Strong premating reproductive isolation drives incipient speciation in Mimulus aurantiacus

Evolution

Volumn 69, Issue 2, 2015, Pages 447-461

  Sobel, James M ^a   Streisfeld, Matthew A ^b  

^a BINGHAMTON UNIVERSITY   (United States)

^b UNIVERSITY OF OREGON   (United States)

Author keywords

Biological species concept; Ecogeographic isolation; Pollinator isolation; Postmating barriers; Premating barriers

Indexed keywords

DICOTYLEDON; DIVERGENCE; ECOTYPE; GENE FLOW; GENOME; HYBRID ZONE; HYBRIDIZATION; MOLECULAR ANALYSIS; PHENOTYPE; REPRODUCTIVE ISOLATION; SPECIES CONCEPT;

CALIFORNIA; UNITED STATES;

DIPLACUS AURANTIACUS;

GENETIC MARKER;

ECOTYPE; FLOWER; GENE FLOW; GENETIC MARKER; GENETICS; HYBRIDIZATION; MIMULUS; PHYSIOLOGY; PIGMENTATION; POLLINATION; REPRODUCTIVE ISOLATION; SPECIES DIFFERENTIATION; UNITED STATES;

CALIFORNIA; ECOTYPE; FLOWERS; GENE FLOW; GENETIC MARKERS; GENETIC SPECIATION; HYBRIDIZATION, GENETIC; MIMULUS; PIGMENTATION; POLLINATION; REPRODUCTIVE ISOLATION;

EID: 84922566986     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12589     Document Type: Article

References (108)

1. Aldridge, G., and D. R. Campbell. 2007. Variation in pollinator preference between two Ipomopsis contact sites that differ in hybridization rate. Evolution 61:99-110.
2. Angert, A. L., and D. W. Schemske. 2005. The evolution of species' distributions: reciprocal transplants across the elevation ranges of Mimulus cardinalis and M. lewisii. Evolution 59:1671-1684.
3. Barton, N. H., and G. M. Hewitt. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113-148.
4. Beardsley, P. M., S. E. Schoenig, J. B. Whittall, and R. G. Olmstead. 2004. Patterns of evolution in Western North American Mimulus (Phrymaceae). Am. J. Bot. 91:474-489.
5. Beeks, R. M. 1962. Variation and hybridization in southern California populations of Diplacus (Scrophulariaceae). El Aliso 5:83-122.
6. Bolnick, D. I., and B. M. Fitzpatrick. 2007. Sympatric speciation: models and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 38:459-487.
7. Bradshaw, H. D., and D. W. Schemske. 2003. Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176-178.
8. Bush, G. L. 1969. Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera, Tephritidae). Evolution 23:237-251.
9. Campbell, D. R. 2004. Natural selection in Ipomopsis hybrid zones: implications for ecological speciation. New Phytol. 161:83-90.
10. Campbell, D., and L. Bernatchez. 2004. Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol. Biol. Evol. 21:945-956.
11. Campbell, D. R., N. M. Waser, G. Aldridge, and C. A. Wu. 2008. Lifetime fitness in two generations of ipomopsis hybrids. Evolution 62:2616-2627.
12. Catchen, J., A. Amores, P. A. Hohenlohe, W. A. Cresko, and J. H. Postlethwait. 2011. Stacks: building and genotyping loci de novo from short-read sequences. G3 1:171-182.
13. Catchen, J., P. A. Hohenlohe, S. Bassham, A. Amores, and W. A. Cresko. 2013. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22:3124-3140.
14. Chase, V. C., and P. H. Raven. 1975. Evolutionary and evological relationships between Aquilegia formosa and Aquilegia pubescens (Ranunculaceae), 2 perennial plants. Evolution 29:474-486.
15. Chen, G. F. 2013. Sexual isolation in two bee-pollinated Costus (Costaceae). Plant Reprod. 26:3-16.
16. Coyne, J. A., and H. A. Orr. 1989. Patterns of speciation in Drosophila. Evolution 43:362-381.
17. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates, Sunderland, MA.
18. Cruickshank, T. E., and M. W. Hahn. 2014. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 23:3133-3157.
19. Dobzhansky, T. 1937. Genetics and the origin of species. Columbia Univ. Press, New York.
20. Dobzhansky, T. 1970. Genetics of the evolutionary process. Columbia Univ. Press, New York.
21. Durrett, R., L. Buttel, and R. Harrison. 2000. Spatial models for hybrid zones. Heredity 84:9-19.
22. Earl, D. A., and B. M. von Holdt. 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4:359-361.
23. Egan, S. P., P. Nosil, and D. J. Funk. 2008. Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62:1162-1181.
24. Elith, J., S. J. Phillips, T. Hastie, M. Dudík, Y. E. Chee, and C. J. Yates. 2011. A statistical explanation of MaxEnt for ecologists. Divers. Distrib. 17:43-57.
25. Etter, P. D., J. L. Preston, S. Bassham, W. A. Cresko, and E. A. Johnson. 2011. Local de novo assembly of RAD paired-end contigs using short sequencing reads. PLoS ONE 6:e18561.
26. Evanno, G., S. Regnaut, and J. Goudet. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14:2611-2620.
27. Excoffier, L., G. Laval, and S. Schneider. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. 1:47-50.
28. Feder, J. L., X. F. Xie, J. Rull, S. Velez, A. Forbes, B. Leung, H. Dambroski, K. E. Filchak, and M. Aluja. 2005. Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis. Proc. Natl. Acad. Sci. USA 102:6573-6580.
29. Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35:124-138.
30. Fishman, L., and A. Saunders. 2008. Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322:1559-1562.
31. Fishman, L., and J. H. Willis. 2001. Evidence for Dobzhansky-Muller incompatibilities contributing to the sterility of hybrids between Mimulus guttatus and M. nasutus. Evolution 55:1932-1942.
32. Fishman, L., A. J. Kelly, E. Morgan, and J. H. Willis. 2001. A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159:1701-1716.
33. Fishman, L., A. Stathos, P. M. Beardsley, C. F. Williams, and J. P. Hill. 2013. Chromosomal rearrangements and the genetics of reprodictive barriers in Mimulus (monkeyflowers). Evolution 69:2547-2560.
34. Fulton, M., and S. A. Hodges. 1999. Floral isolation between Aquilegia formosa and Aquilegia pubescens. Proc. R. Soc. Lond. B Biol. Sci. 266:2247-2252.
35. Glennon, K. L., L. J. Rissler, and S. A. Church. 2012. Ecogeographic isolation: a reproductive barrier between species and between cytotypes in Houstonia (Rubiaceae). Evol. Ecol. 26:909-926.
36. Grant, V. 1949. Pollination systems as isolating mechanisms in angiosperms. Evolution 3:82-97.
37. Grant V. 1981. Plant speciation. Columbia Univ. Press, New York.
38. Grant, V. 1993a. Effect of hybridization and selection on floral isolation. Proc. Natl. Acad. Sci. USA 90:990-993.
39. Grant, V. 1993b. Origin of floral isolation between ornithophilous and sphingophilous plant species. Proc. Natl. Acad. Sci. USA 90:7729-7733.
40. Grant, V. 1994. Modes and origins of mechanical and ethological isolation in angiosperms. Proc. Natl. Acad. Sci. USA 91:3-10.
41. Hendry, A. P. 2009. Ecological speciation! Or the lack thereof? Can. J. Fish. Aquat. Sci. 66:1383-1398.
42. Hendry, A. P., D. I. Bolnick, D. Berner, and C. L. Peichel. 2009. Along the speciation continuum in sticklebacks. J. Fish Biol. 75:2000-2036.
43. Heslop-Harrison, J., and Y. Heslop-Harrison. 1970. Evaluation of pollen viability by enzymatically induced fluorescence: intracellular hydrolysis of fluorescein diacetate. Stain Technol. 45:115-120.
44. Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, and A. Jarvis. 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25:1965-1978.
45. Hodges, S. A., and M. L. Arnold. 1994a. Columbines-a geographically widespread species flock. Proc. Natl. Acad. Sci. USA 91:5129-5132.
46. Hodges, S. A., and M. L. Arnold 1994b. Floral and ecological isolation between Aquilegia formosa and Aquilegia pubescens. Proc. Natl. Acad. Sci. USA 91:2493-2496.
47. Hodges, S. A., M. Fulton, J. Y. Yang, and J. B. Whittall. 2004. Verne Grant and evolutionary studies of Aquilegia. New Phytol. 161:113-120.
48. Hohenlohe, P. A., S. Bassham, P. D. Etter, N. Stiffler, E. A. Johnson, and W. A. Cresko. 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6:e1000862.
49. Hohenlohe, P. A., S. Bassham, M. Currey, and W. A. Cresko. 2012. Extensive linkage disequilibrium and parallel adaptive divergence across threespine stickleback genomes. Philos. Trans. R. Soc. B Biol. Sci. 367:395-408.
50. Hopkins, R., and M. D. Rausher. 2012. Pollinator-mediated selection on flower color allele drives reinforcement. Science 335:1090-1092.
51. Howard, D. J. 1999. Conspecific sperm and pollen precedence and speciation. Annu. Rev. Ecol. Syst. 30:109-132.
52. Husband, B. C., and H. A. Sabara. 2004. Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium. New Phytol. 161:713-713.
53. Jakobsson, M., and N. A. Rosenberg. 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801-1806.
54. Jiggins, C. D., M. Linares, R. E. Naisbit, C. Salazar, Z. H. Yang, and J. Mallet. 2001. Sex-linked hybrid sterility in a butterfly. Evolution 55:1631-1638.
55. Kay, K. M. 2006. Reproductive isolation between two closely related hummingbird-pollinated Neotropical gingers. Evolution 60:538-552.
56. Kay, K. M., and R. D. Sargent. 2009. The role of animal pollination in plant speciation: integrating ecology, geography, and genetics. Annu. Rev. Ecol. Evol. Syst. 40:637-656.
57. Kirkpatrick, M., and V. Ravigne. 2002. Speciation by natural and sexual selection: models and experiments. Am. Nat. 159:S22-S35.
58. Lewinton, R. C., and J. Krakauer. 1973. Distribution of gene frequency as a test of theory of selective neutrality of polymorphisms. Genetics 74:175-195.
59. Lowry, D. B. 2012. Ecotypes and the controversy over stages in the formation of new species. Biol. J. Linn. Soc. 106:241-257.
60. Lowry, D. B., J. L. Modliszewski, K. M. Wright, C. A. Wu, and J. H. Willis. 2008a. The strength and genetic basis of reproductive isolating barriers in flowering plants. Philos. Trans. R. Soc. B Biol. Sci. 363:3009-3021.
61. Lowry, D. B., R. C. Rockwood, and J. H. Willis. 2008b. Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution 62:2196-2214.
62. Mani, G. S., and B. C. Clarke. 1990. Mutational order: a major stochastic process in evolution. Proc. R. Soc. Lond. B Biol. Sci. 240:29-37.
63. Martin, N. H., and J. H. Willis. 2007. Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61:68-82.
64. Mayr, E. 1942. Systematics and the origin of species. Columbia Univ. Press, New York.
65. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, MA.
66. McKinnon, J. S., S. Mori, B. K. Blackman, L. David, D. M. Kingsley, L. Jamieson, J. Chou, and D. Schluter. 2004. Evidence for ecology's role in speciation. Nature 429:294-298.
67. McMinn, H. E. 1951. Studies in the genus Diplacus. Madrono 11:1-32.
68. Muller, H. J. 1939. Reversibility in evolution considered from the standpoint of genetics. Biol. Rev. 14:261-280.
69. Munz, P. A. 1973. A california flora and supplement. University of California Press, Los Angeles.
70. Nakazato, T., D. L. Warren, and L. C. Moyle. 2010. Ecological and geographic modes of species divergence in wild tomatoes. Am. J. Bot. 97:680-693.
71. Nosil, P. 2008. Speciation with gene flow could be common. Mol. Ecol. 17:2103-2106.
72. Nosil, P., and J. L. Feder. 2012. Genomic divergence during speciation: causes and consequences Introduction. Philos. Trans. R. Soc. B Biol. Sci. 367:332-342.
73. Nosil, P., S. R. Egan, and D. J. Funk. 2008. Heterogeneous genomic differentiation between walking-stick ecotypes: "Isolation by adaptation" and multiple roles for divergent selection. Evolution 62:316-336.
74. Nosil, P., L. J. Harmon, and O. Seehausen. 2009. Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 24:145-156.
75. Orr, H. A., and M. Turelli. 2001. The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55:1085-1094.
76. Phadnis, N., and H. A. Orr. 2009. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323:376-379.
77. Phillips, S. J., R. P. Anderson, and R. E. Schapire. 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190:231-259.
78. Presgraves, D. C. 2007. Speciation genetics: epistasis, conflict and the origin of species. Curr. Biol. 17:R125-R127.
79. Price, T. D., and M. M. Bouvier. 2002. The evolution of F-1 postzygotic incompatibilities in birds. Evolution 56:2083-2089.
80. Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
81. Ramsey, J., H. D. Bradshaw, and D. W. Schemske. 2003. Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520-1534.
82. Rasband, W. S. 2013. ImageJ. U.S. National Institutes of Health, Bethesda, MA.
83. Rice, W. R., and E. E. Hostert. 1993. Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47:1637-1653.
84. Rundle, H. D., and P. Nosil. 2005. Ecological speciation. Ecol. Lett. 8:336-352.
85. Sambatti, J. B. M., and K. J. Rice. 2006. Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution 60:696-710.
86. Schemske, D. W. 2000. Understanding the origin of species. Evolution 54:1069-1073.
87. Schluter, D. 2001. Ecology and the origin of species. Trends Ecol. Evol. 16:372-380.
88. Schluter, D. 2009. Evidence for ecological speciation and its alternative. Science 323:737-741.
89. Seehausen, O., R. K. Butlin, I. Keller, C. E. Wagner, J. W. Boughman, P. A. Hohenlohe, C. L. Peichel, G.-P. Saetre, C. Bank, A. Braennstroem, et al. 2014. Genomics and the origin of species. Nat. Rev. Genet. 15:176-192.
90. Simpson, G. G. 1944. Tempo and mode in evolution. Columbia Univ. Press, New York.
91. Sobel, J. M. 2014. Ecogeographic isolation and speciation in the genus Mimulus. Am. Nat. 184:565-579.
92. Sobel, J. M., and G. F. Chen. 2014. Unification of methods for estimating the strength of reproductive isolation. Evolution 68:1511-1522.
93. Sobel, J. M., and M. A. Streisfeld. 2013. Flower color as a model system for studies of plant evo-devo. Front. Plant Sci. 4:321.
94. Sobel, J. M., G. F. Chen, L. R. Watt, and D. W. Schemske. 2010. The biology of speciation. Evolution 64:295-315.
95. Sokal, R. R., and F. J. Rohlf. 2011. Biometry, 4th ed. W. H. Freeman, San Francisco.
96. Stebbins, G. L. 1950. Variation and evolution in plants. Columbia Univ. Press, New York.
97. Strauss, S. Y., and J. B. Whittall. 2006. Non-pollinator agents of selection on floral traits. Pp. 120-138 in L. D. Harder, and S. C. H. Barrett, eds. Ecology and evolution of flowers. Oxford Univ. Press, Oxford, U.K.
98. Streisfeld, M. A., and J. R. Kohn. 2005. Contrasting patterns of floral and molecular variation across a cline in Mimulus aurantiacus. Evolution 59:2548-2559.
99. Streisfeld, M. A., and J. R. Kohn 2007. Environment and pollinator-mediated selection on parapatric floral races of Mimulus aurantiacus. J. Evol. Biol. 20:122-132.
100. Streisfeld, M. A., W. N. Young, and J. M. Sobel. 2013. Divergent selection drives genetic differentiation in an R2R3-Myb transcription factor that contributes to incipient speciation in Mimulus aurantiacus. PLoS Genet. 9:e1003385.
101. Sweigart, A. L., A. R. Mason, and J. H. Willis. 2007. Natural variation for a hybrid incompatibility between two species of Mimulus. Evolution 61:141-151.
102. Team, R. C. 2013. R: a language and environment for satistical computing. R Foundation for Statistical Computing, Vienna, Austria.
103. Tulig, M. 2000. Morphological variation in Mimulus section Diplacus (Scrophulariaceae). California State Polytechnic University, Pomona.
104. Turelli, M., N. H. Barton, and J. A. Coyne. 2001. Theory and speciation. Trends Ecol. Evol. 16:330-343.
105. Turner, T. L., M. W. Hahn, and S. V. Nuzhdin. 2005. Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 3:1572-1578.
106. Via, S. 2001. Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol. Evol. 16:381-390.
107. Via, S. 2009. Natural selection in action during speciation. Proc. Natl. Acad. Sci. USA 106:9939-9946.
108. Waayers, G. M. 1996. Hybridization, introgression, and selection in Mimulus aurantiacus ssp. australis and Mimulus puniceus. M.Sc. thesis. San Diego State University, San Diego, CA.