Skip to main content

Advertisement

SpringerLink
Log in

Were There Miocene Meridiolestidans? Assessing the Phylogenetic Placement of Necrolestes patagonensis and the Presence of a 40 Million Year Meridiolestidan Ghost Lineage

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

The enigmatic mammal Necrolestes patagonensis from the Miocene of Patagonia possesses a highly apomorphic osteological form that has confounded phylogenetic interpretation for over a century. In this time it has been affiliated with both eutherians and metatherians; however, a recent study by Rougier et al. (Proc Natl Acad Sci USA 109:19871–19872, 2012) raises the intriguing possibility that Necrolestes is a relictual member of a clade of South American non-therian dryolestoids, the Meridiolestida. This group is known chiefly from the Cretaceous of South America and assignment of Necrolestes to Meridiolestida implies a ghost lineage of about 40 million years. Such a lengthy ghost lineage requires strong evidence, which minimizes potentially circular assumptions of anatomical homology. Here, we vary the coding of cusp homologies in Necrolestes, previously assumed to diverge from the metatherian pattern, and add zalambdodont and incipiently zalambdodont metatherian taxa to the analyses, in order to assess the effects of non-independent characters and taxon sampling on the original topology. The results of both maximum parsimony and Bayesian analysis using the Mk model show that these possible sources of bias have little effect on the topology and ultimately increase confidence in the placement of Necrolestes in Meridiolestida and its concomitant 40 million year ghost lineage. Additionally, our Bayesian analysis resolves Australosphenida in a trichotomy with Peramus and Vincelestes + Boreosphenida. This contrasts with the majority of existing topologies, and raises interesting questions regarding both the evolution of tribospheny and the use of the Mk model with paleontological datasets.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ameghino F (1891) Nuevos restos de mamíferos fósiles descubiertos por Carlos Ameghino en el Eoceno inferior de la Patagonia austral. Especies nuevas adiciones y correcciones. Rev Arg Hist Nat 1:289–328

    Google Scholar 

  • Archer M, Beck R, Gott M, Hand S, Godthelp H, Black K (2011) Australia’s first fossil marsupial mole (Notoryctemorphia) resolves controversies about their evolution and palaeoenvironmental origins. Proc R Soc B 278:1498–1506

    Google Scholar 

  • Archer M, Hand S, Godthelp H (1988) A new order of Tertiary zalambdodont marsupials. Science 239:1528–1531

    Article  CAS  PubMed  Google Scholar 

  • Asher RJ, Horovitz I, Martin T, Sánchez-Villagra M (2007) Neither a rodent nor a platypus: a reexamination of Necrolestes patagonensis Ameghino. Am Mus Novitates 3546:1–40

    Article  Google Scholar 

  • Asher RJ, Maree S, Bronner G, Bennett NC, Bloomer P, Czechowski P, Meyer M, Hofreiter M (2010) A phylogenetic estimate for golden moles (Mammalia, Afrotheria, Chrysochloridae). BMC Evol Biol 10:69

    Article  PubMed Central  PubMed  Google Scholar 

  • Asher RJ, Sánchez-Villagra M (2005) Locking yourself out: diversity among dentally zalambdodont therian mammals. J Mammal Evol 12:265–282

    Google Scholar 

  • Averianov A, Lopatin A (2008) ‘Protocone’ in a pretribosphenic mammal and upper dentition of tinodontid ‘symmetrodontans’. J Vertebr Palaeontol 28:548–552

    Google Scholar 

  • Averianov AO, Martin T, Lopatin AV (2013) A new phylogeny for basal Trechnotheria and Cladotheria and affinities of South American endemic Late Cretaceous mammals. Naturwissenschaften 100:311–326

    Article  CAS  PubMed  Google Scholar 

  • Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV (2012) Improving the accuracy of demographic and molecular clock comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29:2157–2167

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Beck RMD (2009) Was the Oligo-Miocene Australian metatherian Yalkaparidon a ‘mammalian woodpecker’? Biol J Linn Soc 97:1–17

    Article  Google Scholar 

  • Beck RMD, Travouillon KJ, Aplin KP, Godthelp H, Archer M (2013) The osteology and systematics of the enigmatic Australian Oligo-Miocene metatherian Yalkaparidon (Yalkaparidontidae; Yalkaparidontia; ?Australidelphia; Marsupialia). J Mammal Evol DOI 10.1007/s10914-013-9236-3

    Google Scholar 

  • Bown TM, Kraus MJ (1979) Origin of the tribosphenic molar and metatherian and eutherian dental formulae. In: Lillegraven JA, Kielan-Jaworowska Z, Clemens WA (eds) Mesozoic Mammals: The First Two-thirds of Mammalian History. University of California Press, Berkeley, pp 172–181

    Google Scholar 

  • Brandley MC, Schmitz A, Reeder TW (2005) Partitioned Bayesian analyses, partition choice and the phylogenetic relationships of scincid lizards. Syst Biol 54:373–390

    Article  PubMed  Google Scholar 

  • Bremer K (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795–803

    Article  CAS  Google Scholar 

  • Bremer K (1994) Branch support and tree stability. Cladistics 10:295–304

    Article  Google Scholar 

  • Chimento NR, Agnolin FL, Novas FE (2012) The patagonian fossil mammal Necrolestes: a Neogene survivor of Dryolestoidea. Rev Mus Argent Cienc Nat 14:1–47

    Google Scholar 

  • Chow M, Rich THV (1982) Shuotherium dongi, n. gen . and sp., a therian with pseudo-tribosphenic molars from the Jurassic of Sichuan, China. Aust Mammal 5:127–142

    Google Scholar 

  • Clemens WA, Mills JRE (1971) Review of Peramus tenuirostris. Bull Brit Mus (Nat Hist) Geol 20: 89–113

    Google Scholar 

  • Crompton AW (1971) The origin of the tribosphenic molar. In: DM Kermack, KA Kermack (eds) Early Mammals. Zool J Linn Soc 50, Suppl 1: 65–87

  • Davis BM (2011) Evolution of the tribosphenic molar pattern in early mammals, with comments on the “dual-origin” hypothesis. J Mammal Evol 18:227–244

    Article  Google Scholar 

  • de Pinna MGG (1991) Concepts and tests of homology in the cladistics paradigm. Cladistics 7:367–394

    Article  Google Scholar 

  • Fan Y, Wu R, Chen M-H, Kuo L, Lewis PO (2011) Choosing among partition models in Bayesian phylogenetics. Mol Biol Evol 28:523–532

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Felsenstein J (1978) The number of evolutionary trees. Syst Zool 27:27–33

    Article  Google Scholar 

  • Flynn JJ, Parrish JM, Rakotosamimanana B, Simpson WF, Wyss AE (1999) A Middle Jurassic mammal from Madagascar. Nature 401:57–60

    Article  CAS  Google Scholar 

  • Gelfo JN, Goin FJ, Woodburne MO, Muizon C de (2009) Biochronological relationships of the earliest South American Paleogene mammalian faunas. Palaeontology 52:251–269

    Google Scholar 

  • Gelfo JN, Pascual R (2001) Peligrotherium tropicalis (Mammalia, Dryolestida) from the early Paleocene of Patagonia, a survival from a Mesozoic Gondwanan radiation. Geodiversitas 23: 369–379

    Google Scholar 

  • Goin FJ, Abello A, Bellosi E, Kay R, Madden R, Carlini A (2007) Los Metatheria sudamericanos de comienzos del Neógeno (Mioceno temprano, edad-mamífero Colhuehuapense). Part I: Introducción, Didelphimorphia y Sparassodonta [The South American early Neogene Metatheria (early Miocene, Colhuehuapian mammal age). Part I: Introduction, Didelphimorphia and Sparassodonta]. Ameghiniana 44:29–71

    Google Scholar 

  • Gurovich Y, Beck RMD (2009) The phylogenetic affinities of the enigmatic mammaliam clade Gondwanatheria. J Mammal Evol 16:25–49

    Article  Google Scholar 

  • Hennig W (1966) Phylogenetic Systematics. University of Illinois Press, Urbana

    Google Scholar 

  • Kangas AT, Evans AR, Thesleff I, Jernvall J (2004) Nonindependence of mammalian dental characters. Nature 432:211–214

    Article  CAS  PubMed  Google Scholar 

  • Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795

    Article  Google Scholar 

  • Kielan-Jaworowska Z, Cifelli RL, Luo Z-X (2004) Mammals from the Age of Dinosaurs: Origins, Evolution and Structure. Columbia University Press, New York

    Google Scholar 

  • Ladevéze S, Asher RJ, Sánchez-Villagra MR (2008) Petrosal anatomy in the fossil mammal Necrolestes: evidence for metatherian affinities and comparisons with the extant marsupial mole. J Anat 213:686–697

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee MSY, Worthy TH (2012) Likelihood reinstates Archaeopteryx as a primitive bird. Biol Lett 8:299–303

    Article  PubMed Central  PubMed  Google Scholar 

  • Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50:913–925

    Article  CAS  PubMed  Google Scholar 

  • Lillegraven JA (1974) Biogeographical considerations of the marsupial-placental dichotomy. Annu Rev Ecol Syst 5:263–283

    Article  Google Scholar 

  • Luo Z-X, Cifelli RL, Kielan-Jaworowska Z (2001) Dual origin of tribosphenic mammals. Nature 409:53–57

    Article  CAS  PubMed  Google Scholar 

  • Luo Z-X, Ji Q, Yuan C-X (2007) Convergent dental adaptations in pseudo-tribosphenic and tribosphenic mammals. Nature 450:93–97

    Article  CAS  PubMed  Google Scholar 

  • Luo Z-X, Kielan-Jaworowska Z, Cifelli RL (2002) In quest for a phylogeny of Mesozoic mammals. Acta Palaeontol Pol 47:1–78

    Google Scholar 

  • Luo Z-X, Martin T (2007) Analysis of molar structure and phylogeny of docodont genera. Bull Carnegie Mus Nat Hist 39:27–47

    Google Scholar 

  • Maddison WP (1993) Missing data versus missing characters in phylogenetic analysis. Syst Biol 42:576–581

    Article  Google Scholar 

  • Maddison WP, Maddison DR (2010) Mesquite: a modular system for evolutionary analysis. Version 2.75 http://mesquiteproject.org

  • Martin T, Rauhut OWM (2005) Mandible and dentition of Asfaltomylos patagonicus (Australosphenida, Mammalia) and the evolution of tribosphenic teeth. J Vertebr Paleontol 25:414–425

    Article  Google Scholar 

  • McKenna MC (1975) Toward a phylogenetic classification of the Mammalia. In: Luckett WP, Szalay FS (eds) Phylogeny of the Primates. Plenum Press, New York, pp 21–46

    Chapter  Google Scholar 

  • Murray PF, Megirian D (2006) The Pwerte Marnte Marnte local fauna: a new vertebrate assemblage of presumed Oligocene age from the Northern Territory of Australia. Alcheringa Sp1:211–228

    Google Scholar 

  • Nixon KC (1999–2002) WinClada ver. 1.0000. Published by the author, Ithaca, NY, USA

  • Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67

    Article  PubMed  Google Scholar 

  • Patterson B (1958) Affinities of the patagonian fossil mammal Necrolestes. Breviora Mus Comp Zool 94:1–14

    Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.4, Available from http://beast.bio.ed.ac.uk/Tracer

  • Rauhut OWM, Martin T, Ortiz-Jaureguizar E, Puerta P (2002) A Jurassic mammal from South America. Nature 416:165–168

    Article  CAS  PubMed  Google Scholar 

  • Rich TH, Flannery TF, Trusler P, Kool L, Klaveren NA, Vickers-Rich P (2002) Evidence that monotremes and ausktribosphenids are not sister groups. J Vertebr Paleontol 22:466–479

    Google Scholar 

  • Rich TH, Vickers-Rich P (2010) Pseudotribosphenic: the history of a concept. Vertebr PalAsiatic 48:336–347

    Google Scholar 

  • Rodgers J (2008) Notoryctes typhlops Digital Morphology http://digimorph.org/specimens/Notoryctes_typhlops/

  • Ronquist F, Teslenko M, Mark P, van der Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Google Scholar 

  • Ronquist F, van der Mark P, Huelsenbeck JP (2009) Bayesian phylogenetic analysis using MrBayes, Theory. In: Lemey P, Salemi M, Vandamme A-M (eds) The Phylogenetic Handbook, a Practical Approach to Phylogenetic Analysis and Hypothesis Testing, 2nd edn. Cambridge University Press, Cambridge, pp 210–236

    Chapter  Google Scholar 

  • Rougier GW, Apesteguia S, Gaetano LC (2011) Highly specialized mammalian skulls from the Late Cretaceous of South America. Nature 479:98–102

    Article  CAS  PubMed  Google Scholar 

  • Rougier GW, Martinelli AG, Forasiepi AM, Novacek MJ (2007) New Jurassic mammals from Patagonia, Argentina: a reappraisal of australosphenidan morphology and interrelationships. Am Mus Novitates 3566:1–54

    Google Scholar 

  • Rougier GW, Wible JR, Beck RMD, Apesteguia S (2012) The Miocene mammal Necrolestes demonstrates the survival of a Mesozoic nontherian lineage into the late Cenozoic of South America. Proc Natl Acad Sci USA 109:19871–19872

    Article  Google Scholar 

  • Rowe T, Rich TH, Vickers-Rich P, Springer M, Woodburne MO (2008) The oldest platypus and its bearing on divergence timing of the platypus and echidna clades. Proc Natl Acad Sci USA 105:1238–1242

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Scott WB (1905) Insectivora and Glires. Reports of the Princeton University Expedition to Patagonia 1896–1899 5:365–499

    Google Scholar 

  • Sigogneau-Russell D (2003) Docodonts from the British Mesozoic. Acta Palaeontol Polonica 48:357–374

    Google Scholar 

  • Sigogneau-Russell D, Hooker JJ, Ensom PC (2001) The oldest tribosphenic mammal from Laurasia (Purbeck Limestone Group, Berriasian, Cretaceous, U.K.) and its bearing on the ‘dual origin’ of Tribosphenida. C R Acad Sci Paris, Earth Planet Sci 333:141–147

    Google Scholar 

  • Simmons MP (2012a) Radical instability and supurious branch support by likelihood when applied to matrices with non-random distributions of missing data. Mol Phylogenet Evol 62:472–484

    Article  PubMed  Google Scholar 

  • Simmons MP (2012b) Misleading results of likelihood-based phylogenetic analyses in the presence of missing data. Cladistics 28:208–222

    Article  Google Scholar 

  • Spencer MR, Wilberg EW (2013) Efficacy or convenience? Model-based approaches to phylogeny estimation using morphological data. Cladistics DOI: 10.1111/cla.12018

    Google Scholar 

  • Suzuki Y, Glazko GV, Nei M (2002) Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proc Natl Acad Sci USA 99:16138–16143

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland, MA

  • Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37:221–244

    Article  CAS  Google Scholar 

  • Thompson RS, Bärmann EV, Asher RJ (2012) The interpretation of hidden support in combined data phylogenetics. J Zool Syst Evol Res 50:251–263

    Article  Google Scholar 

  • Van Valen L (1988) Faunas of a southern world. Nature 333:113

    Article  Google Scholar 

  • Wiens J, Morrill MC (2011) Missing data in phylogenetic analysis: reconciling results from simulations and empirical data. Syst Biol 60:719–731

    Article  PubMed  Google Scholar 

  • Woodburne MO (2003) Monotremes as pretribosphenic mammals. J Mammal Evol 10:195–248

    Article  Google Scholar 

  • Woodburne MO, Goin FJ, Bond M, Carlini AA, Gelfo JN, López GM, Iglesias A, Zimicz AN (2013) Paleogene land mammal faunas of South America; a response to global climatic changes and indigenous floral diversity. J Mammal Evol doi: 10.1007/s10914-012-9222-1

    Google Scholar 

  • Woodburne MO, Rich TH, Springer MS (2003) The evolution of tribospheny and the antiquity of mammalian clades. Mol Phylogenet Evol 28:360–385

    Google Scholar 

  • Xie W, Lewis PO, Fan Y, Kuo L, Chen M-H (2011) Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst Biol 60:150–160

    Article  PubMed Central  PubMed  Google Scholar 

  • Xu X, Pol D (2013) Archaeopteryx, paravian phylogenetic analyses, and the use of probability-based methods for palaeontological datasets. J Syst Palaeontol DOI: 10.1080/14772019.2013.764357

    Google Scholar 

  • Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov chain Monte Carlo method. Mol Biol Evol 14:717–724

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Robin Beck and one anonymous reviewer for their detailed comments and critique, which greatly improved both the analyses and content of our study. Thanks go to Dr. Robert Asher for providing the premise for this study, his many useful comments on the manuscript, as well as his support and encouragement throughout the project. Matt Lowe and the staff at the University Museum of Zoology, Cambridge provided support and access to specimens of Notoryctes. We also thank Nicola Heckeberg for support and assistance during data analyses, as well as Martin R. Smith for inspiring and assisting with the Bayes Factor analyses. RO’s work is funded by the Cambridge Home and EU Scholarship Scheme (CHESS).

Author information

Authors and Affiliations

  1. The University Museum of Zoology, Downing Street, Cambridge, CB2 3EJ, UK

    Rachel N. O’Meara & Richard S. Thompson

Authors
  1. Rachel N. O’Meara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard S. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard S. Thompson.

Additional information

Rachel N. O’Meara and Richard S. Thompson contributed equally to this work, and consider this a joint first-authorship manuscript.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 88 kb)

OMeara_and_Thompson_matrix

(TXT 26 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

O’Meara, R.N., Thompson, R.S. Were There Miocene Meridiolestidans? Assessing the Phylogenetic Placement of Necrolestes patagonensis and the Presence of a 40 Million Year Meridiolestidan Ghost Lineage. J Mammal Evol 21, 271–284 (2014). https://doi.org/10.1007/s10914-013-9252-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-013-9252-3

Keywords

Search

Navigation