Natural hybridization between genera that diverged from each other approximately 60 million years ago

American Naturalist

Volumn 185, Issue 3, 2015, Pages 433-442

  Rothfels, Carl J ^a   Johnson, Anne K ^b   Hovenkamp, Peter H ^c   Swofford, David L ^b,d   Roskam, Harry C ^c,e   Fraser Jenkins, Christopher R ^f   Windham, Michael D ^b   Pryer, Kathleen M ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b DUKE UNIVERSITY   (United States)

^c NATURALIS BIODIVERSITY CENTER   (Netherlands)

^d NATIONAL EVOLUTIONARY SYNTHESIS CENTER   (United States)

^e LEIDEN UNIVERSITY   (Netherlands)

^f Student Guest House   (Nepal)

Author keywords

Allopolyploidy; Deep hybridization; Divergence time dating; Reproductive isolation; Speciation; Species selection

Indexed keywords

FERN; FERTILIZATION (REPRODUCTION); HYBRIDIZATION; POLYPLOIDY; REPRODUCTIVE ISOLATION; SPECIATION (BIOLOGY);

FRANCE; PYRENEES;

FILICOPHYTA; LEMUR; MAGNOLIOPHYTA; MYA;

EVOLUTION; FERN; FRANCE; GENETICS; HYBRIDIZATION; MOLECULAR GENETICS; PHYLOGENY; REPRODUCTION; SEQUENCE ANALYSIS; SPECIES DIFFERENTIATION;

BIOLOGICAL EVOLUTION; FERNS; FRANCE; GENETIC SPECIATION; HYBRIDIZATION, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; REPRODUCTION; SEQUENCE ANALYSIS, PROTEIN;

EID: 84922724978     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/679662     Document Type: Article

References (93)

1. Abbott, R., D. Albach, S. Ansell, J. W. Arntzen, S. J. E. Baird, N. Bierne, J. Boughman, et al. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26:229-246.
2. Arrigo, N., J. P. Therrien, C. L. Anderson, M. D. Windham, C. H. Haufler, and M. S. Barker. 2013. A total evidence approach to understanding phylogenetic relationships and ecological diversity in Selaginella subg. Tetragonostachys. American Journal of Botany 100:1672-1682.
3. Baldwin, B. G., S. Kalisz, and W. S. Armbruster. 2011. Phylogenetic perspectives on diversification, biogeography, and floral evolution of Collinsia and Tonella (Plantaginaceae). American Journal of Botany 98:731-753.
4. Barbash, D. A., D. F. Siino, A. M. Tarone, and J. Roote. 2003. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proceedings of the National Academy of Sciences of the USA 100:5302-5307.
5. Beck, J. B., M. D. Windham, and K. M. Pryer. 2011. Do asexual polyploid lineages lead short evolutionary lives? a case study from the fern genus Astrolepis. Evolution 65:3217-3229.
6. Blasdell, R. F. 1963. A monographic study of the fern genus Cystopteris. Memoirs of the Torrey Botanical Club 21:1-102.
7. Bolnick, D. I., and T. J. Near. 2005. Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae). Evolution 59:1754-1767.
8. Bouchenak-Khelladi, Y., G. A. Verboom, V. Savolainen, and T. R. Hodkinson. 2010. Biogeography of the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in geographical space and geological time. Botanical Journal of the Linnean Society 162:543-557.
9. Brown, J. W., J. S. Rest, J. García-Moreno, M. D. Sorenson, and D. P. Mindell. 2008. Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages. BMC Biology 6:6.
10. Butlin, R. 1987. Speciation by reinforcement. Trends in Ecology and Evolution 2:8-13.
11. Carlin, B. P., and T. A. Louis. 1997. Bayes and empirical Bayes methods for data analysis. Statistics and Computing 7:153-154.
12. Carson, H. 1976. Inference of the time of origin of some Drosophila species. Nature 259:395-396.
13. Coyne, J. A., and H. A. Orr. 1989. Patterns of speciation in Drosophila. Evolution 43:362-381.
14. Coyne, J. A., and H. A. Orr. 1997. “Patterns of speciation in Drosophila” revisited. Evolution 51:295-303.
15. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland, MA.
16. Cronn, R., M. Cedroni, T. Haselkorn, C. Grover, and J. F. Wendel. 2002. PCR-mediated recombination in amplification products derived from polyploid cotton. Theoretical and Applied Genetics 104: 482-489.
17. Delignette-Muller, M. L., R. Pouillot, J.-B. Denis, and C. Dutang. 2010. Fitdistrplus: help to fit of a parametric distribution to noncensored or censored data. R package. Version 0.1-3. http://cran.r-project.org/web/packages/fitdistrplus/index.html.
18. Dimcheff, D. E., S. V. Drovetski, and D. P. Mindell. 2002. Phylogeny of Tetraoninae and other galliform birds using mitochondrial 12S and ND2 genes. Molecular Phylogenetics and Evolution 24:203-215.
19. Drummond, A. J., S. Y. W. Ho, M. J. Phillips, and A. Rambaut. 2006. Relaxed phylogenetics and dating with confidence. PLOS Biology 4(5):e88. doi:10.1371/journal.pbio.0040088.
20. Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7: 214.
21. Edmands, S. 2002. Does parental divergence predict reproductive compatibility? Trends in Ecology and Evolution 17:520-527.
22. Forster, B. P., and J. E. Dale. 1983. Effects of parental embryo and endosperm mitotic cycle times on development of hybrids between barley and rye. Annals of Botany 52:613-620.
23. Fraser-Jenkins, C. R. 1997. New species syndrome in Indian pteridology and the ferns of Nepal. International Book Distributors, Dehra Dun, India.
24. Fraser-Jenkins, C. R. 2008. Taxonomic revision of three hundred Indian subcontinental pteridophytes with a revised census-list: a new picture of fern-taxonomy and nomenclature in the Indian subcontinent. Bishen Singh Mahendra Pal Singh, Dehra Dun, India.
25. Fraser-Jenkins, C. R., Y. P. S. Pangtey, and S. P. Kullar. 2010. Asplenium laciniatum D. Don (Aspleniaceae), a critical complex, and confused species in the Indian subcontinent. Indian Fern Journal 27:212-214.
26. Garland, M. A., and G. Moore. 2012. Hesperotropsis, a new nothogenus for intergeneric crosses between Hesperocyparis and Callitropsis (Cupressaceae), and a review of the complicated nomenclatural history of the Leyland cypress. Taxon 61:667-670.
27. Graur, D., and W. Martin. 2004. Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends in Genetics 20:80-86.
28. Grusz, A. L., M. D. Windham, and K. M. Pryer. 2009. Deciphering the origins of apomictic polyploids in the Cheilanthes yavapensis complex (Pteridaceae). American Journal of Botany 96:1636-1645.
29. Guindon, S., J. F. Dufayard, V. Lefort, M. Anisimova, W. Hordijk, and O. Gascuel. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59:307-321.
30. Hegde, S. G., J. D. Nason, J. M. Clegg, and N. C. Ellstrand. 2006. The evolution of California’s wild radish has resulted in the extinction of its progenitors. Evolution 60:1187-1197.
31. Hopkins, R., and M. D. Rausher. 2012a. Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii. Nature 469:411-414.
32. Hopkins, R., and M. D. Rausher. 2012b. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335:1090-1092.
33. Jablonski, D. 2008. Species selection: theory and data. Annual Review of Ecology and Systematics 39:501-524.
34. Kay, K. M., C. Voelckel, J. Y. Yang, K. M. Hufford, D. D. Kaska, and S. A. Hodges. 2006. Floral characters and species diversification. Pages 311-325 in L. D. Harder and S. C. H. Barrett, eds. Ecology and evolution of flowers. Oxford University Press, Oxford.
35. Kirkpatrick, M., and V. Ravigné. 2002. Speciation by natural and sexual selection: models and experiments. American Naturalist 159(S3):S22-S35.
36. Lanfear, R., B. Calcott, S. Y. W. Ho, and S. Guindon. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29:1695-1701.
37. Larsson, A. 2014. Systematics of Woodsia. Ferns, bioinformatics and more. PhD thesis. University of Uppsala.
38. Levin, D. A. 2013. The timetable for allopolyploidy in flowering plants. Annals of Botany 112:1201-1208.
39. Lewis, P. O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50: 913-925.
40. Li, F.-W., K. M. Pryer, and M. D. Windham. 2012. Gaga, a new fern genus segregated from Cheilanthes (Pteridaceae). Systematic Botany 37:845-860.
41. Lovis, J. 1978. Evolutionary patterns and processes in ferns. Advances in Botanical Research 4:229-415.
42. Mable, B. K., and J. P. Bogart. 1995. Hybridization between tetraploid and diploid species of treefrogs (genus Hyla). Journal of Heredity 86:432-440.
43. Mallet, J. 2005. Hybridization as an invasion of the genome. Trends in Ecology and Evolution 20:229-237.
44. Mallet, J. 2007. Hybrid speciation. Nature 446:279-283.
45. Manton, I. 1950. Problems of cytology and evolution in the Pteridophyta. Cambridge University Press, Cambridge.
46. Mao, K., R. I. Milne, L. Zhang, Y. Peng, J. Liu, P. Thomas, R. R. Mill, and S. R. Renner. 2012. Distribution of living Cupressaceae reflects the breakup of Pangea. Proceedings of the National Academy of Sciences of the USA 109:7793-7798.
47. Matute, D. R., I. A. Butler, D. A. Turissini, and J. A. Coyne. 2010. A test of the snowball theory for the rate of evolution of hybrid incompatibilities. Science 329:1516-1518.
48. Mayr, E. 1963. Animal species and evolution. Belknap, Cambridge, MA.
49. Mendelson, T. C. 2003. Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma). Evolution 57:317-327.
50. Moyle, L. C., and T. Nakazato. 2010. Hybrid incompatibility “snowballs” between Solanum species. Science 329:1521-1523.
51. Moyle, L. C., M. S. Olson, and P. Tiffin. 2004. Patterns of reproductive isolation in three angiosperm genera. Evolution 58:1195-1208.
52. Orr, H. A. 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139:1805-1813.
53. Parks, C. R., and J. F. Wendel. 1990. Molecular divergence between Asian and North American species of Liriodendron (Magnoliaceae) with implications for interpretation of fossil floras. American Journal of Botany 77:1243-1256.
54. Pereira, S. L., and A. J. Baker. 2006. A molecular timescale for galliform birds accounting for uncertainty in time estimates and heterogeneity of rates of DNA substitutions across lineages and sites. Molecular Phylogenetics and Evolution 38:499-509.
55. Prada, C. 1986. Cystopteris. Pages 115-121 in S. Castroviejo, ed. Flora Iberica. CSIC (Consejo Superior de Investigaciones Científicas), Madrid.
56. Prager, E. M., and A. C. Wilson. 1975. Slow evolutionary loss of the potential for interspecific hybridization in birds: a manifestation of slow regulatory evolution. Proceedings of the National Academy of Sciences of the USA 72:200-204.
57. Presgraves, D. C. 2002. Patterns of postzygotic isolation in Lepidoptera. Evolution 56:1168-1183.
58. Price, T. D. 2008. Speciation in birds. Roberts, Boulder, CO.
59. Price, T. D., and M. M. Bouvier. 2002. The evolution of F1 postzygotic incompatibilities in birds. Evolution 56:2083-2089.
60. Pryer, K. M., and C. H. Haufler. 1993. Isozymic and chromosomal evidence for the allotetraploid origin of Gymnocarpium dryopteris (Dryopteridaceae). Systematic Botany 18:150-172.
61. Rabosky, D. L., and A. McCune. 2010. Reinventing species selection with molecular phylogenies. Trends in Ecology and Evolution 25: 68-74.
62. Rambaut, A., and A. J. Drummond. 2007. Tracer. Version 1.5. http://beast.bio.ed.ac.uk/Tracer.
63. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
64. Rieseberg, L. H., and J. H. Willis. 2007. Plant speciation. Science 317: 910-914.
65. Ronquist, F., and J. P. Huelsenbeck. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
66. Rothfels, C. J. 2012. Phylogenetics of Cystopteridaceae: reticulation and divergence in a cosmopolitan fern family. PhD diss. Duke University, Durham NC.
67. Rothfels, C. J., A. K. Johnson, P. H. Hovenkamp, D. L. Swofford, H. C. Roskam, C. R. Fraser-Jenkins, M. D. Windham, and K. M. Pryer. 2015. Data from: Natural hybridization between genera that diverged from each other approximately 60 million years ago. American Naturalist, Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.r7201.
68. Rothfels, C. J., A. K. Johnson, M. D. Windham, and K. M. Pryer. 2014. Low-copy nuclear data confirm rampant allopolyploidy in the Cystopteridaceae (Polypodiales). Taxon 63:1026-1036.
69. Rothfels, C. J., A. Larsson, L.-Y. Kuo, P. Korall, W.-L. Chiou, and K. M. Pryer. 2012a. Overcoming deep roots, fast rates, and short internodes to resolve the ancient rapid radiation of eupolypod II ferns. Systematic Biology 61:490-509.
70. Rothfels, C. J., A. Larsson, F.-W. Li, E. M. Sigel, L. Huiet, D. O. Burge, M. Ruhsam, et al. 2013a. Transcriptome-mining for singlecopy nuclear markers in ferns. PLoS ONE 8:e76957. doi:10.1371/journal.pone.0076957.
71. Rothfels, C. J., and E. Schuettpelz. 2014. Accelerated rate of molecular evolution for vittarioid ferns is strong and not driven by selection. Systematic Biology 63:31-54.
72. Rothfels, C. J., M. A. Sundue, L.-Y. Kuo, A. Larsson, M. Kato, E. Schuettpelz, and K. M. Pryer. 2012b. A revised family-level classification for eupolypod II ferns (Polypodiidae: Polypodiales). Taxon 61:515-533.
73. Rothfels, C. J., M. D. Windham, and K. M. Pryer. 2013b. A plastid phylogeny of the cosmopolitan fern family Cystopteridaceae (Polypodiopsida). Systematic Botany 38:295-306.
74. Rumsey, F. J. 2003. Bladder-ferns Cystopteris of the British Isles. British Wildlife 15:93-96.
75. Russell, S. T. 2003. Evolution of intrinsic post-zygotic reproductive isolation in fish. Annales Zoologici Fennici 40:321-329.
76. Sasa, M. M., P. T. Chippindale, and N. A. Johnson. 1998. Patterns of postzygotic isolation in frogs. Evolution 52:1811-1820.
77. Schuettpelz, E., A. L. Grusz, M. D. Windham, and K. M. Pryer. 2008. The utility of nuclear gapCp in resolving polyploid fern origins. Systematic Botany 33:621-629.
78. Schuettpelz, E., and K. M. Pryer. 2007. Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56: 1037-1050.
79. Schuettpelz, E., and K. M. Pryer. 2009. Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proceedings of the National Academy of Sciences of the USA 106:11200-11205.
80. Seehausen, O. 2006. Conservation: losing biodiversity by reverse speciation. Current Biology 16:R334-R337.
81. Smith, A. R. 1972. Comparison of fern and flowering plant distributions with some evolutionary interpretations for ferns. Biotropica 4:4-9.
82. Smith, S. A., P. R. Stephens, and J. J. Wiens. 2005. Replicate patterns of species richness, historical biogeography, and phylogeny in Holarctic treefrogs. Evolution 59:2433-2450.
83. Stanley, S. M. 1975. A theory of evolution above the species level. Proceedings of the National Academy of Sciences of the USA 72: 646-650.
84. Stelkens, R. B., K. A. Young, and O. Seehausen. 2010. The accumulation of reproductive incompatibilities in African cichlid fish. Evolution 64:617-633.
85. Taylor, E. B., J. W. Boughman, M. Groenenboom, M. Sniatynski, D. Schluter, and J. L. Gow. 2005. Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Molecular Ecology 15:343-355.
86. Vida, G. 1974. Genome analysis of the European Cystopteris fragilis complex. 1: tetraploid taxa. Acta Botanica Academiae Scientiarum Hungaricae 20:181-192.
87. Vida, G., and J. Mohay. 1980. Cytophotometric DNA studies in polyploid series of the fern genus Cystopteris Bernh. Acta Botanica Academiae Scientiarum Hungaricae 26:455-461.
88. Wagner, W. H., Jr. 1993. New species of Hawaiian pteridophytes. Contributions from the University of Michigan Herbarium 19:63-82.
89. Wagner, W. H., Jr., F. S. Wagner, A. A. Reznicek, and C. R. Werth. 1992. Dryostichum singulare (Dryopteridaceae), a new fern nothogenus from Ontario. Canadian Journal of Botany 70:245-253.
90. Watanabe, T. K. 1979. A gene that rescues the lethal hybrids between Drosophila melanogaster and D. simulans. Japanese Journal of Genetics 54:325-331.
91. Wiens, J. J., T. N. Engstrom, and P. T. Chippindale. 2006. Rapid diversification, incomplete isolation, and the “speciation clock” in North American salamanders (genus Plethodon): testing the hybrid swarm hypothesis of rapid radiation. Evolution 60:2585-2603.
92. Windham, M. D., and G. Yatskievych. 2003. Chromosome studies of cheilanthoid ferns (Pteridaceae: Cheilanthoideae) from the western United States and Mexico. American Journal of Botany 90:1788-1800.
93. Zwickl, D. J. 2006. GARLI: genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD diss. University of Texas, Austin.