REVIEW SUMMARY

VERTEBRATE EVOLUTION

Evolutionary innovation and ecologyin marine tetrapods from the Triassicto the AnthropoceneNeil P Kelley12 and Nicholas D Pyenson13

BACKGROUNDMore than 30 different lin-eages of amphibians reptiles birds andmammals have independently invaded oceansecosystems Prominent examples include ich-thyosaurs andmosasaurs during theMesozoic(252 to 66 million years ago) and penguinsand sea otters during the Cenozoic (66 millionyears ago to the present) In todayrsquos oceansmarine tetrapods are ecologically importantconsumers with trophic influence dispropor-tionate to their abundance They have occu-pied apex roles in ocean food webs for morethan 250million years throughmajor changesin ocean and climate and through mass ex-

tinctions Major paleontological discoveries inthe past 40 years have clarified the early land-sea transitions for some marine tetrapods (egwhales sea cows) although the terrestrial ori-gins of many lineages remain obscure Incipientinvasions appear frequently in marine tetrapodhistory but such early transitions account foronly a small proportion of the total fossil recordof successful marine lineages which in somecases persist for hundreds of millions of years

ADVANCES Marine tetrapods provide idealmodels for testing macroevolutionary hypothe-ses because the repeated transitions between

land and sea have driven innovation conver-gence and diversification against a backdropof changing marine ecosystems and mass ex-tinctions Recent investigations across a broadrange of scalesmdashfrommolecules to food websmdashhave clarified the phylogenetic scope timingand ecological consequences of these repeatedinnovations Studies of the physiology andfunctional morphology of living species haveilluminated the constraints and tradeoffs that

shape the pathway of ini-tialmarine invasionsCom-parative studies on musclemyoglobin concentrationor the evolution of sex de-termination mechanismsfor example have revealed

rampant convergence for these adaptive traitsin the marine realm Exceptionally preservedfossils have also revealed insights into repro-ductivebiology soft tissue structures and trophicinteractions Fossils provide critical baselinesfor understanding historical changes in marinecommunities and diversity through time andthese baselines remain vital for evaluating theongoing and severe anthropogenic disturbanceto marine tetrapod populations and marineecosystems as a whole

OUTLOOK Technological advances in remotesensing and biologgingwill continue to providecrucial insights into the macroecology of ma-rine tetrapods below the waterrsquos edge Fielddata when combined with extensive vouchersrepresented in museum collections providethe basis for integrativemodels of the functionand ecology of these logistically challengingorganisms Placed in a phylogenetic compara-tive framework these data can enable tests ofhypotheses aboutmacroevolutionary patternsAlthough perpetually incomplete new fossildiscoveries continue to improve our under-standing of the early land-sea transitions inlineages and reveal past ecologies that couldnot have otherwise been predicted Emerg-ing imaging molecular and isotopic tech-niques provide an opportunity to expand theinvestigational scope for studying extincttaxa and to inform our understanding of howliving species evolved Lastly resolving thefull evolutionary scope of marine tetrapod his-tory provides context for the origins of mod-ern ecological patterns and interactions whichare fundamentally being altered by humanactivities

RESEARCH

SCIENCE sciencemagorg 17 APRIL 2015 bull VOL 348 ISSUE 6232 301

1Department of Paleobiology National Museum of NaturalHistory Smithsonian Institution Washington DC 20013USA 2Department of Earth and Environmental SciencesVanderbilt University Nashville TN 37240 USA3Departments of Mammalogy and Paleontology BurkeMuseum of Natural History and Culture Seattle WA 98195USACorresponding author E-mail kelleynpsieduCite this article as N P Kelley N D Pyenson Science 348aaa3716 (2015) DOI101126scienceaaa3716

A unified view of marine tetrapod evolution Circles mark initial invasions of marine tetrapodgroups Extinct and extant lineages are denoted by open and solid circles respectively (yellow am-phibians green nonavian reptiles blue birds red mammals)Top curve summarizes marine tetrapodfossil richness through timeSchematic limbdrawingsdemonstrateconvergenthydrodynamic forelimbsin marine tetrapods (top to bottom) sea lion whale penguin sea turtle mosasaur ichthyosaur Mamillions of years agoC

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ON OUR WEB SITE

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on June 16 2020

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REVIEW

VERTEBRATE EVOLUTION

Evolutionary innovation and ecologyin marine tetrapods from the Triassicto the AnthropoceneNeil P Kelley12 and Nicholas D Pyenson13

Many top consumers in todayrsquos oceans are marine tetrapods a collection of lineagesindependently derived from terrestrial ancestorsThe fossil record illuminates their transitionsfrom land to sea yet these initial invasions account for a small proportion of their evolutionaryhistoryWe review the history of marine invasions that drove major changes in anatomyphysiology and ecologyovermore than 250million yearsMany innovations evolved convergentlyinmultiple cladeswhereas others are unique to individual lineagesThe evolutionary arcs of theseecologically important clades are framed against the backdrop of mass extinctions and regimeshifts in ocean ecosystems Past and present human disruptions to marine tetrapods withcascading impacts on marine ecosystems underscore the need to link macroecology withevolutionary change

More than 30 lineages of tetrapods (amphi-bians reptiles birds and mammals) in-dependently invaded marine ecosystemsduring the Phanerozoic (Fig 1) Such re-peated transitions from terrestrial or

freshwater to marine habitats are generally un-common in other clades (1) Reconfigurations inmorphology physiology life history and sensorysystems characterize each transition For exampledifferential constraints on movement betweenthese realmsmdashgravity on land versus drag inwatermdashled to similar locomotory adaptations inmarine tetrapods (2) (Fig 2)Sequences of fossil cetaceans (3) and sirenians

(4) from Eocene rocks provide the best examplesof major morphological transformations follow-ing marine invasions Both groups show pelvicdecoupling from the vertebral column and sub-sequent reduction of the pelvis and hindlimbslater specializations included forelimb stream-lining tail propulsion and posterior migrationof the nostrils Unfortunately the early historiesof most other marine tetrapod lineages remainobscure For example the freshwater carnivoranPuijila darwini provides clues about the originsof pinnipeds (5) but it is geologically youngerthan othermarine stem pinnipeds (6) and is thusnot likely a direct ancestor of modern pinnipedsLikewise semi-aquatic Permian reptiles initiallyproposed to represent plesiosaur ancestors (7) arenot closely related to plesiosaurs in recent analy-ses (8) the Early Cretaceous turtle Santanachelys(9) was once viewed as a stem predecessor tomod-

ern sea turtles but this position is no longer sup-ported (10) Thus origins of several importantmarine tetrapod groups remain essentially un-known with the oldest known fossil represent-atives exhibiting derived morphologies withoutobvious terrestrial antecedents Prominent exam-ples include penguins (11) and ichthyosaurs (12)although the recently described basal ichthyosauri-form Cartorhynchus may clarify the origins ofthe latter (13)The history of terrestrial-marine transitions

reveals links between Earth system changes andmarine tetrapod invasions modulated by ecologyand physiologyMarine transgressions andwarm-ing episodes coincided with Mesozoic and EarlyCenozoic marine tetrapod invasions (3 4 14ndash18)Modern marginal marine tetrapods are concen-trated in low-latitude mangroves estuaries andarchipelagos (19) The paleoenvironmental con-text of marginal marine tetrapod fossils (7 20)likewise indicates that warm shallow marginalmarine habitats provide favorable settings forterrestrial-marine transitions especially in ecto-therms Conversely mid-Cenozoic cooling andincreases in marine productivitymdashparticularly inthe North Pacific and Southern Oceanmdashcoincidedwith bird and mammal invasions (21 22) andthese regions remain hotspots of marine mam-mal diversity (23) However such relationshipsare not always rigid throughout the history of aclade Cetaceans evolved in shallow equatorialseas (18) but now thrive in high-latitude oceansthe origin of penguins preceded Southern Hem-isphere cooling by several million years (24)Studies of living marginal marine species illu-

minate ecological (25 26) functional (2 27ndash29)and physiological (30ndash32) pathways that facilitatetransitions A common theme is the high degree ofplasticity in ecologically marginal taxa (26 28 31)Isotopic investigations of fossils suggest similar

patterns demonstrating mixed habitat and re-source use (33) Repeated independent invasionsamong some clades suggest that certain ecologiesandor body plans may predispose groups tomarine transitions Independent adaptation tomarine lifestyles among close relatives simulta-neously or in close succession would complicateefforts to decipher and enumerate transitions inthe fossil record (34 35)

Convergent evolution frommoleculesto morphology

Marine tetrapods provide canonical illustrationsof evolutionary convergence (Fig 2) (36) widelyregarded as repeated solutions to problems im-posed by physical contrasts between land andwater Simple visual comparisons however can-not fully decipher the processes that shape evo-lutionary convergence Apparent similarities canmask differences in functional performance (37)and mechanical convergence can be achieved withalternative morphological solutions often con-strained by phylogeny (38) Thus the dorsoven-tral caudal propulsion of cetaceans derives fromthe bounding locomotory mode of terrestrial ma-mmalian ancestors (2) while the lateral caudalpropulsion of ichthyosaurs evolved from the lo-comotion of lizard-like predecessors (39)Quantitative functional morphology provides

a means to quantify and compare performanceand functional trade-offs particularly in speciesthat spend time both on land and in the watersuch as snakes (29) and pinnipeds (40) Func-tional trade-offs can ultimately drive specializa-tion and steer evolutionary convergence as withrepeated loss of flight among seabirds specializedfor aquatic locomotion (41) In vivo studies offeeding performance provide similar insight intofunctional trade-offs and specialization (42ndash44)which shaped convergence in marine tetrapodfeeding systems (45)Increased bone density evolved repeatedly in

coastal marine tetrapods for stability and buoy-ancy regulation (46ndash51) Conversely decreasedbone density has evolved among many pelagicgroups reducing the costs of sustained swim-ming or as a consequence of increased growthrates (50) Some lineages such as cetaceans (4849)ichthyosaurs (13 49) and sauropterygians (51)transitioned through these contrasting phases se-quentially with increased bone density duringearly evolution followed by reduced bone densityafter open marine adaptation The evolution ofinsulating structures inmarinemammals follows asimilar progression with thick fur in coastal in-vaders replaced by thick insulating fat for energystorage and streamlining in more oceanic marinemammals (52) Fossil anatomy reveals the evolu-tion of countercurrent heat exchange in penguins(53) convergent with similar systems in marinemammalsThe scope of recent studies of convergent evo-

lution extends beyond morphology to includemolecular physiology (54) metabolism and ther-moregulation (55 56) and life history (56 57)Genomic investigations have revealed convergentgenetic origins of important innovations such as

RESEARCH

SCIENCE sciencemagorg 17 APRIL 2015 bull VOL 348 ISSUE 6232 aaa3716-1

1Department of Paleobiology National Museum of NaturalHistory Smithsonian Institution Washington DC 20013 USA2Department of Earth and Environmental Sciences VanderbiltUniversity Nashville TN 37240 USA 3Departments ofMammalogy and Paleontology Burke Museum of NaturalHistory and Culture Seattle WA 98195 USACorresponding author E-mail kelleynpsiedu

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sex determination mechanisms (58) myoglobinadaptations facilitating deep diving (54) andecholocation (59) Stable isotopes from fossilselucidate parallel histories of habitat shift in earlycetaceans and sirenians (33) and convergent evo-lution of endothermy in Mesozoic marine rep-tiles (53) Recent breakthroughs in fossil pigmentreconstruction have resolved structural and pig-ment adaptations in fossil seabird feathers (60)and have revealed widespread dark coloration in

fossil marine reptiles possibly for temperatureregulation or ultraviolet light protection (55)Exceptionally preserved fossils (57 61 62) doc-

ument convergent reproductive adaptations inmarine reptiles Recently discovered early ich-thyosaur fossils (62) extend the history of vivi-parity in this group back to the Early Triassic andindicate that viviparity evolved in terrestrial fore-runners as an enabling factor for rather thanan adaptive response to aquatic life Fossils sug-

gest that some marine reptiles converged uponK-selected life histories observed among marinemammals (57) Aquatic birth evolved early in ceta-cean and sirenian evolution but these transitionsare so far only partly constrained by fossils (63)

Causes and consequences of convergenceinnovation and radiation

In addition to external drivers convergent evo-lution is shaped by the underlying genetic anddevelopmental pathways that give rise to con-vergent structures Thus repeated evolution ofhydrodynamic limbs (Fig 2E) (64) and axial mod-ifications (65) likely exploited parallel develop-mental mechanisms Such shared pathways mayextend to the level of gene regulation linkinggenomic and phenotypic convergence and inno-vation Recent work on marine mammal genomicconvergence has questioned the prevalence ofsuch linkages (66) however more work is neededto evaluate potential scaling of convergence fromgene to phenotypeInnovations facilitate and constrain downstream

evolution as illustrated in the discrete pathwaysfrom drag-based to lift-based swimming in limb-and tail-propelled aquaticmammals (2) Likewiseindependent innovation of aquatic birth in mul-tiplemarine reptile andmarinemammal lineagesremoved the constraints of terrestrial locomo-tion enabling limb and skeletal modificationto increase swimming performance as well asgigantism in some clades Convergent evolu-tionary pathways [eg the emergence of tail-driven locomotion in ichthyosaurs mosasaursandwhales (Fig 2A)]might follow similar temposacross groups (67) but this hypothesis awaitsfurther testingParticularly diverse clades have frequently been

characterized as adaptive radiations facilitated bynew ecological opportunities after marine in-vasions (68) However external factors may beequally important in shaping and pacing theseradiations (69) Although diverse clades are oftenecologically and morphologically disparate aspredicted under adaptive radiation models (70)diversity and disparity are not tightly coupled inother radiations (71)Diversification can be triggered by innovations

that occur well after initial invasions For exam-ple echolocation and baleenmdashtwo key innova-tions that evolved tens of millions of years afterwhales first entered the oceansmdashmark the emer-gence of crown cetaceans (72) the most species-rich marine tetrapod clade Hydrophiine seasnakes which entered marine environments inthe last 6million years and now comprise at least60 species (71 73) provide a key example of amarine tetrapod group in the midst of major ra-diation Even within this group diversity is het-erogeneously distributed within subclades andlinked to specific intraclade innovations ratherthan simply reflecting rapid niche expansion afterinitial marine invasion (71)

Iterative evolution and ecological turnover

Marine tetrapods first diversified during the re-structuring of marine ecosystems that followed

aaa3716-2 17 APRIL 2015 bull VOL 348 ISSUE 6232 sciencemagorg SCIENCE

50100150200250300

Paleozoic Mesozoic CenozoicC P Tr J K Pg Ng Q

350

D

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Time (Ma)

Amphibiansdagger

2

Mammals

Crocodiles

dagger

dagger

19

20

24

25 28

31

32

lsquoReptilesrsquo

Birds

Turtles

Snakes

daggerdagger

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dagger

daggerdagger

dagger

dagger

dagger

dagger daggerdagger

dagger

daggerdagger

dagger1

3

4

5

69

7

8

14

16

10

13

11

15

12Aquatic-terrestrialtransition

17

18

21

22

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2627

29

30

33

Tetrapods

Fig 1 Temporal and phylogenetic distribution of marine tetrapod groups Circles indicate first ap-pearance datum (FAD) for each lineage based on fossils or divergence estimates for groups lacking afossil record (136) daggers denote extinctionsMarine tetrapod taxa are numbered in order of appearancein the fossil record (1) Mesosauria (2) Trematosauria (3) Ichthyosauromorpha (4) Sauropterygia (5)Thalattosauriformes (6) Tanystropheidae (7) Thalattosuchia (8) Pleurosauridae (9) Plesiochelyidae(10) Pholidosauridae (11) Simiolophiidae (12) Mosasauroidea (13) Protostegidae (14) Hesperornithiformes(15) Chelonioidea (16) Dyrosauridae (17) Acrochordoidea (18) Sphenisciformes (19) Cetacea (20)Sirenia (21) Gryposuchinae (22) Plotopteridae (23) Alcidae (24) Pinnipedimorpha (25) Desmostylia(26) Laticaudini (27) Hydrophiini (28) Thalassocnus (29) Pelecanoides (30) Tachyeres (31) Enhydra (32)Ursusmaritimus (33)AmblyrhynchusColored boxesmatch convergent taxa shown in Fig 2 A to D Ma millionsof years ago (Silhouettes from phylopicorg see supplementary materials for usage and attribution details)

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the end-Permian mass extinction and the rise ofthe so-called ldquoModern Faunardquo (74) Their appear-ance has been characterized as a final step inthe bottom-up reassembly of marine ecosystemsafter a delayed recovery (75 76) However theearly appearance of predatory marine tetrapodsin the Triassic has recently been cited as evi-dence that recovery was not delayed after all (77)Although later Mesozoic and Cenozoic invasionsreplaced these early groups marine tetrapodshave remained a persistent fixture of marine eco-systems since the Triassic Some replacementscoincided with mass extinctions (Fig 1) (78)

others were staggered across intervals of grad-ual faunal change (78 79)Persistent biological processes such as compe-

tition (ldquoRed Queenrdquo) and stochastic environ-mental factors (ldquoCourt Jesterrdquo) (80) may regulatemarine tetrapod community structure and diver-sity at different time scales (81) Pelagic habitatsare typically dominated by one or two cosmopol-itan marine tetrapod clades with long histories[eg ichthyosaurs from the Triassic to Cretaceous(78) plesiosaurs from the Jurassic to theCretaceous-Paleogene (K-Pg) boundary (78) cetaceans sincethe Eocene (3)] Near-shore communities often

host more lineages with higher endemism andfrequent turnover (16 82ndash84) Specific spatial andtemporal successions hint at competitive inter-actions as among flightless seabirds and marinemammals competing for shore space (22) re-placement of herbivorous desmostylians by sire-nians in the North Pacific (82) and replacementof phocids by otariids in South America (83)These episodes of replacement between lin-

eages are mirrored by iterative patterns withinlineages For example evolution of herbivory anddurophagy (feeding on hard-shelled prey) droverepeated convergent feeding morphologies inliving and fossil sea turtles (85) Similarly inde-pendent invasions of freshwater ecosystems bydifferent odontocete lineages gave rise to a con-vergent ldquoriver dolphinrdquo morphotype (86) Ecolo-gical interactions among sympatric relatives alsodrive iterative evolution Multispecies fossil sire-nian assemblages show parallel patterns of eco-morphological partitioning (82) contrasting withthe relictual and disjunct distribution of livingspecies Sympatric or parapatric ecomorphs ob-served in widely distributed odontocetes (87 88)have arisen through niche differentiation andonshore-offshore partitioning Cryptic specia-tion and iteration is common among sea snakeswith repeated parallel evolution of morphotypes(71) Iterative evolution and resource partition-ing may account for contrasting morphotypesin co-occurring fossil taxa (82 89) and repeatedevolution of certain morphotypes such as poly-phyletic ldquopliosaursrdquo (90)Marine tetrapods themselves constituted an

important trophic resource for other species inMesozoic ecosystems beginning in the Triassic(76) Intriguingly although hypercarnivory evol-ved repeatedly among Cenozoic marine mam-mals (91 92) many lineages later specialized onresources at lower trophic levels Hypercarnivo-rous species that regularly consume other tetra-pods are comparatively rare in modern oceansrepresented only by killer whales leopard sealsand marginal marine crocodiles all generalist pred-ators that also feed regularly at lower trophiclevels (42 88) The comparative rarity of hyper-carnivorous marine tetrapods in modern oceansmay reflect different structuring of MesozoicEarly Cenozoic and modern marine food webs

Contrasting Mesozoic and Cenozoicpatterns of fossil richness

Patterns in raw marine tetrapod fossil speciesrichness (Fig 3) resemble those observed in themarine invertebrate record (93ndash95) FluctuatingMesozoic diversity reflects repeated extinctionsof incumbent clades (Fig 1) followed by diversi-fication of new groups (78) as well as geologicbiases on the marine tetrapod fossil record (14)Contrasting patterns between coastal and pelagicMesozoicmarine tetrapod groups (14 15) point toldquocommon-causerdquo dynamics whereby geologic pro-cesses that affect marine diversity also control se-dimentary rock accumulation (95) The pronounceddrop in richness at the K-Pg boundary correspondsto the simultaneous extinction of mosasaursplesiosaurs and other lineages (Figs 1 and 3)

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U R

H

c

mp

Fig 2 Convergent morphology in marine tetrapods Similar anatomy evolved among lineages that in-dependently adopted marine lifestyles From top to bottom (A) early whale Dorudon mosasaur Platecarpusichthyosaur Cymbospondylus (scale bars 1 m) (B) ichthyosaur Stenopterygius dolphin Stenella (C)early seal Acrophoca sauropterygian Nothosaurus (scale bars 50 cm) (D) penguin Pygoscelis (left) greatauk Pinguinus (right) (E) Forelimbs of select marine tetrapods (from left to right ichthyosaur mosasaurwhale sea turtle sea lion penguin) showing anatomical convergence reflecting limb streamlining[adapted from (36 64)] Colors identify homologous elements labeled on ichthyosaur H humerus(pink) R radius (yellow) U ulna (orange) c carpals (blue) mmetacarpals (green) p phalanges (white)Phylogeny and contrasting locomotory patterns account for finer scale differences such as proportionallylonger humeri in forelimb-driven swimmers (sea turtle sea lion penguin) relative to tail-driven swimmers(ichthyosaur mosasaur whale) See supplementary materials for image sources

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After the K-Pg mass extinction Early Cenozoicdiversification of cetaceans (3) sirenians (96)and penguins (24 97) brought Paleogene marinetetrapod richness back to peak Mesozoic levelsThe emergence of crown cetaceans (72) and theinvasion of pinnipeds (21) alongwith other groupscoincide with a marked increase in fossil rich-ness to even higher levels The apparent Cenozoicmarine tetrapod diversity increase like marineinvertebrate richness (94) may be inflated by pre-servation biases (eg ldquopull of the recentrdquo) How-ever recent investigations of fossil invertebrates(93) and marine mammals (98 99) propose thatincreasing Cenozoic richness largely reflects areal biological signal Fossil bias has been eval-uated for some marine tetrapod groups (14 98)but integrated comparisons of biases across theMesozoic and Cenozoic are still neededChanges in ocean productivity regimes (100)

and ecological escalation (101) may help to ex-plain the differing trajectories of Cenozoic andMesozoic marine tetrapod diversification Excep-tional diversification rates of eutherian mammals(102) might also account for increasing Cenozoicdiversity given the repeated marine invasions ofplacental mammals during the Cenozoic How-ever other groups with elevated diversificationrates including Neoaves and squamates also in-vaded marine ecosystems with varying degreesof success indicating that phylogenetic differ-ences alone cannot account for these differencesIncreasing marine tetrapod diversity since the

Mesozoic also tracks increasing marine resourcesand expandingniches Clear evidence of herbivoryis unknown among marine reptiles until herbiv-

orous sea turtles evolved coincident with the firstseagrasses in the Cretaceous (85) which is con-sistent with ldquodelayed herbivoryrdquo in other marineclades (103) Likewise there is no evidence forpelagic suspensionndashfeeding marine tetrapods inthe Mesozoic (104) and little evidence for deep-diving mesopelagic feeders until the Jurassic (37)These absent ecologies suggest that Early Meso-zoic marine food webs were less complex thanmodern equivalents

Shifted baselines and marine tetrapodmacroecology since the Pleistocene

Marine tetrapod and hominid ecological inter-actions began at least by the Late Pleistocenewith evidence for Neandertal (Homo neander-thalensis) exploitation of marine mammals inGibraltar Spain (105) Humans have continuedto directly and indirectly interact with marineecosystems ever since this time (106) Althoughthese impacts have lagged behind profound hu-man perturbations to terrestrial ecosystems tech-nological innovation has escalated their rate andmagnitude in recent centuries (107)The extinction of Stellerrsquos sea cow (Hydro-

damalis gigas) marks the first well-documentedmarine mammal species extinction in historictimes (108) Hunting brought some cetacean spe-cies perilously close to extinction (109) and exter-minated at least two pinniped species (110 111)Historically severalmarinemammal species werethought extinct until refugial populations wererediscovered (112 113) Seabirds have been sim-ilarly vulnerable to human hunting with historicand prehistoric extinctions of large flightless

seabirds (114ndash116) and others critically endan-gered (117) Many living marine reptiles alsorisk extinctionmdashincluding six of seven sea turtlespeciesmdashlargely because of human exploitationand habitat alteration (117) The conservationstatus of many marine tetrapod species is poor-ly known because of the difficulties of studyingwild marine populationsThe only cetacean extinction at human hands

the Yangtze River dolphin (Lipotes) was largelycaused by habitat degradation (118) Before theend of this decade another cetacean the vaquita(Phocoena sinus) may be driven extinct throughby-catch in small-scale fisheries in the Gulf ofCalifornia (119) Such indirect impacts are agrowing concern with recent attention turningto ship collisions (120) shipping noise (121) mil-itary sonar (122) microplastics (123) and human-borne pathogens (124) among other emergingthreats (107)Anthropogenic climate change is already driv-

ing changes inmarine tetrapod populations par-ticularly in polar ecosystems (125) Shrinking seaice and changing ocean thermal gradients are alsodriving range shifts most strikingly documentedby repeated recent dispersal from the Pacific intothe Atlantic by gray whales (Eschrichtius) via anice-free northwest passage (126) potentially anti-cipating a recolonization of the Atlantic follow-ing extirpation four centuries ago (127) Globalwarming may have major impacts on ectother-mic marine reptiles potentially altering rangelimits activity levels (128) and even the sex ratioin species with temperature-dependent reproduc-tion (129) Potential feedbacks between anthropo-genic warming and complex climate dynamicssuch as El Nintildeomdashknown to trigger marine tetra-pod population collapses (130)mdashsuggest that im-pacts of climate change onmarine tetrapodsmaybe abrupt episodic and difficult to predict (100)Anthropogenic declines inmarinemammal pop-

ulations also have downstream effects onmarinefoodwebs (131) via trophic cascades for examplewith killer whalendashsea otterndashmysticete interactionsoff southeast Alaska (132) and mysticete-seal-penguin interactions in the Southern Ocean (133)Emerging technologies such as animal-borne re-cording devices (used in biologging) promise toreveal new details about marine tetrapod ecology(134) and the state of the oceans themselves suchas information about ocean currents provided bybiologged data (135)

Conclusions

Despite their status as conservation icons majorquestions remain concerning marine tetrapodmacroecology morphology and even alpha tax-onomy New discoveries and new techniques arehelping to frame and test hypotheses about ma-rine tetrapod evolution Realizing the full poten-tial of these advances requires integrating datasets from disparate disciplines to address uni-fying questions in ecology evolutionary biologyand Earth systems history Marine tetrapods havebeen ecologically influential members of oceanfood webs since the end-Permian mass extinctionpersisting through later mass extinctions anoxic

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BirdsReptilesAmphibians

Mammals

0

100

200

300

400

500

050100150200250

NeogPaleogeneCretaceousJurassicTriassic

Sea level Transgression

Time (Ma)

Mar

ine

tetr

apo

d f

oss

il sp

ecie

s

NgPgKJTr0

1000

2000

3000

P0100200

Time (Ma)

Marine invertebrates

Higher sea level

Fig 3 Marine tetrapod fossil richness Raw marine tetrapod fossil occurrence binned at intervals of~10 million years [from (81)] and marine invertebrate genera [from (94)] Both groups show episodicvariation in fossil richness during the Mesozoic ending with abrupt drop at the K-Pg mass extinctionfollowed by continually increasing richness during the Cenozoic Partial correspondence with marinetransgressionregression [second order cycles of ~10 to 100 million years from (134)] suggests influ-ence of sea level on shallow marine diversity andor rock record bias particularly in the Mesozoic

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events and ocean restructuring The ecologicalimportance of marine tetrapods in modern foodwebs raises questions about their role duringmajor episodes of change and their sensitivityto bottom-up perturbations in the past Eval-uating the place of tetrapods in contemporaryocean ecosystems also requires accounting forshifts from baseline abundances driven by hu-man activities Understanding the full history ofmarine tetrapods provides necessary context forconstraining the scope of potential future shiftsin marine ecosystems

REFERENCES AND NOTES

1 G J Vermeij R Dudley Why are there so few evolutionarytransitions between aquatic and terrestrial ecosystemsBiol J Linn Soc London 70 541ndash554 (2000) doi 101111j1095-83122000tb00216x

2 F E Fish Transitions from drag-based to lift-based propulsionin mammalian swimming Am Zool 36 628ndash641 (1996)

3 M D Uhen The origin(s) of whales Annu Rev Earth Sci 38189ndash219 (2010) doi 101146annurev-earth-040809-152453

4 D P Domning The earliest known fully quadrupedal sirenianNature 413 625ndash627 (2001) doi 10103835098072pmid 11675784

5 N Rybczynski M R Dawson R H Tedford A semi-aquaticArctic mammalian carnivore from the Miocene epoch andorigin of Pinnipedia Nature 458 1021ndash1024 (2009)doi 101038nature07985 pmid 19396145

6 A Berta C E Ray A R Wyss Skeleton of the oldest knownpinniped Enaliarctos mealsi Science 244 60ndash62 (1989)doi 101126science244490060 pmid 17818847

7 R L Carroll Plesiosaur ancestors from the Upper Permianof Madagascar Philos Trans R Soc London Ser B 293315ndash383 (1981) doi 101098rstb19810079

8 J M Neenan N Klein T M Scheyer European origin ofplacodont marine reptiles and the evolution of crushingdentition in Placodontia Nat Commun 4 1621 (2013)doi 101038ncomms2633

9 R Hirayama Oldest known sea turtle Nature 392 705ndash708(1998) doi 10103833669

10 W G Joyce J F Parham T R Lyson R C WarnockP C Donoghue A divergence dating analysis of turtles usingfossil calibrations An example of best practices J Paleontol87 612ndash634 (2013) doi 10166612-149

11 D T Ksepka S Bertelli N P Giannini The phylogeny of theliving and fossil Sphenisciformes (penguins) Cladistics 22412ndash441 (2006) doi 101111j1096-0031200600116x

12 M W Maisch Phylogeny systematics and origin of theIchthyosauriamdashthe state of the art Palaeodiversity 3 151ndash214(2010)

13 R Motani et al A basal ichthyosauriform with a short snoutfrom the Lower Triassic of China Nature 517 485ndash488(2015) doi 101038nature13866

14 R B Benson R J Butler Uncovering the diversificationhistory of marine tetrapods Ecology influences the effect ofgeological sampling biases Geol Soc London Spec Publ358 191ndash208 (2011) doi 101144SP35813

15 N P Kelley R Motani D Y Jiang O Rieppel L SchmitzSelective extinction of Triassic marine reptiles duringlong-term sea-level changes illuminated by seawaterstrontium isotopes Palaeogeogr Palaeoclimatol Palaeoecol400 9ndash16 (2014) doi 101016jpalaeo201207026

16 J E Martin R Amiot C Leacutecuyer M J Benton Sea surfacetemperature contributes to marine crocodylomorphevolution Nat Commun 5 4658 (2014) doi 101038ncomms5658

17 N Bardet A Houssaye J C Rage X Pereda Suberbiola TheCenomanian-Turonian (Late Cretaceous) radiation of marinesquamates (Reptilia) The role of the Mediterranean TethysBull Soc Geol Fr 179 605ndash622 (2008) doi 102113gssgfbull1796605

18 P D Gingerich N A Wells D E Russell S M Shah Originof whales in epicontinental remnant seas New evidence fromthe early Eocene of Pakistan Science 220 403ndash406 (1983)doi 101126science2204595403 pmid 17831411

19 J C Murphy Marine invasions by non-sea snakes withthoughts on terrestrial-aquatic-marine transitions IntegrComp Biol 52 217ndash226 (2012) doi 101093icbics060pmid 22576813

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21 T A Demeacutereacute A Berta P J Adam Pinnipedimorphevolutionary biogeography Bull Am Mus Nat Hist 27932ndash76 (2003) doi 1012060003-0090(2003)279lt0032Cgt20CO2

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24 J A Clarke et al Paleogene equatorial penguins challengethe proposed relationship between biogeography diversityand Cenozoic climate change Proc Natl Acad Sci USA104 11545ndash11550 (2007) doi 101073pnas0611099104pmid 17601778

25 W A Buttemer W R Dawson Temporal pattern of foragingand microhabitat use by Galapagos marine iguanasAmblyrhynchus cristatus Oecologia 96 56ndash64 (1993)doi 101007BF00318031

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32 F Brischoux Y V Kornilev Hypernatremia in dice snakes(Natrix tessellata) from a coastal population Implications forosmoregulation in marine snake prototypes PLOS ONE 9e92617 (2014) doi 101371journalpone0092617

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34 M W Caldwell A challenge to categories ldquoWhat if anythingis a mosasaurrdquo Bull Soc Geol Fr 183 7ndash34 (2012)doi 102113gssgfbull18317

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36 A B Howell Aquatic Mammals Their Adaptations to Life inthe Water (Charles C Thomas Baltimore MD 1930)

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42 D P Hocking A R Evans E M Fitzgerald Leopard seals(Hydrurga leptonyx) use suction and filter feeding whenhunting small prey underwater Polar Biol 36 211ndash222(2013) doi 101007s00300-012-1253-9

43 E A Kane C D Marshall Comparative feeding kinematicsand performance of odontocetes Belugas Pacific white-sideddolphins and long-finned pilot whales J Exp Biol 2123939ndash3950 (2009) doi 101242jeb034686 pmid 19946072

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47 E Amson C de Muizon M Laurin C Argot V de BuffreacutenilGradual adaptation of bone structure to aquatic lifestyle inextinct sloths from Peru Proc R Soc B 281 20140192(2014) doi 101098rspb20140192 pmid 24621950

48 N M Gray K Kainec S Madar L Tomko S Wolfe Sinkor swim Bone density as a mechanism for buoyancy controlin early cetaceans Anat Rec 290 638ndash653 (2007)doi 101002ar20533 pmid 17516430

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51 A Krahl N Klein P M Sander Evolutionary implications ofthe divergent long bone histologies of Nothosaurus andPistosaurus (Sauropterygia Triassic) BMC Evol Biol 13123 (2013) doi 1011861471-2148-13-123 pmid 23773234

52 H E Liwanag A Berta D P Costa S M BudgeT M Williams Morphological and thermal properties ofmammalian insulation The evolutionary transition to blubberin pinnipeds Biol J Linn Soc 107 774ndash787 (2012)doi 101111j1095-8312201201992x

53 D B Thomas D T Ksepka R E Fordyce Penguinheat-retention structures evolved in a greenhouse EarthBiol Lett 7 461ndash464 (2011) doi 101098rsbl20100993pmid 21177693

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57 F R OrsquoKeefe L M Chiappe Viviparity and K-selectedlife history in a Mesozoic marine plesiosaur (ReptiliaSauropterygia) Science 333 870ndash873 (2011) doi 101126science1205689 pmid 21836013

58 C L Organ D E Janes A Meade M Pagel Genotypic sexdetermination enabled adaptive radiations of extinct marinereptiles Nature 461 389ndash392 (2009) doi 101038nature08350 pmid 19759619

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62 R Motani D Y Jiang A Tintori O Rieppel G B ChenTerrestrial origin of viviparity in Mesozoic marine reptilesindicated by early Triassic embryonic fossils PLOS ONE 9e88640 (2014) doi 101371journalpone0088640

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nloaded from

63 P D Gingerich W von Koenigswald W J SandersB H Smith I S Zalmout New protocetid whale fromthe middle Eocene of Pakistan Birth on land precocialdevelopment and sexual dimorphism PLOS ONE 4 e4366(2009) doi 101371journalpone0004366

64 M W Caldwell From fins to limbs to fins Limb evolutionin fossil marine reptiles Am J Med Genet 112 236ndash249(2002) doi 101002ajmg10773 pmid 12357467

65 J Muumlller et al Homeotic effects somitogenesis and theevolution of vertebral numbers in recent and fossil amniotesProc Natl Acad Sci USA 107 2118ndash2123 (2010)doi 101073pnas0912622107 pmid 20080660

66 A D Foote et al Convergent evolution of the genomesof marine mammals Nat Genet 47 272ndash275 (2015)doi 101038ng3198 pmid 25621460

67 J Lindgren M W Caldwell T Konishi L M ChiappeConvergent evolution in aquatic tetrapods Insights from anexceptional fossil mosasaur PLOS ONE 5 e11998 (2010)doi 101371journalpone0011998

68 J H Lipps E Mitchell Trophic model for the adaptiveradiations and extinctions of pelagic marine mammalsPaleobiology 2 147ndash155 (1976)

69 M E Steeman et al Radiation of extant cetaceans drivenby restructuring of the oceans Syst Biol 58 573ndash585(2009) doi 101093sysbiosyp060 pmid 20525610

70 G J Slater S A Price F Santini M E Alfaro Diversityversus disparity and the radiation of modern cetaceansProc R Soc B 277 3097ndash3104 (2010) doi 101098rspb20100408 pmid 20484243

71 K L Sanders M S Mumpuni M S Y Lee Uncouplingecological innovation and speciation in sea snakes(Elapidae Hydrophiinae Hydrophiini) J Evol Biol 232685ndash2693 (2010) doi 101111j1420-9101201002131xpmid 21077974

72 J Gatesy et al A phylogenetic blueprint for a modern whaleMol Phylogenet Evol 66 479ndash506 (2013) doi 101016jympev201210012 pmid 23103570

73 K L Sanders et al Multilocus phylogeny and recent rapidradiation of the viviparous sea snakes (ElapidaeHydrophiinae) Mol Phylogenet Evol 66 575ndash591 (2013)doi 101016jympev201209021 pmid 23026811

74 J J Sepkoski Jr A kinetic model of Phanerozoic taxonomicdiversity III Post-Paleozoic families and mass extinctionsPaleobiology 10 246ndash267 (1984)

75 Z Q Chen M J Benton The timing and pattern of bioticrecovery following the end-Permian mass extinctionNat Geosci 5 375ndash383 (2012) doi 101038ngeo1475

76 N B Froumlbisch J Froumlbisch P M Sander L SchmitzO Rieppel Macropredatory ichthyosaur from the MiddleTriassic and the origin of modern trophic networks ProcNatl Acad Sci USA 110 1393ndash1397 (2013) doi 101073pnas1216750110 pmid 23297200

77 T M Scheyer C Romano J Jenks H Bucher Early Triassicmarine biotic recovery the predatorsrsquo perspective PLOS ONE9 e88987 (2014) doi 101371journalpone0088987

78 N Bardet Extinction events among Mesozoic marine reptilesHist Biol 7 313ndash324 (1994) doi 10108010292389409380462

79 R B Benson P S Druckenmiller Faunal turnover of marinetetrapods during the Jurassic-Cretaceous transition BiolRev Camb Philos Soc 89 1ndash23 (2014) doi 101111brv12038 pmid 23581455

80 M J Benton The Red Queen and the Court Jester Speciesdiversity and the role of biotic and abiotic factors throughtime Science 323 728ndash732 (2009) doi 101126science1157719 pmid 19197051

81 N D Pyenson N P Kelley J F Parham Marine tetrapodmacroevolution Physical and biological drivers on 250 Ma ofinvasions and evolution in ocean ecosystems PalaeogeogrPalaeoclimatol Palaeoecol 400 1ndash8 (2014) doi 101016jpalaeo201402018

82 J Velez-Juarbe D P Domning N D Pyenson Iterativeevolution of sympatric seacow (Dugongidae Sirenia)assemblages during the past ~26 million yearsPLOS ONE 7 e31304 (2012) doi 101371journalpone0031304

83 A M Valenzuela-Toro C S Gutstein R M Varas-MalcaM E Suarez N D Pyenson Pinniped turnover in the SouthPacific Ocean New evidence from the Plio-Pleistocene of theAtacama Desert Chile J Vertebr Paleontol 33 216ndash223(2013) doi 101080027246342012710282

84 D P Domning An ecological model for late Tertiary sirenianevolution in the North Pacific Ocean Syst Biol 25 352ndash362(1976)

85 J F Parham N D Pyenson New sea turtle from the Mioceneof Peru and the iterative evolution of feeding ecomorphologiessince the Cretaceous J Paleontol 84 231ndash247 (2010)doi 10166609-077R1

86 H Hamilton S Caballero A G Collins R L Brownell JrEvolution of river dolphins Proc R Soc B 268 549ndash556(2001) doi 101098rspb20001385 pmid 11296868

87 A E Moura et al Recent diversification of a marine genus(Tursiops spp) tracks habitat preference and environmentalchange Syst Biol 62 865ndash877 (2013) doi 101093sysbiosyt051 pmid 23929779

88 P J de Bruyn C A Tosh A Terauds Killer whale ecotypesIs there a global model Biol Rev Camb Philos Soc 8862ndash80 (2013) doi 101111j1469-185X201200239xpmid 22882545

89 J E Martin V Fischer P Vincent G Suan A longirostrineTemnodontosaurus (Ichthyosauria) with comments on EarlyJurassic ichthyosaur niche partitioning and disparityPalaeontology 55 995ndash1005 (2012) doi 101111j1475-4983201201159x

90 F R OrsquoKeefe The evolution of plesiosaur and pliosaurmorphotypes in the Plesiosauria (Reptilia Sauropterygia)Paleobiology 28 101ndash112 (2002) doi 1016660094-8373(2002)028lt0101TEOPAPgt20CO2

91 E M Fitzgerald Archaeocete-like jaws in a baleen whale BiolLett 8 94ndash96 (2012) doi 101098rsbl20110690 pmid21849306

92 O Lambert et al The giant bite of a new raptorial spermwhale from the Miocene epoch of Peru Nature 466 105ndash108(2010) doi 101038nature09067 pmid 20596020

93 D Jablonski K Roy J W Valentine R M PriceP S Anderson The impact of the pull of the recent on thehistory of marine diversity Science 300 1133ndash1135 (2003)doi 101126science1083246 pmid 12750517

94 J Alroy et al Phanerozoic trends in the global diversityof marine invertebrates Science 321 97ndash100 (2008)doi 101126science1156963 pmid 18599780

95 A B Smith G T Lloyd A J McGowan Phanerozoic marinediversity Rock record modelling provides an independenttest of large-scale trends Proc R Soc B 279 4489ndash4495(2012) doi 101098rspb20121793 pmid 22951734

96 J Veacutelez-Juarbe Ghost of seagrasses past Using sirenians asa proxy for historical distribution of seagrasses PalaeogeogrPalaeoclimatol Palaeoecol 400 41ndash49 (2014) doi 101016jpalaeo201305012

97 D T Ksepka J A Clarke The basal penguin (AvesSphenisciformes) Perudyptes devriesi and a phylogeneticevaluation of the penguin fossil record Bull Am Mus NatHist 337 1ndash77 (2010) doi 1012066531

98 M D Uhen N D Pyenson Diversity estimates biases andhistoriographic effects Resolving cetacean diversity in theTertiary Palaeontol Electronica 10 11ndash22 (2007)

99 F G Marx M D Uhen Climate critters and cetaceansCenozoic drivers of the evolution of modern whales Science327 993ndash996 (2010) doi 101126science1185581pmid 20167785

100 R D Norris S K Turner P M Hull A Ridgwell Marineecosystem responses to Cenozoic global change Science341 492ndash498 (2013) doi 101126science1240543pmid 23908226

101 G J Vermeij On escalation Annu Rev Earth Sci 41 1ndash19(2013) doi 101146annurev-earth-050212-124123

102 M E Alfaro et al Nine exceptional radiations plus highturnover explain species diversity in jawed vertebratesProc Natl Acad Sci USA 106 13410ndash13414 (2009)doi 101073pnas0811087106 pmid 19633192

103 G J Vermeij D R Lindberg Delayed herbivory and theassembly of marine benthic ecosystems Paleobiology 26419ndash430 (2000) doi 1016660094-8373(2000)026lt0419DHATAOgt20CO2

104 R Collin C M Janis in Ancient Marine Reptiles J M CallawayE L Nicholls Eds (Academic Press San Diego CA 1997)pp 451ndash466

105 C B Stringer et al Neanderthal exploitation of marinemammals in Gibraltar Proc Natl Acad Sci USA 10514319ndash14324 (2008) doi 101073pnas0805474105pmid 18809913

106 T C Rick J Erlandson Eds Human Impacts on AncientMarine Ecosystems A Global Perspective (Univ of CaliforniaPress Berkeley 2008)

107 D J McCauley et al Marine defaunation Animal loss in theglobal ocean Science 347 1255641 (2015) doi 101126science1255641 pmid 25593191

108 S T Turvey C L Risley Modelling the extinction of Stellerrsquossea cow Biol Lett 2 94ndash97 (2006) doi 101098rsbl20050415 pmid 17148336

109 R R Reeves T D Smith in Whales Whaling and OceanEcosystems J A Estes et al Eds (Univ of California PressBerkeley 2006) pp 82ndash101

110 L R Gerber R Hilborn Catastrophic events and recoveryfrom low densities in populations of otariids Implications forrisk of extinction Mammal Rev 31 131ndash150 (2001)doi 101046j1365-2907200100081x

111 D M Scheel et al Biogeography and taxonomy of extinctand endangered monk seals illuminated by ancient DNA andskull morphology ZooKeys 409 1ndash33 (2014) doi 103897zookeys4096244 pmid 24899841

112 C L Hubbs K S Norris in Antarctic Pinnipedia W H BurtEd (American Geophysical Union Washington DC 1971)pp 35ndash52

113 M L Bonnell R K Selander Elephant seals Geneticvariation and near extinction Science 184 908ndash909(1974) doi 101126science1844139908pmid 4825892

114 G J Vermeij Biogeography of recently extinct marinespecies Implications for conservation Conserv Biol 7391ndash397 (1993) doi 101046j1523-1739199307020391x

115 S Boessenkool et al Relict or colonizer Extinction andrange expansion of penguins in southern New ZealandProc R Soc B 276 815ndash821 (2009) doi 101098rspb20081246 pmid 19019791

116 T L Jones et al The protracted Holocene extinction ofCaliforniarsquos flightless sea duck (Chendytes lawi) and itsimplications for the Pleistocene overkill hypothesis ProcNatl Acad Sci USA 105 4105ndash4108 (2008) doi 101073pnas0711140105 pmid 18334640

117 IUCN Red List of Species version 20143 wwwiucnredlistorg118 N D Pyenson Requiem for Lipotes An evolutionary

perspective on marine mammal extinction Mar Mamm Sci25 714ndash724 (2009) doi 101111j1748-7692200800266x

119 T Gerrodette L Rojas‐Bracho Estimating the successof protected areas for the vaquita Phocoena sinusMar Mamm Sci 27 E101ndashE125 (2011) doi 101111j1748-7692201000449x

120 F Ritter Collisions of sailing vessels with cetaceansworldwide First insights into a seemingly growing problemJ Cetacean Res Manage 12 119ndash128 (2012)

121 R M Rolland et al Evidence that ship noise increases stressin right whales Proc R Soc B 279 2363ndash2368 (2012)doi 101098rspb20112429 pmid 22319129

122 P L Tyack et al Beaked whales respond to simulated andactual navy sonar PLOS ONE 6 e17009 (2011) doi 101371journalpone0017009

123 M C Fossi et al Large filter feeding marine organismsas indicators of microplastic in the pelagic environmentThe case studies of the Mediterranean basking shark(Cetorhinus maximus) and fin whale (Balaenoptera physalus)Mar Environ Res 100 17ndash24 (2014) doi 101016jmarenvres201402002 pmid 24612776

124 F F Mazzillo K Shapiro M W Silver A new pathogentransmission mechanism in the ocean The case of sea otterexposure to the land-parasite Toxoplasma gondii PLOS ONE8 e82477 (2013) doi 101371journalpone0082477

125 O Schofield et al How do polar marine ecosystems respondto rapid climate change Science 328 1520ndash1523 (2010)doi 101126science1185779 pmid 20558708

126 S E Alter et al Climate impacts on transocean dispersaland habitat in gray whales from the Pleistocene to 2100Molec Ecol 24 1510ndash1522 (2015) doi 10111mec13121

127 S E Noakes N D Pyenson G McFall Late Pleistocene graywhales (Eschrichtius robustus) offshore Georgia USA andthe antiquity of gray whale migration in the North AtlanticOcean Palaeogeogr Palaeoclimatol Palaeoecol 392502ndash509 (2013) doi 101016jpalaeo201310005

128 H Heatwole A Grech J F Monahan S King H MarshThermal biology of sea snakes and sea kraits Integr CompBiol 52 257ndash273 (2012) doi 101093icbics080pmid 22669175

129 L I Wright et al Turtle mating patterns buffer againstdisruptive effects of climate change Proc R Soc B 2792122ndash2127 (2012) doi 101098rspb20112285pmid 22279164

130 P C Fiedler Environmental change in the eastern tropicalPacific Ocean Review of ENSO and decadal variabilityMar Ecol Prog Ser 244 265ndash283 (2002) doi 103354meps244265

aaa3716-6 17 APRIL 2015 bull VOL 348 ISSUE 6232 sciencemagorg SCIENCE

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131 J A Estes et al Trophic downgrading of planet EarthScience 333 301ndash306 (2011) doi 101126science1205106pmid 21764740

132 J A Estes M T Tinker T M Williams D F Doak Killerwhale predation on sea otters linking oceanic andnearshore ecosystems Science 282 473ndash476 (1998)doi 101126science2825388473 pmid 9774274

133 D G Ainley G Ballard K M Dugger Competition amongpenguins and cetaceans reveals trophic cascades in thewestern Ross Sea Antarctica Ecology 87 2080ndash2093(2006) doi 1018900012-9658(2006)87[2080CAPACR]20CO2 pmid 16937647

134 B A Block et al Tracking apex marine predator movementsin a dynamic ocean Nature 475 86ndash90 (2011) doi 101038nature10082 pmid 21697831

135 K I Ohshima et al Antarctic Bottom Water productionby intense sea-ice formation in the Cape Darnleypolynya Nat Geosci 6 235ndash240 (2013) doi 101038ngeo1738

136 See supplementary materials on Science Online137 TSCreator version 64 httpsengineeringpurdueedu

Stratigraphytscreatorindexindexphp138 J Veacutelez-Juarbe C A Brochu H Santos A gharial from the

Oligocene of Puerto Rico Transoceanic dispersal in the history

of a non-marine reptile Proc R Soc B 274 1245ndash1254 (2007)doi 101098rspb20060455 pmid 17341454

139 T H Worthy A J D Tennyson C Jones J A McNamaraB J Douglas Miocene waterfowl and other birds fromCentral Otago New Zealand J Syst Palaeontol 5 1ndash39(2007) doi 101017S1477201906001957

140 T L Fulton B Letts B Shapiro Multiple losses of flight andrecent speciation in steamer ducks Proc R Soc B 2792339ndash2346 (2012) doi 101098rspb20112599 pmid 22319122

141 T L Fulton C Strobeck Multiple fossil calibrations nuclearloci and mitochondrial genomes provide new insight intobiogeography and divergence timing for true seals (PhocidaePinnipedia) J Biogeogr 37 814ndash829 (2010) doi 101111j1365-2699201002271x

142 F Hailer et al Nuclear genomic sequences reveal thatpolar bears are an old and distinct bear lineageScience 336 344ndash347 (2012) doi 101126science1216424 pmid 22517859

143 K Rassmann D Tautz F C Trillmich C GliddonThe microevolution of the Galaacutepagos marine iguanaAmblyrhynchus cristatus assessed by nuclear andmitochondrial genetic analyses Mol Ecol 6 437ndash452(1997) doi 101046j1365-294X199700209x

144 TimeTree wwwtimetreeorg

145 S B Hedges J Dudley S Kumar TimeTree A publicknowledge-base of divergence times among organismsBioinformatics 22 2971ndash2972 (2006) doi 101093bioinformaticsbtl505 pmid 17021158

146 Fossil Calibration Database httpfossilcalibrationsorg147 F Gradstein J Ogg M Schmitz G Ogg The Geologic Time

Scale 2012 (Elsevier Amsterdam 2012)

ACKNOWLEDGMENTS

We thank D Erwin J Jackson M Carrano J Goldbogen J ParhamJ Velez-Juarbe and J Oster for helpful comments on previous versionsof this paper and three anonymous reviewers for helpful suggestionsD Johnston provided the penguin photograph for Fig 2 Supportedby a Smithsonian Institution Peter Buck Postdoctoral Fellowship(NPK) a Smithsonian Institution National Museum of Natural HistorySmall Grant Award and the Remington Kellogg Fund (NDP) andthe Basis Foundation (NDP and NPK)

SUPPLEMENTARY MATERIALS

wwwsciencemagorgcontent3486232aaa3716supplDC1Materials and MethodsReferences (137ndash147)

101126scienceaaa3716

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AnthropoceneEvolutionary innovation and ecology in marine tetrapods from the Triassic to the

Neil P Kelley and Nicholas D Pyenson

DOI 101126scienceaaa3716 (6232) aaa3716348Science

this issue 101126scienceaaa3716Sciencefor such convergence of form and the threats they face from future environment changedescribe the innovations that facilitated the evolution of these marine forms the environmental conditions that selected evolved are remarkably similar Kelley and Pyenson review the literature on marine vertebrate groups over time andAlthough these groups are widely distributed among reptiles mammals amphibians and birds the shapes they have

Over biological history several different groups of vertebrate tetrapods have reinvaded the marine environmentSimilar shapes inhabit the sea

ARTICLE TOOLS httpsciencesciencemagorgcontent3486232aaa3716

MATERIALSSUPPLEMENTARY httpsciencesciencemagorgcontentsuppl201504153486232aaa3716DC1

CONTENTRELATED filecontentpendingyes

REFERENCES

httpsciencesciencemagorgcontent3486232aaa3716BIBLThis article cites 135 articles 36 of which you can access for free

PERMISSIONS httpwwwsciencemagorghelpreprints-and-permissions

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is a registered trademark of AAASScienceScience 1200 New York Avenue NW Washington DC 20005 The title (print ISSN 0036-8075 online ISSN 1095-9203) is published by the American Association for the Advancement ofScience

Copyright copy 2015 American Association for the Advancement of Science

on June 16 2020

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nloaded from