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Stable Isotope Evidence for an Amphibious Phase in Early Proboscidean Evolution

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Stable Isotope Evidence for an Amphibious Phase in Early Proboscidean Evolution Stable isotope evidence for an amphibious phase in early proboscidean evolution Alexander G. S. C. Liu*†, Erik R. Seiffert‡, and Elwyn L. Simons†§ *Department of Earth Sciences, University of Oxford, Parks Road, Oxford OX1 3PR, United Kingdom; ‡Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794-8081; and §Division of Fossil Primates, Duke Lemur Center, 1013 Broad Street, Durham, NC 27705 Contributed by Elwyn L. Simons, February 7, 2008 (sent for review December 19, 2007) The order Proboscidea includes extant elephants and their extinct and it exhibits none of the characteristics that would facilitate relatives and is closely related to the aquatic sirenians (manatees and underwater hearing (14). Moeritherium’s postcranial morphology is dugongs) and terrestrial hyracoids (hyraxes). Some analyses of em- not well known, but similarities to members of the extinct aquatic bryological, morphological, and paleontological data suggest that or semiaquatic clade Desmostylia have been noted (15). The pelvis proboscideans and sirenians shared an aquatic or semiaquatic com- associated with the most complete axial skeleton of Moeritherium mon ancestor, but independent tests of this hypothesis have proven has a very small hip socket (E.L.S., unpublished observation on elusive. Here we test the hypothesis of an aquatic ancestry for Yale Moeritherium skeleton), suggesting hindlimb reduction as in ␦18 advanced proboscideans by measuring O in tooth enamel of two aquatic mammals. It has been argued that many of the features late Eocene proboscidean genera, Barytherium and Moeritherium, Moeritherium shares with sea cows might be convergences resulting which are sister taxa of Oligocene-to-Recent proboscideans. The in part from adaptation to shared aquatic lifestyle (13, 16, 17). ␦18 ␦18 combination of low O values and low O standard deviations in Much less is known about contemporaneous Barytherium.Itis Barytherium and Moeritherium matches the isotopic pattern seen in likely that the genus occupies a key position in proboscidean aquatic and semiaquatic mammals, and differs from that of terrestrial phylogeny, being either a sister group of Oligocene-to-Recent mammals. ␦13C values of these early proboscideans suggest that both elephantiforms (ref. 4, Fig. 1), or perhaps a derived sister group of genera are likely to have consumed freshwater plants, although a an older (early Eocene) genus such as Daouitherium or Numido- component of C3 terrestrial vegetation cannot be ruled out. The simplest explanation for the combined evidence from isotopes, dental therium (1). Barytherium grave was first recovered from the Dir Abu functional morphology, and depositional environments is that Bar- Lifa Member of the Qasr el-Sagha Formation in the Fayum region ytherium and Moeritherium were at least semiaquatic and lived in of Egypt, which preserves both nearshore and alluvial deposits (18), freshwater swamp or riverine environments, where they grazed on and is estimated to have approached the size of modern Asian freshwater vegetation. These results lend new support to the hy- elephants (11). Barytherium remains from Libya derive from evap- pothesis that Oligocene-to-Recent proboscideans are derived from orite deposits that are probably diagenetic in origin (19). The genus amphibious ancestors. was evidently more plantigrade than modern elephants (20). Ideally, diverse lines of evidence, such as sedimentology, Barytherium ͉ Eocene ͉ Fayum ͉ Moeritherium ͉ Proboscidea taphonomy, functional morphology, and analysis of coexisting fauna and flora could be used to determine the paleoecology he elephants Elephas and Loxodonta (order Proboscidea) are and habitat of these early proboscideans, but in this case the Tthe only living remnants of a major adaptive radiation whose situation is complicated by the large number of possible origin can now be traced back to the earliest Eocene (Ϸ55 million environments involved and a dearth of well-preserved post- years ago) in Africa (1). Genomic data place proboscideans within cranial skeletal material. This study employs stable isotopic the placental mammalian superorder Afrotheria (2) and the more evidence from tooth enamel to test the hypothesis that early restricted supraordinal clade Paenungulata, which also contains the proboscideans were amphibious, and it focuses on two late aquatic manatees and dugongs (order Sirenia) and terrestrial Eocene genera, Barytherium and Moeritherium, based on sam- hyraxes (order Hyracoidea). Genetic evidence has thus far failed to ples recently collected from early late Eocene (Ϸ37 million- resolve relationships among paenungulate orders (2, 3), but a recent year-old) deposits of the Birket Qarun Formation in northern analysis of genomic and morphological evidence provided weak Egypt. The fossil-bearing sediments at the primary fossil support for a Proboscidea–Sirenia clade (Tethytheria) to the ex- locality in the area, Birket Qarun Locality 2 or BQ-2, were clusion of Hyracoidea (4). A monophyletic Tethytheria has long deposited during periodic flooding events of a landscape that been seen as the best explanation for available morphological otherwise might have regularly become ponded and stagnant; evidence (5) and is key to the hypothesis [also based on develop- vertebrate fossils are predominantly of terrestrial animals, but mental (6) and paleontological (5, 7) evidence] that the common the presence of shark and marine fish remains, and marine ancestor of elephants and sea cows might have been at least sediments above and below BQ-2, indicate that deposition semiaquatic. occurred very close to the coast (21). Therefore the Birket Eocene proboscideans were radically different from living ele- Qarun proboscideans could have inhabited a wide range of phants in their size, skeletal and dental morphology, and presum- habitats, including fluvial, coastal, lagoonal, or estuarine ably many aspects of their ecology and behavior as well (5, 7–9). environments. Moeritherium was tapir-sized and possibly had a prehensile upper lip rather than a trunk (8). Moeritherium’s lifestyle has been debated for over a century, with different lines of evidence supporting an Author contributions: A.G.S.C.L., E.R.S., and E.L.S. designed research; A.G.S.C.L. performed aquatic, semiaquatic, or terrestrial mode of life (7, 9–13). Cranial research; A.G.S.C.L. analyzed data; and A.G.S.C.L. and E.R.S. wrote the paper. features of Moeritherium that are seen in some aquatic or semia- The authors declare no conflict of interest. quatic mammals, such as a long, tubular cranium and anteriorly †To whom correspondence may be addressed. E-mail: [email protected] or esimons@ positioned orbits, have previously been cited as evidence for an duke.edu. amphibious lifestyle, but they are not restricted to aquatic mammals This article contains supporting information online at www.pnas.org/cgi/content/full/ (10). The auditory region of Moeritherium is more similar to that of 0800884105/DCSupplemental. extant elephants than to those of sirenians or older proboscideans, © 2008 by The National Academy of Sciences of the USA 5786–5791 ͉ PNAS ͉ April 15, 2008 ͉ vol. 105 ͉ no. 15 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0800884105 Downloaded by guest on September 28, 2021 ods (25), which are suitable provided that diagenetic alteration has not changed the original in vivo isotopic signatures of the teeth. Studies incorporating carbon and oxygen isotope analyses of tooth enamel hydroxyapatite have demonstrated that they are legitimate proxies for the habitat and diet of aquatic and terrestrial mammals in modern environments (22). Carbon isotope ratios recorded in mammalian tooth enamel can be used as a proxy for diet (26) because different types of vegetation have distinct ␦13C values (27). Such differences result from isotopic fractionation during photosynthesis, productivity changes, and dissolved CO2 and bicarbonate levels in the surrounding envi- ronment (22). Carbon is integrated into mammalian body tissue in a ratio that is proportional to that in which it is taken up by the animal in the form of food (22). Therefore the carbon isotopes incorporated into body tissues record the isotopic signature of the food the mammal eats, and, by correcting for several fractionation steps, allow the ␦13C values of the plants in an environment to be correlated with the ␦13C of tooth enamel in their consumers all of the way up the food chain (22). There Fig. 1. Phylogenetic relationships of Paleogene proboscideans, from is considerable overlap between the ␦13C ranges of certain Seiffert (4). vegetation types (Fig. 2B), but the use of other isotopic proxies (e.g., strontium) can potentially resolve such problems (28). The standard deviation of ␦18O values in tooth enamel has Inferring the Habitat and Dietary Preferences of Early been found to differ between terrestrial and aquatic mammals, Proboscideans Through Stable Isotope Analysis with most terrestrial species showing markedly higher standard The stable isotopes analyzed in this study are those of carbon (in the deviations than aquatic ones (22). The oxygen isotope ratio recorded in body tissues depends on three factors: the temper- form of ␦13C) and oxygen (as ␦18O). Because the degree of isotope ature at which the tissue/mineral is deposited, fractionation fractionation differs in different organic tissues, comparative anal- during metabolic and biological activity within the organism, and yses of fossil taxa should be based on one tissue type (22). Tooth the fluxes and isotopic composition of the oxygen-containing enamel bioapatite is favored for isotopic studies of extinct taxa matter entering the animal (29). The physiological fractionation because of its durability and abundance in the fossil record. Enamel of isotopes varies by species (30, 31), being determined by the is also not easily altered during diagenesis, giving it an advantage animal’s metabolism and the oxygen exchanges into and out of over dentin and bone (23). its body (32), which are, in turn, dependent on its size and mode Tooth enamel grows in layers from the crown to the base at a rate of life. Because the fractionations for fossil taxa cannot be EVOLUTION of Ϸ30–60 mm/yr in large herbivores (24).
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