Immigration prevents inbreeding in a growing colony of a long‐lived and philopatric seabird

Mating between close relatives can have deleterious effects on reproductive success or offspring fitness, which should favour the evolution of active or passive inbreeding avoidance mechanisms. In birds, evidence for active inbreeding avoidance by kin-discriminative mate choice is scarce; many studies describe random mating in relation to kinship and thus support passive inbreeding avoidance by natal dispersal. However, most studies were conducted in island populations of short-lived passerines with fast alternation of generations. In this study, we present inbreeding estimates based on pedigree data from a 16-year study in a coastal colony of Common Terns Sterna hirundo, a long-lived seabird with delayed sexual maturation and low rates of extra-pair paternity. Incestuous mating was rare (four of 2387 pairs), even if partially accounting for incomplete pedigrees. Although the average relatedness of observed pairs was lower than would be expected from random pairing, the inbreeding coefficient did not differ from random mating. Hence, we found no clear evidence for active inbreeding avoidance by kin-discriminative mate choice, and the low level of inbreeding seems to be related to the high immigration rate in the colony and thus to be maintained passively by dispersal.

[1]  L. Keller,et al.  Inbreeding effects in wild populations. , 2002 .

[2]  Sewall Wright,et al.  Coefficients of Inbreeding and Relationship , 1922, The American Naturalist.

[3]  P. Parker,et al.  Long-term isolation of a highly mobile seabird on the Galapagos , 2011, Proceedings of the Royal Society B: Biological Sciences.

[4]  B. C. Glass,et al.  Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data , 2004, Heredity.

[5]  L. Kruuk,et al.  Severe inbreeding depression in collared flycatchers (Ficedula albicollis) , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  J. Pemberton Measuring inbreeding depression in the wild: the old ways are the best. , 2004, Trends in ecology & evolution.

[7]  B. Sheldon,et al.  Inbreeding avoidance under different null models of random mating in the great tit. , 2009, The Journal of animal ecology.

[8]  U. Steiner,et al.  Reproductive consequences of natal dispersal in a highly philopatric seabird , 2005 .

[9]  B. Sheldon,et al.  Inbreeding depression along a life‐history continuum in the great tit , 2007, Journal of evolutionary biology.

[10]  P. Grant,et al.  INBREEDING IN DARWIN'S MEDIUM GROUND FINCHES (GEOSPIZA FORTIS) , 1989, Evolution; international journal of organic evolution.

[11]  H. Weimerskirch,et al.  Surviving with low genetic diversity: the case of albatrosses , 2007, Proceedings of the Royal Society B: Biological Sciences.

[12]  P. Becker,et al.  Is Divorce in Young Common Terns, Sterna hirundo, after Recruitment just a Question of Timing? , 2007 .

[13]  Derek A Roff,et al.  Inbreeding depression in the wild , 1999, Heredity.

[14]  L. Keller INBREEDING AND ITS FITNESS EFFECTS IN AN INSULAR POPULATION OF SONG SPARROWS (MELOSPIZA MELODIA) , 1998, Evolution; international journal of organic evolution.

[15]  P. Becker,et al.  The hurdle of recruitment: Influences of arrival date, colony experience and sex in the common tern Sterna hirundo , 2003 .

[16]  C. Wernham The migration atlas : movements of the birds of Britain and Ireland , 2002 .

[17]  K. Byrne,et al.  Heterozygosity, inbreeding and neonatal traits in Soay sheep on St Kilda , 2005, Molecular ecology.

[18]  Shinichi Nakagawa,et al.  ‘O sibling, where art thou?’‐ a review of avian sibling recognition with respect to the mammalian literature , 2004, Biological reviews of the Cambridge Philosophical Society.

[19]  B. Sheldon,et al.  Dispersal as a means of inbreeding avoidance in a wild bird population , 2008, Proceedings of the Royal Society B: Biological Sciences.

[20]  G. Pasinelli,et al.  Inbreeding in red-cockaded woodpeckers: Effects of natal dispersal distance and territory location , 2006 .

[21]  Zuleyma Tang-Martinez,et al.  The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation , 2001, Behavioural Processes.

[22]  I. Jamieson,et al.  The imprecision of heterozygosity‐fitness correlations hinders the detection of inbreeding and inbreeding depression in a threatened species , 2011, Molecular ecology.

[23]  B. Hatchwell,et al.  Kin recognition: function and mechanism in avian societies. , 1999, Trends in ecology & evolution.

[24]  J. González‐Solís,et al.  Divorce and asynchronous arrival in common terns, Sterna hirundo , 1999, Animal Behaviour.

[25]  M. Wink,et al.  Population sex ratio shift from fledging to recruitment: consequences for demography in a philopatric seabird , 2008 .

[26]  Peter H. Becker,et al.  A new application for transponders in population ecology of the Common Tern , 1997 .

[27]  J. González‐Solís,et al.  Courtship feedings, copulations and paternity in common terns, Sterna hirundo , 2001, Animal Behaviour.

[28]  P. Becker,et al.  Supply and demand: causes and consequences of assortative mating in common terns Sterna hirundo , 2008, Behavioral Ecology and Sociobiology.

[29]  P. Becker,et al.  What do pairing patterns in common tern, Sterna hirundo, recruits reveal about the significance of sex and breeding experience? , 2005, Behavioral Ecology and Sociobiology.

[30]  V. Bretagnolle,et al.  Natal Philopatry and Close Inbreeding in Cory's Shearwater (Calonectris diomedea) , 1998 .

[31]  H. Weimerskirch,et al.  The seabird paradox: dispersal, genetic structure and population dynamics in a highly mobile, but philopatric albatross species , 2008, Molecular ecology.

[32]  P. Becker,et al.  Dispersal decisions: common terns, Sterna hirundo, choose between colonies during prospecting , 2005, Animal Behaviour.

[33]  W. Reid Age correlations within pairs of breeding birds , 1988 .

[34]  T. C. Marshall,et al.  Estimating the prevalence of inbreeding from incomplete pedigrees , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  F. Balloux,et al.  Does heterozygosity estimate inbreeding in real populations? , 2004, Molecular ecology.

[36]  E. Matthysen,et al.  Seasonal and lifetime reproductive consequences of inbreeding in the great tit Parus major , 2003 .

[37]  J. Piedrafita,et al.  Pedigree analysis of eight Spanish beef cattle breeds , 2003, Genetics Selection Evolution.

[38]  J. Merilä,et al.  Multilocus heterozygosity and inbreeding in the Siberian jay , 2009, Conservation Genetics.

[39]  L. Lehmann,et al.  Inbreeding Avoidance through Kin Recognition: Choosy Females Boost Male Dispersal , 2003, The American Naturalist.

[40]  V. Bretagnolle,et al.  GENETIC RELATIONSHIPS OF CORY'S SHEARWATER: PARENTAGE, MATING ASSORTMENT, AND GEOGRAPHIC DIFFERENTIATION REVEALED BY DNA FINGERPRINTING , 2000 .

[41]  L. Keller,et al.  No Evidence for Inbreeding Avoidance in a Natural Population of Song Sparrows (Melospiza melodia) , 1998, The American Naturalist.

[42]  D. Coltman,et al.  PARASITE‐MEDIATED SELECTION AGAINST INBRED SOAY SHEEP IN A FREE‐LIVING ISLAND POPULATON , 1999, Evolution; international journal of organic evolution.

[43]  A. J. Noordwijk,et al.  INBREEDING IN AN ISLAND POPULATION OF THE GREAT TIT , 1981, Evolution; international journal of organic evolution.

[44]  R. Frankham Do island populations have less genetic variation than mainland populations? , 1997, Heredity.

[45]  J. R. Chapman,et al.  A quantitative review of heterozygosity–fitness correlations in animal populations , 2009, Molecular ecology.

[46]  J. Díez,et al.  Using pedigree information to monitor genetic variability of endangered populations: the Xalda sheep breed of Asturias as an example , 2003 .

[47]  A. Pusey Sex-biased dispersal and inbreeding avoidance in birds and mammals. , 1987, Trends in ecology & evolution.

[48]  B. Grant,et al.  Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G. scandens) , 2004, Heredity.

[49]  Dispersal, kinship and inbreeding in an island population of the Great Tit , 1988 .

[50]  M. Wink,et al.  Influences of sex, sex composition of brood and hatching order on mass growth in common terns Sterna hirundo , 2003, Behavioral Ecology and Sociobiology.

[51]  J. Aparicio,et al.  Increase of heterozygosity in a growing population of lesser kestrels , 2007, Biology Letters.

[52]  N. Taylor,et al.  Inbreeding coefficient and heterozygosity–fitness correlations in unhatched and hatched song sparrow nestmates , 2010, Molecular ecology.

[53]  J. Pemberton,et al.  Wild pedigrees: the way forward , 2008, Proceedings of the Royal Society B: Biological Sciences.

[54]  H. Kokko,et al.  Why some species of birds do not avoid inbreeding: insights from New Zealand robins and saddlebacks , 2009 .

[55]  C. Ritland,et al.  Inbreeding in Japanese quail estimated by pedigree and microsatellite analyses. , 2007, The Journal of heredity.

[56]  J. Dale,et al.  Individual recognition: it is good to be different. , 2007, Trends in ecology & evolution.

[57]  I. Jamieson Founder Effects, Inbreeding, and Loss of Genetic Diversity in Four Avian Reintroduction Programs , 2011, Conservation biology : the journal of the Society for Conservation Biology.

[58]  P. VanRaden,et al.  Accounting for Inbreeding and Crossbreeding in Genetic Evaluation of Large Populations , 1992 .

[59]  A. J. Noordwijk,et al.  Genealogical evidence for random mating in a natural population of the great tit (Parus major L.) , 1985, Naturwissenschaften.

[60]  Baumung Roswitha,et al.  Pedigree and marker information requirements to monitor genetic variability , 2003, Genetics Selection Evolution.

[61]  A. Pusey,et al.  Inbreeding avoidance in animals. , 1996, Trends in ecology & evolution.

[62]  R. Mauck,et al.  Asymmetrical incest avoidance in the choice of social and genetic mates , 2006, Animal Behaviour.

[63]  B. Grant,et al.  ENVIRONMENTAL CONDITIONS AFFECT THE MAGNITUDE OF INBREEDING DEPRESSION IN SURVIVAL OF DARWIN'S FINCHES , 2002, Evolution; international journal of organic evolution.

[64]  S. Bensch,et al.  No evidence for inbreeding avoidance in a great reed warbler population , 2007 .

[65]  T. Clutton‐Brock,et al.  Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. , 2010, Trends in ecology & evolution.

[66]  L. Keller,et al.  Inbreeding and Loss of Genetic Variation in a Reintroduced Population of Mauritius Kestrel , 2008, Conservation biology : the journal of the Society for Conservation Biology.

[67]  Léa Riffaut,et al.  Population genetics of the common guillemot Uria aalge in the North Atlantic: geographic impact of oil spills , 2005 .

[68]  Peter Arcese,et al.  Selection against inbred song sparrows during a natural population bottleneck , 1994, Nature.

[69]  I. Jamieson,et al.  Moderate inbreeding depression in a reintroduced population of North Island robins , 2007 .

[70]  S. L. Burson Population genetics and gene flow of the common tern , 1990 .

[71]  J. Coulson,et al.  Measuring immigration and philopatry in seabirds; recruitment to Black‐legged Kittiwake colonies , 2007 .

[72]  F. Goyache,et al.  A note on ENDOG: a computer program for analysing pedigree information. , 2005, Journal of animal breeding and genetics = Zeitschrift fur Tierzuchtung und Zuchtungsbiologie.