A Relaxed Molecular Clock Study Within Xenarthrans
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Influence of Tertiary paleoenvironmental changes onthe diversification of South American mammals: a relaxed molecular clock study within xenarthrans. Frédéric Delsuc, Sergio Vizcaíno, Emmanuel Douzery To cite this version: Frédéric Delsuc, Sergio Vizcaíno, Emmanuel Douzery. Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans.. BMC Evolutionary Biology, BioMed Central, 2004, 4, pp.11. 10.1186/1471-2148-4-11. halsde-00192953 HAL Id: halsde-00192953 https://hal.archives-ouvertes.fr/halsde-00192953 Submitted on 29 Nov 2007 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. 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BMC Evolutionary Biology BioMed Central Research article Open Access Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans Frédéric Delsuc*1,2, Sergio F Vizcaíno3 and Emmanuel JP Douzery1 Address: 1Laboratoire de Paléontologie, Paléobiologie et Phylogénie, Institut des Sciences de l'Evolution, Université Montpellier II, Montpellier, France, 2The Allan Wilson Centre for Molecular Ecology and Evolution, Massey University, Palmerston North, New Zealand and 3Departamento Científico Paleontología de Vertebrados, Museo de La Plata, Paseo del Bosque s/n, 1900 La Plata, Argentina Email: Frédéric Delsuc* - [email protected]; Sergio F Vizcaíno - [email protected]; Emmanuel JP Douzery - [email protected] * Corresponding author Published: 28 April 2004 Received: 25 December 2003 Accepted: 28 April 2004 BMC Evolutionary Biology 2004, 4:11 This article is available from: http://www.biomedcentral.com/1471-2148/4/11 © 2004 Delsuc et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL. MammalsXenarthransEvolutionPalaeontologyPhylogenyRelaxed molecular clockBayesian datingGlobal changeTertiarySouth America Abstract Background: Comparative genomic data among organisms allow the reconstruction of their phylogenies and evolutionary time scales. Molecular timings have been recently used to suggest that environmental global change have shaped the evolutionary history of diverse terrestrial organisms. Living xenarthrans (armadillos, anteaters and sloths) constitute an ideal model for studying the influence of past environmental changes on species diversification. Indeed, extant xenarthran species are relicts from an evolutionary radiation enhanced by their isolation in South America during the Tertiary era, a period for which major climate variations and tectonic events are relatively well documented. Results: We applied a Bayesian approach to three nuclear genes in order to relax the molecular clock assumption while accounting for differences in evolutionary dynamics among genes and incorporating paleontological uncertainties. We obtained a molecular time scale for the evolution of extant xenarthrans and other placental mammals. Divergence time estimates provide substantial evidence for contemporaneous diversification events among independent xenarthran lineages. This correlated pattern of diversification might possibly relate to major environmental changes that occurred in South America during the Cenozoic. Conclusions: The observed synchronicity between planetary and biological events suggests that global change played a crucial role in shaping the evolutionary history of extant xenarthrans. Our findings open ways to test this hypothesis further in other South American mammalian endemics like hystricognath rodents, platyrrhine primates, and didelphid marsupials. Background of organisms. To be reliable these macroevolutionary Paleobiological studies aim at assessing the influence of studies must consider groups possessing a high quality past environmental changes on the evolutionary history fossil record coupled with a well documented history of Page 1 of 13 (page number not for citation purposes) BMC Evolutionary Biology 2004, 4 http://www.biomedcentral.com/1471-2148/4/11 past environmental changes encompassing geological, During this period of isolation, xenarthrans were one of ecological, climatic and biogeographical events [1]. Infer- the dominant groups of placental mammals in the succes- ring the impact of these historical events on the evolution sive South American faunas. They occupied a wide range of faunas is particularly difficult in cases where dispersal of ecological niches with fossorial, terrestrial and semi- occurred repeatedly between biogeographic areas. For this arboreal taxa, gigantic forms such as armoured glypto- reason, islands have for long attracted particular interest donts and ground sloths [17], and sloths even extending by acting as natural laboratories for the study of evolution their adaptations to the aquatic environment [18]. The [2]. Owing to its "splendid isolation" from other conti- late arrival of North American immigrants seems to have nental land masses for a great part of the Tertiary era [3], only slightly affected xenarthrans and giant terrestrial South America offers a special case of continental island- forms noteworthy became successful southern invaders of like evolution with its very peculiar mammalian fauna Central and North America [16]. Nevertheless, a great part composed of an initial nucleus of autochthonous taxa of the xenarthran diversity disappeared with the dramatic subsequently enriched by few successive waves of success- extinctions that took place at the end of the Pleistocene ful immigrants. [7] and essentially affected the largest forms [19]. This massive and global extinction event left only 30 living Numerous studies have attempted to relate the evolution- xenarthran species whose paleontological origins and ary history of mammalian fossil faunas in South America phylogenetic relationships are very difficult to decipher with well documented environmental changes [4-6]. from the available fossil record [7], although progresses However, these studies primarily rely on the quality of the have recently been made for understanding the origin of paleontological record which is by essence incomplete. some groups of living armadillos [20]. Since the seminal paper of Patterson and Pascual [7] sev- eral advances have been made on the understanding of Molecular phylogenetics is now providing a new tool to the fossil record from this Southern hemisphere continent complement paleontological and geological studies by [8]. This includes the discovery of additional fossil sites allowing to reconstruct both the phylogenetic relation- from the previously poorly sampled Tropical zone and ships of living species and the timing of their diversifica- new faunal horizons from key ages filling gaps in the tion [21]. Indeed, it is likely that global environmental stratigraphic sequence. These advances coupled with changes left their footprints in the DNA of living organ- progress from multidisciplinary studies encompassing isms from which the evolutionary history can be reliably tectonic [9], isotopic [10] and radiochemical dating [11] inferred [22]. Furthermore, there is at present accumulat- evidences have shed new light on the biotic and environ- ing molecular evidence that past environmental changes mental history of South America. have shaped the evolution of diverse terrestrial organisms such as frogs [23], squirrels [24], eulipotyphlan mammals Armadillos, anteaters, and sloths belong to Xenarthra and [25] and elephant-shrews [26]. A robust molecular picture represent the only placental group with living representa- of living xenarthran phylogenetic relationships have been tives from the initial South American mammalian stock recently established [27,28] and estimates of their diver- [7]. Owing to their longstanding evolutionary history on gence dates have already been used to test biogeographic this island continent, xenarthrans constitute a promising hypotheses [29]. However, the recent development of model for studying the influence of past environmental improved molecular dating methods offers new possibili- changes on living organisms. Indeed, the earliest records ties in estimating divergence times and allows to go one of Xenarthra in the Paleocene, about 58 million years ago step forward [21]. (Mya) [12,13] already show the morphological features proper to the group (homodonty with simple hypsodont Recent methodological advances in molecular dating teeth lacking enamel) and possess armadillo-like carapace have aimed at relaxing the assumption of the global scutes, suggesting that the group likely originated earlier molecular clock [30] by modelling the variation of the during the Paleocene or even possibly during the Late Cre- evolutionary rate along the phylogenetic tree [31-35]. taceous [14]. Xenarthra subsequently underwent an Among these newly developed methods, the Bayesian impressive Tertiary radiation which led to a great diversity