Conflicting Evolutionary Histories of the Mitochondrial and Nuclear Genomes in New World Myotis Bats

Systematic Biology

Volumn 67, Issue 2, 2018, Pages 236-249

  Platt, Roy N ^a   Faircloth, Brant C ^b   Sullivan, Kevin A M ^a   Kieran, Troy J ^c   Glenn, Travis C ^c   Vandewege, Michael W ^a   Lee, Thomas E ^d   Baker, Robert J ^a   Stevens, Richard D ^a   Ray, David A ^a  

^a TEXAS TECH UNIVERSITY   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d ABILENE CHRISTIAN UNIVERSITY   (United States)

Author keywords

concatenation; phylogenomics; Summary tree methods; UCE; ultraconserved elements; vespertilionidae

Indexed keywords

ANIMAL; BAT; CLASSIFICATION; GENETICS; GENOME; MITOCHONDRIAL GENOME; PHYLOGENY;

ANIMALS; CHIROPTERA; GENOME; GENOME, MITOCHONDRIAL; PHYLOGENY;

EID: 85043475686     PISSN: 10635157     EISSN: 1076836X     Source Type: Journal    
DOI: 10.1093/sysbio/syx070     Document Type: Article

References (87)

1. Aberer A.J., Kobert K., Stamatakis A. 2014. ExaBayes: massively parallel Bayesian tree inference for the whole-genome era. Mol. Biol. Evol. 31:2553-2556.
2. Bayzid M.S., Mirarab S., Boussau B., Warnow T. 2015. Weighted statistical binning: enabling statistically consistent genome-scale phylogenetic analyses. PLoS One. 10:e0129183.
3. Bernt M., Donath A., Jühling F., Externbrink F., Florentz C., Fritzsch G., Pütz J., Middendorf M., Stadler P.F. 2013. MITOS: improvedde novo metazoan mitochondrial genome annotation. Mol. Phylogenet. Evol. 69:313-319.
4. Bogdanowicz W., Piksa K., Tereba A. 2012. Hybridization hotspots at bat swarming sites. PLoS One 7:e53334.
5. Boyles J.G., Storm J.J. 2007. The perils of picky eating: dietary breadth is related to extinction risk in insectivorous bats. PLoS One 2:e672.
6. Caceres M.C., Barclay R.M.R. 2000. Myotis septentrionalis. Mamm. Species 634:1-4.
7. Carstens B.C., Dewey T.A. 2010. Species delimitation using a combined coalescent and information-theoretic approach: an example from North American Myotis bats. Syst Biol. 59:400-414.
8. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17:540-552.
9. Chevreux B., Wetter T., Suhai S. 1999. Genome sequence assembly using trace signals and additional sequence information. Proceedings of the German Conference on Bioinformatics 99:45-56.
10. Chifman J., Kubatko L. 2014. Quartet inference from SNP data under the coalescent model. Bioinformatics 30:3317-3324.
11. Darriba D., Posada D. 2015. The impact of partitioning on phylogenomic accuracy. bioRxiv. Available from: URL https://doi.org/10.1101/023978.
12. DeGiorgio M., Degnan J.H. 2014. Robustness to divergence time underestimation when inferring species trees from estimated gene trees. Syst. Biol. 63:66-82.
13. Degnan J.H., Rosenberg N.A. 2009. Gene tree discordance, phylogen-etic inference and the multispecies coalescent. Trends Ecol. Evol. 24:332-340.
14. Derti A., Roth F.P., Church G.M., Wu C.T. 2006. Mammalian ultraconserved elements are strongly depleted among segmental duplications and copy number variants. Nat. Genet. 38:1216-1220.
15. Douady C.J., Delsuc F., Boucher Y., Doolittle W.F., Douzery E.J.P. 2003. Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol. Biol. Evol. 20:248-254.
16. Dzeverin I. 2008. The stasis and possible patterns of selection in evolution of a group of related species from the bat genus Myotis (Chiroptera, Vespertilionidae). J. Mamm. Evol. 15:123-142.
17. Edwards S., Bensch S. 2009. Looking forwards or looking backwards in avian phylogeography? A comment on Zink and Carrowclough 2008. Mol. Ecol. 18:2930-2933.
18. Faircloth B.C. 2016. PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32:786-788.
19. Faircloth B.C., Branstetter M.G., White N.D., Brady S.G. 2015. Target enrichment of ultraconserved elements from arthropods provides a genomic perspective on relationships among Hymenoptera. Mol. Ecol. Resour. 15:489-501.
20. Faircloth B.C., McCormack J.E., Crawford N.G., Harvey M.G., Brumfield R.T., Glenn T.C. 2012. Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales. Syst. Biol. 61:717-726.
21. Findley J.S. 1972. Phenetic relationships among bats of the genus Myotis. Syst. Biol. 21:31-52.
22. Fitch J.H., Shump K.A. 1979. Myotis keenii. Mamm. Species Archive 121:1-3.
23. Glenn T.C., Nilsen R., Kieran T.J., Finger J.W., Pierson T.W., Bentley K.E., Hoffberg S., Louha S., Garcia-De-Leon F.J., Angel del Rio Portilla M., Reed K., Anderson J.L., Meece J.K., Aggery S., Rekaya R., Alabady M., Belanger M., Winker K., Faircloth B.C. 2016. Adapterama I: universal stubs and primers for thousands of dual-indexed Illumina libraries (iTru & iNext). bioRxiv. Available from: URL https://doi.org/10.1101/049114.
24. Good J.M., Vanderpool D., Keeble S., Bi K. 2015. Negligible nuclear introgression despite complete mitochondrial capture between two species of chipmunks. Evolution 69:1961-1972.
25. Gordon A., Hannon G. 2010. Fastx-toolkit. Available from: URL http://hannonlab.cshl.edu/fastx-toolkit.
26. Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q., Chen Z., Mauceli E., Hacohen N., Gnirke A., Rhind N., di Palma F., Birren B.W., Nusbaum C., Lindblad-Toh K., Friedman N., Regev A. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotech. 29:644-652.
27. Green R.E., Braun E.L., Armstrong J., Earl D., Nguyen N., Hickey G., Vandewege M.W., St. John J.A., Capella-Gutiérrez S., Castoe T.A., Kern C., Fujita M.K., Opazo J.C., Jurka J., Kojima K.K., Caballero J., Hubley R.M., Smit A.F., Platt R.N., Lavoie C.A., Ramakodi M.P., Finger J.W., Suh A., Isberg S.R., Miles L., Chong A.Y., Jaratlerdsiri W., Gongora J., Moran C., Iriarte A., McCormack J., Burgess S.C., Edwards S.V., Lyons E., Williams C., Breen M., Howard J.T., Gresham C.R., Peterson D.G., Schmitz J., Pollock D.D., Haussler D., Triplett E.W., Zhang G., Irie N., Jarvis E.D., Brochu C.A., Schmidt C.J., McCarthy F.M., Faircloth B.C., Hoffmann F.G., Glenn T.C., Gabaldón T., Paten B., Ray D.A. 2014. Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 346:1254449.
28. Hahn C., Bachmann L., Chevreux B. 2013. Reconstructing mitochon-drial genomes directly from genomic next-generation sequencing reads-a baiting and iterative mapping approach. Nucleic Acids Res. 41:e129.
29. Haynie M.L., Tsuchiya M.T.N., Ospina-Garcés S.M., Arroyo-Cabrales J., Medellín R.A., Polaco O.J., Maldonado J.E. 2016. Placement of the rediscovered Myotis planiceps (Chiroptera: Vespertilionidae) within the Myotis phylogeny. J. Mammal. 97:701-712.
30. Hedtke S.M., Townsend T.M., Hillis D.M. 2006. Resolution of phylo-genetic conflict in large data sets by increased taxon sampling. Syst. Biol. 55:522-529.
31. Hollister N. 1909. Two new bats from the southwestern United States. Proc. Biol. Soc. Wash. 22:43-44.
32. Hosner P.A., Faircloth B.C., Glenn T.C., Braun E.L., Kimball R.T. 2016. Avoiding missing data biases in phylogenomic inference: An empirical study in the landfowl (Aves: Galliformes). Mol. Biol. Evol. 33:1110-1125.
33. Huang H., He Q., Kubatko L.S., Knowles L.L. 2010. Sources of error inherent in species-tree estimation: impact of mutational and coalescent effects on accuracy and implications for choosing among different methods. Syst. Biol. 59:573-583.
34. Huang W., Zhou G., Marchand M., Ash J.R., Morris D., Van Dooren P., Brown J.M., Gallivan K. A., Wilgenbusch J.C. 2016. TreeScaper: visualizing and extracting phylogenetic signal from sets of trees. Mol. Biol. Evol. 33:3314-3316.
35. Hudson R.R., Coyne J.A., Huelsenbeck J. 2002. Mathematical consequences of the genealogical species concept. Evolution 56:1557-1565.
36. Kapusta A., Suh A., Feschotte C. 2017. Dynamics of genome size evolution in birds and mammals. Proc. Natl. Acad. Sci. U. S. A. 114:E1460-E1469.
37. Katoh K., Misawa K., Kuma K.I., Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059-3066.
38. Lack J.B., Roehrs Z.P., Stanley C.E., Ruedi M., Van Den Bussche R.A. 2010. Molecular phylogenetics of Myotis indicate familial-level divergence for the genus Cistugo (Chiroptera). J. Mammal. 91:976-992.
39. Lanfear R., Calcott B., Ho S.Y.W., Guindon S. 2012. Partition-Finder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29: 1695-1701.
40. Larsen R.J., Knapp M.C., Genoways H.H., Khan F.A.A., Larsen P.A., Wilson D.E., Baker R.J. 2012. Genetic diversity of neotropical Myotis (Chiroptera: Vespertilionidae) withanemphasisonSouth American species. PLoS One 7:e46578.
41. LaVal R.K. 1973. A revision of the Neotropical bats of the genus Myotis Los Angeles County: Natural History Museum.
42. Leaché A.D., Rannala B. 2011. The accuracy of species tree estimation under simulation: a comparison of methods. Syst. Biol. 60: 126-137.
43. Leavitt D.H., Marion A.B., Hollingsworth B.D., Reeder T.W. 2017. Multilocus phylogeny of alligator lizards (Elgaria, Anguidae): testing mtDNA introgression as the source of discordant molecular phylogenetic hypotheses. Mol. Phylogenet. Evol. 110: 104-121.
44. Lewin-Koh N. 2011. Hexagon binning: an overview. Available from: URL ftp://ftp.naist.jp/pub/lang/R/CRAN/web/packages/hexbin/vignettes/hexagon-binning.pdf.
45. Li G., Davis B.W., Eizirik E., Murphy W.J. 2016. Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae). Genome Res. 26:1-11.
46. Li H., Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
47. Liu L., Edwards S.V. 2015. Comment on "Statistical binning enables an accurate coalescent-based estimation of the avian tree". Science 350:171.
48. Liu L., Yu L., Kubatko L., Pearl D.K., Edwards S.V. 2009. Coalescent methods for estimating phylogenetic trees. Mol. Phylogenet. Evol. 53:320-328.
49. Manning R.W., Jones J.K. 1989. Myotis evotis. Mamm. Species Archive 329:1-5.
50. McCormack J.E., Harvey M.G., Faircloth B.C., Crawford N.G., Glenn T.C., Brumfield R.T. 2013. A Phylogeny of birds based on over 1, 500 loci collected by target enrichment and high-throughput sequencing. PLoS One 8:e54848.
51. McGee M.D., Faircloth B.C., Borstein S.R., Zheng J., Darrin Hulsey C., Wainwright P.C., Alfaro M.E. 2016. Replicated divergence in cichlid radiations mirrorsa major vertebrate innovation. Proc. R. Soc. Lond. B Biol. Sci. 283:20151413.
52. Meiklejohn K.A., Faircloth B.C., Glenn T.C., Kimball R.T., Braun E.L. 2016. Analysis of a rapid evolutionary radiation using Ultraconserved Elements: Evidence for a bias in some multispecies coalescent methods. Syst. Biol. 65:612-627.
53. Miller G.S. Jr., Allen G. 1928. The American bats of the genus Myotis and Pixonyx. Bull. US Nat. Mus. 144:1-218.
54. Mirarab S., Bayzid M.S., Boussau B., Warnow T. 2014. Statistical binning enables an accurate coalescent-based estimation of the avian tree. Science 346:1250463.
55. Mirarab S., Bayzid M.S., Warnow T. 2016. Evaluating summary methods for multilocus species tree estimation in the presence of incomplete lineage sorting. Syst. Biol. 65:366-380.
56. Mirarab S., Warnow T. 2015. ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31:i44-i52.
57. Morales A.E., Jackson N.D., Dewey T.A., O'Meara B.C., Carstens B.C. 2016. Speciation with geneflowinNorth American Myotisbats. Syst. Biol. 66:440-452.
58. O'Farrell M.J., Studier E.H. 1980. Myotis thysanodes. Mamm. Species 137:1-5.
59. Pagan H.J.T., Smith J.D., Hubley R.M., Ray D.A. 2010. PiggyBac-ing on a Primate genome: novel elements, recent activity and horizontal transfer. Genome Biol. Evol. 2:293-303.
60. Pattengale N.D., Alipour M., Bininda-Emonds O.R.P., Moret B.M.E., Stamatakis A. 2009. How many bootstrap replicates are necessary? In: Batzoglou S, editor. Research in Computational Molecular Biology: 13th Annual International Conference, RECOMB 2009, Tucson, AZ, USA, May 18-21, 2009. Proceedings. Berlin, Heidelberg: Springer Berlin Heidelberg, p. 184-200.
61. Piaggio A.J., Valdez E.W., Bogan M.A., Spicer G.S. 2002. Systematics of Myotis occultus (Chiroptera: Vespertilionidae) inferred from sequences of two mitochondrial genes. J. Mammal. 83:386-395.
62. Platt R.N., Mangum S.F., Ray D.A. 2016. Pinpointing the vesper bat transposon revolution using the Miniopterus natalensis genome. Mob. DNA 7:12.
63. Platt R.N., Vandewege M.W., Kern C., Schmidt C.J., Hoffmann F.G., Ray D.A. 2014. Large numbers of novelmi RNAsoriginate from DNA transposons and are coincident with a large species radiation in bats. Mol. Biol. Evol. 31:1536-1545.
64. Platt R.N., Zhang Y., Witherspoon D.J., Xing J., Suh A., Keith M.S., Jorde L.B., Stevens R.D., Ray D.A. 2015. Targeted capture of phylogenetically informative ves SINE insertions in genus myotis. Genome Biol. Evol. 7:1664-1675.
65. Pritham E.J., Feschotte C. 2007. Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus. Proc. Natl. Acad. Sci. U. S. A. 104:1895-1900.
66. Puechmaille S.J., Allegrini B., Boston E.S.M., Dubourg-Savage M.-J., Evin A., Knochel A., Le Bris Y., Lecoq V., Lemaire M., Rist D., Teeling E.C. 2012. Genetic analyses reveal further cryptic lineages within the Myotis nattereri species complex. Mammal. Biol. 77:224-228.
67. Rambaut A., Drummond A. 2013. TreeAnnotator v1. 7.0. Available from: URL http://beast.bio.ed.ac.uk.
68. Rambaut A., Suchard M., Xie D., Drummond A. 2014. Tracer v1.6. Available from: URL http://beast.bio.ed.ac.uk.
69. Ray D.A., Feschotte C., Pagan H.J.T., Smith J.D., Pritham E.J., Arensburger P., Atkinson P.W., Craig N.L. 2008. Multiple waves of recent DNA transposon activity in the bat, Myotis lucifugus. Genome Res. 18:717-728.
70. Ray D.A., Pagan H.J.T., Thompson M.L., Stevens R.D. 2007. Bats with hATs: evidence for recent DNA transposon activity in genus Myotis. Mol. Biol. Evol. 24:632-639.
71. Rice P., Longden I., Bleasby A. 2000. EMBOSS:theEuropean molecular biology open software suite. Curr. Trends 16:276-277.
72. Rodríguez-Ezpeleta N., Brinkmann H., Roure B., Lartillot N., Lang B.F., Philippe H. 2007. Detecting and overcoming systematic errors in genome-scale phylogenies. Syst. Biol. 56:389-399.
73. Roehrs Z.P., Lack J.B., Van Den Bussche R.A. 2010. Tribal phylogenetic relationshipswithin Vespertilioninae (Chiroptera: Vespertilionidae) based on mitochondrial and nuclear sequence data. J. Mammal. 91:1073-1092.
74. Ruedi M., Mayer F. 2001. Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. Mol. Phylogenet. Evol. 21:436-448.
75. Ruedi M., Stadelmann B., Gager Y., Douzery E.J.P., Francis C.M., Lin L.-K., Guillén-Servent A., Cibois A. 2013. Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera). Mol. Phylogenet. Evol. 69:437-449.
76. Seo T.-K. 2008. Calculating bootstrap probabilities of phylogeny using multilocus sequence data. Mol. Biol. Evol. 25:960-971.
77. Simões B.F., Rebelo H., Lopes R.J., Alves P.C., Harris D.J. 2007. Patterns of genetic diversity within and between Myotis d. daubentonii and M. d. nathalinae derived from cytochrome b mtDNA sequence data. Acta Chiropt. 9:379-389.
78. Sota T. 2002. Radiation and reticulation: extensive introgressive hybridization in the carabid beetles Ohomopterus inferred from mitochondrial gene genealogy. Population Ecol. 44: 0145-0156.
79. Stadelmann B., Lin L.K., Kunz T.H., Ruedi M. 2007. Molecular phylo-geny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. Mol. Phylogenet. Evol. 43:32-48.
80. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
81. Swofford D.L. 2003. PAUP∗. Phylogenetic analysis using parsimony (∗ and other methods). Version 4. http://paup.sc.fsu.edu/
82. Thomas J., Sorourian M., Ray D., Baker R.J., Pritham E.J. 2011. The limited distribution of Helitrons to vesper bats supports horizontal transfer. Gene 474:52-58.
83. Vachaspati P., Warnow T. 2015. ASTRID: Accurate Species TRees from Internode Distances. BMC Genomics 16:S3.
84. Valdez E.W., Choate J.R., Bogan M.A., Yates T.L. 1999. Taxonomic status of Myotis occultus. J. Mammal. 80:545-552.
85. Warner R.M. 1982. Myotis auriculus. Mamm. Species 191:1-3.
86. Wiens J.J., Kuczynski C.A., Smith S.A., Mulcahy D.G., Sites J.J.W., Townsend T.M., Reeder T.W. 2008. Branch lengths, support, and congruence: testing the phylogenomic approach with 20 nuclear loci in snakes. Syst. Biol. 57:420-431.
87. Willis S.C., Farias I.P., Ortí G. 2014. Testing mitochondrial capture and deep coalescence in Amazonian cichlid fishes (Cichlidae: Cichla). Evolution 68:256-268.