Adaptive evolution of M3 Lysin-A candidate gamete recognition protein in the mytilus edulis species complex

Molecular Biology and Evolution

Volumn 30, Issue 12, 2013, Pages 2688-2698

  Lima, Thiago G ^a,b   McCartney, Michael A ^a  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

adaptive evolution; gamete recognition; lysin; Mytilus; speciation; sperm protein

Indexed keywords

BINDING PROTEIN; GAMETE RECOGNITION PROTEIN; LECTIN; LIGAND; M3 LYSIN; M7 LYSIN; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CODON; GAMETE; HYBRIDIZATION; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOLECULAR MODEL; MOLECULAR RECOGNITION; MUSSEL; MYTILUS EDULIS; MYTILUS GALLOPROVINCIALIS; MYTILUS TROSSULUS; NONHUMAN; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADAPTIVE EVOLUTION; GAMETE RECOGNITION; LYSIN; MYTILUS; SPECIATION; SPERM PROTEIN;

ALLELES; ANIMALS; CANADA; CLONING, MOLECULAR; EVOLUTION, MOLECULAR; GENETIC SPECIATION; GENETIC VARIATION; MALE; MODELS, MOLECULAR; MUCOPROTEINS; MYTILUS EDULIS; POLYMORPHISM, GENETIC; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SELECTION, GENETIC; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECIES SPECIFICITY; SPERMATOZOA;

EID: 84890367487     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mst165     Document Type: Article

References (72)

1. Bandelt HJ, Forster P, Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 16:37-48.
2. Biermann CH. 1998. The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). Mol Biol Evol. 15:1761-1771.
3. Cameron RA, Minor JE, Nishioka D, Britten RJ, Davidson EH. 1990. Locale and level of bindin mRNA in maturing testis of the sea urchin, Strongylocentrotus purpuratus. Dev Biol. 142:44-49.
4. Clark NL, Findlay GD, Yi X, MacCoss MJ, SwansonWJ. 2007. Duplication and selection on abalone sperm lysin in an allopatric population. Mol Biol Evol. 24:2081-2090.
5. Clark NL, Gasper J, Sekino M, Springer SA, Aquadro CF, Swanson WJ. 2009. Coevolution of interacting fertilization proteins. PLoS Genet. 5: e1000570.
6. Cummings RD, McEver RP. 2009. C-type lectins. In: Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME, editors. Essentials of glycobiology. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press. p. 439-458.
7. Drickamer K, Taylor ME. 1993. Biology of animal lectins. Annu Rev Cell Biol. 9:237-264.
8. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. 1994. DNA primers fro amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 3: 294-299.
9. Frohman MA. 1994. On beyond classic RACE (rapid amplification of cDNA ends). Genome Res. 4:S40-S58.
10. Fu Y-X, Li W-H. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
11. Gosling EM. 1992. Genetics of Mytilus. In: Gosling EM, editor. The mussel Mytilus: ecology, physiology, genetics and culture. Amsterdam: Elsevier. p. 309-382.
12. Heß AK, Bartel M, Roth K, Messerschmidt K, Heilmann K, Kenchington E, Micheel B, Stuckas H. 2012. Expression of M6 and M7 lysin in Mytilus edulis is not restricted to sperm, but occurs also in oocytes and somatic tissue of males and females. Mol Reprod Dev. 79: 517-524.
13. Haino-Fukushima K. 1974. Studies on the egg-membrane lysin of Tegula pfeifferi the reaction mechanism of the egg-membrane lysin. Biochim Biophys Acta. 352:179-191.
14. Hellberg ME, Dennis AB, Arbour-Riley P, Aagaard JE, Swanson WJ. 2012. The Tegula tango: a coevolutionary dance of interacting, positively selected sperm and egg proteins. Evolution 66:1681-1694.
15. Hellberg ME, Vacquier VD. 1999. Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol Biol Evol. 16:839-848.
16. Hudson RR, Kaplan NL. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164.
17. Hudson RR, Kreitman M, Aguadé M. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159.
18. Kamei N, Glabe CG. 2003. The species-specific egg receptor for sea urchin sperm adhesion is EBR1, a novel ADAMTS protein. Genes Dev. 17:2502-2507.
19. Kijewski T, Śmietanka B, Zbawicka M, Gosling E, Hummel H, Wenne R. 2011. Distribution of Mytilus taxa in European coastal areas as inferred from molecular markers. J Sea Res. 65:224-234.
20. Kreitman M, Akashi H. 1995. Molecular evidence for natural selection. Annu Rev Ecol Syst. 26:403-422.
21. Lee YH, Ota T, Vacquier VD. 1995. Positive selection is a general phenomenon in the evolution of abalone sperm lysin. Mol Biol Evol. 12: 231-238.
22. Lessios H, Pearse J. 1996. Hybridization and introgression between Indo-Pacific species of Diadema. Mar Biol. 126:715-723.
23. Lewis CA, Talbot CF, Vacquier VD. 1982. A protein from abalone Haliotis rufescens sperm dissolves the egg vitelline layer by a nonenzymatic mechanism. Dev Biol. 92:227-239.
24. Librado P, Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
25. McCartney MA, Lessios HA. 2002. Quantitative analysis of gametic incompatibility between closely related species of neotropical sea urchins. Biol Bull. 202:166-181.
26. McCartney MA, Lessios HA. 2004. Adaptive evolution of sperm bindin tracks egg incompatibility in neotropical sea urchins of the genus Echinometra. Mol Biol Evol. 21:732-745.
27. McCartneyMA, Lima TG. 2011. Evolutionary consequences of introgression at M7 Lysin, a gamete recognition locus, following secondary contact between blue mussel species. Integr Comp Biol. 51:474-484.
28. McDonald J, Kreitman M. 1991. Adaptive protein evolution at adh locus in Drosophila. Nature 351:652-654.
29. Metz EC, Palumbi SR. 1996. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol Biol Evol. 13:397-406.
30. Metz EC, Robles-Sikisaka R, Vacquier VD. 1998. Nonsynonymous substitution in abalone sperm fertilization gene exceeds substitution in introns and mitochondrial DNA. Proc Natl Acad Sci USA. 95: 10676-10681.
31. NeiM. 1987. Molecular evolutionary genetics. New York (NY): Columbia University Press.
32. Nei M, Miller JC. 1990. A simple method for estimating average number of nucleotide substitutions within and between populations from restriction data. Genetics 125:873-879.
33. Nishioka D, Ward RD, Poccia D, Kostacos C, Minor JE. 1990. Localization of bindin expression during sea urchin spermatogenesis. Mol Reprod Dev. 27:181-190.
34. Owen B, McLean JH, Meyer RJ. 1971. Hybridization in the eastern Pacific abalones (Haliotis). Sci Bull Nat Hist Mus Los Ang. 9:1-37.
35. Palumbi SR. 1998. Species formation and the evolution of gamete recognition loci. In: Howard D-J, Berlocher SH, editors. Endless forms: species and speciation. New York (NY): Oxford University Press. p. 271-278.
36. Palumbi SR, Metz EC. 1991. Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol Biol Evol. 8: 227-239.
37. Polzin T, Daneshmand SV. 2003. On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett. 31:12-20.
38. Rawson PD, Harper F. 2009. Colonization of the northwest Atlantic by the blue mussel, Mytilus trossulus postdates the last glacial maximum. Mar Biol. 156:1857-1868.
39. Rawson PD, Hilbish TJ. 1995. Evolutionary relationships among the male and female mitochondrial DNA lineages in the Mytilus edulis species complex. Mol Biol Evol. 12:893-901.
40. Rawson PD, Hilbish TJ. 1998. Asymmetric introgression of mitochondrial DNA among European populations of blue mussels (Mytilus spp.). Evolution 52:100-108.
41. Rawson PD, Slaughter C, Yund PO. 2003. Patterns of gamete incompatibility between the blue mussels Mytilus edulis and M. trossulus. Mar Biol. 143:317-325.
42. Riginos C, Cunningham CW. 2005. Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol Ecol. 14:381-400.
43. Riginos C, Henzler CM. 2008. Patterns of mtDNA diversity in North Atlantic populations of the mussel Mytilus edulis. Mar Biol. 155: 399-412.
44. Riginos C,McDonald JH. 2003. Positive selection on an acrosomal sperm protein, M7 lysin, in three species of the mussel genus Mytilus. Mol Biol Evol. 20:200-207.
45. Riginos C, Wang D, Abrams AJ. 2006. Geographic variation and positive selection on M7 lysin, an acrosomal sperm protein in mussels (Mytilus spp.). Mol Biol Evol. 23:1952-1965.
46. Rost B, Sander C. 1993. Prediction of protein secondary structure at better than 70% accuracy. J Mol Biol. 232:584-599.
47. Slaughter C, McCartney MA, Yund PO. 2008. A comparison of gamete compatibility between species in allopatric and sympatric populations of blue mussels. Biol Bull. 214:57-66.
48. Springer SA, Crespi BJ.2007. Adaptive gamete-recognition divergence in a hybridizing Mytilus population. Evolution.61.772-783.
49. Swanson WJ, Vacquier VD. 1997. The abalone egg vitelline envelope receptor for sperm lysin is a giant multivalent molecule. Proc Natl Acad Sci USA. 94:6724-6729.
50. Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nat Rev Genet. 3:137-144.
51. Swofford DL. 2003. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods)Version 4. Sunderland (MA): Sinauer Associates.
52. Tajima F. 1983. Evolutionary relationship of DNA sequences in finitepopulations. Genetics 105:437-460.
53. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
54. Takagi T, Nakamura A, Deguchi R, Kyozuka KI. 1994. Isolation, characterization, and primary structure of three major proteins obtained from Mytilus edulis sperm. J Biochem. 116:598-605.
55. Taylor ME, Drickamer K. 2006. Introduction to glycobiology. Oxford: Oxford University Press.
56. Thompson JD, HigginsDG, Gibson TJ. 1994. Clustalw: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
57. Vacquier VD. 1998. Evolution of gamete recognition proteins. Science 281:1995-1998.
58. Vacquier VD, Carner KR, Stout CD. 1990. Species-specific sequences of abalone lysin, the sperm protein that creates a hole in the egg envelope. Proc Natl Acad Sci USA. 87:5792-5796.
59. Vacquier VD, Swanson WJ. 2011. Selection in the rapid evolution of gamete recognition proteins in marine invertebrates. Cold Spring Harb Perspect Biol. 3:a002931.
60. Venier P, Pallavicini A, De Nardi B, Lanfranchi G. 2003. Towards a catalogue of genes transcribed in multiple tissues of Mytilus galloprovincialis. Gene 314:29-40.
61. Walker JR, Nagar B, Young NM, Hirama T, Rini JM. 2004. X-ray crystal structure of a galactose-specific C-type lectin possesing a novel decameric quaternary structure. Biochemistry 43:3783-3792.
62. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 7: 256-276.
63. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
64. Yang Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol. 15: 568-573.
65. Yang Z. 2007. PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol. 24:1586-1591.
66. Yang Z, Nielsen R. 1998. Synonomous and nonsynonomous rate variation in nuclear genes of mammals. J Mol Evol. 46: 409-418.
67. Yang Z, Nielsen R. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol. 19:908-917.
68. Yang Z, Swanson WJ, Vacquier VD. 2000. Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites. Mol Biol Evol. 17: 1446-1455.
69. Yang Z, Wong WS, Nielsen R. 2005. Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol. 22: 1107-1118.
70. Zhai W, Nielsen R, Slatkin M. 2009. An investigation of the statistical power of neutrality tests based on comparative and population genetic data. Mol Biol Evol. 26:273-283.
71. Zhang J, Nielsen R, Yang Z. 2005. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol. 22:2472-2479.
72. Zigler K, Lessios HA. 2003. Evolution of bindin in the pantropical sea urchin Tripneustes: comparisons to bindin of other genera. Mol Biol Evol. 20:220-231.