Testing the Hamilton-Zuk hypothesis: Past, present, and future

Integrative and Comparative Biology

Volumn 54, Issue 4, 2014, Pages 601-613

  Balenger, Susan L ^a   Zuk, Marlene ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ANIMAL PARASITOSIS; BIOLOGICAL MODEL; EVOLUTION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; SEXUAL DEVELOPMENT;

ANIMALS; BIOLOGICAL EVOLUTION; GENETIC VARIATION; MODELS, GENETIC; PARASITIC DISEASES, ANIMAL; SELECTION, GENETIC; SEX CHARACTERISTICS;

EID: 84923063148     PISSN: 15407063     EISSN: 15577023     Source Type: Journal    
DOI: 10.1093/icb/icu059     Document Type: Conference Paper

References (95)

1. Able DJ. 1996. The contagion indicator hypothesis for parasite mediated sexual selection. Proc Nat Acad Sci USA 93:2229-33.
2. Adamo S. 2012. The importance of physiology for ecoimmunology: lessons from the insects. In: Demas GE, Nelson RJ, editors. Ecoimmunology. Oxford: Oxford University Press. p. 413-39.
3. Agrawal A, Lively CM. 2002. Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol Ecol Res 4:79-90.
4. Allen EE, Banfield JF. 2005. Community genomics in microbial ecology and evolution. Nat Rev Microbiol 3:489-98.
5. Anderson RM, May RM. 1978. Regulation and stability of host-parasite population interactions: I. Regulatory processes. J Anim Ecol 47:219-47.
6. Anderson RM, May RM. 1979. Population biology of infectious diseases: Part I. Nature 280:361-7.
7. Backström N, Zhang Q, Edwards SV. 2013. Evidence from a house finch (Haemorhous mexicanus) spleen transcriptome for adaptive evolution and biased gene conversion in passerine birds. Mol Biol Evol 30:1046-50.
8. Baird NA, Etter PD, Atwood TS, Currey MA, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA. 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376.
9. Barber I. 2013. Sticklebacks as model hosts in ecological and evolutionary parasitology. Trends Parasitol 29:556-66.
10. Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA. 2001. Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc R Soc Lond B 268:71-6.
11. Barber I, Scharsack JP. 2010. The three-spined stickleback - Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology 137:411-24.
12. Barrett RD, Hoekstra HE. 2011. Molecular spandrels: tests of adaptation at the genetic level. Nat Rev Genet 12:767-80.
13. Bell M, Foster S. 1994. The evolutionary biology of the threespine stickleback. Oxford, UK: Oxford University Press.
14. Bonneaud C, Balenger SL, Russell AF, Zhang J, Hill GE, Edwards SV. 2011. Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proc Nat Acad Sci USA 108:7866-71.
15. Borgia G. 1979. Sexual selection and the evolution of mating systems. In: Blum MS, Blum NA, editors. Sexual selection and reproductive competition in insects. New York: Academic Press. p. 19-80.
16. Borgia G. 1986. Satin bowerbird parasites: a test of the bright male hypothesis. Behav Ecol Sociobiol 19:355-8.
17. Brawner WR III, Hill GE, Sundermann CA. 2000. Effects of coccidial and mycoplasmal infections on carotenoidbased plumage pigmentation in male house finches. Auk 117:952-63.
18. Cantacessi C, Campbell BE, Jex AR, Young ND, Hall RS, Ranganathan S, Gasser RB. 2012. Bioinformatics meets parasitology. Parasite Immunol 34:265-75.
19. Colosimo PF, Peichel CL, Nereng K, Blackman BK, Shapiro MD, Schulter D, Kingsley DM. 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol 2:e109.
20. Davey JW, Blaxter ML. 2011. RADSeq: next-generation population genetics. Brief Funct Genomics 9:416-23.
21. Davey JW, Hohenlohe PA, Etter PD, Boone PD, Boone JQ, Catchen JM, Blaxter ML. 2011. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499-510.
22. Delaney NF, Balenger SL, Bonneaud C, Marx CJ, Hill GE, Ferguson-Noel N, Tsai P, Rodrigo A, Edwards SV. 2012. Ultrafast evolution and loss of CRISPRs following a host shift in a novel wildlife pathogen, Mycoplasma gallisepticum. PLoS Genet 8:e1002511.
23. Demas GE, Nelson RJ. 2012. Ecoimmunology. Oxford: Oxford University Press.
24. De Wit P, Pespeni MH, Ladner JT, Barshis DJ, Seneca F, Jaris H, OverGaard Therkildsen N, Morikawa M, Palumbi SR. 2012. The simple fool's guide to population genomics via RNA-Seq: an introduction to high-throughput sequencing data analysis. Mol Ecol Res 12:1058-67.
25. Duckworth RA, Badyaev AV, Parlow AF. 2003. Elaborately ornamented males avoid costly parental care in the house finch (Carpodacus mexicanus): a proximate perspective. Behav Ecol Sociobiol 55:176-83.
26. Ellegren H. 2014. Genome sequencing and population genomics in non-model organisms. Trends Ecol Evol 29:51-63.
27. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE. 2011. A robust, simple genotyping- by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379.
28. Eizaguirre C, Lenz TL, Sommerfeld RD, Harrod C, Kalbe M, Milinski M. 2011. Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes. Evol Ecol 25:605-22.
29. Eizaguirre C, Lenz TL, Kalbe M, Milinski M. 2012. Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat Commun 3:621.
30. Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat 125:1-15.
31. Flor HH. 1971. Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275-96.
32. Folstad I, Karter AJ. 1992. Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603-22.
33. Folstad I, Mette HA, Karter A, Skorping A. 1994. Sexually selected color in male sticklebacks - a signal of both parasite exposure and parasite resistance. Oikos 69:511-5.
34. Gaba S, Ebert D. 2009. Time-shift experiments as a tool to study antagonistic coevolution. Trends Ecol Evol 24:226-32.
35. Garamszegi LZ, Møller AP. 2012. The interspecific relationship between prevalence of blood parasites and sexual traits in birds when considering recent methodological advancements. Behav Ecol Sociobiol 66:107-19.
36. Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F, et al. 2011. Current trends in microsatellite genotyping. Mol Ecol Res 11:591-611.
37. Guo Y, Sheng Q, Li J, Ye F, Samuels DC, Shyr Y. 2013. Large scale comparison of gene expression levels by microarrays and RNAseq using TCGA data. PLoS One 8:e71462.
38. Hamilton WD, Poulin R. 1997. The Hamilton and Zuk hypothesis revisted: a meta-analytical approach. Behaviour 134:299-320.
39. Hamilton WD, Zuk M. 1982. Heritable true fitness and bright birds: a role for parasites? Science 218:384-7.
40. Harvey PH, Pagel MD. 1991. The comparative method in evolutionary biology. Oxford: Oxford University Press.
41. Hawley DM, Osnas EE, Dobson AP, Hochachka WM, Ley DH, Dhondt AA. 2013. Parallel patterns of increased virulence in a recently emerged wildlife pathogen. PLoS Biol 11:e1001570.
42. Head SR, Komori HK, LaMere SA, Whisenant T, Van Nieuwerburgh F, Salomon DR, Ordoukhanian P. 2014. Library construction for next-generation sequencing: overviews and challenges. Biotechniques 56:61-77.
43. Hill GE. 1990. Female house finches prefer colorful males: sexual selection for a condition-dependent trait. Anim Behav 40:563-72.
44. Hill GE. 1991. Plumage coloration is a sexually selected indicator of male quality. Nature 350:337-9.
45. Hill GE. 1992. Proximate basis of variation in carotenoid pigmentation in male house finches. Auk 109:1-12.
46. Hill GE. 2000. Energetic constraints on expression of carotenoid- based plumage coloration. J Avian Biol 31:559-66.
47. Hill GE, Farmer KL. 2005. Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch. Naturwissenschaften 92:30-4.
48. Hill GE, Farmer KL, Beck ML. 2004. The effect of mycoplasmosis on carotenoid coloration in male house finches. J Exp Biol 207:2095-9.
49. Hill GE, Inouye CY, Montgomerie R. 2002. Dietary carotenoids predict plumage coloration in wild house finches. Proc R Soc Lond B 269:1119-24.
50. Hoekstra HE, Hirschman RJ, Bundey RA, Insel PA, Crossland JP. 2006. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313:101-4.
51. Hohenlohe PA, Bassham S, Etter P, Stiffler N, Johnson EA, Cresko WA. 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 6:e1000682.
52. Jackson CL, Hartwell LH. 1990. Courtship in S. cerevisiae: both cell types choose mating partners by responding to the strongest pheromone signal. Cell 63:1039-51.
53. Jex AR, Koehler AV, Ansell BR, Baker L, Karunajeewa H, Gasser RB. 2013. Getting to the guts of the matter: the status and potential of 'omics' research of parasitic protists of the human gastrointestinal system. Int J Parasitol 43:971-82.
54. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, Swofford R, Pirun M, Zody MC, White S, et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55-61.
55. Kraaijeveld AR, Godfray HCJ. 2009. Evolution of host resistance and parasitoid counter resistance. In: Prevost G, editor. Advances in parasitology. New York: Academic Press. Vol. 70. p. 257-80.
56. Kurokawa K, Itoh T, Kuwahara T, Oshima K, Toh H, Toyoda A, Takami H, Morita H, Sharma VK, Srivastava TP, et al. 2007. Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14:169-81.
57. Lawniczak MKN, Barnes AI, Linklater JR, Boone JM, Wigby S, Chapman T. 2007. Mating and immunity in invertebrates. Trends Ecol Evol 22:48-55.
58. Leonard KJ. 1993. Stability of equilibria in a gene-forgene coevolution model of host-parasite interactions. Phytopathology 84:70-7.
59. Ley DH, Berkhoff JE, McLaren JM. 1996. Mycoplasma gallisepticum isolated from house finches (Carpodacus mexicanus) with conjunctivitis. Avian Dis 40:480-3.
60. Luijckx P, Fienberg H, Duneau D, Ebert D. 2013. A matching- allele model explains host resistance to parasites. Curr Biol 23:1085-8.
61. Malone JH, Oliver B. 2011. Microarrays, deep sequencing and the true measure of the transcriptome. BMC Biol 9:34.
62. May RM. 1972. Limit cycles in predator-prey communities. Science 177:900-2.
63. May RM, Anderson RM. 1979. Population biology of infectious diseases: Part II. Nature 280:455-61.
64. May RM, Anderson RM. 1978. Regulation and stability of host-parasite population interactions: II. Destabilizing processes. J Anim Ecol 47:249-67.
65. Milinski M, Bakker TCM. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasites. Nature 344:330-4.
66. Møller AP. 1990. Parasites and sexual selection: current status of Hamilton and Zuk hypothesis. J Evol Biol 3:319-28.
67. Møller AP, Christe P, Lux E. 1999. Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3-20.
68. Montgomerie R. 2006. Analyzing colors. In: Hill GE, McGraw KJ, editors. Bird coloration 1: mechanisms and measurements. Cambridge: Harvard University Press. p. 90-147.
69. Nadeau N, Jiggins CD. 2010. A golden age for evolutionary genetics? Genomic studies of adaptation in natural populations. Trends Genet 26:484-92.
70. Ng TFF, Willner DL, Lim YW, Schmeider R, Chau B, Nilsson C, Anthony S, Ruan Y, Rohwer F, Breitbart M. 2011. Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS One 6:e20579.
71. Omland KE, Hofmann CM. 2006. Adding color to the past: ancestral-state reconstruction of coloration. In: Hill GE, McGraw KJ, editors. Bird coloration 2: function and evolution. Cambridge: Harvard University Press. p. 417-54.
72. Ostlund-Nilsson S, Mayer I, Huntingford FA. 2006. Biology of the three-spined stickleback. Boca Raton (FL): CRC Press.
73. Papazisi L, Gorton TS, Kutish G, Markham PF, Browning GF, Nguyen DK, Swartzell S, Madan A, Mahairas G, Geary SJ. 2003. The complete genome sequence of the avian pathogen Mycoplasma gallisepticum strain Rlow. Microbiology 149:2307-16.
74. Price PW. 1980. Evolutionary biology of parasites. Monographs in population biology. Vol. 15. Princeton: Princeton University Press.
75. Read AF. 1988. Sexual selection and the role of parasites. Trends Ecol Evol 3:97-102.
76. Read AF, Weary DM. 1990. Sexual selection and the evolution of bird song: a test of the Hamilton-Zuk hypothesis. Behav Ecol Sociobiol 26:47-56.
77. Roberts ML, Buchanan KL, Evans MR. 2004. Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227-39.
78. Rokas A, Abbott P. 2009. Harnessing genomics for evolutionary insights. Trends Ecol Evol 24:192-200.
79. Rolff J. 2002. Bateman's principle and immunity. Proc R Soc Lond B 269:867-72.
80. Rolff J, Kraaijeveld AR. 2003. Selection for parasitoid resistance alters mating success in Drosophila. Proc R Soc Lond B 270:S154-5.
81. Rolff J, Siva-Jothy MT. 2003. Invertebrate ecology immunology. Science 301:472-5.
82. Savolainen O, Lascoux M, MerihäJ. 2013. Ecological genomics of local adaptation. Nat Rev Genet 14:807-20.
83. Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, Jonsson B, Schulter D, Kingsley DM. 2004. Genetic and developmental basis of evolutionary pelvis reduction in threespine sticklebacks. Nature 428:717-23.
84. Shapiro MD, Kronenberg Z, Li C, Domyan ET, Pan H, Campbell M, Tan H, Huff CD, Hu H, Vickrey AI, et al. 2013. Genomic diversity and evolution of the head crest in the rock pigeon. Science 339:1063-7.
85. Sheldon BC, Verhulst S. 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317-21.
86. Stapley J, Reger J, Feuler PGD, Smadja C, Galindo J, Ekblom R, Bennison C, Ball AD, Beckerman AP, Slate J. 2010. Adaptation genomics: the next generation. Trends Ecol Evol 25:705-12.
87. The Human Gut Microbiome Consortium. 2012. Structure, function, and diversity of the healthy human gut microbiome. Nature 486: 207-14.
88. Thompson JN, Burdon JJ. 1992. Gene-for-gene coevolution between plants and parasites. Nature 360:121-5.
89. Tulman ER, Liao X, Szczepanek SM, Ley DH, Kutish GF, Geary SJ. 2012. Extensive variation in surface lipoprotein gene content and genomic changes associated with virulence during evolution of a novel North American house finch epizootic strain of Mycoplasma gallisepticum. Microbiology 158:2073-88.
90. Vorobyev M, Osario D, Bennett ATD, Marshall NJ, Cuthill IC. 1998. Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621-33.
91. Wang Z, Gerstein M, Snyder M. 2009. RNASeq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57-63.
92. Wertheim B, Kraaijeveld AR, Schuster E, Blanc E, Hopkins M, Pletcher SD, Strand MR, Partridge L, Godfray HCJ. 2005. Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biol 6:R94.
93. Wertheim B, Kraaijeveld AR, Hopkins MG, Walther Boer M, Godfray HCJ. 2011. Functional genomics of the evolution of increased resistance to parasitism in Drosophila. Mol Ecol 20:932-49.
94. Wooley JC, Ye Y. 2010. Metagenomics: facts and artifacts, and computational challenges. J Comput Sci Technol 25:71-81.
95. Zuk M. 1992. The role of parasites in sexual selection: current evidence and future directions. Adv Study Behav 21:39-68. New York: Academic Press.