The deleterious effects of high inbreeding on male Drosophila melanogaster attractiveness are observed under competitive but not under non-competitive conditions

Behavior Genetics

Volumn 44, Issue 2, 2014, Pages 144-154

  Valtonen, Terhi M ^a   Roff, Derek A ^b   Rantala, Markus J ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Attractiveness; Copulation duration; Courtship; Honest signals of quality; Inbreeding depression; Mating speed; Mating success

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; COPULATION; DIRECTIONAL SELECTION; DROSOPHILA MELANOGASTER; GENETIC VARIABILITY; INBRED STRAIN; INBREEDING; INBREEDING DEPRESSION; LIFE HISTORY TRAIT; MATING; MATING SUCCESS; MORPHOLOGICAL TRAIT; NONHUMAN; OUTBRED STRAIN; OUTCROSSING; SEXUAL SELECTION;

ANIMALS; COMPETITIVE BEHAVIOR; DROSOPHILA MELANOGASTER; FEMALE; GENETIC VARIATION; INBREEDING; MALE; SEXUAL BEHAVIOR, ANIMAL;

EID: 84896390918     PISSN: 00018244     EISSN: 15733297     Source Type: Journal    
DOI: 10.1007/s10519-013-9639-1     Document Type: Article

References (68)

1. Ala-Honkola O, Uddström A, Pauli BD, Lindström K (2009) Strong inbreeding depression in male mating behaviour in a poeciliid fish. J Evol Biol 22:1396-1406
2. Ala-Honkola O, Manier MK, Lüpold S, Pitnick S (2011) No evidence for postcopulatory inbreeding avoidance in Drosophila melanogaster. Evolution 65:2699-2705
3. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJ
4. Armbuster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235-242
5. Aspi J (2000) Inbreeding and outbreeding depression in male courtship song characters in Drosophila montana. Heredity 84:273-282
6. Averhoff WW, Richardson RH (1974) Pheromonal control of mating patterns in Drosophila melanogaster. Behav Genet 4:207-225
7. Bennet-Clark HC, Ewing AW (1969) Pulse interval as a critical parameter in the courtship song of Drosophila melanogaster. Anim Behav 17:755-759
8. Biémont C (2010) Inbreeding effects in the epigenetic era. Nat Rev Genet 11:234
9. Bolund E, Martin K, Kempenaers B, Forstmeier W (2010) Inbreeding depression of sexually selected traits and attractiveness in the zebra finch. Anim Behav 79:947-955
10. Carr DE, Dudash MR (2003) Recent approaches into the genetic basis of inbreeding depression in plants. Philos Trans R Soc Lond B 358:1071-1084
11. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Ann Rev Ecol Syst 18:237-268
12. Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74:329-340
13. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783-796
14. Collins MF, Hewitt JK (1984) The genetic architecture of the male courtship sequence in Drosophila melanogaster. Heredity 53:321-337
15. Cotton S, Fowler K, Pomiankowski A (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B 271:771-783
16. Crnokrak E, Roff DA (1995) Dominance variance: associations with selection and fitness. Heredity 75:530-540
17. DeRose MA, Roff DA (1999) A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53:1288-1292
18. Drayton JM, Hunt J, Brooks R, Jennions MD (2007) Sounds different: inbreeding depression in sexually selected traits in the cricket Teleogryllus commodus. J Evol Biol 20:1138-1147
19. Drayton JM, Milner RNC, Hunt J, Jennions MD (2010) Inbreeding and advertisement calling in the cricket Teleogryllus commodus: laboratory and field experiments. Evolution 64:3069-3083
20. Fisher R (1930) The genetical theory of natural selection. Oxford University Press, Oxford
21. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131-140
22. Grossfield J (1975) Behavioral mutants of Drosophila. In: King RC (ed) Handbook of genetics, vol 3. Plenum, NY, pp 679-702
23. Hall JC (1994) The mating of a fly. Science 264:1702-1714
24. Ilmonen P, Stundner G, Thoß M, Penn DJ (2009) Females prefer the scent of outbred males: good-genes-as heterozygosity? BMC Evol Biol 9:104
25. Joron M, Brakefield PM (2003) Captivity masks inbreeding effects on male mating success in butterflies. Nature 424:191-194
26. Kotiaho JS, Puurtinen M (2007) Mate choice for indirect genetic benefits: scrutiny of the current paradigm. Funct Ecol 21:638-644
27. Kristensen TN, Pedersen KS, Vermeulen CJ, Loeschcke V (2010) Research on inbreeding in the 'omic' era. Trends Ecol Evol 25:44-52
28. Latter BDH, Sved JA (1994) A reevaluation of data from competitive tests shows high levels of heterosis in Drosophila melanogaster. Genetics 137:509-511
29. Lawniczak MKN, Barnes AI, Linklater JR, Boone JM, Wigby S, Chapman T (2007) Mating and immunity in invertebrates. Trends Ecol Evol 22:48-55
30. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA
31. Mack PD, Hammock BA, Promislow DEL (2002) Sperm competitive ability and genetic relatedness in Drosophila melanogaster: similarity breeds contempt. Evolution 56:1789-1795
32. Mariette M, Kelley JL, Brooks R, Evans JP (2006) The effects of inbreeding on male courtship behavior and coloration in guppies. Ethology 112:807-814
33. Markow TA (1981) Genetic and sensory aspects of mating success of phototactic strain of Drosophila melanogaster. Behav Genet 11:273-279
34. Maynard Smith J (1956) Fertility, mating behavior and sexual selection in Drosophila subobscura. J Genet 54:261-279
35. Meagher S, Penn DJ, Potts WK (2000) Male-male competition magnifies inbreeding depression in wild house mice. Proc Natl Acad Sci USA 97:3324-3329
36. Menon DU, Meller VH (2010) Germ line imprinting in Drosophila: epigenetics in search of function. Fly (Austin) 4:48-52
37. Michalczyk L, Martin OY, Millard AL, Emerson BC, Gage MJG (2010) Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum. Proc R Soc Lond B 277:3483-3491
38. Miller PS, Glasner J, Hedrick PW (1993) Inbreeding depression and male-mating behavior in Drosophila melanogaster. Genetica 88:29-36
39. Okada K, Blount JD, Sharma MD, Snook RR, Hosken DJ (2011) Male attractiveness, fertility and susceptibility to oxidative stress are influenced by inbreeding in Drosophila simulans. J Evol Biol 24:363-371
40. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525-567
41. Parsons PA (1964) A diallel cross for mating speeds in Drosophila melanogaster. Genetica 35:141-151
42. Partridge L, Farquhar M (1983) Lifetime mating success of male fruitflies (Drosophila melanogaster) is related to their size. Anim Behav 31:871-877
43. Partridge L, Ewing A, Chandler A (1987a) Male size and mating success in Drosophila melanogaster: the roles of male and female behaviour. Anim Behav 35:555-562
44. Partridge L, Hoffmann A, Jones JS (1987b) Male size and mating success in Drosophila melanogaster and D. pseudoobscura under field conditions. Anim Behav 35:468-476
45. Pendlebury WW, Kidwell JF (1974) The effect of inbreeding on male mating ability in Drosophila melanogaster. Theor Appl Genet 44:128-132
46. Pölkki M, Indrikis I, Kangassalo K, Rantala MJ (2012) Inbreeding affects sexual signaling in males but not females of Tenebrio molitor. Biol Lett 8:423-425
47. Prokop ZM, Les JE, Banas PK, Koteja P, Radwan J (2010) Low inbreeding depression in a sexual trait in the stalk-eyed fly Teleopsis dalmanni. Evol Ecol 24:827-837
48. Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New York
49. Roff DA (1998) Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus Firmus. Heredity 81:28-37
50. Roff DA (2002) Inbreeding depression: tests of the overdominance and partial dominance hypotheses. Evolution 56:768-775
51. Roff DA, Emerson K (2006) Epistasis and dominance: evidence for differential effects in life-history versus morphological traits. Evolution 60:1981-1990
52. Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B 263:1415-1421
53. Rybak F, Sureau G, Aubin T (2002a) Functional coupling of acoustic and chemical signals in the courtship behaviour of the male Drosophila melanogaster. Proc R Soc Lond B 269:695-701
54. Rybak F, Aubin T, Moulin B, Jallon J-M (2002b) Acoustic communication in Drosophila melanogaster courtship: are pulse- and sine-song frequencies important for courtship success? Can J Zool 80:987-996
55. Sharp PM (1984) The effect of inbreeding on competitive male-mating ability in Drosophila melanogaster. Genetics 106:601-612
56. Simmons LW (2011) Inbreeding depression in the competitive fertilization success of male crickets. J Evol Biol 24:415-421
57. Taylor ML, Wedell N, Hosken DJ (2007) The heritability of attractiveness. Curr Biol 17:R959-R960
58. Tomkins JL, Radwan J, Kotiaho JS, Tregenza T (2004) Genic capture and resolving the lek paradox. Trends Ecol Evol 19:323-328
59. Valtonen TM, Roff DA, Rantala MJ (2011a) Analysis of the effects of inbreeding on lifespan and starvation resistance in Drosophila melanogaster. Genetica 139:525-533
60. Valtonen TM, Roff DA, Rantala MJ (2011b) Analysis of the effects of early nutritional environment on inbreeding depression in Drosophila melanogaster. J Evol Biol 24:196-205
61. van den Berg MJ, Thomas G, Hedriks H, van Delden W (1984) A reexamination of the negative assortative mating phenomenon and its underlying mechanism in Drosophila melanogaster. Behav Genet 14:45-61
62. van Oosterhout C, Trigg RE, Carvalho GR, Magurran AE, Hauser L, Shaw PW (2003) Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J Evol Biol 16:273-281
63. Vergeer P, Wagemaker N, Ouborg NJ (2012) Evidence for an epigenetic role in inbreeding depression. Biol Lett 8:798-801
64. Veuille M, Mazeau S (1986) Variation in sexual behavior and negative assortative mating in Drosophila melanogaster. Behav Genet 16:307-317
65. Wittkopp PJ, Haerum BK, Clark AG (2006) Parent-of-origin effects on mRNA expression in Drosophila melanogaster not caused by genomic imprinting. Genetics 173:1817-1821
66. Wright LI, Tregenza T, Hosken DJ (2008) Inbreeding, inbreeding depression and extinction. Conserv Genet 9:833-843
67. Zahavi A (1975) Mate selection - selection for a handicap. J Theor Biol 53:205-214
68. Zajitschek SRK, Brooks RC (2010) Inbreeding depression in male traits and preference for outbred males in Poecilia reticulata. Behav Ecol 21:884-891