Phenotypic and genomic plasticity of alternative male reproductive tactics in sailfin mollies

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1781, 2014, Pages

  Fraser, Bonnie A ^a,b   Janowitz, Ilana ^a   Thairu, Margaret ^a,c   Travis, Joseph ^a   Hughes, Kimberly A ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Courtship; Mating behaviour; Plasticity; Poecilia latipinna; Transcriptome

Indexed keywords

TRANSCRIPTOME;

ADAPTATION; COURTSHIP; FISH; GENE EXPRESSION; GENOMICS; MATING BEHAVIOR; NUMERICAL MODEL; PHENOTYPIC PLASTICITY; PHYSIOLOGICAL RESPONSE;

ADAPTATION; ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BODY SIZE; BRAIN; COURTSHIP; EVOLUTION; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; GENOTYPE; MALE; MATING BEHAVIOUR; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYSIOLOGY; PLASTICITY; POECILIA; POECILIA LATIPINNA; SEQUENCE ANALYSIS; SEXUAL BEHAVIOR; STATISTICAL MODEL; UNITED STATES;

COURTSHIP; MATING BEHAVIOUR; PLASTICITY; POECILIA LATIPINNA; TRANSCRIPTOME;

ADAPTATION, BIOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; BODY SIZE; BRAIN; FLORIDA; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENETICS; GENOTYPE; LINEAR MODELS; MALE; METABOLISM; MOLECULAR SEQUENCE DATA; PHENOTYPE; PHYSIOLOGY; POECILIA; SEQUENCE ANALYSIS, RNA; SEXUAL BEHAVIOR, ANIMAL;

EID: 84896878008     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.2310     Document Type: Article

References (70)

1. Travis J. 1994 Evaluating the adaptive role of morphological plasticity. In Ecological morphology: integrative organismal biology (eds PC Wainwright, SM Reilly), pp. 99-122. Chicago, IL: University of Chicago Press.
2. Schlichting CD, Pigliucci M. 1998 Phenotypic evolution: a reaction norm perspective. Sunderland, MA: Sinauer Associates Incorporated.
3. West-Eberhard MJ. 2003 Developmental plasticity and evolution. Oxford, UK: Oxford University Press.
4. Schmitt J, Stinchcombe JR, Heschel MS, Huber H. 2003 The adaptive evolution of plasticity: phytochromemediated shade avoidance responses. Integr. Comp. Biol. 43, 459-469. (doi:10.1093/icb/43.3.459)
5. Pigliucci M, Murren CJ, Schlichting CD. 2006 Phenotypic plasticity and evolution by genetic assimilation. J. Exp. Biol. 209, 2362-2367. (doi:10.1242/jeb.02070)
6. Draghi JA, Whitlock MC. 2012 Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 66, 2891-2902. (doi:10.1111/j. 1558-5646.2012.01649.x)
7. Renn SCP, Schumer ME. 2013 Genetic accommodation and behavioural evolution: insights from genomic studies. Anim. Behav. 85, 1012-1022. (doi:10.1016/j.anbehav.2013.02.012)
8. Grant V. 1977 Organismic evolution. San Francisco, CA: Freeman.
9. Falconer DS. 1981 Introduction to quantitative genetics. New York, NY: Ronald Press Co.
10. Levin DA. 1988 Plasticity, canalization and evolutionary stasis in plants. In Plant population ecology (eds AJ Davy, MJ Hutchings, AR Watkinson), pp. 35-45. Oxford, UK: Blackwell Scientific Publications.
11. Anderson RW. 1995 Learning and evolution: a quantitative genetics approach. J. Theor. Biol. 175, 89-101. (doi:10.1006/jtbi.1995.0123)
12. Ancel LW. 2000 Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution? Theor. Popul. Biol. 58, 307-319. (doi:10.1006_tpbi.2000.1484)
13. Baldwin JM. 1896 A new factor in evolution. Am. Nat. 30, 441-451. (doi:10.1086/276408)
14. Waddington CH. 1942 Canalization of development and the inheritance of acquired characters. Nature 150, 563-565. (doi:10.1038/150563a0)
15. Schmalhausen II. 1949 Factors of evolution. Philadelphia, PA: Blakiston.
16. Hinton GE, Nowlan SJ. 1987 How learning can guide evolution. Complex Syst. 1, 495-502. (doi:10.1177/ 089443938900700128)
17. Price TD, Qvarnström A, Irwin DE. 2003 The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. Lond. B 270, 1433-1440. (doi:10. 1098/rspb.2003.2372)
18. Fierst JL. 2011 A history of phenotypic plasticity accelerates adaptation to a new environment. J. Evol. Biol. 24, 1992-2001. (doi:10.1111/j. 1420-9101.2011.02333.x)
19. Espinosa-Soto C, Martin OC, Wagner A. 2011 Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits. BMC Evol. Biol. 11, 5. (doi:10.1186/1471-2148-11-5)
20. West-Eberhard MJ. 2005 Phenotypic accommodation: adaptive innovation due to developmental plasticity. J. Exp. Zool. 304B, 610-618. (doi:10.1002/jez.b.21071.PHENOTYPIC)
21. De Jong G. 2005 Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytol. 166, 101-117. (doi:10.1111/j.1469-8137.2005.01322.x)
22. Ghalambor CK, McKay JK, Carroll SP, Reznick DN. 2007 Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394-407. (doi:10.1111/j.1365-2435.2007. 01283.x)
23. Mayley G. 1996 Landscapes, learning costs and genetic assimilation. Evol. Comput. 4, 213-234. (doi:10.1162/evco.1996.4.3.213)
24. Alaux C et al. 2009 Honey bee aggression supports a link between gene regulation and behavioral evolution. Proc. Natl Acad. Sci. USA 106, 15 400-15 405. (doi:10.1073/pnas.0907043106)
25. Scoville AG, Pfrender ME. 2010 Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl Acad. Sci USA 107, 4260-4263. (doi:10.1073/pnas.0912748107)
26. Van Buskirk J, Steiner U. 2009 The fitness costs of developmental canalization and plasticity. J. Evol. Biol. 22, 852-860. (doi:10.1111/j.1420-9101.2009. 01685.x)
27. Auld JR, Agrawal AA, Relyea RA. 2010 Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc. R. Soc. B 277, 503-511. (doi:10. 1098/rspb.2009.1355)
28. Newman RA. 1992 Adaptive plasticity in amphibian metamorphosis. BioScience 42, 671-678. (doi:10. 2307/1312173)
29. DeWitt TJ, Sih A, Wilson DS. 1998 Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13, 77-81. (doi:10.1111/j.1558-5646.2009.00647.x)
30. Van Kleunen M, Fischer M. 2005 Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol. 166, 49-60. (doi:10.1111/j.1469-8137. 2004.01296.x)
31. Pigliucci M. 2001 Phenotypic plasticity: beyond nature and nurture. Baltimore, MD: Johns Hopkins University Press.
32. Callahan HS, Maughan H, Steiner UK. 2008 Phenotypic plasticity, costs of phenotypes, and costs of plasticity: toward an integrative view. Ann. NY Acad. Sci. 1133, 44-66. (doi:10.1196/annals.1438.008)
33. Ghalambor CK, Angeloni L, Carrol SP. 2010 Behavior as phenotypic plasticity. In Evolutionary behavioral ecology (eds C Fox, D Westneat), pp. 90-107. New York, NY: Oxford University Press.
34. Foster SA. 2013 Evolution of behavioural phenotypes: influences of ancestry and expression. Anim. Behav. 85, 1061-1075. (doi:10.1016/j. anbehav.2013.02.008)
35. Bell AM, Robinson GE. 2011 Behavior and the dynamic genome. Science 332, 1161-1162. (doi:10.1126/science.1203295)
36. Stamps J, Groothuis TGG. 2010 The development of animal personality: relevance, concepts and perspectives. Biol. Rev. Camb. Phil. Soc. 85, 301-325. (doi:10.1111/j.1469-185X.2009.00103.x)
37. Sih A, Bell A, Johnson JC. 2004 Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol. Evol. 19, 372-378. (doi:10.1016/j.tree. 2004.04.009)
38. Sih A, Bell AM. 2008 Insights for behavioral ecology from behavioral syndromes. Adv. Study Behav. 38, 227-281. (doi:10.1016/S0065-3454(08)00005-3)
39. Travis J. 1994 Size dependent behavioral variation and its genetic control within and among populations. In Quantitative genetic studies of behavioral evolution (ed. BRC Boake), pp. 165-187. Chicago, IL: University of Chicago Press.
40. Farr JA, Travis J, Trexler JC. 1986 Behavioural allometry and interdemic variation in sexual behaviour of the sailfin molly, Poecilia latipinna (Pisces: Poeciliidae). Anim. Behav. 34, 497-509. (doi:10.1016/S0003-3472(86)80118-X)
41. Trexler JC, Travis J, Trexler M. 1990 Phenotypic plasticity in the sailfin molly, Poecilia latipinna (Pisces: Poeciliidae). II. Laboratory experiment. Evolution 44, 157-167. (doi:10.2307/2409531)
42. Trexler JC, Travis J. 1990 Phenotypic plasticity in the sailfin molly, Poecilia latipinna (Pisces: Poeciliidae). I. Field experiments. Evolution 44, 143-156. (doi:10.2307/2409530)
43. Ptacek MB, Travis J. 1996 Inter-population variation in male mating behaviours in the sailfin mollie, Poecilia latipinna. Anim. Behav. 52, 59-71. (doi:10. 1006/anbe.1996.0152)
44. Seda JB, Childress MJ, Ptacek MB. 2012 Individual variation in male size and behavioral repertoire in the Sailfin Molly Poecilia latipinna. Ethology 118, 411-421. (doi:10.1111/j.1439-0310.2012.02025.x)
45. Travis J, Woodward BD. 1989 Social context and courtship flexibility in male sailfin mollies, Poecilia latipinna (Pisces: Poeciliidae). Anim. Behav. 38, 1001-1011. (doi:10.1016/S0003-3472(89)80139-3)
46. Whitehead A, Roach JL, Zhang S, Galvez F. 2011 Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient. Proc. Natl Acad. Sci. USA 108, 6193-6198. (doi:10.1073/pnas. 1017542108)
47. Hunt BG, Ometto L, Wurm Y, Shoemaker D, Yi SV, Keller L. 2011 Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc. Natl Acad. Sci. USA 108, 15 936-15 941. (doi:10.1073/pnas. 1104825108)
48. Burmeister SS, Jarvis ED, Fernald RD. 2005 Rapid behavioral and genomic responses to social opportunity. PLoS Biol. 3, 1996-2004. (doi:10. 1371/journal.pbio.0030363)
49. Snell-Rood EC, Cash A, Han MV, Kijimoto T, Andrews J, Moczek AP. 2011 Developmental decoupling of alternative phenotypes: insights from the transcriptomes of horn-polyphenic beetles. Evolution 65, 231-245. (doi:10.1111/j.1558-5646. 2010.01106.x)
50. Aubin-Horth N, Landry CR, Letcher BH, Hofmann HA. 2005 Alternative life histories shape brain gene expression profiles in males of the same population. Proc. R. Soc. B 272, 1655-1662. (doi:10.1098/rspb. 2005.3125)
51. Gibson G. 2008 The environmental contribution to gene expression profiles. Nat. Rev. Genet. 9, 575-581. (doi:10.1038/nrg2383)
52. Aubin-Horth N, Renn SCP. 2009 Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity. Mol. Ecol. 18, 3763-3780. (doi:10.1111/j.1365-294X.2009.04313.x)
53. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008 Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628. (doi:10.1038/nmeth.1226)
54. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. 2008 RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 18, 1509-1517. (doi:10.1101/gr.079558.108)
55. Farr JA, Travis J. 1989 The effect of ontogenetic experience on variation in growth, maturation, and sexual behavior in the sailfin molly, Poecilia latipinna (Pisces: Poeciliidae). Environ. Biol. Fish. 26, 39-48. (doi:10.1007/BF00002474)
56. Ptacek MB, Travis J. 1997 Mate choice in the Sailfin molly, Poecilia latipinna. Evolution 51, 1217-1231. (doi:10.1006/anbe.2001.1982)
57. Sumner IT, Travis J, Johnson CD. 1994 Methods of female fertility advertisement and variation among males in responsiveness in the sailfin molly (Poecilia latipinna). Copeia 1994, 27-34. (doi:10.2307/ 1446667)
58. Altmann J. 1974 Observational study of behavior: sampling methods. Behaviour 49, 227-267. (doi:10.2307/4533591)
59. Robinson MD, Oshlack A. 2010 A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25. (doi:10.1186/gb-2010-11-3-r25)
60. Inc SI. 2011 SAS/STAT 9.3 User's guide. Cary, NC: SAS Institute.
61. Alexa A, Rahnenführer J, Lengauer T. 2006 Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22, 1600-1607. (doi:10.1093/ bioinformatics/btl140)
62. Whitfield CW, Cziko A-M, Robinson GE. 2003 Gene expression profiles in the brain predict behavior in individual honey bees. Science 302, 296-299. (doi: 10.1126/science.1086807)
63. Wagner A. 2005 Energy constraints on the evolution of gene expression. Mol. Biol. Evol. 22, 1365-1374. (doi:10.1093/molbev/msi126)
64. Stoebel DM, Dean AM, Dykhuizen DE. 2008 The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Genetics 178, 1653-1660. (doi:10.1534/genetics. 107.085399)
65. Lang GI, Murray AW, Botstein D. 2009 The cost of gene expression underlies a fitness trade-off in yeast. Proc. Natl Acad. Sci. USA 106, 5755-5760. (doi:10.1073/pnas.0901620106)
66. Eames M, Kortemme T. 2012 Cost-benefit tradeoffs in engineered lac operons. Science 336, 911-915. (doi:10.1126/science.1219083)
67. Krebs RA, Feder ME. 1997 Deleterious consequences of Hsp70 overexpression in Drosophila melanogaster larvae. Cell Stress Chaperones 2, 60-71. (doi:10.1379/ 1466-1268(1997)002,0060:DCOHOI.2.3.CO;2)
68. Kotrschal A, Rogell B, Bundsen A, Svensson B, Zajitschek S, Brännström I, Immler S, Maklakov AA, Kolm N. 2013 Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr. Biol. 23, 168-171. (doi:10.1016/j.cub.2012.11.058)
69. Mery F, Kawecki TJ. 2004 An operating cost of learning in Drosophila melanogaster. Anim. Behav. 68, 589-598. (doi:10.1016/j.anbehav.2003.12.005)
70. Mery F, Kawecki TJ. 2003 A fitness cost of learning ability in Drosophila melanogaster. Proc. R. Soc. Lond. B 270, 2465-2469. (doi:10.1098/rspb. 2003.2548)