Functional similarity and molecular divergence of a novel reproductive transcriptome in two male-pregnant Syngnathus pipefish species

Ecology and Evolution

Volumn 3, Issue 12, 2013, Pages 4092-4108

  Small, Clayton M ^a,b   Harlin Cognato, April D ^c   Jones, Adam G ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF OREGON   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Male pregnancy; Molecular evolution; Pyrosequencing; RNA seq; Syngnathidae; Transcriptome

Indexed keywords

ANIMALIA; PISCES; SYNGNATHIDAE; SYNGNATHUS; SYNGNATHUS FLORIDAE; SYNGNATHUS SCOVELLI;

EID: 84887924771     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.763     Document Type: Article

References (85)

1. Aagaard, J. E., S. A. Springer, S. D. Soelberg, and W. J. Swanson. 2013. Duplicate abalone egg coat proteins bind sperm lysine similarly, but evolve oppositely, consistent with molecular mimicry at fertilization. PLoS Genet. 9:e1003287.
2. Altenoff, A. M., and C. Dessimov. 2009. Phylogenetic and functional assessment of orthologs inference projects and methods. PloS Comp. Biol. 5:e1000262.
3. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
4. Arnqvist, G. and L. Rowe. 2005. Sexual conflict. Princeton University Press, Princeton, NJ.
5. Artieri, C. G., W. Haerty, B. P. Gupta, and R. S. Singh. 2008. Sexual selection and maintenance of sex: evidence from comparisons of rates of genomic accumulation of mutations and divergence of sex-related genes in sexual and hermaphroditic species of Caenorhabditis. Mol. Biol. Evol. 25:972-979.
6. Benjamini, Y. and Y. Hochberg. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B-Methodol. 57:289-300.
7. Birkhead, T. R. and T. Pizzari. 2002. Postcopulatory sexual selection. Nat. Rev. Genet. 3:262-273.
8. Blanca, J. M., L. Pascual, P. Ziarsolo, F. Nuez, and J. Canizares. 2011. ngs_backbone: a pipeline for read cleaning, mapping and SNP calling using next generation sequence. BMC Genomics 12:285.
9. Brandley, M. C., R. L. Young, D. L. Warren, M. B. Thompson, and G. P. Wagner. 2012. Uterine gene expression in the live-bearing lizard, Chalcides ocellatus, reveals convergence of squamate reptile and mammalian pregnancy mechanisms. Genome Biol. Evol. 4:394-411.
10. Camacho, C., G. Coulouris, V. Avagyan, N. Ma, J. Papadopoulos, K. Bealer, et al. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421.
11. Chapman, T., L. F. Liddle, J. M. Kalb, M. F. Wolfner, and L. Partridge. 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory-gland products. Nature 373:241-244.
12. Chapman, T., G. Arnqvist, J. Bangham, and L. Rowe. 2003. Sexual conflict. Trends Ecol. Evol. 18:41-47.
13. Chuong, E. B., W. F. Tong, and H. E. Hoekstra. 2010. Maternal-fetal conflict: rapidly evolving proteins in the rodent placenta. Mol. Biol. Evol. 27:1221-1225.
14. Clark, N. L., J. E. Aagaard, and W. J. Swanson. 2006. Evolution of reproductive proteins from animals to plants. Reproduction 131:11-22.
15. Claw, K. G. and W. J. Swanson. 2012. Evolution of the egg:new findings and challenges. Annu. Rev. Genomics Hum. Genet. 13:109-125.
16. Clutton-Brock, T. H. 1991. The evolution of parental care. Princeton University Press, Princeton, NJ.
17. Coppe, A., C. Agostini, I. A. Marino, L. Zane, L. Bargelloni, S. Bortoluzzi, et al. 2013. Genome evolution in the cold:antarctic icefish muscle transcriptome reveals selective duplications increasing mitochondrial function. Genome Biol. Evol. 5:45-60.
18. Dawson, C. E. 1985. Indo-Pacific pipefishes. Gulf Coast Research Laboratories, Ocean Springs, MS.
19. Dodd, R. B. and K. Drickamer. 2001. Lectin-like proteins in model organisms: implications for evolution of carbohydrate-binding activity. Glycobiology 11:71R-79R.
20. Duret, L. and D. Mouchiroud. 2000. Determinates of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17:68-74.
21. Elmer, K. R., S. Fan, H. M. Gunter, J. C. Jones, S. Boekhoff, S. Kuraku, et al. 2010. Rapid evolution and selection inferred from the transcriptomes of sympatric crater lake cichlid fishes. Mol. Ecol. 19(Suppl. 1):197-211.
22. Francis, W. R., L. M. Christianson, R. Kiko, M. L. Powers, N. C. Shaner, and S. H. D. Haddock. 2013. A comparison across non-model animals suggests an optimal sequencing depth for de novo transcriptome assembly. BMC Genomics 14:167.
23. Fricke, C., S. Wigby, R. Hobbs, and T. Chapman. 2009. The benefits of male ejaculate sex peptide transfer in Drosophila melanogaster. J. Evol. Biol. 22:275-286.
24. Galindo, B. E., V. D. Vacquier, and W. J. Swanson. 2003. Positive selection in the egg receptor for abalone sperm lysin. Proc. Natl Acad. Sci. USA 100:4639-4643.
25. Ghadessy, F. J., D. Chen, R. M. Kini, M. C. Chung, K. Jeyaseelan, H. E. Koo, et al. 1996. Stonustoxin is a novel lethal factor from stonefish (Synanceia horrida) venom:cloning and characterization. J. Biol. Chem. 271:25575-25581.
26. Good, J. M. and N. W. Nachman. 2005. Rates of protein evolution are positively correlated with developmental timing of expression during mouse spermatogenesis. Mol. Biol. Evol. 22:1044-1052.
27. Gotz, S., J. M. Garcia-Gomez, J. Terol, T. D. Williams, S. H. Nagaraj, M. J. Nueda, et al. 2008. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 36:3420-3435.
28. Gross, M. R. 2005. The evolution of parental care. Q. Rev. Biol. 80:37-45.
29. Haase, D., O. Roth, M. Kalbe, G. Schmiedeskamp, J. P. Scharsack, P. Rosenstiel, et al. 2013. Absence of major histocompatibility complex class II mediated immunity in pipefish, Syngnathus typhle: evidence from deep transcriptome sequencing. Biol. Lett. 9:20130044.
30. Harlin-Cognato, A., E. A. Hoffman, and A. G. Jones. 2006. Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish. Proc. Natl Acad. Sci. USA 103:19407-19412.
31. Herald, E. S. 1959. From pipefishes to seahorse -A study of phylogenetic relationships. Proc. Natl Acad. Sci. USA 29:465-473.
32. Jones, A. G. and J. C. Avise. 1997a. Microsatellite analysis of maternity and the mating system in the Gulf pipefish, a species with male pregnancy and sex-role reversal. Mol. Ecol. 6:203-213.
33. Jones, A. G. and J. C. Avise. 1997b. Polygynandry in the dusky pipefish Syngnathus floridae revealed by microsatellite DNA markers. Evolution 51:1611-1622.
34. Jones, A. G., D. Walker, and J. C. Avise. 2001. Genetic evidence for extreme polyandry and extraordinary sex-role reversal in a pipefish. Proc. Roy. Soc. Lond. B 268:2531-2535.
35. Kvarnemo, C., K. B. Mobley, C. Partridge, A. G. Jones, and I. Ahnesj̈o. 2011. Evidence of paternal nutrient provisioning to embryos in broad-nosed pipefish Syngnathus typhle. J. Fish Biol. 78:1725-1737.
36. Lee, Y.-H. and V. D. Vacquier. 1992. The divergence of species-specific abalone sperm lysins is promoted by positive Darwinian selection. Biol. Bull. 182:97-104.
37. Lee, C. G., C. A. Da Silva, C. S. De La Cruz, F. Ahangari, B. Ma, M. J. Kang, et al. 2011. Role of chitin and chitinase-like proteins in inflammation, tissue remodeling, and injury. Annu. Rev. Physiol. 73:479-501.
38. Looso, M., J. Preussner, K. Sousounis, M. Bruckskotten, C. S. Michael, E. Lignelli, et al. 2013. A de novo assembly of the newt transcriptome combined with proteomic validation identifies new protein families expressed during tissue regeneration. Genome Biol. 14:R16.
39. Melamed, P., Y. Xue, J. F. Poon, Q. Wu, H. Xie, J. Yeo, et al. 2005. The male seahorse synthesizes and secretes a novel C-type lectin into the brood pouch during early pregnancy. FEBS J. 272:1221-1235.
40. Metz, E. C. and S. R. Palumbi. 1996. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Bio. Evol. 13:397-406.
41. Mobley, K. B. and A. G. Jones. 2007. Geographical variation in the mating system of the dusky pipefish (Syngnathus floridae). Mol. Ecol. 16:2596-2606.
42. Mobley, K. B. and A. G. Jones. 2009. Environmental, demographic, and genetic mating system variation among five geographically distinct dusky pipefish (Syngnathus floridae) populations. Mol. Ecol. 18:1476-1490.
43. Mobley, K. B., C. Kvarnemo, I. Ahnesjo, C. Partridge, A. Berglund, and A. G. Jones. 2011. The effect of maternal body size on embryo survivorship in the broods of pregnant male pipefish. Behav. Ecol. Sociobiol. 65:1169-1177.
44. Moffett, A. and C. Loke. 2006. Immunology of placentation in eutherian mammals. Nat. Rev. Immunol. 6:584-594.
45. Nam, B.-H., K. J. Ahn, Y.-O. Kim, H. J. Kong, W.-J. Kim, H. S. Kim, et al. 2010. Molecular cloning and characterization of LPS-binding protein/bactericidal permeability-increasing protein (LBP/BPI) from olive flounder, Paralichthys olivaceus. Vet. Immunol. and Immunopath. 133:256-263.
46. Nielsen, R. and Z. H. Yang. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929-936.
47. O'Neill, M. J., B. R. Lawton, M. Mateos, D. M. Carone, G. C. Ferreri, T. Hrbek, et al. 2007. Ancient and continuing Darwinian selection on insulin-like growth factor II in placental fishes. Proc. Natl Acad. Sci. USA 104:12404-12409.
48. Paczolt, K. and A. G. Jones. 2010. Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy. Nature 464:401-404.
49. Palumbi, S. R. 1994. Genetic divergence, reproductive isolation, and marine speciation. Annu. Rev. Ecol. Syst. 25:547-572.
50. Parker, G. A. 1979. Sexual selection and sexual conflict. Pp. 123-166 in M. S. Blum, N. A. Blum, eds. Sexual selection and reproductive competition in insects, Academic, New York.
51. Partridge, C., A. Boettcher, and A. G. Jones. 2010. Short-term exposure to a synthetic estrogen disrupts mating dynamics in a pipefish. Horm. Behav. 58:800-807.
52. Renaut, S., A. W. Nolte, and L. Bernatchez. 2010. Mining transcriptome sequences towards identifying adaptive single nucleotide polymorphisms in lake whitefish species pairs (Coregonus spp. Salmonidae). Mol. Ecol. 19(Suppl. 1):115-131.
53. Ripley, J. L. 2009. Osmoregulatory role of the paternal brood pouch for two Syngnathus species. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 154:98-104.
54. Ripley, J. L. and C. M. Foran. 2006. Differential parental nutrient allocation in two congeneric pipefish species (Syngnathidae: Syngnathus spp.). J. Exp. Biol. 209:1112-1121.
55. Ripley, J. L. and C. M. Foran. 2009. Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.). J. Comp. Physiol. B. 179:325-333.
56. Rivera, M. C., R. Jain, J. E. Moore, and J. A. Lake. 1998. Genomic evidence for two functionally distinct gene classes. Proc. Natl Acad. Sci. USA 95:6239-6244.
57. Rokyta, D. R., K. P. Wray, A. R. Lemmon, E. M. Lemmon, and S. B. Caudle. 2011. A high-throughput venom-gland transcriptome for the Eastern Diamondback Rattlesnake (Crotalus adamanteus) and evidence for pervasive positive selection across toxin classes. Toxicon 57:657-671.
58. Sagebakken, G., I. Ahnesjö, K. B. Mobley, I. Braga Gonçalves, and C. Kvarnemo. 2010. Brooding fathers, not siblings, take up nutrients from embryos. Proc. Roy. Soc. Lond. B 277:971-977.
59. Shields, D. C., P. M. Sharp, D. G. Higgins, and F. Wright. 1988. "Silent" sites in Drosophila genes are not neutral:evidence of strong selection among synonymous codons. Mol. Biol. Evol. 5:704-716.
60. Sokal, R. R. and F. J. Rohlf. 1994. Biometry. W. H. Freeman and Co., New York, NY.
61. Swanson, W. J. and V. D. Vacquier. 2002a. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3:137-144.
62. Swanson, W. J. and V. D. Vacquier. 2002b. Reproductive protein evolution. Ann. Rev. Ecol. Syst. 33:161-179.
63. Swanson, W. J., Z. H. Zhang, M. F. Wolfner, and C. F. Aquadro. 2001a. Positive Darwinian selection drives the evolution of several reproductive proteins in mammals. Proc. Natl Acad. Sci. USA 98:2509-2514.
64. Swanson, W. J., A. G. Clark, H. M. Waldrip-Dali, M. F. Wolfner, and C. F. Aquadro. 2001b. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proc. Natl Acad. Sci. USA 98:7375-7379.
65. Swanson, W. J., A. Wong, M. F. Wolfner, and C. F. Aquadro. 2004. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics 168:1457-1465.
66. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: 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.
67. Torgerson, D. G., R. J. Kulathinal, and R. S. Singh. 2002. Mammalian sperm proteins are rapidly evolving: evidence of positive selection in functionally diverse genes. Mol. Biol. Evol. 19:1973-1980.
68. Trivers, R. L. 1972. Parental investment and sexual selection. Pp. 136-179 in B. Campbell ed. Sexual selection and the descent of man, Aldine, Chicago.
69. Turner, L. M. and H. E. Hoekstra. 2006. Adaptive evolution of fertilization proteins within a genus: variation in ZP2 and ZP3 in deer mice (Peromyscus). Mol. Biol. Evol. 23:1656-1669.
70. Turner, L. M. and H. E. Hoekstra. 2008. Causes and consequences of the evolution of reproductive proteins. Int. J. Dev. Biol. 52:769-780.
71. Ueda, A., M. Suzuki, T. Honma, H. Nagai, Y. Nagashima, and K. Shiomi. 2006. Purification, properties, and cDNA cloning of neoverrucotoxin (neoVTX), a hemolytic lethal factor from the stonefish Synanceia verrucosa venom. Biochim. Biophys. Acta 1760:1713-1722.
72. Walters, J. R. and R. G. Harrison. 2010. Combined EST and proteomic analysis identifies rapidly evolving seminal fluid proteins in Heliconius butterflies. Mol. Biol. Evol. 27:2000-2013.
73. Wang, L. K., Z. X. Feng, X. Wang, X. W. Wang, and X. G. Zhang. 2010. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136-138.
74. Wang, Y., N. Ghaffari, C. D. Johnson, U. M. Braga-Neto, H. Wang, R. Chen, et al. 2011. Evaluation of the coverage and depth of transcriptome by RNA-seq in chickens. BMC Bioinformatics 12:S5.
75. Wilson, A. B. and J. W. Orr. 2011. The evolutionary origins of Syngnathidae: pipefishes and seahorses. J. Fish Biol. 78:1603-1623.
76. Wilson, N. G. and G. W. Rouse. 2010. Convergent camouflage and the non-monophyly of 'seadragons' (Syngnathidae:Teleostei): suggestions for a revised taxonomy of syngnathids. Zoolog. Scr. 39:551-558.
77. Wilson, A. B., A. Vincent, I. Ahnesj̈o, and A. Meyer. 2001. Male pregnancy in seahorses and pipefishes (Family Syngnathidae):rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny. J. Hered. 92:159-166.
78. Wilson, A. B., I. Ahnesj̈o, A. Vincent, and A. Meyer. 2003. The dynamics of male brooding, mating patterns, and sex roles in pipefishes and seahorses (family Syngnathidae). Evolution 57:1374-1386.
79. Wyckoff, G. J., W. Wang, and C. I. Wu. 2000. Rapid evolution of male reproductive genes in the descent of man. Nature 403:304-309.
80. Yang, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13:555-556.
81. Yang, Z. and J. P. Bielawski. 2000. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15:496-503.
82. Yang, R. and X. Wang. 2013. Organ evolution in angiosperms driven by correlated divergences of gene sequences and expression patterns. Plant Cell 25:71-82.
83. Zhang, L. and W. H. Li. 2004. Mammalian housekeeping genes evolve more slowly than tissue-specific genes. Mol. Biol. Evol. 21:236-239.
84. Zhang, N., B. Xu, C. Mou, W. Yang, J. Wei, L. Lu, et al. 2003. Molecular profile of the unique species of traditional Chinese medicine, Chinese seahorse (Hippocampus kuda Bleeker). FEBS Lett. 550:124-134.
85. Zhang, J., R. Nielsen, and Z. Yang. 2005. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22:2472-2479.