Parentage analyses suggest female promiscuity and a disadvantage for athletic males in the colour-polymorphic lizard Podarcis melisellensis

Behavioral Ecology and Sociobiology

Volumn 68, Issue 8, 2014, Pages 1357-1366

  Huyghe, Katleen ^a   Van Damme, Raoul ^a   Breugelmans, Karin ^c   Herrel, Anthony ^d,e   Vanhooydonck, Bieke ^a   Tadič, Zoran ^b   Backeljau, Thierry ^a,c  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF ZAGREB   (Croatia)

^c ROYAL BELGIAN INSTITUTE OF NATURAL SCIENCES   (Belgium)

^d Départment D'Ecologie et de Gestion de la Biodiversité   (France)

^e GHENT UNIVERSITY   (Belgium)

Author keywords

Bateman's principle; Lacertidae; Microsatellites; Sexual selection; Whole animal performance

Indexed keywords

COLOR MORPH; FITNESS; INDIVIDUAL VARIATION; LIFE HISTORY TRAIT; LIZARD; PARENTAGE; PARENTAL INVESTMENT; REPRODUCTIVE SUCCESS; SEXUAL SELECTION;

ANIMALIA; LACERTIDAE; PODARCIS MELISELLENSIS; SQUAMATA;

EID: 84904564247     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-014-1746-3     Document Type: Article

References (98)

1. Alonzo SH, Sinervo B (2000) Mate choice games, context-dependent good genes, and genetic cycles in the side-blotched lizard, Uta stansburiana. Behav Ecol Sociobiol 49: 176-186.
2. Ancona S, Drummond H, Zaldívar-Rae J (2010) Male whiptail lizards adjust energetically costly mate guarding to male-male competition and female reproductive value. Anim Behav 79: 75-82.
3. Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23: 347-361.
4. Bakker TCM, Milinski M (1991) Sequential female choice and the previous male effect in sticklebacks. Behav Ecol Sociobiol 29: 205-210.
5. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2: 349-368.
6. Bateman PW, Gilson LN, Ferguson JWH (2001) Male size and sequential mate preference in the cricket Gryllus bimaculatus. Anim Behav 61: 631-637.
7. Bennett AF, Huey RB, John-Alder HB (1984) Physiological correlates of natural activity and locomotor capacity in two species of lacertid lizards. J Comp Physiol 154: 113-118.
8. Böhme W (1981) Handbuch der Reptilien und Amphibien Europas. AULA-Verlag, Wiesbaden.
9. Calsbeek R, Bonneaud C, Prabhu S, Manoukis N, Smith TB (2007) Multiple paternity and sperm storage lead to increased genetic diversity in Anolis lizards. Evol Ecol Res 9: 495-503.
10. Censky E (1995) Mating strategy and reproductive success in the teiid lizard, Ameiva plei. Behaviour 132: 529-557.
11. Clutton-Brock T (2009) Sexual selection in females. Anim Behav 77: 3-11.
12. Cooper WE Jr (1999) Tradeoffs between courtship, fighting and antipredatory behaviour by a lizard, Eumeces laticeps. Behav Ecol Sociobiol 47: 54-59.
13. Cramer ERA (2013) Physically challenging song traits, male quality, and reproductive success in house wrens. PLoS ONE 8: e59209.
14. Crudgington HS, Siva-Jothy MT (2000) Genital damage, kicking and early death. Nature 407: 855-856.
15. Depeiges A, Force A, Dufaure JP (1987) Production and glycosylation of sperm constitutive proteins in the lizard Lacerta vivipara: evolution during the reproduction period. Comp Biochem Physiol B 86: 233-240.
16. Dewsbury DA (2005) The Darwin-Bateman paradigm in historical context. Integr Comp Biol 45: 831-837.
17. Fitze PF, Le Galliard JF, Federici P, Richard M, Clobert J (2005) Conflict over multiple partner mating among males and females of polygynandrous common lizards. Evolution 59: 2451-2459.
18. Gabor CR, Halliday TR (1997) Sequential mate choice by multiply mating smooth newts: females become more choosy. Behav Ecol 8: 162-166.
19. Garland T Jr (1988) Genetic basis of activity metabolism. I. Inheritance of speed, stamina, and antipredator displays in the garter snake Thamnophis sirtalis. Evolution 42: 335-350.
20. Garland T Jr, Hankins E, Huey RB (1990) Locomotor capacity and social dominance in male lizards. Funct Ecol 4: 243-250.
21. Gist DH, Congdon JD (1998) Oviductal sperm storage as a reproductive tactic of turtles. J Exp Zool 282: 526-534.
22. Gopurenko D, Williams RN, DeWoody JA (2007) Reproductive and mating success in the small-mouthed salamander (Ambystoma texanum) estimated via microsatellite parentage analysis. Evol Biol 34: 130-139.
23. Gowaty PA, Kim Y-K, Anderson WW (2012) No evidence of sexual selection in a repetition of Bateman's classic study of Drosophila melanogaster. Proc Natl Acad Sci U S A 109: 11740-11745.
24. Hall MD, McLaren L, Brooks RC, Lailvaux SP (2010) Interactions among performance capacities predict male combat outcomes in the field cricket. Funct Ecol 24: 159-164.
25. Herrel A, Bonneaud C (2012) Trade-offs between burst performance and maximal exertion capacity in a wild amphibian, Xenopus tropicalis. J Exp Biol 215: 3106-3111.
26. Husak JF, Fox SF (2006) Field use of sprint speed by collared lizards (Crotaphytus collaris): compensation and sexual selection. Evolution 60: 1888-1895.
27. Husak JF, Fox SF, van Den Bussche RA (2008) Faster male lizards are better defenders not sneakers. Anim Behav 75: 1725-1730.
28. Husak JF, Lappin AK, van Den Bussche RA (2009) The fitness advantage of a high-performance weapon. Biol J Linn Soc 96: 840-845.
29. Huyghe K, Vanhooydonck B, Scheers H, Molina-Borja M, van Damme R (2005) Morphology, performance and fighting capacity in male lizards, Gallotia galloti. Funct Ecol 19: 800-807.
30. Huyghe K, Vanhooydonck B, Herrel A, Tadic Z, van Damme R (2007) Morphology, performance, behaviour and ecology of three colour morphs in males of the lizard Podarcis melisellensis. Integr Comp Biol 47: 211-220.
31. Huyghe K, Husak JF, Herrel A, Tadic Z, Moore IT, van Damme R, Vanhooydonck B (2009) Relationships between hormones, physiological performance and immunocompetence in a color-polymorphic lizard species, Podarcis melisellensis. Horm Behav 55: 488-494.
32. Huyghe K, Small M, Vanhooydonck B, Herrel A, Tadic Z, van Damme R, Backeljau T (2010) Genetic divergence among sympatric colour morphs of the Dalmatian wall lizard (Podarcis melisellensis). Genetica 138: 387-393.
33. Huyghe K, Vanhooydonck B, Herrel A, Tadic Z, van Damme R (2012) Female lizards ignore the sweet scent of success: male characteristics implicated in female mate preference. Zoology 115: 217-222.
34. Huyghe K, San-Jose LM, Peñalver Alcázar M, Fitze PS (2013) An ecomorphological analysis of the determinants of mating success. Biol J Linn Soc 110: 658-664.
35. In den Bosch HAJ (1994) First record of mating plugs in lizards. Amphibia-Reptilia 15: 89-93.
36. Irschick DJ, Meyers JJ (2007) An analysis of the relative roles of plasticity and natural selection on morphology and performance in a lizard (Urosaurus ornatus). Oecologia 153: 489-499.
37. Irschick DJ, Herrel A, Vanhooydonck B, van Damme R (2007) A functional approach to sexual selection. Funct Ecol 21: 621-626.
38. Jayne BC, Bennett AF (1990) Selection on locomotor capacity in a natural population of garter snakes. Evolution 44: 1204-1229.
39. Keogh JS, Noble WA, Wilson EE, Whiting MJ (2012) Activity predicts male reproductive success in a polygynous lizard. PLoS ONE 7: e38856.
40. Lailvaux SP, Irschick DJ (2006) A functional perspective on sexual selection: insights and future prospects. Anim Behav 72: 263-273.
41. Lailvaux SP, Herrel A, Vanhooydonck B, Meyers JJ, Irschick DJ (2004) Performance capacity, fighting tactics and the evolution of life-stage male morphs in the green anole lizard (Anolis carolinensis). Proc R Soc Lond B 271: 2501-2508.
42. Lailvaux SP, Hathway J, Pomfret J, Knell RJ (2005) Horn size predicts physical performance in the beetle Euoniticellus intermedius (Coleoptera: Scarabaeidae). Funct Ecol 19: 632-639.
43. Laloi D, Eizaguirree C, Fédérici P, Massot A (2011) Female choice for heterozygous mates changes along successive matings in a lizard. Behav Process 88: 149-154.
44. Le Galliard JF, Clobert J, Ferrière R (2004) Physical performance and Darwinian fitness in lizards. Nature 432: 502-505.
45. Le Galliard JF, Cote J, Fitze PS (2008) Lifetime and intergenerational fitness consequences of harmful male interactions for female lizards. Ecology 89: 56-64.
46. LeBas NR, Marshall NJ (2000) The role of colour in signalling and mate choice in the agamid lizard Ctenophorus ornatus. Proc R Soc Lond B 267: 445-452.
47. Madsen T, Shine R, Loman J, Hakansson T (1992) Why do female adders copulate so frequently? Nature 355: 440-441.
48. Marshall T, Slate J, Kruuk L, Pemberton J (1998) Statistical confidence for likelihood-based paternity inference in natural conditions. Mol Ecol 7: 639-655.
49. Martín J, López P (2000) Chemoreception, symmetry and mate choice in lizards. Proc R Soc Lond B 267: 1265-1269.
50. Matsumasa M, Murai M (2005) Changes in blood glucose and lactate levels of male fiddler crabs: effects of aggression and claw waving. Anim Behav 69: 569-577.
51. Mayer W, Arribas OJ (2003) Phylogenetic relationships of the European lacertid genera Archaeolacerta and Iberolacerta and their relationships to some other 'Archaeolacertae' (sensu lato) from Near East, derived from mitochondrial DNA sequences. J Zool Syst Evol Res 41: 157-161.
52. Mclean CA, Stuart-Fox D (2010) Do female Lake Eyre dragon lizards adjust courtship rejection behaviour under higher predation risk? Behaviour 147: 1803-1818.
53. Mclean CA, Moussalli A, Stuart-Fox D (2010) The predation cost of female resistance. Behav Ecol 21: 861-867.
54. Miles DB (2004) The race goes to the swift: fitness consequences of variation in sprint performance in juvenile lizards. Evol Ecol Res 6: 63-75.
55. Moreira P, Birkhead TR (2004) Copulatory plug displacement and prolonged copulation in the Iberian rock lizard (Lacerta monticola). Behav Ecol Sociobiol 56: 290-297.
56. Moreira PL, Nunes VL, Martin J, Paulo OS (2007) Copulatory plugs do not assure high first male fertilisation success: sperm displacement in a lizard. Behav Ecol Sociobiol 62: 281-288.
57. Nespolo RF, Scheihing RA, Artacho P (2013) Sexual selection on locomotor performance in the calanoid copepod Tigriopus californicus. Evol Ecol Res 15: 557-566.
58. Nicoletto P (1991) The relationship between male ornamentation and swimming performance in the guppy, Poecilia reticulata. Behav Ecol Sociobiol 28: 365-370.
59. Nicoletto P (1993) Female sexual response to condition-dependent ornaments in the guppy, Poecilia reticulata. Anim Behav 46: 441-450.
60. O'Steen S, Cullum AJ, Bennett AF (2002) Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulata). Evolution 56: 776-784.
61. Olsson M (1993) Male choice for large females and assortative mating for large females in the sand lizard, Lacerta agilis. Behav Ecol Sociobiol 32: 337-341.
62. Olsson M (1995) Forced copulation and costly female resistance behavior in the Lake Eyre dragon, Ctenophorus maculosus. Herpetologica 51: 19-24.
63. Olsson M, Madsen T (1994) Female choice on male quantitative traits in lizards: why is it so rare? Behav Ecol Sociobiol 36: 179-184.
64. Olsson M, Madsen T (1996) Costs of mating with infertile males selects for late emergence in female sand lizards. Copeia 1996: 462-464.
65. Olsson M, Madsen T (1998) Sexual selection and sperm competition in reptiles. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, Cambridge, pp 503-577.
66. Olsson M, Madsen T (2001) Promiscuity in sand lizards (Lacerta agilis) and adder snakes (Vipera berus): causes and consequences. J Hered 92: 190-197.
67. Olsson M, Madsen T, Shine R (1997) Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc R Soc Lond B 264: 455-459.
68. Olsson M, Madsen T, Ujvari B, Wapstra E (2004) Fecundity and MHC affects ejaculation tactics and paternity bias in sand lizards. Evolution 58: 906-909.
69. Olsson M, Schwartz T, Uller T, Healey M (2007) Sons are made from old stores: sperm storage effects on sex ratio in a lizard. Biol Lett 3: 491-493.
70. Orrell KS, Jenssen TA (2002) Male mate choice by the lizard Anolis carolinensis: a preference for novel females. Anim Behav 63: 1091-1102.
71. Pellitteri-Rosa D, Sacchi R, Pupin F, Bellati A, Cocca W, Gentilli A, Galeotti P, Fasola M (2012) Testing the ability to store sperm: an experimental manipulation of mating opportunities in the common wall lizard, Podarcis muralis. Acta Herpetol 7: 111-118.
72. Pitcher TE, Neff BD, Rodd FH, Rowe L (2003) Multiple mating and sequential mate choice in guppies: females trade up. Proc R Soc Lond B 270: 1623-1629.
73. Qvarnström A, Forsgren E (1998) Should females prefer dominant males? Trends Ecol Evol 13: 498-501.
74. Robson MA, Miles DB (2000) Locomotor performance and dominance in tree lizards, Urosaurus ornatus. Funct Ecol 14: 338-344.
75. Salvador A, Díaz JA, Veiga JP, Bloor P, Brown RP (2008) Correlates of reproductive success in male lizards of the alpine species Iberolacerta cyreni. Behav Ecol 19: 169-176.
76. Sinervo B, Svensson E, Comendant T (2000) Density cycles and an offspring quantity and quality game driven by natural selection. Nature 406: 985-988.
77. Stapley J (2008) Female mountain skinks are more likely to mate with males that court more, not males that are dominant. Anim Behav 75: 529-538.
78. Stow AJ, Sunnucks P (2004) Inbreeding avoidance in Cunningham's skinks (Egernia cunninghami) in natural and fragmented habitat. Mol Ecol 13: 443-447.
79. Swierk L, Myers A, Langkilde T (2013) Male mate preference is influenced by both female behaviour and morphology. Anim Behav 85: 1451-1457.
80. Takahashi D, Kohda M (2004) Courtship in fast water currents by a male stream goby. Behav Ecol Sociobiol 55: 431-438.
81. Tang-Martinez Z, Ryder TB (2005) The problem with paradigms: Bateman's worldview as a case study. Integr Comp Biol 45: 821-830.
82. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871-1971. Aldine, Chicago, pp 136-179.
83. Tryanowski P, Hromada M (2005) Do males of the great grey shrike, Lanius excubitor, trade food for extrapair copulations? Anim Behav 69: 529-533.
84. Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17: 2566-2580.
85. Vahed K (1998) The function of nuptial feeding in insects: review of empirical studies. Biol Rev 73: 43-78.
86. Vanhooydonck B, James RS, Tallis J, Aerts P, Tadic Z, Tolley KA, Measey GJ, Herrel A (2014) Is the whole more than the sum of its parts? Evolutionary trade-offs between burst and sustained locomotion in lacertid lizards. Proc R Soc Lond B 281: 20132677.
87. Vitousek MN, Mitchell MA, Woakes AJ, Niemack MD, Wikelski M (2007) High costs of female choice in a lekking lizard. PLoS ONE 6: e567.
88. Wade MJ, Shuster SM (2002) The evolution of parental care in the context of sexual selection: a critical reassessment of parental investment theory. Am Nat 160: 285-292.
89. Wapstra E, Swain R, Jones SM, O'Reilly J (1999) Geographic and annual variation in reproductive cycles in the Tasmanian spotted snow skink, Niveoscincus ocellatus (Squamata: Scincidae). Aust J Zool 47: 539-550.
90. Watkins TB (1996) Predator-mediated selection on burst swimming performance in tadpoles of the Pacific tree frog, Pseudacris regilla. Physiol Zool 69: 154-167.
91. Watson PJ (1991) Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linyphia litigiosa (Linyphiidae). Anim Behav 41: 343-360.
92. Watson PJ, Arnqvist G, Stallmann RR (1998) Sexual conflict and the energetic costs of mating and mate choice in water striders. Am Nat 151: 46-58.
93. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17: 313-320.
94. While GM, Sinn DL, Wapstra E (2008) Female aggression predicts mode of paternity acquisition in a social lizard. Proc R Soc Lond B 276: 2021-2029.
95. White J, Richard M, Massot M, Meylan S (2011) Cloacal bacterial diversity increases with multiple mates: evidence of sexual transmission in female common lizards. PLoS ONE 6: e22339.
96. Wilson RS, James RS, van Damme R (2002) Trade-offs between speed and endurance in the frog Xenopus laevis: a multi-level approach. J Exp Biol 205: 1145-1152.
97. Wilson RS, Condon CH, David G, FitzGibbon SI, Niehaus AC, Pratt K (2010) Females prefer athletes, males fear the disadvantaged: different signals used in female choice and male competition have varied consequences. Proc R Soc Lond B 277: 1923-1928.
98. Zamudio KR, Sinervo B (2000) Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. P Natl Acad Sci USA 97: 14427-14432.