Skip to main content
Log in

Fossil Calibration of Mitochondrial Phylogenetic Relationships of North American Pine Martens, Martes, Suggests an Older Divergence of M. americana and M. caurina than Previously Hypothesized

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

Abstract

As molecularly derived phylogenies have become more prominent in determining evolutionary relationships, researchers have developed multiple methods of time-calibration to estimate ages of speciation or dispersal events. These methods, however, do not always arrive at congruent node ages. Fossil evidence is one of the most common forms of calibration for phylogenies, but age estimates can vary greatly depending on fossil choice, the taxa in question, and methodologies chosen. Using the North American pine martens, Martes americana and M. caurina, as exemplar taxa, previously calculated divergence dates derived from mutation rates and dates estimated using fossil-informed time-calibration are compared. Two fossil calibrated Bayesian phylogenies are generated: one constructed from cytochrome b; and another from a concatenated sequence matrix of 12S, 16S, cytochrome b, and Dloop. Both phylogenies are calibrated based on the fossil record of Martes at three nodes: divergence between ingroup and outgroup clades; node for crown M. americana; and node for crown M. caurina. Both phylogenies support the presence of two clades within Martes and estimate these clades, and thus species, diverged between 540 kya and 234 kya. This is approximately 200,000 years older than divergence ages calculated from mutation rates. The older dates generated here place Martes divergence within the Pre-Illinoan glacial episode instead of the younger Wisconsin glaciation as was previously hypothesized. The results of this study suggest that this clade likely evolved under the climatic influence of multiple glacial cycles throughout the Pleistocene.

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

Access this article

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

  • Aliabadian M, Kaboli M, Nijman V, Vences M (2009) Molecular identification of birds: performance of distance-based DNA barcoding in three genes to delimit parapatric species. PLoS One 4:e4119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ambriz-Morales P, De La Rosa-Reyna XF, Sifuentes-Rincon AM, Parra-Bracamonte GM, Villa-Melchor A, Chassin-Noria O, Arellano-Vera W (2016) The complete mitochondrial genomes of nine white-tailed deer subspecies and their genomic differences. J Mammal 97:234–245

    Article  Google Scholar 

  • Anderson E (1970) Quaternary evolution of the genus Martes (Carnivora, Mustelidae). Acta Zool Fenn 130:1–132

    Google Scholar 

  • Anderson E (1994) Evolution, prehistoric distribution, and systematics of Martes. In: Buskirk SW (ed) Martens, Sables and Fishers: Biology and Conservation. Cornell University Press, Ithaca, pp 13–25

  • Baltensperger AP, Morton JM, Huettmann F (2017) Expansion of American marten (Martes americana) distribution in response to climate and landscape change on the Kenai Peninsula, Alaska. J Mammal 98:703–714

    Article  Google Scholar 

  • Barido-Sottani J, Bošková V, du Plessis L, Kühnert D, Magnus C, Mitov V, Müller NF, Pečerska J, Rasmussen DA, Zhang C, Drummond AJ, Heath TA, Pybus OG, Vaughan TG, Stadler T (2016) Taming the BEAST – a community teaching material resource for BEAST 2. Syst Biol 67:170–174

    Article  Google Scholar 

  • Barnett R, Shapiro B, Barnes IAN, Ho SYW, Burger J, Yamaguchi N, Higham TFG, Wheeler HT, Rosendahl W, Sher AV, Sotnikova M, Kuznetsova T, Baryshnikov GF, Martin LD, Harington CR, Burns JA, Cooper A (2009) Phylogeography of lions (Panthera leo ssp.) reveals three distinct taxa and a late Pleistocene reduction in genetic diversity. Mol Ecol 18:1668–1677

    Article  PubMed  Google Scholar 

  • Baryshnikov G, Batyrov B (1994) Sredneplejstocenovye hisnye mlekopitaûsie (Carnivora, Mammalia) Srednej Azii. Tr ZIN/Proc Zool Inst RAN 256:3–43

    Google Scholar 

  • Behrensmeyer AK, Turner A (2013) Taxonomic occurences of Martes americana recorded in the Paleobiology Database. In: Fossilworks. http://fossilworks.org

  • Bell C, Lundelius EL Jr, Barnosky A, Graham RW, Lindsay E, Ruez DR Jr, Semken HA Jr, Webb DS, Zakrzewski RJ (2004) The Blancan, Irvingtonian, and Rancholabrean Mammal Ages. In: Woodburne MO (ed) Late Cretaceous and Cenozoic Mammals of North America. Columbia University Press, New York, pp 232–315

    Chapter  Google Scholar 

  • Benton MJ, Donoghue PCJ (2007) Paleontological evidence to date the tree of life. Mol Biol Evol 24:26–53

    Article  CAS  PubMed  Google Scholar 

  • Bibi F (2013) A multi-calibrated mitochondrial phylogeny of extant Bovidae (Artiodactyla, Ruminantia) and the importance of the fossil record to systematics. BMC Evol Biol 13:166

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradley RD, Baker RJ (2001) A test of the genetic species concept: cytochrome-b sequences and mammals. J Mammal 82:960–973

    Article  Google Scholar 

  • Broquet T, Johnson CA, Petit E, Thompson I, Burel F, Fryxell JM (2006a) Dispersal and genetic structure in the American marten, Martes americana. Mol Ecol 15:1689–1697

    Article  CAS  PubMed  Google Scholar 

  • Broquet T, Ray N, Petit E, Fryxell J, Burel F (2006b) Genetic isolation by distance and landscape connectivity in the American marten (Martes americana). Landscape Ecol 21:877–889

    Article  Google Scholar 

  • Brower AV (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA 91:6491–6495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burns JA (1991) Mid-Wisconsinan vertebrates and their environment from January Cave, Alberta, Canada. Quaternary Res 35:130–143

    Article  Google Scholar 

  • Carr SM, Hicks SA (1997) Are there two species of marten in North America? Genetic and evolutionary relationships within Martes. In: Proulx G, Bryant HN, Woodward PM (eds) Martes: Taxonomy, Ecology, Techniques, and Management. The Provincial Museum of Alberta, Edmonton, pp 15–28

    Google Scholar 

  • Clare EL, Lim BK, Engstrom MD, Eger JL, Hebert PD (2007) DNA barcoding of Neotropical bats: species identification and discovery within Guyana. Mol Ecol Notes 7:184–190

    Article  CAS  Google Scholar 

  • Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM (2009) The last glacial maximum. Science 325:710–714

    Article  CAS  PubMed  Google Scholar 

  • Colella JP, Johnson EJ, Cook JA (2018a) Reconciling molecules and morphology in North American Martes. J Mammal 99:1323–1335

    Article  Google Scholar 

  • Colella JP, Wilson RE, Talbot SL, Cook JA (2018b) Implications of introgression for wildlife translocations: the case of North American martens. Conserv Genet 20:153–166

    Article  CAS  Google Scholar 

  • Dawson NG, Colella JP, Small MP, Stone KD, Talbot SL, Cook JA (2017) Historical biogeography sets the foundation for contemporary conservation of martens (genus Martes) in northwestern North America. J Mammal 98:715–730

    Article  Google Scholar 

  • Dawson NG, Cook JA (2012) Behind the genes. In: Aubry KB, Zielinski WJ, Raphael MG, Proulx G, Buskirk SW (eds) Biology and Conservation of Martens, Sables, and Fishers: A New Synthesis. Cornell University Press, Ithaca, pp 23–38

    Google Scholar 

  • Demboski JR, Stone KD, Cook JA (1999) Further perspectives on the Haida Gwaii glacial refugium. Evolution 53:2008–2012

    Article  PubMed  Google Scholar 

  • Donoghue PCJ, Benton MJ (2007) Rocks and clocks: calibrating the Tree of Life using fossils and molecules. Trends Ecol Evol 22:424–431

    Article  PubMed  Google Scholar 

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duchêne S, Lanfear R, Ho SYW (2014) The impact of calibration and clock-model choice on molecular estimates of divergence times. Mol Phylogen Evol 78:277–289

    Article  Google Scholar 

  • Dyke AS (2004) An outline of North American deglaciation with emphasis on central and northern Canada. In: Ehlers J, Gibbard PL (eds) Developments in Quaternary Sciences. Elsevier, Amsterdam, pp 373–424

    Google Scholar 

  • Edwards CJ, Suchard MA, Lemey P, Welch J, Barnes I, Fulton TL, Barnett R, O'Connell TC, Coxon P, Monaghan N, Valdiosera CE, Lorenzen ED, Willerslev E, Baryshnikov GF, Rambaut A, Thomas MG, Bradley DG, Shapiro B (2011) Ancient hybridization and an Irish origin for the modern polar bear matriline. Curr Biol 21:1251–1258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards RL, Cheng H, Murrell MT, Goldstein SJ (1997) Protactinium-231 dating of carbonates by thermal ionization mass spectrometry: implications for Quaternary climate change. Science 276:782–786

    Article  CAS  PubMed  Google Scholar 

  • Eshelman R, Grady F (1986) Quaternary vertebrate localities of Virginia and their avian and mammalian fauna. In: McDonald JN, Bird SO (eds) The Quaternary of Virginia: A Symposium Volume. Department of Mines, Minerals and Energy, Division of Mineral Resources, Charlottesville, pp 43–71

    Google Scholar 

  • Feranec RS (2009) Implications of radiocarbon dates from Potter Creek Cave, Shasta County, California, USA. Radiocarbon 51:931

    Article  CAS  Google Scholar 

  • Gandolfo MA, Nixon KC, Crepet WL (2008) Selection of fossils for calibration of molecular dating models. Ann Mo Bot Gard 95:34–42

    Article  Google Scholar 

  • Grady F (1984) A Pleistocene occurrence of Geomys (Rodentia: Geomyidae) in West Virginia. In: Genoways H, Dawson M (eds) Contributions in Quaternary Vertebrate Paleontology: A Volume in Memorial to John E Guilday. Carnegie Mus Nat Hist Spec Publ 8:161–168

    Google Scholar 

  • Graur D, Martin W (2004) Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet 20:80–86

    Article  CAS  PubMed  Google Scholar 

  • Guilday JE, Hamilton HW (1978) Ecological significance of displaced boreal mammals in West Virginia caves. J Mammal 59:176–181

    Article  Google Scholar 

  • Guilday JE, Parmalee PW, Hamilton HW (1977) The Clark's Cave bone deposit and the late Pleistocene paleoecology of the central Appalachian Mountains of Virginia. Bull Carnegie Mus Nat Hist 2:1–87

    Google Scholar 

  • Hassanin A (2015) The role of Pleistocene glaciations in shaping the evolution of polar and brown bears. Evidence from a critical review of mitochondrial and nuclear genome analyses. C R Biol 338:494–501

    Article  PubMed  Google Scholar 

  • Hedges SB, Kumar S (2004) Precision of molecular time estimates. Trends Genet 20:242–247

    Article  CAS  PubMed  Google Scholar 

  • Heintzman PD, Zazula GD, MacPhee RDE, Scott E, Cahill JA, McHorse BK, Kapp JD, Stiller M, Wooller MJ, Orlando L, Southon J, Froese DG, Shapiro B (2017) A new genus of horse from Pleistocene North America. eLife 6:e29944

    Article  PubMed  PubMed Central  Google Scholar 

  • Hipsley CA, Müller J (2014) Beyond fossil calibrations: realities of molecular clock practices in evolutionary biology. Front Genet 5:1–11

    Article  CAS  Google Scholar 

  • Ho SY, Duchêne S (2014) Molecular-clock methods for estimating evolutionary rates and timescales. Mol Ecol 23:5947–5965

    Article  PubMed  Google Scholar 

  • Ho SYW, Lanfear R, Bromham L, Phillips MJ, Soubrier J, Rodrigo AG, Cooper A (2011) Time-dependent rates of molecular evolution. Mol Ecol 20:3087–3101

    Article  PubMed  Google Scholar 

  • Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568

    Article  CAS  PubMed  Google Scholar 

  • Ho SYW, Saarma U, Barnett R, Haile J, Shapiro B (2008) The effect of inappropriate calibration: three case studies in molecular ecology. PLoS One 3:e1615

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoberg E, Koehler A, Cook J (2012) Complex host–parasite systems in Martes: implications for conservation biology of endemic faunas. In: Aubry KB, Zielinski WJ, Raphael MG, Proulx G, Buskirk SW (eds) Biology and Conservation of Martens, Sables and Fishers: A New Synthesis. Cornell University Press, Ithaca, pp 39–57

    Google Scholar 

  • Hope AG, Ho SY, Malaney JL, Cook JA, Talbot SL (2014) Accounting for rate variation among lineages in comparative demographic analyses. Evolution 68:2689–2700

    Article  PubMed  Google Scholar 

  • Howell N, Smejkal CB, Mackey DA, Chinnery PF, Turnbull DM, Herrnstadt C (2003) The pedigree rate of sequence divergence in the human mitochondrial genome: there is a difference between phylogenetic and pedigree rates. Am J Hum Genet 72:659–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes SS (2009) Noble marten (Martes americana nobilis) revisited: its adaptation and extinction. J Mammal 90:74–92

    Article  Google Scholar 

  • Hughes SS (2012) Synthesis of Martes evolutionary history. In: Aubry KB, Zielinski WJ, Raphael MG, Proulx G, Buskirk SW (eds) Biology and Conservation of Martens, Sables, and Fishers: A New Synthesis. Cornell University Press, Ithaca, pp 3–22

    Google Scholar 

  • Kingman JFC (1982) The coalescent. Stoch Process Their Appl 13:235–248

    Article  Google Scholar 

  • Kishino H, Painter IS, Thorne JL (1998) Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 15:1647–1657

    Article  PubMed  Google Scholar 

  • Koehler AVA, Hoberg EP, Dokuchaev NE, Tranbenkova NA, Whitman JS, Nagorsen DW, Cook JA (2009) Phylogeography of a Holarctic nematode, Soboliphyme baturini, among mustelids: climate change, episodic colonization, and diversification in a complex host–parasite system. Biol J Linn Soc 96:651–663

    Article  Google Scholar 

  • Koepfli K-P, Deere K, Slater G, Begg C, Begg K, Grassman L, Lucherini M, Veron G, Wayne R (2008) Multigene phylogeny of the Mustelidae: resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation. BMC Biol 6:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Koepfli K-P, Wayne R (1998) Phylogenetic relationships of otters (Carnivora: Mustelidae) based on mitochondrial cytochrome b sequences. J Zool 246:401–416

    Article  Google Scholar 

  • Kumar S, Stetcher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kyle CJ, Davis CS, Strobeck C (2000) Microsatellite analysis of North American pine marten (Martes americana) populations from the Yukon and Northwest Territories. Can J Zool 78:1150–1157

    Article  Google Scholar 

  • Kyle CJ, Strobeck C (2003) Genetic homogeneity of Canadian mainland marten populations underscores the distinctiveness of Newfoundland pine martens (Martes americana atrata). Can J Zool 81:57–66

    Article  Google Scholar 

  • Law CJ, Slater GJ, Mehta RS (2018) Lineage diversity and size disparity in Musteloidea: testing patterns of adaptive radiation using molecular and fossil-based methods. Syst Biol 67:127–144

    Article  CAS  PubMed  Google Scholar 

  • Lee MSY, Skinner A (2011) Testing fossil calibrations for vertebrate molecular trees. Zool Scr 40:538–543

    Article  Google Scholar 

  • Li B, Wolsan M, Wu D, Zhang W, Xu Y, Zeng Z (2014) Mitochondrial genomes reveal the pattern and timing of marten (Martes), wolverine (Gulo), and fisher (Pekania) diversification. Mol Phylogen Evol 80:156–164

    Article  CAS  Google Scholar 

  • Long CA (1971) Significance of the late Pleistocene fauna from the Little Box Elder Cave, Wyoming, to studies of zoogeography of recent mammals. Great Basin Nat 31:93–105

    Google Scholar 

  • Lorenzen ED, De Neergaard R, Arctander P, Siegismund HR (2007) Phylogeography, hybridization and Pleistocene refugia of the kob antelope (Kobus kob). Mol Ecol 16:3241–3252

    Article  CAS  PubMed  Google Scholar 

  • Lorenzen ED, Nogues-Bravo D, Orlando L, Weinstock J, Binladen J, Marske KA, Ugan A, Borregaard MK, Gilbert MTP, Nielsen R, Ho SYW, Goebel T, Graf KE, Byers D, Stenderup JT, Rasmussen M, Campos PF, Leonard JA, Koepfli K-P, Froese D, Zazula G, Stafford TW, Aaris-Sorensen K, Batra P, Haywood AM, Singarayer JS, Valdes PJ, Boeskorov G, Burns JA, Davydov SP, Haile J, Jenkins DL, Kosintsev P, Kuznetsova T, Lai X, Martin LD, McDonald HG, Mol D, Meldgaard M, Munch K, Stephan E, Sablin M, Sommer RS, Sipko T, Scott E, Suchard MA, Tikhonov A, Willerslev R, Wayne RK, Cooper A, Hofreiter M, Sher A, Shapiro B, Rahbek C, Willerslev E (2011) Species-specific responses of late Quaternary megafauna to climate and humans. Nature 479:359–364

  • Lyman RL (2011) Paleoecological and biogeographical implications of late Pleistocene noble marten (Martes americana nobilis) in eastern Washington state, USA. Quaternary Res 75:176–182

    Article  Google Scholar 

  • Lynch LM (2018) Mitochondrial and skeletal limb Evolution in the North American pine marten, Martes. Doctor of Philosophy, Oklahoma State University, Tulsa

  • Lynch LM, Holleman G, Booth W (2019) Accurate phylogenetic relationships can be produced from fragments of DNA. Society for Integrative and Comparative Biology, Annual Meeting Abstracts:252

  • Maul LC, Markova AK (2007) Similarity and regional differences in Quaternary arvicolid evolution in Central and Eastern Europe. Quaternary Internatl 160:81–99

    Article  Google Scholar 

  • Mayer F, Dietz C, Kiefer A (2007) Molecular species identification boosts bat diversity. Front Zool 4:4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mead EM, Mead JI (1989) Snake Creek Burial Cave and a review of the Quaternary mustelids of the Great Basin. West N Am Nat 49:143–154

    Google Scholar 

  • Melo-Ferreira J, Boursot P, Randi E, Kryukov A, Suchentrunk F, Ferrand N, Alves P (2007) The rise and fall of the mountain hare (Lepus timidus) during Pleistocene glaciations: expansion and retreat with hybridization in the Iberian Peninsula. Mol Ecol 16:605–618

    Article  CAS  PubMed  Google Scholar 

  • Merriam CH (1890) Description of a new marten (Mustela caurina) from the northwest coast region of the United States. In: North American Fauna. US Government Printing Office, Washington, pp 27–30

    Google Scholar 

  • Meyers JI (2007) Basicranial analysis of Martes and the extinct Martes nobilis (Carnivora: Mustelidae) using geometric morphometrics. Master of Science, Northern Arizona University, Flagstaff

    Google Scholar 

  • Moruzzi TL, Royar KJ, Grove C, Brooks RT, Bernier C, Thompson FL, DeGraaf RM, Fuller TK (2003) Assessing an American marten, Martes americana, reintroduction in Vermont. Can Field-Nat 117:190–195

    Article  Google Scholar 

  • Nabholz B, Glémin S, Galtier N (2008) Strong variations of mitochondrial mutation rate across mammals—the longevity hypothesis. Mol Biol Evol 25:120–130

    Article  CAS  PubMed  Google Scholar 

  • Nowak RM (1999) Walker's Mammals of the World, 6th ed. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • O'Shea KA (2014) Genetic study of Recent samples of American marten (Martes americana) from Vermont. Honors College Senior Thesis, University of Vermont, Burlington

    Google Scholar 

  • Oshida T, Lin L-K, Chang S-W, Dang CN, Nguyen ST, Nguyen NX, Nguyen DX, Endo H, Kimura J, Sasaki M, Hayashida A, Takano A (2015) Mitochondrial DNA evidence suggests challenge to the conspecific status of the hairy-footed flying squirrel Belomys pearsonii from Taiwan and Vietnam. Mammal Study 40:29–33

    Article  Google Scholar 

  • Parham JF, Donoghue PCJ, Bell CJ, Calway TD, Head JJ, Holroyd PA, Inoue JG, Irmis RB, Joyce WG, Ksepka DT, Patané JSL, Smith ND, Tarver JE, van Tuinen M, Yang Z, Angielczyk KD, Greenwood JM, Hipsley CA, Jacobs L, Makovicky PJ, Müller J, Smith KT, Theodor JM, Warnock RCM, Benton MJ (2012) Best practices for justifying fossil calibrations. Syst Biol 61:346–359

    Article  PubMed  Google Scholar 

  • Prost S, Guralnick RP, Waltari E, Fedorov VB, Kuzmina E, Smirnov N, Van Kolfschoten T, Hofreiter M, Vrieling K (2013) Losing ground: past history and future fate of Arctic small mammals in a changing climate. Global Change Biol 19:1854–1864

    Article  Google Scholar 

  • Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. Available from http://tree.bio.ed.ac.uk/software/tracer.

  • Rannala B, Yang Z (2007) Inferring speciation times under an episodic molecular clock. Syst Biol 56:453–466

    Article  PubMed  Google Scholar 

  • Reisz RR, Müller J (2004) Molecular timescales and the fossil record: a paleontological perspective. Trends Genet 20:237–241

    Article  CAS  PubMed  Google Scholar 

  • Rosel PE, Hancock-hanser BL, Archer FI, Robertson KM, Martien KK, Leslie MS, Berta A, Cipriano F, Viricel A, Viaud-Martinez KA, Taylor BL (2017) Examining metrics and magnitudes of molecular genetic differentiation used to delimit cetacean subspecies based on mitochondrial DNA control region sequences. Mar Mammal Sci 33:76–100

    Article  CAS  Google Scholar 

  • Rovey CW, Balco G (2011) Summary of early and middle Pleistocene glaciations in northern Missouri, USA. In: Ehlers J, Gibbard PL, Hughes PD (eds) Developments in Quaternary Sciences. Elsevier, Amsterdam, pp 553–561

    Google Scholar 

  • Rutschmann F (2006) Molecular dating of phylogenetic trees: a brief review of current methods that estimate divergence times. Diversity Distrib 12:35–48

    Article  Google Scholar 

  • Sanderson M (1997) A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol Biol Evol 14:1218–1218

    Article  CAS  Google Scholar 

  • Sanderson MJ (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 19:101–109

  • Shackleton NJ, Sánchez-Goñi MF, Pailler D, Lancelot Y (2003) Marine isotope substage 5e and the Eemian interglacial. Global Planet Change 36:151–155

    Article  Google Scholar 

  • Sigurðardóttir S, Helgason A, Gulcher JR, Stefansson K, Donnelly P (2000) The mutation rate in the human mtDNA control region. Am Hum Gen 66:1599–1609

    Article  Google Scholar 

  • Sinclair WJ (1907) The Exploration of the Potter Creek Cave. University of California Press, Oakland

    Google Scholar 

  • Slauson KM, Zielinski WJ, Stone KD (2009) Characterizing the molecular variation among American marten (Martes americana) subspecies from Oregon and California. Conserv Genet 10:1337–1341

    Article  Google Scholar 

  • Small MP, Stone KD, Cook JA (2003) American marten (Martes americana) in the Pacific Northwest: population differentiation across a landscape fragmented in time and space. Mol Ecol 12:89–103

    Article  CAS  PubMed  Google Scholar 

  • Stirling CH, Esat TM, Lambeck K, McCulloch MT (1998) Timing and duration of the Last Interglacial: evidence for a restricted interval of widespread coral reef growth. Earth Planet Sci Lett 160:745–762

    Article  CAS  Google Scholar 

  • Stone KD, Cook JA (2002) Molecular evolution of Holarctic martens (genus Martes, Mammalia: Carnivora: Mustelidae). Mol Phylogen Evol 24:169–179

    Article  CAS  Google Scholar 

  • Stone KD, Flynn RW, Cook JA (2002) Post-glacial colonization of northwestern North America by the forest-associated American marten (Martes americana, Mammalia: Carnivora: Mustelidae). Mol Ecol 11:2049–2063

    Article  CAS  PubMed  Google Scholar 

  • Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4:vey016

  • Tankersley KB (1997) Sheriden: a Clovis cave site in eastern North America. Geoarchaeology 12:713–724

    Article  Google Scholar 

  • Tinn O, Oakley TH (2008) Erratic rates of molecular evolution and incongruence of fossil and molecular divergence time estimates in Ostracoda (Crustacea). Mol Phylogen Evol 48:157–167

    Article  CAS  Google Scholar 

  • Valdiosera CE, García N, Anderung C, Dalén L, Crégut-Bonnoure E, Kahlke R-D, Stiller M, Brandström M, Thomas MG, Arsuaga JL (2007) Staying out in the cold: glacial refugia and mitochondrial DNA phylogeography in ancient European brown bears. Mol Ecol 16:5140–5148

    Article  CAS  PubMed  Google Scholar 

  • Vences M, Thomas M, van der Meijden A, Chiari Y, Vieites DR (2005) Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Front Zool 2:5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Welch JJ, Bromham L (2005) Molecular dating when rates vary. Trends Ecol Evol 20:320–327

    Article  PubMed  Google Scholar 

  • Wetmore A (1962) Notes on fossil and subfossil birds. Smithson Misc Collect 145(2):1–17

  • Wiszniowska T (1989) Middle Pleistocene Carnivora (Mammalia) from Kozi Grzbiet in the Swietokrzyskie Mts, Poland. Acta Zool Cracov 32:589–630

    Google Scholar 

  • Wolsan M (1987) Quaternary carnivores of Poland. In: Programme with Abstracts, XII International Congress, International Union for Quaternary Research, July 1987, National Research Council of Canada, Ottawa, p 290

  • Wolsan M (1989) Drapiezne—Carnivora. In: Kowalski K (ed) Historia i Ewolucja La˛dowej Fauny Polski. Folia Quat, pp 177-196

  • Wolsan M (1990) Lower Pleistocene carnivores of Poland. Quartärpaläontologie 8:277–280

    Google Scholar 

  • Wolsan M (1993a) Evolution des carnivores quaternaires en Europe centrale dans leur contexte stratigraphique et paleoclimatique. l’Anthropologie 97:203-222

  • Wolsan M (1993b) Phylogeny and classification of early European Mustelida (Mammalia: Carnivora). Acta Theriol 38:345–384

    Article  Google Scholar 

  • Youngman PM, Schueler FW (1991) Martes nobilis is a synonym of Martes americana, not an extinct Pleistocene-Holocene species. J Mammal 72:567–577

    Article  Google Scholar 

  • Zuckerkandl E, Pauling L (1962) Molecular disease, evolution and genetic heterogeneity. In: Pullman KM (ed) Horizons in Biochemistry. Academic Press, New York, pp 189–225

    Google Scholar 

Download references

Acknowledgements

Thank you to A. Weil for assistance in developing and writing this research, as well as partial funding. Thank you to H. O’Brien, P. Gignac, W. Booth, N. Wilson, and J. Dudgeon for project design. Thanks to A. Morehardt for manuscript suggestions. Thank you to my reviewers for their thoughtful comments. Thank you to J. Colella for sequences of M. caurina and K. Pilgrim at the National Genomics Center for Wildlife and Fish Conservation for access to tissue for preliminary analyses. Thank you to W. Booth, N. Wilson, and J. Dudgeon for access to laboratory facilities and equipment. Also, thanks to S. Wallace (ETMNH), J. Dunnum (MSB), C. Thompson (UMMZ), J. Bopp (NYSM), B. Coyner (SNOMNH), A. Gunderson (UAMN), S. Peurach (USNM), V. Mathis (FMNH) and J. Bradley (BMUW) for access to collections and for specimen loans. Thank you to Oklahoma State University Center for Health Sciences for stipend and funding for the duration of this project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leigha M. Lynch.

Additional information

This work was supported by Sigma Xi Grants in Aid of Research, Oklahoma State University Robberson Summer Graduate Research Fellowship, Oklahoma State University Women’s Faculty Council Research Award; and Oklahoma State University Center for Health Sciences.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lynch, L.M. Fossil Calibration of Mitochondrial Phylogenetic Relationships of North American Pine Martens, Martes, Suggests an Older Divergence of M. americana and M. caurina than Previously Hypothesized. J Mammal Evol 27, 535–548 (2020). https://doi.org/10.1007/s10914-019-09476-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-019-09476-7

Keywords

Navigation