Advertisement

Behavioral Ecology and Sociobiology

, Volume 70, Issue 9, pp 1457–1465 | Cite as

No behavioural response to kin competition in a lekking species

  • Christophe LebigreEmail author
  • Catherine Timmermans
  • Carl D. Soulsbury
Original Article

Abstract

The processes of kin selection and competition may occur simultaneously if limited individual dispersal, i.e. population viscosity, is the only cause of the interactions between kin. Therefore, the net indirect benefits of a specific behaviour may largely depend on the existence of mechanisms dampening the fitness costs of competing with kin. Because of female preference for large aggregations, males in lekking species may gain indirect fitness benefits by displaying with close relatives. At the same time, kin selection may also lead to the evolution of mechanisms that dampen the costs of kin competition. As this mechanism has largely been ignored to date, we used detailed behavioural and genetic data collected in the black grouse Lyrurus tetrix to test whether males mitigate the costs of kin competition through the modulation of their fighting behaviours according to kinship and the avoidance of close relatives when establishing a lek territory. We found that neighbouring males’ fighting behaviour was unrelated to kinship and males did not avoid settling with close relatives on leks. As males’ current and future mating success are strongly related to their behaviour on the lek (including fighting behaviour and territory position), the costs of kin competition may be negligible relative to the direct benefits of successful male-male contests. As we previously showed that the indirect fitness benefits of group membership were very limited in this black grouse population, these behavioural data support the idea that direct fitness benefits gained by successful male-male encounters likely outbalance any indirect fitness benefits.

Significance statement

Kin selection might be involved in the formation of groups because the fitness benefits of increasing group size can be accrued when groups hold close relatives. However, the fitness costs of competing with kin could counter-balance these indirect fitness benefits unless mechanisms enabling individuals to limit kin competition. Here we show in a lekking species that males do not modulate their fight frequency and intensity according to their kinship and do not avoid establishing territories with closely related neighbours. As the indirect fitness benefits of group display were very small in this system and as this study shows that males do not show any sign of kin competition avoidance, the indirect effects associated with male group display are likely to be very small.

Keywords

Dominance Indirect fitness benefits Kin selection Kin competition Territoriality Sexual selection Sociality 

Notes

Acknowledgments

This paper is dedicated to Prof. Rauno Veli Alatalo who passed away on November 9th 2012. We thank Jefferson Graves, Matti Kervinen and two anonymous reviewers for their insightful comments on previous versions of this manuscript. We are grateful to Elina Virtanen, Juho Niva, Anssi Lipponen, Sami Kyröläinen and Henna Ojaniemi for their help in the lab. This project was founded by the Academy of Finland (grant nos. 7211271 and 7119165) and a fellowship of the Belgian Fond National pour la Recherche Scientifique (FNRS). Part of the statistical analysis was conducted within the SMCS (Support en Méthodologie et Calcul Statistique – Université Catholique de Louvain).

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This work was carried out with the permission of Central Finland Environmental Centre and the Animal Care Committee of the University of Jyväskylä (permissions KSU-2003-L-25/254 and KSU-2002-L-4/254). This article does not contain any studies with human participants performed by any of the authors.

Conflict of interest

CL declares that he has no conflict of interest. CT declares that she has no conflict of interest. CDS declares that he has no conflict of interest.

Funding

This study was funded by the Academy of Finland (grant numbers 7211271 and 7119165), the Finnish Centre of Excellence in Evolutionary Research (211271), and the Fond National de la Recherche Scientifique (FNRS A4/5 - MCF/DM).

Supplementary material

265_2016_2154_MOESM1_ESM.docx (102 kb)
ESM 1 (DOCX 101 kb)

References

  1. Alatalo RV, Höglund J, Lundberg A (1991) Lekking in the black grouse - A test of male viability. Nature 352:155–156Google Scholar
  2. Alatalo RV, Höglund J, Lundberg A, Sutherland WJ (1992) Evolution of black grouse leks: female preferences benefit males in larger leks. Behav Ecol 3:53–59CrossRefGoogle Scholar
  3. Alizon S, Taylor P (2008) Empty sites can promote altruistic behavior. Evolution 62:1335–1344CrossRefPubMedGoogle Scholar
  4. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  5. Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399CrossRefGoogle Scholar
  6. Bitume EV, Bonte D, Ronce O, Bach F, Flaven E, Olivieri I, Nieberding CM (2013) Density and genetic relatedness increase dispersal distance in a subsocial organism. Ecol Lett 16:430–437CrossRefPubMedGoogle Scholar
  7. Bouzat JL, Johnson K (2004) Genetic structure among closely spaced leks in a peripheral population of lesser prairie-chickens. Mol Ecol 13:499–505CrossRefPubMedGoogle Scholar
  8. Briffa M, Sneddon LU (2007) Physiological constraints on contest behaviour. Funct Ecol 21:627–637CrossRefGoogle Scholar
  9. Brown GE, Brown JA (1996) Kin discrimination in salmonids. Rev Fish Biol Fisher 6:201–219CrossRefGoogle Scholar
  10. Caizergues A, Ellison LN (2002) Natal dispersal and its consequences in Black Grouse Tetrao tetrix. Ibis 144:478–487CrossRefGoogle Scholar
  11. Culp M (2011) Spa: a semi-supervised R package for semi-parametric graph-based estimation. J Stat Softw 40:1–29CrossRefGoogle Scholar
  12. Edenbrow M, Croft DP (2012) Kin and familiarity influence association preferences and aggression in the mangrove killifish Kryptolebias marmoratus. J Fish Biol 80:503–518CrossRefPubMedGoogle Scholar
  13. Fiske P, Rintamäki PT, Karvonen E (1998) Mating success in lekking males: a meta-analysis. Behav Ecol 9:328–338CrossRefGoogle Scholar
  14. Gibson RM, Pirs D, Delaney KS, Wayne RK (2005) Microsatellite DNA analysis shows that greater sage grouse leks are not kin groups. Mol Ecol 14:4453–4459CrossRefPubMedGoogle Scholar
  15. Gosling LM, Petrie M, Rainy ME (1987) Lekking in topi: a high cost, specialist strategy. Anim Behav 35:616–618CrossRefGoogle Scholar
  16. Grafen A (2006) Optimization of inclusive fitness. J Theor Biol 238:541–563CrossRefPubMedGoogle Scholar
  17. Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21CrossRefGoogle Scholar
  18. Hämäläinen A, Alatalo RV, Lebigre C, Siitari H, Soulsbury CD (2012) Fighting behaviour as a correlate of male mating success in black grouse Tetrao tetrix. Behav Ecol Sociobiol 66:1577–1586CrossRefGoogle Scholar
  19. Hamilton WD (1964) The genetical evolution of social behaviour I & II. J Theor Biol 7:1–52CrossRefPubMedGoogle Scholar
  20. Hatchwell BJ (2010) Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology 116:203–216CrossRefGoogle Scholar
  21. Höglund J (2003) Lek-kin in birds—provoking theory and surprising new results. Ann Zool Fenn 40:249–253Google Scholar
  22. Höglund J, Alatalo RV (1995) Leks. Princeton University Press, PrincetonCrossRefGoogle Scholar
  23. Höglund J, Alatalo RV, Lundberg A, Ratti O (1994) Context-dependent effects of tail-ornament damage on mating success in black grouse. Behav Ecol 5:182–187CrossRefGoogle Scholar
  24. Höglund J, Alatalo RV, Lundberg A, Rintamäki PT, Lindell J (1999) Microsatellite markers reveal the potential for kin selection on black grouse leks. Proc R Soc Lond B 266:813–816CrossRefGoogle Scholar
  25. Höglund J, Johansson T, Pelabon C (1997) Behaviourally mediated sexual selection: characteristics of successful male black grouse. Anim Behav 54:255–264CrossRefGoogle Scholar
  26. Höglund J, Kålås JA, Fiske P (1992) The costs of secondary sexual characters in the lekking great snipe (Gallinago media). Behav Ecol Sociobiol 30:309–315CrossRefGoogle Scholar
  27. Höner OP, Wachter B, East ML, Streich WJ, Wilhelm K, Burke T, Hofer H (2007) Female mate-choice drives the evolution of male-biased dispersal in a social mammal. Nature 448:798–801CrossRefPubMedGoogle Scholar
  28. Hood GM (2011) PopTools version 3.2.5, http://www.poptools.org
  29. Hovi M, Alatalo RV, Höglund J, Lundberg A, Rintamäki PT (1994) Lek centre attracts black grouse females. Proc R Soc Lond B 258:303–305CrossRefGoogle Scholar
  30. Hsu Y, Earley RL, Wolf LL (2006) Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol Rev 81:33–74CrossRefPubMedGoogle Scholar
  31. Isvaran K, Ponkshe A (2013) How general is a female mating preference for clustered males in lekking species? A meta-analysis. Anim Behav 86:417–425CrossRefGoogle Scholar
  32. Kervinen M, Alatalo RV, Lebigre C, Siitari H, Soulsbury CD (2012) Determinants of yearling male lekking effort and mating success in black grouse (Tetrao tetrix). Behav Ecol 23:1209–1217Google Scholar
  33. Kervinen M, Lebigre C, Alatalo RV, Siitari H, Soulsbury CD (2015) Life history differences in age-dependent expressions of multiple ornaments and behaviors in a lekking bird. Am Nat 185:13–27CrossRefPubMedGoogle Scholar
  34. Kervinen M, Lebigre C, Soulsbury CD (2016) Simultaneous age-dependent and age-independent sexual selection in the lekking black grouse (Lyrurus tetrix). J Anim Ecol 85:715–725CrossRefPubMedGoogle Scholar
  35. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38CrossRefGoogle Scholar
  36. Kokko H, Lindström J (1996) Kin selection and the evolution of leks: whose success do young males maximize? Proc R Soc Lond B 263:919–923CrossRefGoogle Scholar
  37. Kokko H, Lindström J, Alatalo RV, Rintamäki PT (1997) Queuing for territory positions in the lekking black grouse (Tetrao tetrix). Behav Ecol 9:376–383CrossRefGoogle Scholar
  38. Kokko H, Rintamäki PT, Alatalo RV, Höglund J, Karvonen E, Lundberg A (1999) Female choice selects for lifetime lekking performance in black grouse males. Proc R Soc Lond B 266:2109–2115CrossRefGoogle Scholar
  39. Komdeur J (1994) The effect of kinship on helping in the cooperative breeding Seychelles warbler (Acrocephalus sechellensis). Proc R Soc Lond B 256:47–52CrossRefGoogle Scholar
  40. Koprowski JL (1996) Natal philopatry, communal nesting, and kinship in fox squirrels and gray squirrels. J Mammal 77:1006–1016CrossRefGoogle Scholar
  41. Krakauer AH (2005) Kin selection and cooperative courtship in wild turkeys. Nature 434:69–72CrossRefPubMedGoogle Scholar
  42. Krützen M, Sherwin WB, Barre LM, Connor RC, Van de Casteele T, Mann J, Brooks R (2003) Contrasting relatedness patterns in bottlenose dolphins (Tursiops sp.) with different alliance strategies. Proc R Soc Lond B 270:497–502CrossRefGoogle Scholar
  43. Lebigre C, Alatalo RV, Forss HE, Siitari H (2008) Low levels of relatedness on black grouse leks despite male philopatry. Mol Ecol 17:4512–4521CrossRefPubMedGoogle Scholar
  44. Lebigre C, Alatalo RV, Kilpimaa J, Staszewski V, Siitari H (2012) Leucocyte counts variation and measures of male fitness in the lekking black grouse. J Ornithol 153:95–102CrossRefGoogle Scholar
  45. Lebigre C, Alatalo RV, Siitari H (2010) Female-biased dispersal alone can reduce the occurrence of inbreeding in black grouse. Mol Ecol 19:1929–1939CrossRefPubMedGoogle Scholar
  46. Lebigre C, Alatalo RV, Siitari H (2013) Physiological costs enforce the honesty of lek display in the black grouse (Tetrao tetrix). Oecologia 172:983–993CrossRefPubMedGoogle Scholar
  47. Lebigre C, Alatalo RV, Siitari H, Parri S (2007) Restrictive mating by females on black grouse leks. Mol Ecol 16:4380–4389CrossRefPubMedGoogle Scholar
  48. Lebigre C, Alatalo RV, Soulsbury CD, Höglund J, Siitari H (2014) Limited indirect fitness benefits of male group membership in a lekking species. Mol Ecol 23:5356–5365CrossRefPubMedGoogle Scholar
  49. Lion S, Gandon S (2009) Habitat saturation and the spatial evolutionary ecology of altruism. J Evol Biol 22:1487–1502CrossRefPubMedGoogle Scholar
  50. Loiselle BA, Ryder TB, Durães R, Tori W, Blake JG, Parker PG (2007) Kin selection does not explain male aggregation at leks of 4 manakin species. Behav Ecol 18:287–291CrossRefGoogle Scholar
  51. MacColl ADC, Piertney SB, Moss R, Lambin X (2000) Spatial arrangement of kin affects recruitment success in young male red grouse. Oikos 90:261–270CrossRefGoogle Scholar
  52. Magaña M, Alonso JC, Palacín C (2011) Age-related dominance helps reduce male aggressiveness in great bustard leks. Anim Behav 82:203–211CrossRefGoogle Scholar
  53. McElligott AG, Gammell MP, Harty HC, Paini DR, Murphy DT, Walsh JT, Hayden TJ (2001) Sexual size dimorphism in fallow deer (Dama dama): Do larger, heavier males gain greater mating success? Behav Ecol Sociobiol 49:266–272CrossRefGoogle Scholar
  54. McElligott AG, Naulty F, Clarke WV, Hayden TJ (2003) The somatic cost of reproduction: what determines reproductive effort in prime-aged fallow bucks? Evol Ecol Res 5:1239–1250Google Scholar
  55. Mitteldorf J, Wilson DS (2000) Population viscosity and the evolution of altruism. J Theor Biol 204:481–496CrossRefPubMedGoogle Scholar
  56. Moore JC, Loggenberg A, Greeff JM (2006) Kin competition promotes dispersal in a male pollinating fig wasp. Biol Lett 2:17–19Google Scholar
  57. Parker GA, Sutherland WJ (1986) Ideal free distributions when individuals differ in competitive ability: phenotype-limited ideal free models. Anim Behav 34:1222–1242CrossRefGoogle Scholar
  58. Piertney SB, Lambin X, Maccoll ADC et al (2008) Temporal changes in kin structure through a population cycle in a territorial bird, the red grouse Lagopus lagopus scoticus. Mol Ecol 17:2544–2551CrossRefPubMedGoogle Scholar
  59. Piertney SB, MacColl ADC, Lambin X, Moss R, Dallas JF (1999) Spatial distribution of genetic relatedness in a moorland population of red grouse (Lagopus lagopus scoticus). Biol J Linn Soc 68:317–331CrossRefGoogle Scholar
  60. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1-108, https://cran.r-project.org/web/packages/nlme/index.html
  61. Pravosudova EV, Grubb TC, Parker PG (2001) The influence of kinship on nutritional condition and aggression levels in winter social groups of Tufted Titmice. Condor 103:821–828CrossRefGoogle Scholar
  62. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  63. R Core Development Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/ Google Scholar
  64. Reeve HK, Westneat DF, Noon WA, Sherman PW, Aquadro CF (1990) DNA ‘fingerprinting’ reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. Proc Natl Acad Sci U S A 87:2496–2500CrossRefPubMedPubMedCentralGoogle Scholar
  65. Reynolds SM, Christman MC, Uy JAC, Patricelli GL, Braun MJ, Borgia G (2009) Lekking satin bowerbird males aggregate with relatives to mitigate aggression. Behav Ecol 20:410–415CrossRefGoogle Scholar
  66. Rintamäki PT, Höglund J, Alatalo RV, Lundberg A (2001) Correlates of male mating success on black grouse (Tetrao tetrix L.) leks. Ann Zool Fenn 38:99–109Google Scholar
  67. Russell AF, Hatchwell BJ (2001) Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate. Proc R Soc Lond B 268:2169–2174CrossRefGoogle Scholar
  68. Segelbacher G, Wegge P, Sivkov AV, Höglund J (2007) Kin groups in closely spaced capercaillie leks. J Ornithol 148:79–84CrossRefGoogle Scholar
  69. Shorey L, Piertney SB, Stone J, Höglund J (2000) Fine-scale genetic structuring on Manacus manacus leks. Nature 408:352–353CrossRefPubMedGoogle Scholar
  70. Silk JB (2002) Kin selection in primate groups. Int J Primatol 23:849–875CrossRefGoogle Scholar
  71. Smith JE, Van Horn RC, Powning KS, Cole AR, Graham KE, Memenis SK, Holekamp KE (2010) Evolutionary forces favoring intragroup coalitions among spotted hyenas and other animals. Behav Ecol 21:284–303CrossRefGoogle Scholar
  72. Taylor P (1992) Altruism in viscous populations—an inclusive fitness model. Evol Ecol 6:352–356CrossRefGoogle Scholar
  73. Templeton CN, Reed VA, Campbell SE, Beecher MD (2012) Spatial movements and social networks in juvenile male song sparrows. Behav Ecol 23:141–152CrossRefPubMedGoogle Scholar
  74. Van Dyken JD (2010) The components of kin competition. Evolution 64:2840–2854PubMedPubMedCentralGoogle Scholar
  75. Vehrencamp SL, Bradbury JW, Gibson RM (1989) The energetic cost of display in male sage grouse. Anim Behav 38:885–896CrossRefGoogle Scholar
  76. Wahaj SA, Van Horn RC, Van Horn TL, Dreyer R, Hilgris R, Schwarz J, Holekamp KE (2004) Kin discrimination in the spotted hyena (Crocuta crocuta): nepotism among siblings. Behav Ecol Sociobiol 56:237–247CrossRefGoogle Scholar
  77. Warren PK, Baines D (2002) Dispersal, survival and causes of mortality in black grouse Tetrao tetrix in northern England. Wildlife Biol 8:91–97Google Scholar
  78. West Eberhard MJ (1975) The evolution of social behavior by kin selection. Q Rev Biol 50:1–33Google Scholar
  79. Wilson DS, Pollock G, Dugatkin L (1992) Can altruism evolve in purely viscous populations? Evol Ecol 6:331–341CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Christophe Lebigre
    • 1
    Email author
  • Catherine Timmermans
    • 2
    • 3
    • 4
  • Carl D. Soulsbury
    • 3
  1. 1.Earth and Life InstituteCatholic University of LouvainLouvain-la-NeuveBelgium
  2. 2.Institute of Statistics, Biostatistics and Actuarial SciencesCatholic University of LouvainLouvain-la-NeuveBelgium
  3. 3.Joseph Banks Laboratories, School of Life SciencesUniversity of LincolnLincolnUK
  4. 4.Department of MathematicsUniversity of LiègeLiègeBelgium

Personalised recommendations