Functional genomics of physiological plasticity and local adaptation in killifish

Journal of Heredity

Volumn 102, Issue 5, 2011, Pages 499-511

  Whitehead, Andrew ^a   Galvez, Fernando ^a   Zhang, Shujun ^a   Williams, Larissa M ^b   Oleksiak, Marjorie F ^c  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MIAMI   (United States)

Author keywords

AFLPs; comparative transcriptomics; Fundulus heteroclitus; gene expression; microarrays; natural populations; phenotypic plasticity

Indexed keywords

AQUAPORIN 3; CREATINE KINASE; HISTONE; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTOME;

ADAPTIVE BEHAVIOR; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; BODY WEIGHT; CELL CYCLE REGULATION; COMPARATIVE STUDY; CONFERENCE PAPER; CONVERGENT EVOLUTION; CYPRINODONTIFORMES; ENZYME ACTIVITY; EVOLUTIONARY ADAPTATION; FISH; FUNCTIONAL GENOMICS; FUNDULUS HETEROCLITUS; GENE EXPRESSION; GENE FREQUENCY; GENE REGULATORY NETWORK; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HYPOOSMOTIC STRESS; LOCAL ADAPTATION; NATURAL POPULATION; NONHUMAN; OSMOTIC STRESS; PHENOTYPIC PLASTICITY; PHENOTYPIC VARIATION; POLLUTION; PRIORITY JOURNAL; STRESS; TRANSCRIPTION REGULATION;

ACCLIMATIZATION; ANIMALS; CLUSTER ANALYSIS; FUNDULIDAE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE-ENVIRONMENT INTERACTION; GENETIC VARIATION; GENOMICS; HOMEOSTASIS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; WATER POLLUTION;

CYPRINODONTOIDEI; FUNDULUS; FUNDULUS HETEROCLITUS;

EID: 80052060253     PISSN: 00221503     EISSN: 14657333     Source Type: Journal    
DOI: 10.1093/jhered/esq077     Document Type: Conference Paper

References (72)

1. Beaumont M, Nichols R. 1996. Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond. 263:1619-1626. (Pubitemid 27055553)
2. Bergen BJ, Rahn K, Nelson WG. 1998. Remediation at a marine Superfund site: surficial sediment PCB congener concentration, composition and redistribution. Environ Sci Technol. 32:3496-3501. (Pubitemid 28527740)
3. Bieri R, Hein C, Huggett R, Shou P, Slone H. 1986. Polycyclic aromatic hydrocarbons in surface sediments from the Elizabeth River subestuary. Int J Environ Anal Chem. 26:97-113.
4. Black D, Gutjahr-Gobell R, Pruell R, Bergen B, Mills L, McElroy A. 1998. Reproduction and polychlorinated biphenyls in Fundulus heteroclitus (Linnaeus) from New Bedford Harbor, Massachusetts. Environ Toxicol Chem. 17:1405-1414. (Pubitemid 28275267)
5. Bozinovic G, Oleksiak MF. 2010. Embryonic gene expression among pollutant resistant and sensitive Fundulus heteroclitus populations. Aquat Toxicol. 98:221-229.
6. Brugarolas J, Lei K, Hurley RL, Manning BD, Reiling JH, Hafen E, et al. 2004. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 18(23): 2893-2904. (Pubitemid 39602308)
7. Burnett KG, Bain LJ, Baldwin WS, Callard GV, Cohen S, Di Giulio RT, et al. 2007. Fundulus as the premier teleost model in environmental biology: opportunities for new insights using genomics. Comp Biochem Physiol Part D Genomics Proteomics. 2:257-286. (Pubitemid 350020840)
8. Childs AC, Mehta DJ, Gerner EW. 2003. Polyamine-dependent gene expression. Cell Mol Life Sci. 60(7):1394-1406. (Pubitemid 36900522)
9. Clutton-Brock TH, Albon SD, Guinness FE. 1984. Maternal dominance, breeding success and birth sex ratios in red deer. Nature. 308:358-360. (Pubitemid 15273625)
10. Conrad PW, Rust RT, Han J, Millhorn DE, Beitner-Johnson D. 1999. Selective activation of p38a and p38c by hypoxia. J Biol Chem. 274(33):23570-23576.
11. Cutler CP, Martinez AS, Cramb G. 2007. The role of aquaporin 3 in teleost fish. Comp Biochem Physiol A Mol Integr Physiol. 148(1):82-91. (Pubitemid 47077655)
12. de Hoon MJ, Imoto S, Nolan J, Miyano S. 2004. Open source clustering software. Bioinformatics. 20(9):1453-1454. (Pubitemid 38931415)
13. Elskus AA, Monosson E, McElroy AE, Stegeman JJ, Woltering DS. 1999. Altered CYP1A expression in Fundulus heteroclitus adults and larvae: a sign of pollutant resistance? Aquatic Toxicol. 45(2-3):99-113.
14. Evans DH, Piermarini PM, Choe KP. 2005. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev. 85(1):97-177. (Pubitemid 40173994)
15. Evans RM. 1988. The steroid and thyroid-hormone receptor superfamily. Science. 240(4854):889-895.
16. Evans TG, Somero GN. 2008. A microarray-based transcriptomic timecourse of hyper- and hypo-osmotic stress signaling events in the euryhaline fish Gillichthys mirabilis: osmosensors to effectors. J Exp Biol. 211(22):3636-3649.
17. Fiol DF, Chan SY, Kultz D. 2006. Identification and pathway analysis of immediate hyperosmotic stress responsive molecular mechanisms in tilapia (Oreochromis mossambicus) gill. Comp Biochem Physiol D Genomics Proteomics. 1(3):344-356. (Pubitemid 44437819)
18. Fiol DF, Kultz D. 2005. Rapid hyperosmotic coinduction of two tilapia (Oreochromis mossambicus) transcription factors in gill cells. Proc Natl Acad Sci. U S A. 102(3):927-932. (Pubitemid 40282767)
19. Fiol DF, Kultz D. 2007. Osmotic stress sensing and signaling in fishes. Febs Journal. 274(22):5790-5798. (Pubitemid 350045792)
20. Fisher MA, Oleksiak MF. 2007. Convergence and divergence in gene expression among natural populations exposed to pollution. BMC Genomics. 8:108.
21. Griffith RW. 1974. Environment and salinity tolerance in the genus Fundulus. Copeia. 319-331.
22. Hochachka PW, Somero GN. 2002. Biochemical adaptation: mechanism and process in physiological evolution. New York: Oxford University Press.
23. Hoffmann EK, Schettino T, Marshall WS. 2007. The role of volumesensitive ion transport systems in regulation of epithelial transport. Comp Biochem Physiol A Mol Integr Physiol. 148(1):29-43. (Pubitemid 47077657)
24. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protocols. 4(1):44-57.
25. Huggett R, Van Veld P, Smith C, Hargis W, Vogelbein W. 1992. The effects of contaminated sediments in the Elizabeth River. Boca Raton (FL): Lewis Publishers. pp. 403-430
26. Hughes I, Saito M, Schlesinger PH, Ornitz DM. 2007. Otopetrin 1 activation by purinergic nucleotides regulates intracellular calcium. Proc Natl Acad Sci U S A. 104(29):12023-12028. (Pubitemid 47185623)
27. Iannuzzi TJ, Armstrong TN, Thelen JB, Ludwig DF, Firstenberg CE. 2005. Characterization of chemical contamination in shallow-water estuarine habitats of an industrialized river. Part 1: organic compounds. Soil Sediment Contamin. 14(1):13-33.
28. Kidder GW, Petersen CW, Preston RL. 2006. Energetics of osmoregulation: II. Water flux and osmoregulatory work in the euryhaline fish, Fundulus heteroclitus. J Exp Zool Part A Comp Exp Biol. 305A(4):318-327.
29. Kultz D, Burg M. 1998. Evolution of osmotic stress signaling via map kinase cascades. J Exp Biol. 201(22):3015-3021. (Pubitemid 29006745)
30. Kultz D, Chakravarty D, Adilakshmi T. 2001. A novel 14-3-3 gene is osmoregulated in gill epithelium of the euryhaline teleost Fundulus heteroclitus. J Exp Biol. 204(17):2975-2985. (Pubitemid 34861372)
31. Kultz D, Madhany S, Burg MB. 1998. Hyperosmolality causes growth arrest of murine kidney cells-induction of GADD45 and GADD153 by osmosensing via stress-activated protein kinase. J Biol Chem. 273(22):13645-13651. (Pubitemid 28268409)
32. Laurent P, Chevalier C, Wood CM. 2006. Appearance of cuboidal cells in relation to salinity in gills of Fundulus heteroclitus, a species exhibiting branchial Na but not Cl- uptake in freshwater. Cell Tissue Res. 325(3):481-492. (Pubitemid 44126163)
33. Liebermann D, Hoffman B. 2008. Gadd45 in stress signaling. J Mol Signal. 3(1):15.
34. Lopez-Bojorquez L, Villalobos P, Garcia-G C, Orozco A, Valverde-R C. 2007. Functional identification of an osmotic response element (ORE) in the promoter region of the killifish deiodinase 2 gene (FhDio2). J Exp Biol. 210(17):3126-3132. (Pubitemid 47522707)
35. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P. 2003. The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet. 4(12):981-994. (Pubitemid 37474645)
36. Marshall WS, Bryson SE, Luby T. 2000. Control of epithelial Cl- secretion by basolateral osmolality in the euryhaline teleost Fundulus heteroclitus. J Exp Biol. 203(12):1897-1905. (Pubitemid 30441793)
37. McCormick SD. 2001. Endocrine control of osmoregulation in teleost fish.Am Zool. 41(4):781-794. (Pubitemid 33770250)
38. Meyer J, Di Giulio R. 2002. Patterns of heritability of decreased EROD activity and resistance to PCB 126-induced teratogenesis in laboratory-reared offspring of killifish (Fundulus heteroclitus) from a creosote-contaminated site in the Elizabeth River, VA, USA. Mar Environ Res. 54(3-5):621-626. (Pubitemid 35286486)
39. Meyer J, Di Giulio R. 2003. Heritable adaptation and fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecol Appl. 13:490-503. (Pubitemid 36872854)
40. Nacci D, Champlin D, Coiro L, McKinney R, Jayaraman S. 2002. Predicting the occurrence of genetic adaptation to dioxin like compounds in populations of the estuarine fish Fundulus heteroclitus. Environ Toxicol Chem. 21:1525-1532. (Pubitemid 34694801)
41. Nacci D, Champlin D, Jayaraman S. 2010. Adaptation of the estuarine fish Fundulus heteroclitus (Atlantic Killifish) to polychlorinated biphenyls (PCBs). Estuaries and Coasts.
42. Nacci D, Coiro L, Champlin D, Jayaraman S, McKinney R, Gleason T, et al. 1999. Adaptation of wild fish populations to persistent environmental contaminants. Marine Biol. 134:9-18.
43. Oleksiak MF. 2008. Changes in gene expression due to chronic exposure to environmental pollutants. Aquat Toxicol. 90(3):161-171.
44. Oleksiak MF. 2010. Genomic approaches with natural fish populations. J Fish Biol. 76:1067-1093.
45. Oleksiak MF, Churchill GA, Crawford DL. 2002. Variation in gene expression within and among natural populations. Nat Genetics. 32(2):261-266.
46. Oleksiak MF, Roach JL, Crawford DL. 2005. Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus. Nat Genet. 37(1):67-72. (Pubitemid 40070941)
47. Ownby DR, Newman MC, Mulvey M, Vogelbein WK, Unger MA, Arzayus LF. 2002. Fish (Fundulus hereroclitus) populations with different exposure histories differ in tolerance of creosote-contaminated sediments. Environ Toxicol Chem. 21(9):1897-1902.
48. Padma T, Hale R, Roberts M. 1998. Toxicity of water-soluble fractions derived from whole creosote and creosote-contaminated sediments. Environ Toxicol Chem. 17:1606-1610. (Pubitemid 28372861)
49. Paschall JE, Oleksiak MF, VanWye JD, Roach JL, Whitehead JA, Wyckoff GJ, et al. 2004. FunnyBase: a systems level functional annotation of Fundulus ESTs for the analysis of gene expression. BMC Genomics. 5(1):96.
50. Patrick ML, Part P, Marshall WS, Wood CM. 1997. Characterization of ion and acid-base transport in the fresh water adapted mummichog (Fundulus heteroclitus). J Exp Zool. 279(3):208-219. (Pubitemid 27439915)
51. Powers DA, Lauerman T, Crawford D, DiMichele L. 1991. Genetic mechanisms for adapting to a changing environment. Annu Rev Genet. 25:629-659. (Pubitemid 21903735)
52. Prince R, Cooper KR. 1995. Comparisons of the effects of 2,3,7,8- tetrachlorodibenzo-p-dioxin on chemically impacted and nonimpacted subpopulations of Fundulus heteroclitus: I. TCDD Toxicity. Environ Toxicol Chem. 14(4):579-587.
53. Pruell R, Norwood C, Bowen R, Boothman W, Rogerson P, Hackett M, et al. 1990. Geochemical study of sediment contamination in New Bedford Harbor, Massachusetts. Mar Environ Res. 29:77-101.
54. Saldanha AJ. 2004. Java Treeview-extensible visualization of microarray data. Bioinformatics. 20(17):3246-3248. (Pubitemid 39619217)
55. Sanders HL, Mangelsdorf PC Jr., Hampson GR. 1965. Salinity and faunal distribution in the Pocasset River, Massachusetts. Limnol Oceanogr. 10:216-229.
56. Scott GR, Rogers JT, Richards JG, Wood CA, Schulte PM. 2004. Intraspecific divergence of ionoregulatory physiology in the euryhalineteleost Fundulus heteroclitus: possible mechanisms of freshwater adaptation. J Exp Biol. 207(19):3399-3410. (Pubitemid 39348342)
57. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A. 100(16):9440-9445. (Pubitemid 37033947)
58. Subash Peter MC, Lock RAC, Wendelaar Bonga SE. 2000. Evidence for an osmoregulatory role of thyroid hormones in the freshwater Mozambique Tilapia Oreochromis mossambicus. General Comp Endocrinol. 120(2): 157-167.
59. Tingaud-Sequeira A, Zapater C, Chauvigne F, Otero D, Cerda J. 2009. Adaptive plasticity of killifish (Fundulus heteroclitus) embryos: dehydrationstimulated development and differential aquaporin-3 expression. Am J Physiol Regul Integr Comp Physiol. 296(4):R1041-R1052.
60. Van Veld PA, Nacci DE. 2008. Toxicity resistance. In: Di Giulio RT, Hinton DE, editors. The toxicology of fishes. Boca Raton (FL): Taylor and Francis.
61. Vogelbein WK, Fournie JW, Van Veld PA, Huggett RJ. 1990. Hepatic neoplasms in the mummichog Fundulus heteroclitus from a creosotecontaminated site. Cancer Res. 50(18):5978-5986. (Pubitemid 20331409)
62. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, et al. 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23(21):4407-4414.
63. Watanabe S, Kaneko T, Aida K. 2005. Aquaporin-3 expressed in the basolateral membrane of gill chloride cells in Mozambique tilapia Oreochromis mossambicus adapted to freshwater and seawater. J Exp Biol. 208(14):2673-2682. (Pubitemid 41129985)
64. Weis J. 2002. Tolerance to environmental contaminants in the mummichug, Fundulus heteroclitus. Hum Ecol Risk Assess. 8:933-953. (Pubitemid 41445935)
65. Wernersson R, Juncker AS, Nielsen HB. 2007. Probe selection for DNA microarrays using OligoWiz. Nat Protocols. 2(11):2677-2691.
66. Whitehead A. 2010. The evolutionary radiation of diverse osmotolerant physiologies in killifish (Fundulus sp.). Evolution. doi:10.1111/j.1558- 5646.2010.00957.x.
67. Whitehead A, Crawford DL. 2005. Variation in tissue-specific gene expression among natural populations. Genome Biol. 6(2):R13.
68. Whitehead A, Crawford DL. 2006a. Neutral and adaptive variation in gene expression. Proc Natl Acad Sci U S A. 103(14):5425-5430.
69. Whitehead A, Crawford DL. 2006b. Variation within and among species in gene expression: raw material for evolution. Mol Ecol. 15(5):1197-1211.
70. Williams LM, Ma X, Boyko AR, Bustamante CD, Oleksiak MF. 2010. SNP identification, verification, and utility for population genetics in a nonmodel genus. BMC Genetics. 11:32.
71. Williams LM, Oleksiak MF. 2008. Signatures of selection in natural populations adapted to chronic pollution. BMC Evol Biol. 8:282.
72. Zall DM, Fisher D, Garner MQ. 1956. Photometric determination of chlorides in water. Anal Chem. 28(11):1665-1668