Sexual species are separated by larger genetic gaps than asexual species in rotifers

Evolution

Volumn 68, Issue 10, 2014, Pages 2901-2916

  Tang, Cuong Q ^a   Obertegger, Ulrike ^b   Fontaneto, Diego ^a,c   Barraclough, Timothy G ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b RESEARCH AND INNOVATION CENTRE   (Italy)

^c CNR   (Italy)

Author keywords

Biodiversity; Diversification rate; Ecological speciation; GMYC; Species delimitation

Indexed keywords

AQUATIC ORGANISM; CLADISTICS; GENETIC ANALYSIS; GENOTYPE; INTERSPECIFIC VARIATION; INTRASPECIFIC VARIATION; REPRODUCTIVE ISOLATION;

ROTIFERA;

MITOCHONDRIAL DNA;

ANIMAL; ASEXUAL REPRODUCTION; BIOLOGICAL MODEL; CLASSIFICATION; DNA SEQUENCE; EVOLUTION; GENETICS; PHYLOGENY; PHYSIOLOGY; POPULATION GENETICS; ROTIFERA; STATISTICAL MODEL;

ANIMALS; BIOLOGICAL EVOLUTION; DNA, MITOCHONDRIAL; GENETICS, POPULATION; LINEAR MODELS; MODELS, GENETIC; PHYLOGENY; REPRODUCTION, ASEXUAL; ROTIFERA; SEQUENCE ANALYSIS, DNA;

EID: 84908080590     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12483     Document Type: Article

References (100)

1. Baayen, R. H., D. J. Davidson, andD.M. Bates. 2008. Mixed-effects modeling with crossed random effects for subjects and items. J. Mem. Lang. 59:390-412.
2. Bargues, M. D., A. Marcilla, J. M. Ramsey, J. P. Dujardin, C. J. Schofield, and S. Mas-Coma. 2000. Nuclear rDNA-based molecular clock of the evolution of triatominae (Hemiptera: reduviidae), vectors of Chagas disease. Mem. Inst. Oswaldo Cruz 95:567-573.
3. Barraclough, T. G., and E. A. Herniou. 2003. Why do species exist? Insights from sexuals and asexuals. Zoology 106:275-282.
4. Barraclough, T. G., and S. Nee. 2001. Phylogenetics and speciation. Trends Ecol. Evol. 16:391-399.
5. Barraclough, T. G., C. W. Birky, and A. Burt. 2003. Diversification in sexual and asexual organisms. Evolution 57:2166-2172.
6. Barraclough, T. G., D. Fontaneto, C. Ricci, and E. A. Herniou. 2007. Evidence for inefficient selection against deleterious mutations in cytochrome oxidase I of asexual bdelloid rotifers. Mol. Biol. Evol. 24:1952-1962.
7. Bates, D., and D. Sarkar. 2007. lme4: linear mixed-effects models using S4 classes.
8. Becks, L., and A. F. Agrawal. 2012. The evolution of sex is favoured during adaptation to new environments. PLoS Biol. 10:e1001317.
9. Birky, C. W. 2010. Positively negative evidence for asexuality. J. Hered. 101:S42-S45.
10. Birky, C. W., C. Wolf, H. Maughan, L. Herbertson, and E. Henry. 2005. Speciation and selection without sex. Hydrobiologia 546:29-45.
11. Birky, C. W., and T. G. Barraclough. 2009. Asexual speciation. Pp. 201-216 in I. Schön, K. Martens, and P. van Dijk, eds. Lost sex-the evolutionary biology of parthenogenesis. Springer, Dordrecht.
12. Blair, C., and R. W. Murphy. 2011. Recent trends in molecular phylogenetic analysis: where to next? J. Hered 102:130-138.
13. Burke, J. M., and M. L. Arnold. 2001. Genetics and the fitness of hybrids. Annu. Rev. Genet. 35:31-52.
14. Burt, A. 2000. Perspective: sex, recombination, and the efficacy of selection- was Weismann right? Evolution 54:337-351.
15. Butlin, R. K. 2002. The costs and benefits of sex: new insights from old asexual lineages. Nat. Rev. Genet 3:311-317.
16. Champely, S., and M. S. Champely. 2007. PWR: basic functions for power analysis, R package version 1.1.
17. Charlesworth, B., D. Charlesworth, and N. H. Barton. 2003. The effects of genetic and geographic structure on neutral variation. Annu. Rev. Ecol. Evol. Syst. 34:99-125.
18. Ciros-Perez, J. 2001. On the taxonomy of three sympatric sibling species of the Brachionus plicatilis (Rotifera) complex from Spain, with the description of B. ibericus n. sp. J. Plankton Res. 23:1311-1328.
19. Cohan, F. M. 2001. Bacterial species and speciation. Syst. Biol. 50:513- 524.
20. Cohen, J. 1992. Statistical power analysis. Curr. Dir. Psychol. Sci. 1:98-101.
21. Coyne, J. A., and H. A. Orr. 1998. The evolutionary genetics of speciation. Philos. Trans. R. Soc. Lond. B 353:287-305.
22. Coyne, J. A. H. A. Orr. 2004. Species: reality and concepts. Pp. 1-54 in Speciation. Sinauer Associates, Inc., Sunderland, MA.
23. Cusimano, N., T. Stadler, and S. S. Renner. 2012. A new method for handling missing species in diversification analysis applicable to randomly or nonrandomly sampled phylogenies. Syst. Biol. 61:785-792.
24. Darriba, D., G. L. Taboada, R. Doallo, and D. Posada. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772.
25. De Meester, L., A. Gómez, B. Okamura, and K. Schwenk. 2002. The Monopolization Hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecologica 23:121-135.
26. De Queiroz, K. 2005. Ernst Mayr and the modern concept of species. Proc. Natl. Acad. Sci. USA 102:6600-6607.
27. De Queiroz, K. 2007. Species concepts and species delimitation. Syst. Biol. 56:879- 886.
28. Dobzhansky, T. 1937. Genetics and the origin of species. Columbia Univ. Press, New York.
29. Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
30. Drummond, A. J., M. Kearse, J. Heled, R. Moir, T. Thierer, B. Ashton, A. Wilson, and S. Stones-Havas. 2006. Geneious v5.4.2.
31. Ezard, T., T. Fujisawa, and T. G. Barraclough. 2009. Splits: SPecies' LImits by Threshold Statistics.
32. Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35:124-138.
33. Felsenstein, J. 1985. Phylogenies and the comparative method. Am. Nat. 125:1-15.
34. Fisher, R. A. 1930. The genetical theory of natural selection. Oxford Univ. Press, Oxford, U.K.
35. Flot, J.-F., B. Hespeels, X. Li, B. Noel, I. Arkhipova, E. G. J. Danchin, A. Hejnol, B. Henrissat, R. Koszul, J.-M. Aury, et al. 2013. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500:453-457.
36. Fontaneto, D., and U. Jondelius. 2011. Broad taxonomic sampling of mitochondrial cytochrome c oxidase subunit I does not solve the relationships between Rotifera and Acanthocephala. Zool. Anzeiger 250: 80-85.
37. Fontaneto, D., E. A. Herniou, T. G. Barraclough, C. Ricci, and G. Melone. 2007a. On the reality and recognisability of asexual organisms: morphological analysis of the masticatory apparatus of bdelloid rotifers. Zool. Scr. 36:361-370.
38. Fontaneto, D., E. A. Herniou, C. Boschetti, M. Caprioli, G. Melone, C. Ricci, and T.G. Barraclough. 2007b. Independently evolving species in asexual bdelloid rotifers. PLoS Biol. 5:e87.
39. Fontaneto, D., T. G. Barraclough, K. Chen, C. Ricci, and E. A. Herniou. 2008. Molecular evidence for broad-scale distributions in bdelloid rotifers: everything is not everywhere but most things are very widespread. Mol. Ecol. 17:3136-3146.
40. Fontaneto, D., M. Kaya, E. A. Herniou, and T. G. Barraclough. 2009. Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy. Mol. Phylogenet. Evol. 53:182-189.
41. Fontaneto, D., A. M. Barbosa, H. Segers, and M. Pautasso. 2012a. The "rotiferologist" effect and other global correlates of species richness in monogonont rotifers. Ecography 35:174-182.
42. Fontaneto, D., C. Q. Tang, U. Obertegger, F. Leasi, and T. G. Barraclough. 2012b. Different diversification rates between sexual and asexual organisms. Evol. Biol. 39:262-270.
43. Fu, Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915- 925.
44. Fu, Y. X., and W. H. Li. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
45. Fujisawa, T., and T. G. Barraclough. 2013. Delimiting species using singlelocus data and the Generalized Mixed Yule Coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Syst. Biol. 62:707-724.
46. Gernhard, T. 2008. The conditioned reconstructed process. J. Theor. Biol. 253:769-778.
47. Gómez, A., M. Serra, G. R. Carvalho, and D. H. Lunt. 2002. Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56:1431-1444.
48. Heethoff, M., R. A. Norton, S. Scheu, andM. Maraun. 2009. Parthenogenesis in oribatid mites (Acari, Oribatida): Evolution without sex. Pp. 241-258 in I. Schön, K. Martens, and P. van Dijk, eds. Lost sex-the evolutionary biology of parthenogenesis. Springer, Dordrecht.
49. Ho, S. Y.W., U. Saarma, R. Barnett, J. Haile, and B. Shapiro. 2008. The effect of inappropriate calibration: three case studies in molecular ecology. PLoS One 3:e1615.
50. Holman, E. 1987. Recognizability of sexual and asexual species of rotifers. Syst. Biol. 36:381-386.
51. Jenkins, D. G., and M. O. Underwood. 1998. Zooplankton may not disperse readily in wind, rain, or waterfowl. Hydrobiologia 388:15-21.
52. Katoh, K., G. Asimenos, and H. Toh. 2009. Multiple alignment of DNA sequences with MAFFT. Methods Mol. Biol. 537:39-64.
53. Leasi, F., C. Q. Tang, W. H. De Smet, and D. Fontaneto. 2013. Cryptic diversity with wide salinity tolerance in the putative euryhaline Testudinella clypeata (Rotifera, Monogononta). Zool. J. Linn. Soc. 168:17-28.
54. Librado, P., and J. Rozas. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
55. Lynch, M., and W. Hill. 1986. Phenotypic evolution by neutral mutation. Evolution 40:915-935.
56. Malekzadeh-Viayeh, R., R. Pak-Tarmani, N. Rostamkhani, and D. Fontaneto. 2014. Diversity of the rotifer Brachionus plicatilis species complex (Rotifera: Monogononta) in Iran through integrative taxonomy. Zool. J. Linn. Soc. 170:233-244.
57. Mark Welch, D. B., C. Ricci, and M. Meselson. 2009. Bdelloid rotifers: progress in understanding the success of an evolutionary scandal. Pp. 259-280 in I. Schön, K. Martens, and P. van Dijk, eds. Lost sex-the evolutionary biology of parthenogenesis. Springer, Dordrecht.
58. Maynard Smith, J., and E. Száthmary. 1995. The major transitions in evolution. W. H. Freeman, Oxford, U.K.
59. McPeek, M. A. 2008. The ecological dynamics of clade diversification and community assembly. Am. Nat. 172:E270-E284.
60. Melone, G., and D. Fontaneto. 2005. Trophi structure in bdelloid rotifers. Hydrobiologia 546:197-202.
61. Miller, M. A., W. Pfeiffer, and T. Schwartz. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Pp. 1-8 in Proceedings of the Gateway Computing Environments Workshop (GCE). Institute of Electrical and Electronics Engineers (IEEE), New Orleans, LA.
62. Nee, S., R. M. May, and P. H. Harvey. 1994. The reconstructed evolutionary process. Philos. Trans. R. Soc. Lond. B 344:305-311.
63. Nei, M., and W. H. Li. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA 76:5269-5273.
64. Obertegger, U., D. Fontaneto, and G. Flaim. 2012. Using DNA taxonomy to investigate the ecological determinants of plankton diversity: explaining the occurrence of Synchaeta spp. (Rotifera, Monogononta) in mountain lakes. Freshw. Biol. 57:1545-1553.
65. Ochman, H., and A. Wilson. 1987. Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J. Mol. Evol. 26: 74-86.
66. Paradis, E., J. Claude, and K. Strimmer. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
67. Poinar, G. O., and C. Ricci. 1992. Bdelloid rotifers in Dominican amber: evidence for parthenogenetic continuity. Experientia 48:408-410.
68. Pons, J., T. G. Barraclough, J. Gomez-Zurita, A. Cardoso, D. Duran, S. Hazell, S. Kamoun,W. Sumlin, and A. P. Vogler. 2006. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 55:595-609.
69. Pybus, O. G., and P. H. Harvey. 2000. Testing macro-evolutionary models using incomplete molecular phylogenies. Proc. R. Soc. Lond. B 267:2267- 2272.
70. R Core Team. 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
71. Rabosky, D. L. 2006. LASER: a maximum likelihood toolkit for detecting temporal shifts in diversification rates frommolecular phylogenies. Evol. Bioinform. Online 2:247-250.
72. Rabosky, D. L., and I. J. Lovette. 2008. Density-dependent diversification in North American wood warblers. Proc. R. Soc. Lond. B 275:2363- 2371.
73. Rambaut, A., and A. J. Drummond. 2007. Tracer v1.4.
74. Ramos-Onsins, S. E., and J. Rozas. 2002. Statistical properties of new neutrality tests against population growth. Mol. Biol. Evol. 19:2092- 100.
75. Ricci, C. 1998. Anhydrobiotic capabilities of bdelloid rotifers. Hydrobiologia 387:321.
76. Ricci, C. 2001. Dormancy patterns in rotifers. Hydrobiologia 44-447:1-11.
77. Rice, W. R., and U. Friberg. 2009. A graphical approach to lineage selection between clonals and sexuals. Pp. 75-97 in I. Schön, K. Martens, and P. van Dijk, eds. Lost sex-the evolutionary biology of parthenogenesis. Springer, Dordrecht.
78. Rice, W. R., and E. E. Hostert. 1993. Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47:1637-1653.
79. Ricklefs, R. E. 2007. Estimating diversification rates from phylogenetic information. Trends Ecol. Evol. 22:601-10.
80. Rieseberg, L. H., T. E. Wood, and E. J. Baack. 2006. The nature of plant species. Nature 440:524-527.
81. Robeson, M. S., A. J. King, K. R. Freeman, C.W. Birky,A. P.Martin, and S. K. Schmidt. 2011. Soil rotifer communities are extremely diverse globally but spatially autocorrelated locally. Proc. Natl. Acad. Sci. U. S. A. 108:4406-4410.
82. Rokas, A., B. L. Williams, N. King, and S. B. Carroll. 2003. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425:798-804.
83. Rosenberg, N. A., and M. Nordborg. 2002. Genealogical trees, coalescent theory and the analysis of genetic polymorphisms. Nat. Rev. Genet. 3:380-390.
84. Roughgarden, J. 1979. Theory of population genetics and evolutionary ecology. Macmillan, New York.
85. Schluter, D. 2001. Ecology and the origin of species. Trends Ecol. Evol. 16:372-380.
86. Schön, I., R. L. Pinto, S. Halse, A. J. Smith, K. Martens, and C. W. Birky. 2012. Cryptic species in putative ancient asexual Darwinulids (Crustacea, Ostracoda). PLoS One 7:e39844.
87. Segers, H. 2007. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Magnolia Press, Auckland, New Zealand.
88. Simpson, G. G. 1951. The species concept. Evolution 5:285-298.
89. Stadler, T. 2011. TreePar in R-estimating diversification rates in phylogenies.
90. Suatoni, E., S. Vicario, S. Rice, T. Snell, and A. Caccone. 2006. An analysis of species boundaries and biogeographic patterns in a cryptic species complex: the rotifer Brachionus plicatilis.Mol. Phylogenet. Evol. 41:86-98.
91. Swanstrom, J., K. Chen, K. Castillo, T. G. Barraclough, and D. Fontaneto. 2011. Testing for evidence of inefficient selection in bdelloid rotifers: do sample size and habitat differences matter? Hydrobiologia 622:19-25.
92. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
93. Tamura, K., D. Peterson, N. Peterson, G. Stecher,M. Nei, and S. Kumar. 2011. MEGA5:molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
94. Tang, C. Q., F. Leasi, U. Obertegger, A. Kieneke, T. G. Barraclough, and D. Fontaneto. 2012. The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proc. Natl. Acad. Sci. USA 109:16208-16212.
95. Templeton, A. R. 1989. The meaning of species and speciation: a genetic perspective. Pp. 3-27 in D. Otte and J. A. Endler, eds. Speciation and Its Consequences. Sinauer Associates, Sunderland, MA.
96. Tsai, I. J., D. Bensasson, A. Burt, and V. Koufopanou. 2008. Population genomics of the wild yeast Saccharomyces paradoxus: quantifying the life cycle. Proc. Natl. Acad. Sci. USA 105:4957-4962.
97. Walsh, E. J., H. A. Smith, and R. L. Wallace. 2014. Rotifers of temporary waters. Int. Rev. Hydrobiol. 98:1-17.
98. Weismann, A. 1889. The significance of sexual reproduction in the theory of natural selection. Pp. 251-332 in E. B. Poulton, S. Schonland, and A. E. Shipley, eds. Essays upon heredity and kindred biological problems. Clarendon Press, Oxford, U.K.
99. Wilke, T., R. Schultheib, and C. Albrecht. 2009. As time goes by: a simple fool's guide to molecular clock approaches in invertebrates. Am. Malacol. Bull. 27:25-45.
100. Wilson, C. G., and P. W. Sherman. 2013. Spatial and temporal escape from fungal parasitism in natural communities of anciently asexual bdelloid rotifers. Proc. R. Soc. Lond. B 280:20131255.