Repeated evolution of reproductive isolation in a marine snail: Unveiling mechanisms of speciation

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1547, 2010, Pages 1735-1747

  Johannesson, Kerstin ^a   Panova, Marina ^a   Kemppainen, Petri ^a   André, Carl ^a   Rolan Alvarez, Emilio ^b   Butlin, Roger K ^c  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF VIGO   (Spain)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Ecotype evolution; Evolution in concert; Incipient speciation; Littorina saxatilis; Parallel evolution; Selective sweep

Indexed keywords

ALLOPATRY; ECOTYPE; GENE FLOW; GENETIC VARIATION; HYBRID ZONE; INTROGRESSION; MARINE ECOSYSTEM; MICROHABITAT; MUTATION; NATURAL SELECTION; NUMERICAL MODEL; PARALLEL EVOLUTION; PHYLOGENETICS; POPULATION DISTRIBUTION; REPRODUCTIVE ISOLATION; SNAIL; SPECIES OCCURRENCE;

SPAIN; SWEDEN; UNITED KINGDOM;

GASTROPODA; LITTORINA SAXATILIS;

EID: 77953589377     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0256     Document Type: Conference Paper

References (83)

1. Andersen, O., Wetten, O. F., De Rosa, M. C., Andre, C., Alinovi, C. C., Colafranceschi, M., Brix, O. & Colosimo, A. 2009 Haemoglobin polymorphisms affect the oxygenbinding properties in Atlantic cod populations. Proc. R. Soc. B 276, 833-841. (doi:10.1098/rspb.2008.1529)
2. Arendt, J. & Reznick, D. 2007 Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23, 26-32. (doi:10.1016/j.tree.2007.09.011)
3. Barrett, R. D. H. & Schlüter, D. 2007 Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38-44. (doi:10.1016/j.tree.2007.09. 008)
4. Bolnick, D. I. & Fitzpatrick, B. M. 2007 Sympatric speciation: models and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 38, 459-487. (doi:10.1146/annurev.ecolsys.38.091206.095804)
5. Butlin, R. K., Galindo, J. & Grahame, J. 2008 Sympatric, parapatric or allopatric: the most important way to classify speciation? Phil. Trans. R. Soc. B 363, 2997-3007. (doi:10.1098/rstb.2008.0076)
6. Carballo, M., Garcia, C. & Rolán-Alvarez, E. 2001 Heritability of shell traits in wild Littorina saxatilis populations: results across a hybrid zone. J. Shell Res. 20, 415-422.
7. Chakraborty, R. & Nei, M. 1977 Bottleneck effects on average heterozygosity and genetic distance with the step-wise mutation model. Evolution 31, 347-356. (doi:10.2307/2407757)
8. Colosimo, P. F. et al. 2005 Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307, 1928-1933. (doi:10.1126/science.1107239)
9. Conde-Padin, P., Carvajal-Rodríguez, A., Carballo, M., Caballero, A. & Rolán-Alvarez, E. 2007 Genetic variation for shell traits in a direct-developing marine snail involved in a putative sympatric ecological speciation process. Evol. Ecol. 21, 635-650. (doi:10.1007/s10682-006-9142-8)
10. Conde-Padín, P., Cruz, R., Hollander, J. & Rolán-Alvarez, E. 2008 Revealing the mechanism of sexual isolation in a case of sympatric and parallel ecological divergence. Biol. J. Linn. Soc. 94, 513-526. (doi:10.1111/j.1095-8312.2008.00998.x)
11. Conde-Padín, P., Caballero, A. & Rolán-Alvarez, E. 2009 Relative role of genetic determination and plastic response during ontogeny for shell-shape traits subjected to diversifying selection. Evolution 63, 1356-1363. (doi:10.1111/j.1558-5646.2009.00636.x)
12. Coyne, J. A. & Orr, H. A. 2004 Speciation. Sunderland, MA: Sinauer Associates.
13. Cruz, R. & Garcia, C. 2001 Disruptive selection on female reproductive characters in a hybrid zone of Littorina saxatilis. Evol. Ecol. 15, 167-182. (doi:10.1023/A:1014878523629)
14. Cruz, R., Carballo, M., Conde-Padin, P. & Rolán-Alvarez, E. 2004 Testing alternative models for sexual isolation in natural populations of Littorina saxatilis: indirect support for by-product ecological speciation? J. Evol. Biol. 17, 288-293. (doi:10.1111/j.1420-9101.2003.00689.x)
15. Denny, M. W. 2000 Are there mechanical limits to size in wave-swept organisms? J. Exp. Biol. 202, 3463-3467.
16. Ellegren, H. & Sheldon, B. C. 2008 Genetic basis of fitness differences in natural populations. Nature 452, 169-175. (doi:10.1038/ nature06737)
17. Erlandsson, J., Rolán-Alvarez, E. & Johannesson, K. 1998 Migratory differences between ecotypes of the snail Littorina saxatilis on Galician rocky shores. Evol. Ecol. 12, 913-924. (doi:10.1023/A:1006559904596)
18. Erlandsson, J., Kostylev, V. & Rolán-Alvarez, E. 1999 Mate search and aggregation behaviour in the Galician hybrid zone of Littorina saxatilis. J. Evol. Biol. 12, 891-896. (doi:10.1046/j.1420-9101.1999.00087.x)
19. Feder, J. L., Roethele, F. B., Filchak, K., Niedbalski, J. & Romero-Severson, J. 2003 Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly Rhagoletis pomonella. Genetics 163, 939-953.
20. Fitzpatrick, B. M., Fordyce, J. A. & Gavrilets, S. 2008 What, if anything, is sympatric speciation? J. Evol. Biol. 21, 1452-1459. (doi:10.1111/j.1420-9101.2008.01611.x)
21. Fitzpatrick, B. M., Fordyce, J. A. & Gavrilets, S. 2009 Patterns, processes and geographic modes of speciation. J. Evol. Biol. 22, 2342-2347. (doi:10.1111/j.1420-9101.2009.01833.x)
22. Futuyama, D. J. & Mayer, G. C. 1980 Non-allopatric speciation in mammals. Syst Zool. 29, 254-271.
23. Galindo, J., Morán, P. & Rolán-Alvarez, E. 2009 Comparing geographical genetic differentiation between candidate and noncandidate loci for adaptation strengthens support for parallel ecological divergence in the marine snail Littorina saxatilis. Mol. Ecol. 18, 919-930. (doi:10.1111/j.1365-294X.2008.04076.x)
24. Gavrilets, S. 2004 Fitness landscapes and the origin of species. Princeton, NJ: Princeton University Press.
25. Grahame, J., Wilding, C. S. & Butlin, R. K. 2006 Adaptation to a steep environmental gradient and an associated barrier to gene exchange in Littorina saxatilis. Evolution 60, 268-278.
26. Hollander, J., Lindegarth, M. & Johannesson, K. 2005 Local adaptation but not geographic separation promotes assortative mating in a snail-support for ecological speciation. Anim. Behav. 70, 1209-1219. (doi:10.1016/j.anbehav. 2005.03.014)
27. Hollander, J., Collyer, M. L., Adams, D. C. & Johannesson, K. 2006 Phenotypic plasticity in two marine snails: constraints superseding life-history. J. Evol. Biol. 19, 1861-1872. (doi:10.1111/j.1420-9101.2006.01171. x)
28. Hull, S. L. 1998 Assortative mating between two morphs of Littorina saxatilis on a shore in Yorkshire. Hydrobiologia 378, 79-88. (doi:10.1023/A:1003237521419)
29. Hull, S. L., Grahame, J. & Mill, P. J. 1996 Morphological divergence and evidence for reproductive isolation in Littorina saxatilis (Olivi) in northeast England. J. Moll. Stud. 62, 89-99. (doi:10.1093/mollus/62.1.89)
30. Janson, K. 1982 Genetic and environmental effects on the growth rate of Littorina saxatilis Olivi. Mar. Biol. 69, 73-78. (doi:10.1007/BF00396963)
31. Janson, K. 1983 Selection and migration in two distinct phenotypes of Littorina saxatilis in Sweden. Oecologia 59, 58-61. (doi:10.1007/BF00388072)
32. Janson, K. 1985 Variation in the occurrence of abnormal embryos in females of the intertidal gastropod Littorina saxatilis Olivi. J. Moll. Stud. 51, 64-68.
33. Janson, K. 1987a Genetic drift in small and recently founded populations of the marine snail Littorina saxatilis. Heredity 58, 31-37. (doi:10.1038/hdy.1987.5)
34. Janson, K. 19876 Allozyme and shell variation in two marine snails (Littorina, Prosobranchia) with different dispersal abilities. Biol. J. Linn. Soc. 30, 245-256. (doi:10.1111/j.1095-8312.1987.tb00299.x)
35. Johannesson, K. 1988 The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? Mar. Biol. 99, 507-513. (doi:10.1007/BF00392558)
36. Johannesson, K. 2001 Parallel speciation: a key to sympatric divergence. Trends Ecol. Evol. 16, 148-153. (doi:10.1016/S0169-5347(00)02078-4)
37. Johannesson, K. 2009 Inverting the null-hypothesis of speciation: a marine snail perspective. Evol. Ecol. 23, 5-16. (doi:10.1007/s10682-007-9225-1)
38. Johannesson, K. & Johannesson, B. 1995 Dispersal and population expansion in a direct developing marine snail (Littorina saxatilis) following a severe population bottleneck. Hydrobiologia 309, 173-180. (doi:10.1007/ BF00014485)
39. Johannesson, B. & Johannesson, K. 1996 Population differences in behaviour and morphology in Littorina saxatilis: Phenotypic plasticity or genetic differentiation? J. Zool. 240, 475-493. (doi:10.1111/j.1469-7998.1996. tb05299.x)
40. Johannesson, K. & Tatarenkov, A. 1997 Allozyme variation in a snail (Littorina saxatilis)-deconfounding the effects of microhabitat and gene flow. Evolution 51, 402-409. (doi:10.2307/2411112)
41. Johannesson, K., Johannesson, B. & Rolán-Alvarez, E. 1993 Morphological differentiation and genetic cohesiveness over a microenvironmental gradient in the marine snail Littorina saxatilis. Evolution 47, 1770-1787. (doi:10.2307/2410220)
42. Johannesson, K., Rolán-Alvarez, E. & Ekendahl, A. 1995a Incipient reproductive isolation between two sympatric morphs of the intertidal snail Littorina saxatilis. Evolution 49, 1180-1190. (doi:10.2307/2410443)
43. Johannesson, K., Rolán-Alvarez, E. & Erlandsson, J. 1997 Growth rate differences between upper and lower shore ecotypes of the marine snail Littorina saxatilis (Olivi) (Gastropoda). Biol. J. Linn. Soc. 61, 267-279.
44. Johannesson, K., Larsson, A., Cruz, R., Garcia, C. & RolánAlvarez, E. 2000 Hybrid fitness seems not to be an explanation for the partial reproductive isolation between ecotypes of Galician Littorina saxatilis. J. Moll. Stud. 66, 149-156. (doi:10.1093/mollus/66.2.149)
45. Johannesson, K., Havenhand, J. N., Jonsson, P. R., Lindegarth, M., Sundin, A. & Hollander, J. 2008 Male discrimination of female mucous trails permits assortative mating in a marine snail species. Evolution 62, 3178-3184. (doi:10.1111/j.1558-5646.2008.00510.x)
46. Kemppainen, P., Nes, S., Ceder, C. & Johannesson, K. 2005 Refuge function of marine algae complicates selection in an intertidal snail. Oecologia 143, 402-411. (doi:10.1007/s00442-004-1819-5)
47. Mäkinen, T., Panova, M. & Andre, C. 2007 High levels of multiple paternity in Littorina saxatilis: hedging the bets? J. Hered. 98, 705-711. (doi:10.1093/jhered/esm097)
48. Mäkinen, T., Panova, M., Johannesson, K., Tatarenkov, A., Appelqvist, C. & André, C. 2008 Genetic differentiation on multiple spatial scales in an ecotype-forming marine snail with limited dispersal: Littorina saxatilis. Biol. J. Linn. Soc. 94, 31-40. (doi:10.1111/j.1095-8312. 2008.00960.x)
49. Mallet, J., Meyer, A., Nosil, P. & Feder, J. L. 2009 Space, sympatry and speciation. J. Evol. Biol. 22, 2332-2341. (doi:10.1111/j.1420-9101.2009. 01816.x)
50. Merilä, J. & Crnokrak, P. 2001 Comparison of genetic differentiation at marker loci and quantitative traits. J. Evol. Biol. 14, 892-903. (doi:10.1046/j.1420-9101.2001.00348.x)
51. Morjan, C. L. & Rieseberg, L. H. 2004 How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles. Mol. Ecol. 13, 1341-1356. (doi:10.1111/j.1365-294X.2004. 02164.x)
52. Nei, M., Maruyama, T. & Chakraborty, R. 1975 The bottleneck effect and genetic variability in populations. Evolution 29, 1-10. (doi:10.2307/ 2407137)
53. Nikula, R., Strelkov, P. & Väinölä, R. 2008 A broad transition zone between an inner Baltic hybrid swarm and a pure North Sea subspecies of Macoma balthica (Mollusca, Bivalvia). Mol. Ecol. 17, 1506-1522. (doi:10.1111/j.1365-294X.2007.03688.x)
54. Nosil, P., Harmon, L. J. & Seehausen, O. 2009 Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 24, 145-156. (doi:10.1016/j.tree.2008.10.011)
55. Panova, M., Hollander, J. & Johannesson, K. 2006 Sitespecific genetic divergence in parallel hybrid zones suggests non-allopatric evolution of reproductive barriers. Mol. Ecol. 15, 4021-4031. (doi:10.1111/j.1365-294X.2006. 03067.x)
56. Pickles, A. & Grahame, J. 1999 Mate choice in divergent morphs of Littorina saxatilis (Olivi); speciation in action? Anim. Behav. 58, 181-184. (doi:10.1006/anbe.1999.1115)
57. Quesada, H., Posada, D., Caballero, A., Morán, P. & RolánAlvarez, E. 2007 Phylogenetic evidence for multiple sympatric ecological diversification in a marine snail. Evolution 61, 1600-1612. (doi:10.1111/j.1558-5646.2007.00135.x)
58. Raffaelli, D. G. & Hughes, R. N. 1978 The effects of crevice size and availability on populations of Littorina rudis and Littorina neritoides. J. Anim. Ecol. 47, 71-83. (doi:10.2307/3923)
59. Ranz, J. M. & Machado, C. A. 2006 Uncovering evolutionary patterns of gene expression using microarrays. Trends Ecol. Evol. 21, 29-37. (doi:10.1016/j.tree.2005.09.002)
60. Reid, D. 1996 Systematics and evolution of Littorina. London, UK: Ray Society.
61. Rice, W. R. & Hostert, E. E. 1993 Laboratory experiments on speciation-what have we learned in 40 years. Evolution 47, 1637-1653. (doi:10.2307/2410209)
62. Rieseberg, L. H. & Burke, J. M. 2001 The biological reality of species: gene flow, selection, and collective evolution. Taxon 50, 47-67. (doi:10.2307/1224511)
63. Riginos, C. & Cunningham, C. W. 2005 Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol. Ecol. 14, 381-400. (doi:10.1111/j.1365-294X.2004.02379.x)
64. Riginos, C. & Cunningham, C. W. 2007 Hybridization in postglacial marine habitats. Mol. Ecol. 16, 3971-3972. (doi:10.1111/j.1365-294X.2007.03505. x)
65. Rogers, S. M. & Bernatchez, L. 2005 Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake white-fish (Coregonus clupeaformis). Mol. Ecol. 14, 351-361. (doi:10.1111/j.1365-294X.2004.02396.x)
66. Rolán-Alvarez, E., Rolán, E. & Johannesson, K. 1996 Differentiation in radular and embryonic characters, and further comments on gene flow, between two sympatric morphs of Littorina saxatilis (Olivi). Ophelia 45, 1-15.
67. Rolán-Alvarez, E., Johannesson, K. & Erlandsson, J. 1997 The maintenance of a cline in the marine snail Littorina saxatilis: the role of home site advantage and hybrid fitness. Evolution 51, 1838-1847. (doi:10.2307/2411006)
68. Rolán-Alvarez, E., Erlandsson, J., Johannesson, K. & Cruz, R. 1999 Mechanisms of incomplete prezygotic reproductive isolation in an intertidal snail; testing behavioural models in wild populations. J. Evol. Biol. 12, 879-890. (doi:10.1046/j.1420-9101.1999.00086.x)
69. Rolán-Alvarez, E., Carballo, M., Galindo, J., Moran, P., Fernández, B., Caballero, A., Cruz, R., Boulding, E. G. & Johannesson, K. 2004 Nonallopatric and parallel origin of local reproductive barriers between two snail ecotypes. Mol. Ecol. 13, 3415-3424. (doi:10.1111/j.1365-294X.2004.02330.x)
70. Sadedin, S., Hollander, J., Panova, M., Johannesson, K. & Gavrilets, S. 2009 Case studies and mathematical models of ecological speciation 3. Ecotype formation in a Swedish snail. Mol. Ecol. 18, 4006-4023. (doi:10.1111/j.1365- 294X.2009.04320.x)
71. Saur, M. 1990 Mate discrimination in Littorina littorea (L.) and L. saxatilis (Olivi) (Mollusca: Prosobranchia). Hydrobiologia 193, 261-270. (doi:10.1007/BF00028082)
72. Shiu, S. H. & Borevitz, J. O. 2008 The next generation of microarray research: applications in evolutionary and ecological genomics. Heredity 100, 141-149. (doi:10.1038/sj.hdy.6800916)
73. Schluter, D. & Nagel, L. M. 1995 Parallel speciation by natural selection. Am. Nat. 146, 292-301. (doi:10.1086/285799)
74. Schluter, D. 2009 Evidence for ecological speciation and its alternative. Science 323, 737-741. (doi:10.1126/science.1160006)
75. Schluter, D., Clifford, E. A., Nemethy, M. & McKinnon, J. S. 2004 Parallel evolution and inheritance of quantitative traits. Am. Nat. 163, 809-822. (doi:10.1086/383621)
76. Seehausen, O. et al. 2008 Speciation through sensory drive in cichlid fish. Nature 455, 620-627. (doi:10.1038/nature07285)
77. Smadja, C., Galindo, J. & Butlin, R. K. 2008 Hitching a lift on the road to speciation. Mol. Ecol. 17, 4177-4180. (doi:10.1111/j.1365-294X.2008. 03917.x)
78. Stinchcombe, J. R. & Hoekstra, H. E. 2008 Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100, 158-170. (doi:10.1038/sj.hdy.6800937)
79. Strasburg, J. L. & Rieseberg, L. H. 2008 Molecular demographic history of the annual sunflowers Helianthus annuus and H. petiolaris-large effective population sizes and rates of long-term gene flow. Evolution 62, 1936-1950. (doi:10.1111/j.1558-5646.2008.00415.x)
80. Sundberg, P. 1988 Microgeographic variation in shell characters of Littorina saxatilis Olivi-a question mainly of size. Biol. J. Linn. Soc. 35, 169-184. (doi:10.1111/j.1095-8312.1988.tb00464.x)
81. Via, S. & West, J. 2008 The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol. Ecol. 17, 4334-4345. (doi:10.1111/j.1365-294X.2008.03921.x)
82. Wilding, C. S., Butlin, R. K. & Grahame, J. 2001 Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. J. Evol. Biol. 14, 611-619. (doi:10.1046/j.1420-9101.2001.00304.x)
83. Wood, T. E., Burke, J. M. & Rieseberg, L. H. 2005 Parallel genotypic adaptation: when evolution repeats itself. Genetica 123, 157-170. (doi:10.1007/s10709-003-2738-9)