The evolutionary mechanism maintaining shell shape and molecular differentiation between two ecotypes of the dogwhelk Nucella lapillus

Evolutionary Ecology

Volumn 23, Issue 2, 2009, Pages 261-280

  Guerra Varela, Jorge ^a   Colson, Isabelle ^b,c   Backeljau, Thierry ^d   Breugelmans, K ^d   Hughes, Roger N ^b   Rolán Alvarez, Emilio ^a  

^a UNIVERSITY OF VIGO   (Spain)

^b BANGOR UNIVERSITY   (United Kingdom)

^c NORTHUMBRIA UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Adaptation; Divergent selection; Heritability; Hybrid zone; Molecular variation; Phenotypic plasticity; Quantitative traits

Indexed keywords

ADAPTATION; ALLOPATRY; DIVERGENCE; ECOTYPE; EVOLUTION; GENETIC DIFFERENTIATION; GENETIC STRUCTURE; HERITABILITY; MORPHOMETRY; PHENOTYPIC PLASTICITY; ROCKY SHORE; SHAPE; SHELL; SIZE; SNAIL; SYMPATRY; WAVE ACTION;

EURASIA; EUROPE; SOUTHERN EUROPE; SPAIN;

NUCELLA LAPILLUS;

EID: 60449090347     PISSN: 02697653     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10682-007-9221-5     Document Type: Article

References (80)

1. DC Adams FJ Rohlf DE Slice 2004 Geometric morphometrics: ten years of progress following the 'revolution' Ital J Zool 71 5 16
2. RD Appleton AR Palmer 1988 Water-borne stimuli released by predatory crabs and damaged prey induce more predator-resistant shells in a marine gastropod Proc Nat Acad Sci USA 85 4387 4391
3. CR Bantock CM Cockayne 1975 Chromosomal polymorphism in Nucella lapillus Heredity 34 231 245
4. CR Bantock CM Page 1976
5. MD Bertness SD Gaines 1993 Larval dispersal and local adaptation in acorn barnacles Evolution 47 316 320
6. Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University. Press, New York
7. EG Boulding TK Hay 1993 Quantitative genetics of shell form of an intertidal snail: constraints on short-term response to selection Evolution 47 576 592
8. EG Boulding M Holst V Pilon 1999 Changes in selection on gastropod shell size and thickness with wave exposure on Northern Pacific shores J Exp Mar Biol Ecol 232 217 239
9. M Carballo C García E Rolán-Alvarez 2001 Heritability of shell traits in wild Littorina saxatilis populations: results across a hybrid zone J Shellfish Res 20 415 422
10. A Carvajal-Rodríguez MG Rodríguez 2005 MODICOS: morphometric and distance computation software oriented for evolutionary studies Online J Bioinformatics 6 34 41
11. A Carvajal-Rodriguez P Conde-Padín E Rolan-Alvarez 2005 Decomposing shell form into size and shape by geometric morphometric methods in two sympatric ecotypes of Littorina saxatilis J Molluscan Stud 71 313 318
12. MJ Cavalcanti LR Monteiro PRD Lopes 1999 Landmark-based morphometric analysis in selected species of serranid fishes (Perciformes: Teleostei) Zoological Studies 38 287 294
13. M-P Chapuis A Estoup 2007 Microsatellite null alleles and estimation of population differentiation Mol Biol Evol 24 621 631
14. M Clement D Posada KA Crandall 2000 TCS: a computer program to estimate gene genealogies Mol Ecol 9 1657 1660
15. I Colson RN Hughes 2004 Rapid recovery of genetic diversity of dogwhelk (Nucella lapillus) populations after local extinction and recolonisation contradicts predictions from life-history characteristics Mol Ecol 13 2223 2233
16. I Colson J Guerra-Varela R Hughes E Rolán-Alvarez 2006 Using molecular and quantitative variation for assesing genetic impacts on Nucella lapillus populations after local extinction and recolonization Integr Zool 2 104 107
17. P Conde-Padín A Carvajal-Rodríguez M Carballo A Caballero E Rolán-Alvarez 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
18. JA Coyne 1992 Genetics and speciation Nature 355 511 515
19. Coyne JA, Orr HA (2004) Speciation. Sinauer associates, Inc. Massachusetts
20. JH Crothers 1975 On variation in Nucella lapillus (L.): shell shape in populations from the south coast of England Proc Malacological Soc Lond 41 489 498
21. JH Crothers 1985 Dog-whelks: an introduction to the biology of Nucella lapillus (L.) Field Stud 6 291 360
22. AJ Day 1990 Microgeographic variation in allozyme frequencies in relation to the degree of exposure to wave action in the dogwhelk Nucella lapillus (L.) (Prosobranchia: Muricacea) Biol J Linn Soc 40 245 261
23. DR Dixon PL Pascoe PE Gibbs JJ Pasantes 1999
24. RJ Etter 1996 The effect of wave action, prey type, and foraging time on growth of the predatory snail Nucella lapillus (L.) J Exp Mar Biol Ecol 196 341 356
25. L Excoffier P Smouse J Quattro 1992 Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data Genetics 131 479 491
26. D Falush M Stephens JK Pritchard 2003 Inference of population structure: extensions to linked loci and correlated frequencies Genetics 164 1567 1587
27. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman Group Ltd. Essex
28. O Folmer M Black W Hoeh R Lutz R Vrijenhoek 1994 DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates Mol Mar Biol Biotechnol 3 294 299
29. DJ Futuyma GC Mayer 1980 Non-allopatric speciation in animals Syst Zool 29 254 271
30. D Garant LEB Kruuk TA Wilkin RH McCleery BC Sheldon 2005 Evolution driven by differential dispersal within a wild bird population Nature 433 60 65
31. PE Gibbs 1993 Phenotypic changes in the progeny of Nucella lapillus (Gastropoda) transplanted from an exposed shore to sheltered inlets J Molluscan Stud 59 187 194
32. TA Hall 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symposium Series 41 95 98
33. DJ Hawthorne S Via 2001 Genetic linkage of ecological specialization and reproductive isolation in pea aphids Nature 412 904 907
34. RD Holt R Gomulkiewicz 1996 How does immigration influence local adaptation? A reexamination of a familiar paradigm Am Nat 149 563 572
35. B Johannesson K Johannesson 1996 Population differences in behaviour and morphology in the snail Littorina saxatilis: phenotypic plasticity or genetic differentiation? J Zool Lond 240 475 493
36. K Kawai RN Hughes O Takenaka 2001 Isolation and characterization of microsatellite loci in the marine gastropod Nucella lapillus Mol Ecol Notes 1 270 272
37. JG Kingsolver DW Pfennig MR Servedio 2002 Migration, local adaptation and the evolution of plasticity Trends Ecol Evol 17 540 541
38. RR Kirby 1997 Variation in Mitochondrial DNA in a cline of allele frequencies and shell phenotype in the dog-whelk Nucella lapillus (L.) Biol J Linn Soc 62 299 312
39. RR Kirby 2000 An ancient transpecific polymorphism shows extreme divergence in a multitrait cline in an intertidal snail (Nucella lapillus (L.)) Mol Biol Evol 17 1816 1825
40. JA Kitching L Muntz FJ Ebling 1966 The ecology of Lough Ine. XV. The ecological significance of shell and body forms in Nucella J Anim Ecol 35 113 126
41. TD Kocher WK Thomas A Meyer SV Edwards S Pääbo FX Villablanca AC Wilson 1989 Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers Proc Nat Acad Sci USA 86 6196 6200
42. LEB Kruuk J Merilä BC Sheldon 2003 When environmental variation short-circuits natural selection Trends Ecol Evol 18 207 209
43. V Le Corre A Kremer 2003 Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection Genetics 164 1205 1219
44. M Lynch ME Pfrender K Spitze 1999 The quantitative and molecular genetic architecture of a subdivided species Evolution 53 100 110
45. JK McKay RG Latta 2002 Adaptive population divergence: markers, QTL and traits Trends Ecol Evol 17 285 291
46. J Merilä P Cronokrack 2001 Comparison of genetic differentiation at marker loci and quantitative traits J Evol Biol 14 892 903
47. TJS Merrit L Shi MC Chase MA Rex RJ Etter JM Quattro 1998 Universal cytochrome b primers facilitate intraspecific studies in Molluscan taxa Mol Mar Biol Biotechnol 7 7 11
48. S Mopper M Beck D Simberloff P Stiling 1995 Local adaptation and agents of selection in a mobile insect Evolution 49 810 815
49. AR Palmer 1990 Effect of crab effluent and scent of damaged conspecific on feeding, growth and shell morphology of the Atlantic dogwhelk Nucella lapillus (L.) Hydrobiologia 193 155 182
50. PL Pascoe 2006 Chromosomal polymorphism in the Atlantic dog-whelk, Nucella lapillus (Gastropoda: Muricidae): nomenclature, variation and biogeography Biol J Linn Soc 87 195 210
51. PR Peres-Neto JD Olden 2001 Assessing the robustness of randomization tests: examples from behavioural studies Anim Behav 61 79 86
52. E Postma AJ Van Noordwijk 2005 Gene flow maintains a large genetic difference in clutch size at a small spatial scale Nature 433 65 68
53. JK Pritchard M Stephens P Donnelly 2000 Inference of population structure using multilocus genotype data Genetics 155 945 959
54. JAM Raeymaekers JKJ Van Houdt MHD Larmuseau S Geldof FAM Volckaert 2007 Divergent selection as revealed by PST and QTL-based FST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient Mol Ecol 16 891 905
55. M Raymond F Rousset 1995 GENEPOP (version 1.2): population genetics software for exact test and ecumenism J Hered 86 248 249
56. Reid DG (1996) Systematics and evolution in littorina. The Ray Society, Dorchester
57. Ridley M (1996) Evolution. Blackwell Science, Cambridge
58. Rohlf FJ (1993) Relative warp analysis and an example of its application to mosquito wings. In: Marcus LF, Garcia-Valdecasas AE (eds) Contributions to Morphometrics, Museo Nacional de Ciencias Naturales (CSIC), vol. 8. Madrid, pp 131-159
59. FJ Rohlf 1998 On applications of geometric morphometrics to studies of ontogeny and phylogeny Syst Biol 47 147 158
60. FJ Rohlf FL Bookstein 2003 Computing the uniform component of shape variation Syst Biol 52 66 69
61. FJ Rohlf A Loy M Corti 1996 Morphometric analysis of old world talpidae (Mammalia, Insectivora) using partial-warp scores Syst Biol 5 344 362
62. FJ Rohlf D Slice 1990 Extensions of the Procrustes method for the optimal superimposition of landmarks Syst Zool 39 40 59
63. Rolán E (1983) Molluscs of the Ria of Vigo: I Gastropods. Universidad de Santiago de Compostela, 383 pp (in Spanish)
64. E Rolán J Guerra-Varela I Colson RN Hughes E Rolán-Alvarez 2004 Morphological and genetic analysis of two sympatric morphs of the dogwhelk Nucella lapillus (Mollusca, Neogastropoda) from Galicia (NW Spain) J Molluscan Stud 70 179 185
65. E Rolán-Alvarez 2007 Sympatric speciation as a by-product of ecological adaptation in the Galician Littorina saxatilis hybrid zone J Moll Stud 73 1 10
66. E Rolán-Alvarez M Carballo J Galindo P Morán B Fernández A Caballero R Cruz EG Boulding K Johannesson 2004 Nonallopatric and parallel origin of local reproductive barriers between two snail ecotypes Mol Ecol 13 3415 3424
67. E Rolán-Alvarez K Johannesson J Erlandsson 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
68. J Rozas JC Sánchez-DelBarrio X Messeguer R Rozas 2003 DnaSP, DNA polymorphism analyses by the coalescent and other methods Bioinformatics 19 2496 2497
69. Sokal RR, Rohlf FJ (1995) Biometry. W.H. Freeman and Company, New York
70. C Simon F Frati A Beckenbach B Crespi H Liu P Flook 1994 Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers Ann Entomol Soc Am 87 651 701
71. K Spitze 1993 Population structure in Daphnia obtusa: quantitative genetic and allozymic variation Genetics 135 367 374
72. JW Struhsaker 1968 Selection mechanisms associated with intraspecific shell variation in Littorina picta Evolution 22 459 480
73. GC Trussell 1997 Phenotypic selection in an intertidal snail: effects of a catastrophic storm Ma Ecol Prog Ser 151 73 79
74. GC Trussell RJ Etter 2001 Integrating genetic and environmental forces that shape the evolution of geographic variation in a marine snail Genetica 112-113 321 337
75. AJ Underwood 1981 Techniques of analysis of variance in experimental marine biology and ecology Oceanogr Mar Biol Ann Rev 19 513 605
76. S Via 1993 Adaptative phenotypic plasticity: target or by-product of selection in a variable environment? Am Nat 142 352 522
77. S Via R Gomulkiewicz G De Jong SM Scheiner CD Schlichting PH Van Tienderen 1995 Adaptive phenotypic plasticity: consensus and controversy Trends Ecol Evol 10 212 217
78. BS Weir CC Cockerham 1984 Estimating F-statistics for the analysis of population structure Evolution 38 1358 1370
79. S Wright 1951 The genetic structure of populations Ann Eugen 15 323 354
80. Zelditch ML, Swiderski DL, Sheets HD, Fink WL (2004) Geometric morphometrics for biologists. A primer. Elsevier Academic Press