Abstract
Kin selection and dispersal play a critical role in the evolution of cooperative breeding systems. Limited dispersal increases relatedness in spatially structured populations (population viscosity), with the result that neighbours tend to be genealogical relatives. Yet the increase in neighbours’ fitness-related performance through altruistic interaction may also result in habitat saturation and thus exacerbate local competition between kin. Our goal was to detect the footprint of kin selection and competition by examining the spatial structure of relatedness and by comparing non-effective and effective dispersal in a population of a lekking bird, Tetrao urogallus. For this purpose, we analysed capture–recapture and genetic data collected over a 6-year period on a spatially structured population of T. urogallus in France. Our findings revealed a strong spatial structure of relatedness in males. They also indicated that the population viscosity could allow male cooperation through two non-exclusive mechanisms. First, at their first lek attendance, males aggregate in a lek composed of relatives. Second, the distance corresponding to non-effective dispersal dramatically outweighed effective dispersal distance, which suggests that dispersers incur high post-settlement costs. These two mechanisms result in strong population genetic structuring in males. In females, our findings revealed a lower level of spatial structure of relatedness and genetic structure in respect to males. Additionally, non-effective dispersal and effective dispersal distances in females were highly similar, which suggests limited post-settlement costs. These results indicate that kin-dependent dispersal decisions and costs have a genetic footprint in wild populations and are factors that may be involved in the evolution of cooperative courtship.
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References
Alatalo RV, Höglund J, Lundberg A, Sutherland WJ (1992) Evolution of black grouse leks: female preferences benefit males in larger leks. Behav Ecol 3:53–59
Anderson CD, Epperson BK, Fortin MJ, Holderegger R, James P, Rosenberg MS, Scribner KT, Spear S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575
Baguette M, Blanchet S, Legrand D, Stevens VM, Turlure C (2013) Individual dispersal, landscape connectivity and ecological networks. Biol Rev 88:310–326
Beehler BM, Foster MS (1988) Hotshots, hotspots, and female preference in the organization of lek mating systems. Am Nat 131:203–219
Bonte D, Van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle N, Stevens VM, Vandewoestijne S, Baguette M, Barton K, Benton TG, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier CM, Palmer SCF, Turlure C, Travis JMJ (2012) Costs of dispersal. Biol Rev 87:290–312
Bourke AF (2011) The validity and value of inclusive fitness theory. Proc R Soc Lond B Biol Sci 278:3313–3320
Bradbury JW, Gibson RM (1983) Leks and mate choice. In: Batson P (ed) mate choice. Cambridge University Press, Cambridge, pp 109–138
Broquet T, Petit EJ (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol Syst 40:193–216
Bush KL, Aldridge CL, Carpenter JE, Paszkowski CA, Boyce MS, Coltman DW, Scribner KT (2010) Birds of a feather do not always lek together: genetic diversity and kinship structure of greater sage-grouse (Centrocercus urophasianus) in Alberta. Auk 127:343–353
Cayuela H, Pradel R, Joly P, Besnard A (2017) Analysing movement behaviour and dynamic space-use strategies among habitats using multi-event capture-recapture modelling. Methods Ecol Evol 8:1124–1132
Cayuela H, Pradel R, Joly P, Bonnaire E, Besnard A (2018a) Estimating dispersal in spatiotemporally variable environments using multievent capture–recapture modeling. Ecology 99:1150–1163
Cayuela H, Rougemont Q, Prunier JG, Moore JS, Clobert J, Besnard A, Bernatchez L (2018b) Demographic and genetic approaches to study dispersal in wild animal populations: a methodological review. Mol Ecol 27:3976–4010
Choquet R, Lebreton JD, Gimenez O, Reboulet AM, Pradel R (2009a) U-CARE: utilities for performing goodness of fit tests and manipulating CApture–REcapture data. Ecography 32:1071–1074
Choquet R, Rouan L, Pradel R (2009b) Program E-SURGE: a software application for fitting multievent models. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations. Springer, New York, pp 845–865
Clarke AL, Sæther BE, Røskaft E (1997) Sex biases in avian dispersal: a reappraisal. Oikos 79:429–438
Clobert J, Galliard L, Cote J, Meylan S, Massot M (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 12:197–209
Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72
Clutton-Brock T (2009) Cooperation between non-kin in animal societies. Nature 462(7269):51
Concannon MR, Stein AC, Uy JAC (2012) Kin selection may contribute to lek evolution and trait introgression across an avian hybrid zone. Mol Ecol 21:1477–1486
Corander J, Waldmann P, Sillanpää MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163(1):367–374
Cotto O, Kubisch A, Ronce O (2014) Optimal life-history strategy differs between philopatric and dispersing individuals in a metapopulation. Am Nat 183:384–393
Davis DM, Reese KP, Gardner SC, Bird KL (2015) Genetic structure of Greater Sage-Grouse (Centrocercus urophasianus) in a declining, peripheral population. Condor 117:530–544
Dickinson JL, Euaparadorn M, Greenwald K, Mitra C, Shizuka D (2009) Cooperation and competition: nepotistic tolerance and intrasexual aggression in western bluebird winter groups. Anim Behav 77:867–872
DuVal EH (2007) Adaptive advantages of cooperative courtship for subordinate male lance-tailed manakins. Am Nat 169:423–432
Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
El Mouden C, Gardner A (2008) Nice natives and mean migrants: the evolution of dispersal-dependent social behaviour in viscous populations. J Evol Biol 21:1480–1491
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164:1567–1587
Forero MG, Donázar JA, Hiraldo F (2002) Causes and fitness consequences of natal dispersal in a population of black kites. Ecology 83:858–872
Francisco MR, Gibbs HL, Galetti PM Jr (2009) Patterns of individual relatedness at blue manakin (Chiroxiphia caudata) leks. Auk 126:47–53
Gibson RM, Pires D, Delaney KS, Wayne RK (2005) Microsatellite DNA analysis shows that greater sage grouse leks are not kin groups. Mol Ecol 14:4453–4459
Girard P, Angers B (2008) Assessment of power and accuracy of methods for detection and frequency estimation of null alleles. Genetica 134:187–197
Goudet J, Perrin N, Waser P (2002) Tests for sex-biased dispersal using biparentally inherited genetic markers. Mol Ecol 11:1103–1114
Greenwood PJ, Harvey PH (1982) The natal and breeding dispersal of birds. Annu Rev Ecol Syst 13:1–21
Griffin AS, West SA (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302:634–636
Hamilton WD (1964) The genetical evolution of social behaviour. II. J Theor Biol 7:17–52
Hansson B, Bensch S, Hasselquist D (2004) Lifetime fitness of short-and long-distance dispersing great reed warblers. Evolution 58:2546–2557
Hepper PG (ed) (2005) Kin recognition. Cambridge University Press, Cambridge
Hjeljord O, Wegge P, Rolstad J, Ivanova M, Beshkarev AB (2000) Spring-summer movements of male capercaillie Tetrao urogallus: a test of the ‘landscape mosaic’ hypothesis. Wildl Biol 6:251–256
Höglund J (2003) Lek-kin in birds—provoking theory and surprising new results. Ann Zool Fenn 40:249–253
Höglund J, Alatalo RV (2014) Leks. Princeton University Press, Princeton
Höglund J, Shorey L (2003) Local genetic structure in a white-bearded manakin population. Mol Ecol 12(9):2457–2463
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 Biol Sci 266:813–816
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Jombart T, Devillard S, Dufour AB, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94
Kokko H, Johnstone RA (1999) Social queuing in animal societies: a dynamic model of reproductive skew. Proc R Soc Lond B Biol Sci 266:571–578
Kokko H, Lindstrom J (1996) Kin selection and the evolution of leks: whose success do young males maximize? Proc R Soc Lond B Biol Sci 263:919–923
Kokko H, Mackenzie A, Reynolds JD, Lindström J, Sutherland WJ (1999) Measures of inequality are not equal. Am Nat 154:358–382
Komdeur J, Richardson DS, Hatchwell B (2008) Kin-recognition mechanisms in cooperative breeding systems: ecological causes and behavioral consequences of variation. Ecology of social evolution. Springer, Berlin, Heidelberg, pp 175–193
Krakauer AH (2005) Kin selection and cooperative courtship in wild turkeys. Nature 434:69–72
Lagrange P, Pradel R, Bélisle M, Gimenez O (2014) Estimating dispersal among numerous sites using capture–recapture data. Ecology 95:2316–2323
Landguth EL, Cushman SA, Schwartz MK, McKelvey KS, Murphy M, Luikart G (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19(19):4179–4191
Le Galliard JF, Ferrière R, Dieckmann U (2003) The adaptive dynamics of altruism in spatially heterogeneous populations. Evolution 57:1–17
Le Galliard JF, Ferriere R, Dieckmann U (2004) Adaptive evolution of social traits: origin, trajectories, and correlations of altruism and mobility. Am Nat 165:206–224
Lebigre C, Alatalo RV, Forss HE, Siitari H (2008) Low levels of relatedness on black grouse leks despite male philopatry. Mol Ecol 17:4512–4521
Lebigre C, Alatalo RV, Siitari H (2010) Female-biased dispersal alone can reduce the occurrence of inbreeding in black grouse (Tetrao tetrix). Mol Ecol 19:1929–1939
Lebreton JD, Nichols JD, Barker RJ, Pradel R, Spendelow JA (2009) Modeling individual animal histories with multistate capture–recapture models. Adv Ecol Res 41:87–173
Legendre P, Legendre LFJ (1998) Numerical ecology. Elsevier Science B.V, Amsterdam
Loiselle BA, Ryder TB, Duraes R, Tori W, Blake JG, Parker PG (2006) Kin selection does not explain male aggregation at leks of 4 manakin species. Behav Ecol 18:287–291
Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051
Madden JR, Lowe TJ, Fuller HV, Coe RL, Dasmahapatra KK, Amos W, Jury F (2004) Neighbouring male spotted bowerbirds are not related, but do maraud each other. Anim Behav 68:751–758
Matthysen E (2012) Multicausality of dispersal: a review. Dispers Ecol Evol 27:3–18
McDonald DB (2009) Young-boy networks without kin clusters in a lek-mating manakin. Behav Ecol Sociobiol 63:1029–1034
McDonald DB, Potts WK (1994) Cooperative display and relatedness among males in a lek-mating bird. Science 266:1030–1032
Møller AP, Alatalo RV (1999) Good-genes effects in sexual selection. Proc R Soc Lond B Biol Sci 266:85–91
Nystrand M (2007) Associating with kin affects the trade-off between energy intake and exposure to predators in a social bird species. Anim Behav 74:497–506
Paradis E, Baillie SR, Sutherland WJ, Gregory RD (1998) Patterns of natal and breeding dispersal in birds. J Anim Ecol 67(4):518–536
Peterman WE, Connette GM, Semlitsch RD, Eggert LS (2014) Ecological resistance surfaces predict fine-scale genetic differentiation in a terrestrial woodland salamander. Mol Ecol 23:2402–2413
Petrie M, Krupa A, Burke T (1999) Peacocks lek with relatives even in the absence of social and environmental cues. Nature 401:155
Piertney SB, Lambin X, Maccoll AD, Lock K, Bacon PJ, Dallas JF, Leckie F, Mougeot F, Racey PA, Redpath S, Moss R (2008) Temporal changes in kin structure through a population cycle in a territorial bird, the red grouse Lagopus lagopus scoticus. Mol Ecol 17:2544–2551
Platt TG, Bever JD (2009) Kin competition and the evolution of cooperation. Trends Ecol Evol 24:370–377
Pradel R (2005) Multievent: an extension of multistate capture–recapture models to uncertain states. Biometrics 61:442–447
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Prugnolle F, De Meeûs T (2002) Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88:161
Pusey AE (1987) Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2:295–299
Queller DC (1992) A general model for kin selection. Evolution 46:376–380
Regnaut S, Christe P, Chapuisat M, Fumagalli L (2006) Genotyping faeces reveals facultative kin association on capercaillie’s leks. Conserv Genet 7:665–674
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 20:410–415
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253
Rosher C, Favati A, Dean R, Løvlie H (2017) Relatedness and age reduce aggressive male interactions over mating in domestic fowl. Behav Ecol 28:760–766
Segelbacher G, Wegge P, Sivkov AV, Höglund J (2007) Kin groups in closely spaced capercaillie leks. J Ornithol 148:79–84
Shorey L, Piertney S, Stone J, Höglund J (2000) Fine-scale genetic structuring on Manacus manacus leks. Nature 408:352
Sinervo B, Clobert J (2003) Morphs, dispersal behavior, genetic similarity, and the evolution of cooperation. Science 300:1949–1951
Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573
Städele V, Vigilant L (2016) Strategies for determining kinship in wild populations using genetic data. Ecol Evol 6(17):6107–6120
Storch I (1997) Male territoriality, female range use, and spatial organisation of capercaillie Tetrao urogallus leks. Wildl Biol 3(3/4):149–162
Szulkin M, Sheldon BC (2008) Dispersal as a means of inbreeding avoidance in a wild bird population. Proc R Soc Lond B Biol Sci 275:703–711
Tournier E, Besnard A, Tournier V, Cayuela H (2017) Manipulating waterbody hydroperiod affects movement behaviour and occupancy dynamics in an amphibian. Freshw Biol 62:1768–1782
Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Verkuil YI, Juillet C, Lank DB, Widemo F, Piersma T (2014) Genetic variation in nuclear and mitochondrial markers supports a large sex difference in lifetime reproductive skew in a lekking species. Ecol Evol 4:3626–3632
Wang J (2004) Estimating pairwise relatedness from dominant genetic markers. Mol Ecol 13(10):3169–3178
Wang J (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145
Wang J (2012) Computationally efficient sibship and parentage assignment from multilocus marker data. Genetics 191(1):183–194
Wegge P, Finne MH, Rolstad J (2007) GPS satellite telemetry provides new insight into capercaillie Tetrao urogallus brood movements. Wildl Biol 13:87–94
Acknowledgements
The genetic monitoring of capercaillie in the Vosges Mountains was funded by the Life + Project “Des Forêts pour le Grand tetras”, by the Natura2000 network and by the regional programme of the Capercaillie National Action Plan initiated by the French Ministry of Environment. The project largely relied on the work of volunteers who collected samples during the 6 years of the study: Antoine Andre, Didier Arseguel, Samuel Audinot, Alix Badre, Etienne Barbier, Dominique Becker, Bernard Binetruy, Frédéric Bocquenet, Noémie Castaing, Sebastien Coulette, Stéphane Damervalle, Luc Dauphin, Richard Delaunay, Lucile Demaret, Michel Despoulin, Laurent Domergue, Vincent Drillon, Christian Dronneau, Fabien Dupont, Arnaud Foltzer, Patrick Foltzer, Marc Gehin, Cyril Gerard, Maxime Girardin, Remi Grandemange, Jean-Claude Gregy, Joaquim Hatton, Thibaut Hingray, Thierry Hue, Arnaud Hurstel, Jean-Nöel Journot, Fabien Kilque, Lydie Lallement, Christian Lamboley, Manuel Lembke, Jean-Michel Letz, Vincent Lis, Olivier Marchand, Paul Massard, Yvan Mougel, Michel Munier, Louis-Michel Nageleisen, Yvan Nicolas, Christian Oberle, Pascal Perrotey-Doridant, Christian Philipps, François Rey-Demaneuf, Dorian Toussaint, Jean-Marie Triboulot, Bruno Vaxelaire, Laurent Verard, Jean-Lou Zimmermann, and Alice Zimmermann. We also thank Jacob Höglund and the other anonymous referee for their constructive comments that helped to improve the manuscript.
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GJ, JC and HC conceived the ideas and designed methodology. FP and AL collected the data. HC, ML, FF, JGP and LB analysed the data. HC led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
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Communicated by Robert L. Thomson.
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Cayuela, H., Boualit, L., Laporte, M. et al. Kin-dependent dispersal influences relatedness and genetic structuring in a lek system. Oecologia 191, 97–112 (2019). https://doi.org/10.1007/s00442-019-04484-z
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DOI: https://doi.org/10.1007/s00442-019-04484-z