Population history, phylogeography, and conservation genetics of the last Neotropical mega-herbivore, the lowland tapir (Tapirus terrestris)

Abstract

BackgroundUnderstanding the forces that shaped Neotropical diversity is central issue to explain tropical biodiversity and inform conservation action; yet few studies have examined large, widespread species. Lowland tapir (Tapirus terrrestris, Perissodactyla, Tapiridae) is the largest Neotropical herbivore whose ancestors arrived in South America during the Great American Biotic Interchange. A Pleistocene diversification is inferred for the genus Tapirus from the fossil record, but only two species survived the Pleistocene megafauna extinction. Here, we investigate the history of lowland tapir as revealed by variation at the mitochondrial gene Cytochrome b, compare it to the fossil data, and explore mechanisms that could have shaped the observed structure of current populations.ResultsSeparate methodological approaches found mutually exclusive divergence times for lowland tapir, either in the late or in the early Pleistocene, although a late Pleistocene divergence is more in tune with the fossil record. Bayesian analysis favored mountain tapir (T. pinchaque) paraphyly in relation to lowland tapir over reciprocal monophyly, corroborating the inferences from the fossil data these species are sister taxa. A coalescent-based analysis rejected a null hypothesis of allopatric divergence, suggesting a complex history. Based on the geographic distribution of haplotypes we propose (i) a central role for western Amazonia in tapir diversification, with a key role of the ecological gradient along the transition between Andean subcloud forests and Amazon lowland forest, and (ii) that the Amazon river acted as an barrier to gene flow. Finally, the branching patterns and estimates based on nucleotide diversity indicate a population expansion after the Last Glacial Maximum.ConclusionsThis study is the first examining lowland tapir phylogeography. Climatic events at the end of the Pleistocene, parapatric speciation, divergence along the Andean foothill, and role of the Amazon river, have similarly shaped the history of other taxa. Nevertheless further work with additional samples and loci is needed to improve our initial assessment. From a conservation perspective, we did not find a correspondence between genetic structure in lowland tapir and ecogeographic regions proposed to define conservation priorities in the Neotropics. This discrepancy sheds doubt into this scheme's ability to generate effective conservation planning for vagile species.

A new species of tapir from the Amazon

“…Our results concur partially with previous molecular phylogenies (Norman and Ashley 2000;de Thoisy et al 2010;Steiner and Ryder 2011). The mtDNA gene trees (Cytb, or Cytb þ COI þ COII) show strong support for a unique Neotropical clade, encompassing a strict South American tapir subclade (Fig.…”

“…We thank J. Patton (Museum of Vertebrate Zoology, Berkeley, California) for providing data and measurements of tapir skulls from his institution, initial comments, and advising on early stage of this manuscript; J. Vianna (Pontificia Universidad Católica de Chile, Santiago, Chile) and A. A. Nascimento (Universidade Federal de Minas Gerais, Belo Horizonte, Brazil) for participation and discussion in the initial stages of this work; C. Pedraza (Universidad de Los Andes, Bogotá, Colombia), A. Tapia (Universidad Central del Ecuador, Quito, Ecuador), M. R. Garcia (Universidad Javeriana, Bogotá, Colombia), O. Ramirez (Universidad Peruana Cayetano Heredia, Lima, Peru), and A. G. Silva (University of British Columbia Okanagan, Kelowna, Canada), who provided some samples of Neotropical Tapirus (de Thoisy et al 2010); the San Diego Zoo, San Diego, California, which provided a sample of T. indicus; L. Avilla (Federal University of the State of Rio de Janeiro, UNIRIO), who lent us 2 camera-traps; M. Marmontel (Instituto Sustentável Mamirauá, Tefé, Brazil), P. Médici (Tapir Specialist Group, www.tapirs.org), and C. Maria Jacobi (Universidade Federal de Minas Gerais, Belo Horizonte, Brazil), who helped to improve the manuscript text; and L. Emmons (National Museum of Natural History, Smithsonian Institution, Washington, D.C.), who provided many comments and English review of the final text. We thank the biology student G. Braga, who kindly made the life drawings of the male and female specimens of T. kabomani in Supporting Information S6 and S7.…”

“…Despite popular accounts of the occurrence of more than 1 tapir species in lowland Amazonia, it was assumed that observed diversity of both morphological (Hershkovitz 1954) and molecular (de Thoisy et al 2010) characters represented variations of T. terrestris (Linnaeus, 1758). We present here detailed morphological and molecular (mitochondrial DNA [mtDNA]) comparisons of specimens from western Brazilian Amazon with all other Tapirus species, which indicate the Molecular phylogenetic analyses.-The following total sample numbers, or sequences, or both, were included in the analyses: T. terrestris: n ¼ 52, T. bairdii: n ¼ 3, T. pinchaque: n ¼ 5, T. indicus: n ¼ 4, Tapirus sp.…”

“…The DNA sequences from 3 mtDNA genes (cytochrome b [Cytb], cytochrome oxidase I [COI], and cytochrome oxidase II [COII]) from living Tapirus species were generated and compared to previously published data (Ashley et al 1996;Norman and Ashley 2000;de Thoisy et al 2010). We included a thorough analysis of the Cytb in a large geographic sampling in South America, such as has been shown to be useful in recovering mammalian phylogeny and exposing cryptic species (Baker and Bradley 2006;Redondo et al 2008).…”

Continuous Miocene, Pliocene and Pleistocene Influences on Mitochondrial Diversification of the Capybara (Hydrochoerus Hydrochoeris; Hydrochoeridae, Rodentia): Incapacity to Determine Exclusive Hypotheses on the Origins of the Amazon and Orinoco Diversity for This Species

“…Also, the ancestors of this population were the first to diverge in all of the trees. The Western Amazon area was also the focus for the dispersion of many other mammalian taxa such as the lowland tapir [102][103][104][105], the jaguar [106], and diverse Neotropical primate genera [107][108][109][110].…”