as transversions
only, denotedby an asterisk)that yieldseach cladeis reportedbeloweach corresponding
node. The GenBankaccessionnumberfor 'Inia-GenBank'
is X92534 (Arnason& Gullberg1996).
without clear evidence of sequential forms. Thus alpha
taxonomic assignments are considerablyless controversial
than higher-level systematics. River dolphins provide an
extreme example. Although the generic designations are
not disputed, their taxonomic ranks are undecided, and
many possible combinations of their interrelationship
have been proposed (figure 2). Similarly, the phylogenetic
affinities of the remaining odontocete lineages are also
unresolved (Heyning 1989; Rice 1998). The placement of
the river dolphins among these lineages, as indicated by
our molecular analysis, suggests a resolution that is
notably concordant with the first appearance of these
groups in the fossil record (figure 4).
(a) Thefossil record oSriver dolphins
The fossil record of pelagic animals is understandably
limited. Fossil cetaceans are primarily recovered from
rocks that formed in nearshore and continental-shelf
depositional environments, and only rarely from deep-sea
Proc.R. Soc.Lond.B (2001)
settings.Duringepisodesof low sea level, nearshoresediments are eroded, abridgingthe record.Archaicforms
disappearand more advancedgroupsemergein successive waves with no clear origins. Many fossil cetaceans
are known from single specimens,numeroustaxa have
beenerectedon the basisof undiagnostic,isolatedor fragmentarybones, and the classificationhistoryof extinct
cetaceansis long and bewildering.A confidentgrasp of
modernphylogenywill help clarify the relationshipsof
pastto presenttaxa.
Extincttaxa assignedto the Platanistidae
arewell documented, particularlyZarhachisand Pomatodelphis,
longbeaked Middle to Late Miocene cetaceans recovered
primarilyfromshallowepicontinentalsea depositsof the
Atlanticcoastof NorthAmerica(Kellogg1959;Gottfried
et al. 1994; Morgan 1994; table 1). Possibleplatanistid
relativesareSqualodelphinidae
andat leastsomemembers
of Squalodontidae
(Muizon1994;Fordyce1994),two wellknown, extinct families of archaic, medium-sized
H. Hamilton and others 553
ofriverdolphins
Evolution
I ,1 111 111111111
fL
Early
|
Late
|
Miocene
Early
|
Middle
I
1111111111
111111111
l
Oligocene
y L
0
5
10
15
20
25
30
35
Late
|
| Pliocene |
g
|
|Early|Late |
O
|
_ _ _ _ _ _ _ _ _ _ _ _ _ Mysticeti
_ _ _ _ _ _ _ _ _
_ _ _ Physeteridae
_____________Platanistidae
_____________Ziphiidae
Lipotidae
,, ,,,, _ _ _ _ _ _ _ _ Iniidae
_ _ _ _ _ _ _ _ _ _ Pontoporiidae
,,,,,,,_
_ _ _ _ _ Delphiriidae
I
-
-
-
-
-
-
-
4
s it
_________.
* s
nono ontloae
_ _ _ _ _ _ _ _ _ Phocoenidae
betweenthe hypothesizedphylogenyand fossilrecordof Odontoceti.Finerdottingindicates
Figure4. Generalcorrespondence
the uncertaindatesfor someearliestfossiloccurrences.Lipotidaeis the only cladefor whichfossilsare not yet definitivelyknown.
heterodonts.Other fossil relativesof the Platanistidae
include membersof the Dalpiaziniidae(Muizon 1994)
and Waipatiidae(Fordyce1994, p. 147).If these lineages
are monophyletic,then Platanista is the sole extant
memberof a once-abundantand diversecladeof archaic
odontocetes.The side-swimming,blindand highlyendangered Indian riverdolphinhas long been recognizedas
'thegenus. . . presentingthe greatesttotalof modifications
known in any cetacean' (Miller 1923,p.41). Both fossil
and extant platanistidswarrantfurtherinvestigationfor
potentialinsightsinto cetaceanevolution.
The assignmentof fossil taxa within non-platanistid
river dolphins has been misdirected by inaccurate
conceptsof the systematicrelationshipof extanttaxa. In
most earlierclassifications,Inia and Lipoteswere placed
in earlier
togetherin Iniidae,whilePontoporia(Stenodelphis
works)was sometimesclassifiedwithin Delphinidae,the
marine dolphins(Miller 1923).For over a century,this
conceptof Iniidaewas a repositoryfor earlydolphin-like
fossilodontocetes(Kellogg1944;Rensberger1969;Wilson
(Barnes1984,
1935).Withthe descriptionof Parapontoporia
1985),an extinctgenus consideredintermediatebetween
Lipotes and Pontoporia,subsequentclassificationssometimes placed Lipotes in the Pontoporiidae(Fordyce&
Barnes 1994). Systematicrevision and more rigorous
diagnosisof fossiltaxa leave the majorityof generalized
small odontocetes outside of Lipotidae, Iniidae and
Pontoporiidae.The Lipotidaehave essentiallyno fossil
record. A single mandibularfragmentfrom freshwater
sedimentsin southernChina, known as Prolipotesand
tentativelydatedas Miocene(Zhouet al. 1984),cannotbe
confirmedas a Lipotid.Both Iniidaeand Pontoporiidae
are representedby South American fossil relatives
Proc.R. Soc.Lond.B (2001)
(table 1).With the placement of most previously described
'iniids' in other extinct groups (Muizon 1988b; Cozzuol
1996), the family may be regarded as a freshwaterSouth
American endemic. The partial skull, rostral and
from the
mandibular fragments known as Goniodelphis,
Early Pliocene Palmetto Fauna of central Florida, are the
only fossil remains outside South America that can be
considered plausibly as Iniidae (Morgan 1994). However,
Muizon (1988b) regarded this material as too incomplete
for a confident determination. Significantly, both fossil
and
genera clearly assigned to Iniidae, Ischyrorhynchus
Saurocetes,are found far south of Inids present range,
occurring only in the fluvial Late Miocene Ituzaingo
formation of the Parana basin, Argentina (with the
possible exception of fragmentary mandibular remains
reported from Brasil; Rancy et al. 1989). The Pontoporiidae have a broader geographical and geological
have been described
range. Three species of Parapontoporia
from nearshore shallow water deposits of California and
Baja California (Barnes 1985). The members in this
Northern Hemisphere genus have been placed in their
own subfamily, Parapontoporiinae,based on their asymmetrical cranial vertices. The subfamily Pontoporiinae,
identified by symmetrical cranial vertices, is restricted to
the Southern Hemisphere. Two fossil genera have been
described from the Pisco formation of southern coastal
Peru, the Pliocene Pliopontos,very similar to Pontoporia,
and the geologically youngest occurrence of the family,
(Muizon 1983, 1988c).
the Middle Miocene Brachydelphis
Another fossil, the Late Miocene Pontistes,is found in the
Parana formation, marine sediments of the Parana basin,
Argentina, underlying and adjacent to those with fossil
iniids (Cozzuol 1985).
554 H. Hamilton and others Evolution
ofriverdolphins
Table 1. IdentiWication
andstratigraphy
offossil riverdolphins
taxon
location
stratigraphy:formation/age
Maryland
Florida
Calvert Formation/Middle Miocene Kellogg (1924); Gottfried etal. (1994)
Agricola Fauna, Bone Valley/
Kellogg (1959); Morgan (1994)
Middle Miocene
Southern China
Miocene (?)
Zhou etal. (1984)
coastal Peru
coastal Peru
Argentina
California, Mexico
Pisco Formation/Middle Miocene
Pisco Formation/Early Pliocene
Parana Formation/Late Miocene
SanOiego/LatePliocene;Almejas/
Late Miocene
Muizon (1988c)
Muizon (1983), (1984)
Cozzuol (1985), (1996)
Barnes (1984), (1985)
Ituzaingo Formation/Late Miocene
ItuzaingoFormation/LateMiocene
Palmetto Fauna, Bone Valley/
Late Miocene
Cozzuol (1985), (1996)
Cozzuol (1988), (1996)
Morgan (1994)
reference
family Platanistidae
Zarhachis
Pomatodelphis
family Lipotidae
Prolipotes
(?)
family Pontoporiidae
Brachydelphis
Pliopontos
Pontistes
Parapontoporia
family Iniidae
Ischyrhorhynchus Argentina
Saurocetes
Argentina
Goniodelphis
(?)
Florida
(b) The evolution of river dolphins
The Middle Miocene was a time of globally high sea
levels, with three significantmarine trangressive-regressive
cycles recorded worldwide (Haq et al. 1987). With the
resulting large-scale marine transgressions on to lowlying regions of the continents, shallow epicontinental
seas became prominent marine ecosystems. The IndoGangetic plain of the Indian subcontinent, the Amazon
and Parana river basins of South America, and the
Yangtze river basin of China are vast geomorphic systems
whose fluvio-deltaic regions were penetrated deeply by
marine waters during high sea-level stands. The shallow
estuarine regions created by the mixing of riverine and
marine waters probably supported diverse food resources,
particularly for aquatic animals able to tolerate osmotic
diffierences between fresh and saltwater systems. We
propose that the ancestorsof the four extant river dolphin
taxa were inhabitants of Miocene epicontinental seas.
Draining of the epicontinental seas and reduction of the
nearshore marine ecosystem occurred with a Late
Miocene trend of sea-level regression, which continued
throughout the Pliocene, interrupted by only moderate
and relatively brief events of sea-level rise (Hallam 1992).
As sea levels fell, these archaic odontocetes survived
in river systems, while their marine relatives were
superceeded by the radiation of Delphinoidea. Cassens
et al. (2000) also noted the persistence of river dolphins
during the radiation of delphinoids. They suggest that
extant river dolphin lineages 'escapedextinction' by adaptation to their current riverine habitats. All extant organisms have escaped extinction by being adequately adapted
to their presentcircumstances.By integratingphylogenetic,
palaeoceanographicand fossil data, we provide an explicit
hypothesis for the evolution and modern distribution of
riverdolphins.
The Indo-Gangetic foreland basin is a broad, flat plain
of sediment delivered throughout the Cenozoic by an
intricate network of migrating rivers descending from the
tectonically dynamic Himalayan mountains (Burbank
et al. 1996). The increased sea levels of the Middle
Proc.R. Soc.Lond.B (2001)
Miocene would have inundated large areas of the foreland basin, creating a shallow marine habitat. Fossils
have not yet been recovered from these regions, but platanistids are known to have inhabited Miocene epicontinental seas in North America (table 1; Morgan 1994;
Gottfried et al. 1994). Platanistais the only surviving
descendant of an archaic odontocete that ventured into
the epicontinental seas of the Indo-Gangetic basin, and
remained through its transition to an extensive freshwater
ecosystem during the Late Neogene trend of sea-level
regression. Although the palaeogeography of the two
river systems would suggest a history of isolation, the
genetic distance we observed in our small sample of E
gangetica
and E minor
is surprisinglylow (figure 3).
Several lines of evidence suggest Miocene marine
incursions penetrated deeply into continental South
America (Hoorn et al. 1995; Lovejoy et al. 1998). To the
north, incursions were along the course of the Amazon
river palaeodrainage (Hoorn 1994), and to the south, into
the Parana river basin (Cozzuol 1996). During the
highest global stand of Miocene sea levels, the Parana
and Amazon river basins may have been connected,
forming an interior seaway that divided the continent,
termed the ParanenseSea (Von Ihering 1927).The largely
ignored hypothesis of the Paranense Sea is supported by
sedimentological data (Rasanen et al. 1995) and biogeographical data from foraminifera (Boltovskyl991) and
molluscs (Nuttall 1990). The existence of the Paranense
Sea is consistent with the distribution of both modern
and fossil South American river dolphin taxa.
We hypothesize that the dolphins entered the seaway
from the north, diversified within its complex fluvialestuarine-marine system, and colonized its farthest
reaches, to the south-west Atlantic Ocean. Lowering of
global sea levels drained the inland sea, separating the
northern and southern river basins, and isolating the
taxa. Iniid ancestors remained in the immense Amazon
basin, which was developing its modern transcontinental
aspect with the uplift of the Venezuelan Andes and clockwise rotation of its palaeodrainage (Hoorn et al. 1995).Inia
Evolution
ofriverdolphins
H. Hamilton and others 555
their guidanceregardingtechnicaladvice.We thank D. Lindevolved during the Amazon's transformation to a freshberg andJ. Lippsfor accessto the facilitiesof the Molecular
water system of extraordinary size, diversity and abunPhylogeneticsLaboratory,U.C. Berkeley.The detailed comdance. The Parana river basin is a fraction of the size of its
northerncounterpart.The iniid fossil genera Ischyrorhynchus ments of two anonymousreviewersgreatly improved the
manuscript,whichalsobenefitedfromthe thoughtfulcomments
and Saurocetes)
found along the banks of the Rio Parana,
ofJ. W.Vatentine.
This is UCMPpublication1733.
belong to genera that disappeared with the retreat of the
continental sea ecosystem. Pontoporia
followed the marine
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As this paperexceedsthe maximumlengthnormallypermitted,
the authorshaveagreedto contributeto productioncosts.