Advertisement

Journal of Molecular Evolution

, Volume 86, Issue 2, pp 118–137 | Cite as

Iterative Calibration: A Novel Approach for Calibrating the Molecular Clock Using Complex Geological Events

  • Tzitziki Loeza-Quintana
  • Sarah J. Adamowicz
Original Article

Abstract

During the past 50 years, the molecular clock has become one of the main tools for providing a time scale for the history of life. In the era of robust molecular evolutionary analysis, clock calibration is still one of the most basic steps needing attention. When fossil records are limited, well-dated geological events are the main resource for calibration. However, biogeographic calibrations have often been used in a simplistic manner, for example assuming simultaneous vicariant divergence of multiple sister lineages. Here, we propose a novel iterative calibration approach to define the most appropriate calibration date by seeking congruence between the dates assigned to multiple allopatric divergences and the geological history. Exploring patterns of molecular divergence in 16 trans-Bering sister clades of echinoderms, we demonstrate that the iterative calibration is predominantly advantageous when using complex geological or climatological events—such as the opening/reclosure of the Bering Strait—providing a powerful tool for clock dating that can be applied to other biogeographic calibration systems and further taxa. Using Bayesian analysis, we observed that evolutionary rate variability in the COI-5P gene is generally distributed in a clock-like fashion for Northern echinoderms. The results reveal a large range of genetic divergences, consistent with multiple pulses of trans-Bering migrations. A resulting rate of 2.8% pairwise Kimura-2-parameter sequence divergence per million years is suggested for the COI-5P gene in Northern echinoderms. Given that molecular rates may vary across latitudes and taxa, this study provides a new context for dating the evolutionary history of Arctic marine life.

Keywords

Molecular dating Clock calibration Echinodermata Bering Strait DNA barcoding 

Notes

Acknowledgements

This work was supported by a graduate scholarship from Consejo Nacional de Ciencia y Tecnología (315757 to TLQ) and by the Natural Sciences and Engineering Research Council of Canada (Discovery Grant 2010-386591 and 2016-06199 to SJA). We also acknowledge the Ontario Ministry of Research Innovation for providing funding to Paul Hebert for the development of BOLD, which was the main resource of data for this project. Special thanks to Teresa J. Crease, Elizabeth G. Boulding, Jonathan D.S. Witt, and Mari Kekkonen for discussion and their valuable feedback on earlier versions of this manuscript. We sincerely thank two anonymous reviewers for their helpful and constructive comments. Finally, we want to acknowledge all the researchers who have made public COI barcode sequences from echinoderms.

Supplementary material

239_2018_9831_MOESM1_ESM.xlsx (856 kb)
Supplementary material 1 (XLSX 856 KB)
239_2018_9831_MOESM2_ESM.txt (126 kb)
Supplementary material 2 (TXT 125 KB)
239_2018_9831_MOESM3_ESM.docx (18 kb)
Supplementary material 3 (DOCX 17 KB)

References

  1. Addison JA, Pogson GH (2009) Multiple gene genealogies reveal asymmetrical hybridization and introgression among strongylocentrotid sea urchins. Mol Ecol 18:1239–1251.  https://doi.org/10.1111/j.1365-294X.2009.04094.x PubMedCrossRefGoogle Scholar
  2. Arndt A, Marquez C, Lambert P, Smith MJ (1996) Molecular phylogeny of Eastern Pacific sea cucumbers (Echinodermata: Holothuroidea) based on mitochondrial DNA sequence. Mol Phylogenet Evol 6:425–437.  https://doi.org/10.1006/mpev.1996.0091 PubMedCrossRefGoogle Scholar
  3. Athey T (2013) Assessing errors in DNA barcode sequence records. Master thesis, University of GuelphGoogle Scholar
  4. Bacon CD, Silvestro D, Jaramillo C et al (2015) Biological evidence supports an early and complex emergence of the Isthmus of Panama. Proc Natl Acad Sci 112:E3153–E3153.  https://doi.org/10.1073/pnas.1509107112 CrossRefGoogle Scholar
  5. Bargelloni L, Ritchie PA, Patarnello T et al (1994) Molecular evolution at subzero temperatures: mitochondrial and nuclear phylogenies of fishes from Antarctica (suborder Notothenioidei), and the evolution of antifreeze glycopeptides. Mol Biol Evol 11:854–863PubMedGoogle Scholar
  6. Bastrop R, Blank M (2006) Multiple invasions - a polychaete genus enters the Baltic Sea. Biol Invasions 8:1195–1200.  https://doi.org/10.1007/s10530-005-6186-6 CrossRefGoogle Scholar
  7. Bleidorn C, Kruse I, Albrecht S, Bartolomaeus T (2006) Mitochondrial sequence data expose the putative cosmopolitan polychaete Scoloplos armiger (Annelida, Orbiniidae) as a species complex. BMC Evol Biol 6:47.  https://doi.org/10.1186/1471-2148-6-47 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bleiweiss R (1998a) Relative-rate tests and biological causes of molecular evolution in hummingbirds. Mol Biol Evol 15:481–491CrossRefGoogle Scholar
  9. Bleiweiss R (1998b) Slow rate of molecular evolution in high-elevation hummingbirds. Proc Natl Acad Sci USA 95:612–616.  https://doi.org/10.1073/pnas.95.2.612 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Boissin E, Stöhr S, Chenuil A (2011) Did vicariance and adaptation drive cryptic speciation and evolution of brooding in Ophioderma longicauda (Echinodermata: Ophiuroidea), a common Atlanto-Mediterranean ophiuroid? Mol Ecol 2:4737–4755.  https://doi.org/10.1111/j.1365-294X.2011.05309.x CrossRefGoogle Scholar
  11. Bribiesca-Contreras G, Solís-Marín FA, Laguarda-Figueras A, Zaldívar-Riverón A (2013) Identification of echinoderms (Echinodermata) from an anchialine cave in Cozumel Island, Mexico, using DNA barcodes. Mol Ecol Resour 13:1137–1145.  https://doi.org/10.1111/1755-0998.12098 PubMedGoogle Scholar
  12. Briggs JC (1970) A faunal history of the North Atlantic Ocean. Syst Zool 19:19–34.  https://doi.org/10.2307/2412025 CrossRefGoogle Scholar
  13. Bromham L (2002) Molecular clocks in reptiles: life history influences rate of molecular evolution. Mol Biol Evol 19:302–309.  https://doi.org/10.1093/oxfordjournals.molbev.a004083 PubMedCrossRefGoogle Scholar
  14. Carr CM (2010) The Polychaeta of Canada: exploring diversity and distribution patterns using DNA barcodes. Master thesis, University of GuelphGoogle Scholar
  15. Carr CM, Hardy SM, Brown TM et al (2011) A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PLoS ONE 6:e22232.  https://doi.org/10.1371/journal.pone.0022232 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Coates AG, Obando JA (1996) The geologic evolution of the Central American Isthmus. In: Jackson JBC, Budd AF, Coates AG (eds) Evolution and environment in tropical America. The University of Chicago Press, Chicago, pp 21–56Google Scholar
  17. Collins LS, Coates AG, Berggren WA et al (1996a) The late Miocene Panama isthmian strait. Geology 24:687–690CrossRefGoogle Scholar
  18. Collins TM, Frazer K, Brown WM (1996b) Evolutionary history of Northern Hemisphere Nucella (Gastropoda, Muricidae): molecular, morphological, ecological, and paleontological evidence. Evolution 50:2287–2304PubMedCrossRefGoogle Scholar
  19. Coppard SE, Zigler KS, Lessios H (2013) Phylogeography of the sand dollar genus Mellita: cryptic speciation along the coasts of the Americas. Mol Phylogenet Evol 69:1033–1042.  https://doi.org/10.1016/j.ympev.2013.05.028 PubMedCrossRefGoogle Scholar
  20. Dodson JJ, Tremblay S, Colombani F et al (2007) Trans-Arctic dispersals and the evolution of a circumpolar marine fish species complex, the capelin (Mallotus villosus). Mol Ecol 16:5030–5043.  https://doi.org/10.1111/j.1365-294X.2007.03559.x PubMedCrossRefGoogle Scholar
  21. Drummond AJ, Bouckaert RR (2015) Bayesian evolutionary analysis with BEAST. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  22. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710.  https://doi.org/10.1371/journal.pbio.0040088 CrossRefGoogle Scholar
  23. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973.  https://doi.org/10.1093/molbev/mss075 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Dunton K (1992) Arctic biogeography: the paradox of the marine benthic fauna and flora. Trends Ecol Evol 7:183–189.  https://doi.org/10.1016/0169-5347(92)90070-R PubMedCrossRefGoogle Scholar
  25. Duque-Caro H (1990) Neogene stratigraphy, paleoceanography and paleobiogeography in northwest South America and the evolution of the Panama seaway. Palaeogeogr Palaeoclimatol Palaeoecol 77:203–234.  https://doi.org/10.1016/0031-0182(90)90178-A CrossRefGoogle Scholar
  26. Durham J, MacNeil F (1967) Cenozoic migrations of marine invertebrates through the Bering Strait region. In: Hopkins D (ed) The Bering land bridge. Stanford University Press, Stanford, pp 326–349Google Scholar
  27. Einarsson T, Hopkins DM, Doell RR (1967) The stratigraphy of Tjornes, North Iceland and the history of the Bering land bridge. In: Hopkins D (ed) The Bering land bridge. Stanford University Press, Stanford California, pp 312–325Google Scholar
  28. Feuda R, Smith AB (2015) Phylogenetic signal dissection identifies the root of starfishes. PLoS ONE 10:e0123331.  https://doi.org/10.1371/journal.pone.0123331 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fleischer RC, McIntosh CE, Tarr CL (1998) Evolution on a volcanic conveyor belt: using phylogeographic reconstructions and K-Ar-based ages of the Hawaiian Islands to estimate molecular evolutionary rates. Mol Ecol 7:533–545.  https://doi.org/10.1046/j.1365-294x.1998.00364.x PubMedCrossRefGoogle Scholar
  30. Foltz DW, Nguyen AT, Kiger JR, Mah CL (2008) Pleistocene speciation of sister taxa in a North Pacific clade of brooding sea stars (Leptasterias). Mar Biol 154:593–602.  https://doi.org/10.1007/s00227-008-0952-9 CrossRefGoogle Scholar
  31. Gernhard T (2008) The conditioned reconstructed process. J Theor Biol 253:769–778.  https://doi.org/10.1016/j.jtbi.2008.04.005 PubMedCrossRefGoogle Scholar
  32. Gillooly JF, Allen AP, West GB, Brown JH (2005) The rate of DNA evolution: effects of body size and temperature on the molecular clock. Proc Natl Acad Sci USA 102:140–145.  https://doi.org/10.1073/pnas.0407735101 PubMedCrossRefGoogle Scholar
  33. Gladenkov AY, Gladenkov YB (2004) Onset of connections between the Pacific and Arctic Oceans through the Bering Strait in the Neogene. Stratigr Geol Correl 12:175–187Google Scholar
  34. Gladenkov A, Oleinik A, Marincovich LJ, Barinov K (2002) A refined age for the earlier opening of Bering Strait. Paleogeogr Paleclimatol Paleoecol 183:321–328CrossRefGoogle Scholar
  35. Gregory TR (2008) Understanding evolutionary trees. Evol Educ Outreach 1:121–137.  https://doi.org/10.1007/s12052-008-0035-x CrossRefGoogle Scholar
  36. Haq B, Hardenbol J, Vail P (1987) Chronology of fluctuating sea levels since the Triassic. Science 235:1156–1167.  https://doi.org/10.1126/science.235.4793.1156 PubMedCrossRefGoogle Scholar
  37. Hardy SM, Carr CM, Hardman M et al (2011) Biodiversity and phylogeography of Arctic marine fauna: insights from molecular tools. Mar Biodivers 41:195–210.  https://doi.org/10.1007/s12526-010-0056-x CrossRefGoogle Scholar
  38. Harper FM, Hart MW (2007) Morphological and phylogenetic evidence for hybridization and introgression in a sea star secondary contact zone. Invertebr Biol 126:373–384.  https://doi.org/10.1111/j.1744-7410.2007.00107.x CrossRefGoogle Scholar
  39. Harper FM, Addison JA, Hart MW (2007) Introgression versus immigration in hybridizing high-dispersal echinoderms. Evolution 61:2410–2418.  https://doi.org/10.1111/j.1558-5646.2007.00200.x PubMedCrossRefGoogle Scholar
  40. Harris SA (2005) Thermal history of the Arctic Ocean environs adjacent to North America during the last 3.5 Ma and a possible mechanism for the cause of the cold events (major glaciations and permafrost events). Prog Phys Geogr 29:218–238.  https://doi.org/10.1191/0309133305pp444ra CrossRefGoogle Scholar
  41. Hart MW, Byrne M, Smith MJ (1997) Molecular phylogenetic analysis of life-history evolution in asterinid starfish. Evolution 51:1848–1861PubMedCrossRefGoogle Scholar
  42. Haug GH, Sigman DM, Tiedemann R et al (1999) Onset of permanent startification in the subarctic Pacific Ocean. Nature 401:779–782CrossRefGoogle Scholar
  43. Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003a) Biological identifications through DNA barcodes. Proc R Soc Lond B Biol Sci 270:313–321.  https://doi.org/10.1098/rspb.2002.2218 CrossRefGoogle Scholar
  44. Hebert PDN, Ratnasingham S, DeWaard JR (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B Biol Sci 270 Suppl:S96–S99.  https://doi.org/10.1098/rsbl.2003.0025 CrossRefGoogle Scholar
  45. Held C (2001) No evidence for slow-down of molecular substitution rates at subzero temperatures in Antarctic serolid isopods (Crustacea, Isopoda, Serolidae). Polar Biol 24:497–501.  https://doi.org/10.1007/s003000100245 CrossRefGoogle Scholar
  46. Herman Y, Hopkins DM (1980) Arctic oceanic climate in Late Cenozoic time. Science 209:557–562PubMedCrossRefGoogle Scholar
  47. Ho SYW, Duchêne S (2014) Molecular-clock methods for estimating evolutionary rates and timescales. Mol Ecol 23:5947–5965.  https://doi.org/10.1111/mec.12953 PubMedCrossRefGoogle Scholar
  48. Ho SYW, Larson G (2006) Molecular clocks: when times are a-changin’. Trends Genet 22:79–83.  https://doi.org/10.1016/j.tig.2005.11.006 PubMedCrossRefGoogle Scholar
  49. Ho SYW, Phillips MJ (2009) Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol 58:367–380.  https://doi.org/10.1093/sysbio/syp035 PubMedCrossRefGoogle Scholar
  50. 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.  https://doi.org/10.1093/molbev/msi145 PubMedCrossRefGoogle Scholar
  51. Ho SYW, Lanfear R, Bromham L et al (2011) Time-dependent rates of molecular evolution. Mol Ecol 20:3087–3101.  https://doi.org/10.1111/j.1365-294X.2011.05178.x PubMedCrossRefGoogle Scholar
  52. Ho SYW, Duchêne S, Molak M, Shapiro B (2015) Time-dependent estimates of molecular evolutionary rates: evidence and causes. Mol Ecol 24:6007–6012.  https://doi.org/10.1111/mec.13450 PubMedCrossRefGoogle Scholar
  53. Hoareau TB, Boissin E, Paulay G, Bruggemann JH (2013) The Southwestern Indian Ocean as a potential marine evolutionary hotspot: perspectives from comparative phylogeography of reef brittle-stars. J Biogeogr 40:2167–2179.  https://doi.org/10.1111/jbi.12155 CrossRefGoogle Scholar
  54. Hopkins D (1967) Quaternary marine trangressions in Alaska. In: Hopkins DM (ed) The Bering land bridge. Stanford University Press, Stanford, pp 47–90Google Scholar
  55. Horikawa K, Martin EE, Basak C et al (2015) Pliocene cooling enhanced by flow of low-salinity Bering Sea water to the Arctic Ocean. Nat Commun 6:7587.  https://doi.org/10.1038/ncomms8587 PubMedPubMedCentralCrossRefGoogle Scholar
  56. Hu A, Meehl GA, Han W (2007) Role of the Bering Strait in the thermohaline circulation and abrupt climate change. Geophys Res Lett 34:1–6.  https://doi.org/10.1029/2006GL028906 CrossRefGoogle Scholar
  57. Hurt C, Anker A, Knowlton N (2009) A multilocus test of simultaneous divergence across the Isthmus of Panama using snapping shrimp in the genus Alpheus. Evolution 63:514–530.  https://doi.org/10.1111/j.1558-5646.2008.00566.x PubMedCrossRefGoogle Scholar
  58. Jordan DS (1908) The law of geminate species. Am Nat 42:73–80CrossRefGoogle Scholar
  59. Kamarudin KR, Hashim R, Usup G (2010) Phylogeny of sea cucumber (Echinodermata: Holothuroidea) as inferred from 16 s mitochondrial rRNA gene sequences. Sains Malays 39:209–218Google Scholar
  60. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120.  https://doi.org/10.1007/BF01731581 PubMedCrossRefGoogle Scholar
  61. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Lond B Biol Sci 265:2257–2263CrossRefGoogle Scholar
  62. Kober KM, Bernardi G (2013) Phylogenomics of strongylocentrotid sea urchins. BMC Evol Biol 13:88.  https://doi.org/10.1186/1471-2148-13-88 PubMedPubMedCentralCrossRefGoogle Scholar
  63. Landis MJ (2016) Biogeographic dating of speciation times using paleogeographically informed processes. Syst Biol 66:128–144.  https://doi.org/10.1093/sysbio/syw040 Google Scholar
  64. Layton KKS, Corstorphine EA, Hebert PDN (2016) Exploring Canadian echinoderm diversity through DNA barcodes. PLoS ONE 1–16.  https://doi.org/10.1371/journal.pone.0166118
  65. Lee YH (2003) Molecular phylogenies and divergence times of sea urchin species of Strongylocentrotidae, Echinoida. Mol Biol Evol 20:1211–1221.  https://doi.org/10.1093/molbev/msg125 PubMedCrossRefGoogle Scholar
  66. Leigh EG, O’Dea A, Vermeij GJ (2014) Historical biogeography of the Isthmus of Panama. Biol Rev 89:148–172.  https://doi.org/10.1111/brv.12048 PubMedCrossRefGoogle Scholar
  67. Lessios H (1979) Use of Panamanian sea urchins to test the molecular clock. Nature 280:599–601CrossRefGoogle Scholar
  68. Lessios H (2008) The great American schism: divergence of marine organisms after the rise of the central American Isthmus. Annu Rev Ecol Evol Syst 39:63–91.  https://doi.org/10.1146/annurev.ecolsys.38.091206.095815 CrossRefGoogle Scholar
  69. Lessios H, Pearse J (1996) Hybridization and introgression between Indo-Pacific species of Diadema. Mar Biol 126:715–723.  https://doi.org/10.1007/BF00351338 CrossRefGoogle Scholar
  70. Lessios H, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975.  https://doi.org/10.1111/j.0014-3820.2001.tb00613.x PubMedCrossRefGoogle Scholar
  71. Lessios H, Lockhart S, Collin R et al (2012) Phylogeography and bindin evolution in Arbacia, a sea urchin genus with an unusual distribution. Mol Ecol 21:130–144.  https://doi.org/10.1111/j.1365-294X.2011.05303.x PubMedCrossRefGoogle Scholar
  72. Littlewood DTJ, Smith AB, Clough KA, Emson RH (1997) The interrelationships of the echinoderm classes: morphological and molecular evidence. Biol J Linn Soc 61:409–438.  https://doi.org/10.1111/j.1095-8312.1997.tb01799.x CrossRefGoogle Scholar
  73. Luttikhuizen PC, Drent J, Baker AJ (2003) Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Mol Ecol 12:2215–2229.  https://doi.org/10.1046/j.1365-294X.2003.01872.x PubMedCrossRefGoogle Scholar
  74. Mah CL, Blake DB (2012) Global diversity and phylogeny of the Asteroidea (Echinodermata). PLoS ONE 7:e35644.  https://doi.org/10.1371/journal.pone.0035644 PubMedPubMedCentralCrossRefGoogle Scholar
  75. Mah C, Foltz D (2011) Molecular phylogeny of the Forcipulatacea (Asteroidea: Echinodermata): systematics and biogeography. Zool J Linn Soc 162:646–660.  https://doi.org/10.1111/j.1096-3642.2010.00688.x CrossRefGoogle Scholar
  76. Marincovich LJ (1993) Danian mollusks from the Prince Creek formation Northern Alaska and implications for Arctic Ocean paleogeography. Paleontol Soc Mem 35:1–35.  https://doi.org/10.2307/1315585 Google Scholar
  77. Marincovich LJ (2000) Central American paleogeography controlled Pliocene Arctic Ocean molluscan migrations. Geology 28:551–554CrossRefGoogle Scholar
  78. Marincovich LJ, Gladenkov A (1999) Evidence for an early opening of the Bering Strait. Nature 397:149–151.  https://doi.org/10.1038/16446 CrossRefGoogle Scholar
  79. Marincovich L, Gladenkov AY (2001) New evidence for the age of Bering Strait. Quat Sci Rev 20:329–335.  https://doi.org/10.1016/S0277-3791(00)00113-X CrossRefGoogle Scholar
  80. Marko PB, Moran AL (2002) Correlated evolutionary divergence of egg size and a mitochondrial protein across the Isthmus of Panama. Evolution 56:1303–1309PubMedCrossRefGoogle Scholar
  81. Martin AP, Palumbi SR (1993) Body size, metabolic rate, generation time, and the molecular clock. Proc Natl Acad Sci 90:4087–4091.  https://doi.org/10.1073/pnas.90.9.4087 PubMedPubMedCentralCrossRefGoogle Scholar
  82. Martin AP, Naylor GJ, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155.  https://doi.org/10.1038/357153a0 PubMedCrossRefGoogle Scholar
  83. Maslin MA, Haug G, Sarnthein M, Tiedemann R (1996) The progressive intensification of Northern Hemisphere glaciation as seen from the North Pacific. Geol Rundschau 85:452–465.  https://doi.org/10.1007/BF02369002 CrossRefGoogle Scholar
  84. Matthiessen J, Knies J, Vogt C, Stein R (2009) Pliocene palaeoceanography of the Arctic Ocean and subarctic seas. Philos Trans R Soc Lond A 367:21–48.  https://doi.org/10.1098/rsta.2008.0203 CrossRefGoogle Scholar
  85. McCartney M, Keller G, Lessios H (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol Ecol 9:1391–1400.  https://doi.org/10.1046/j.1365-294X.2000.01022.x PubMedCrossRefGoogle Scholar
  86. Mendes FK, Hahn MW (2016) Gene tree discordance causes apparent substitution rate variation. Syst Biol 65:711–721.  https://doi.org/10.1093/sysbio/syw018 PubMedCrossRefGoogle Scholar
  87. Miura O, Torchin ME, Bermingham E (2010) Molecular phylogenetics reveals differential divergence of coastal snails separated by the Isthmus of Panama. Mol Phylogenet Evol 56:40–48.  https://doi.org/10.1016/j.ympev.2010.04.012 PubMedCrossRefGoogle Scholar
  88. Mooers AO, Harvey PH (1994) Metabolic rate, generation time, and the rate of molecular evolution in birds. Mol Phylogenet Evol 3:344–350.  https://doi.org/10.1006/mpev.1994.1040 PubMedCrossRefGoogle Scholar
  89. O’Dea A, Lessios HA, Coates AG et al (2016) Formation of the Isthmus of Panama. Sci Adv 2:1–12.  https://doi.org/10.1126/sciadv.1600883 Google Scholar
  90. Ogg J, Ogg G, Gradstein F (2016) A concise geological time scale. Elsevier, AmsterdamGoogle Scholar
  91. Palumbi SR, Kessing BD (1991) Population biology of the Trans-Arctic exchange: MtDNA sequence similarity between Pacific and Atlantic sea urchins. Evolution 45:1790–1805PubMedCrossRefGoogle Scholar
  92. Perseke M, Bernhard D, Fritzsch G et al (2010) Mitochondrial genome evolution in Ophiuroidea, Echinoidea, and Holothuroidea: insights in phylogenetic relationships of Echinodermata. Mol Phylogenet Evol 56:201–211.  https://doi.org/10.1016/j.ympev.2010.01.035 PubMedCrossRefGoogle Scholar
  93. Polyakova YI (2001) Late Cenozoic evolution of Northern Eurasian marginal seas based on the diatom record. Polarforschung 69:211–220Google Scholar
  94. Radulovici AE, Archambault P, Dufresne F (2010) DNA barcodes for marine biodiversity. Moving fast forward? Diversity 2:450–472.  https://doi.org/10.3390/d2040450 CrossRefGoogle Scholar
  95. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. Available from http://beast.bio.ed.ac.uk/Tracer
  96. Ratnasingham S, Hebert PDN (2007) BOLD: the barcode of life data system: barcoding. Mol Ecol Notes 7:355–364.  https://doi.org/10.1111/j.1471-8286.2007.01678.x PubMedPubMedCentralCrossRefGoogle Scholar
  97. Ratnasingham S, Hebert PDN (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS One 8:e66213.  https://doi.org/10.1371/journal.pone.0066213 PubMedPubMedCentralCrossRefGoogle Scholar
  98. Robinson M, Gouy M, Gautier C, Mouchiroud D (1998) Sensitivity of the relative-rate test to taxonomic sampling. Mol Biol Evol 15:1091–1098PubMedCrossRefGoogle Scholar
  99. Rohde K (1992) Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65:514–527.  https://doi.org/10.2307/3545569 CrossRefGoogle Scholar
  100. Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evo 4:406–425Google Scholar
  101. Schrader H-J, Bjorklund K, Manum S et al (1976) Cenozoic biostratigraphy, physical stratigraphy and paleooceanography in the Norwegian-Greenland Sea, DSDP Leg 38 paleontological synthesis. In: Talwan M, Al E (eds) Initial reports deep sea drilling project. U.S. Goverment Printing Office, Washington DC, pp 1197–1211Google Scholar
  102. Shackleton NJ, Opdyke ND (1977) Oxygen isotope and palaeomagnetic evidence for early Northern Hemisphere glaciation. Nature 270:216–219.  https://doi.org/10.1038/270216a0 CrossRefGoogle Scholar
  103. Shaffer G, Bendtsen J (1994) Role of the Bering Strait in controlling North Atlantic ocean circulation and climate. Nature 367:354–357.  https://doi.org/10.1038/367354a0 CrossRefGoogle Scholar
  104. Tajima F (1993) Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135:599–607PubMedPubMedCentralGoogle Scholar
  105. Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 PubMedPubMedCentralCrossRefGoogle Scholar
  106. Telford MJ, Lowe CJ, Cameron CB et al (2014) Phylogenomic analysis of echinoderm class relationships supports Asterozoa. Proc R Soc B Biol Sci 281:20140479.  https://doi.org/10.1098/rspb.2014.0479 CrossRefGoogle Scholar
  107. Vermeij GJ (1989) Geographical restriction as a guide to the causes of extinction: the case of the cold Northern Oceans during the Neogene. Paleobiology 15:335–356CrossRefGoogle Scholar
  108. Vermeij GJ (1991) Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17:281–307CrossRefGoogle Scholar
  109. Vogler C, Benzie J, Lessios H et al (2008) A threat to coral reefs multiplied? Four species of crown-of-thorns starfish. Biol Lett 4:696–699.  https://doi.org/10.1098/rsbl.2008.0454 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Ward RD, Holmes BH, O’Hara TD (2008) DNA barcoding discriminates echinoderm species. Mol Ecol Resour 8:1202–1211.  https://doi.org/10.1111/j.1755-0998.2008.02332.x PubMedCrossRefGoogle Scholar
  111. Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469.  https://doi.org/10.1111/j.0014-3820.2001.tb00760.x PubMedCrossRefGoogle Scholar
  112. Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328.  https://doi.org/10.1111/j.1365-294X.2008.03742.x PubMedCrossRefGoogle Scholar
  113. Williams ST, Reid DG (2004) Speciation and diversity on tropical rocky shores: a global phylogeny of snails of the genus Echinolittorina. Evolution 58:2227–2251.  https://doi.org/10.1111/j.0014-3820.2004.tb01600.x PubMedCrossRefGoogle Scholar
  114. Wright S, Keeling J, Gillman L (2006) The road from Santa Rosalia: a faster tempo of evolution in tropical climates. Proc Natl Acad Sci USA 103:7718–7722.  https://doi.org/10.1073/pnas.0510383103 PubMedPubMedCentralCrossRefGoogle Scholar
  115. Yang Z, Rannala B (2006) Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol Biol Evol 23:212–226.  https://doi.org/10.1093/molbev/msj024 PubMedCrossRefGoogle Scholar
  116. Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel H (eds) Evolving genes and proteins. Academic Press, New York, pp 97–166CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Biodiversity Institute of Ontario & Department of Integrative BiologyUniversity of GuelphGuelphCanada

Personalised recommendations