Host–parasite coevolution and the stability of genetic kin recognition

Significance Kin selection theory predicts that individuals should evolve to help their relatives. However, Crozier’s paradox suggests that using genetic markers (tags) to recognize relatives will be evolutionarily unstable. The problem is that more common tags are more likely to be recognized and helped. This causes common tags to increase in frequency, eliminating the genetic variability needed for genetic kin recognition. It has been hypothesized that the genetic variability could be maintained if recognition alleles have an additional role in parasite resistance. We show that the host–parasite coevolution hypothesis does not work as expected because it often causes tags to fluctuate to high frequencies. However, host–parasite coevolution can maintain tag diversity at another (neutral) locus by genetic hitchhiking, resolving Crozier’s paradox.

[1]  S. West,et al.  Multiple social encounters can eliminate Crozier’s paradox and stabilise genetic kin recognition , 2022, Nature Communications.

[2]  J. Ågren The Gene's-Eye View of Evolution , 2021 .

[3]  A. Gardner,et al.  Kin discrimination and demography modulate patterns of sexual conflict , 2020, Nature Ecology & Evolution.

[4]  B. Hatchwell,et al.  Kith or Kin? Familiarity as a Cue to Kinship in Social Birds , 2020, Frontiers in Ecology and Evolution.

[5]  A. Gardner,et al.  Does kin discrimination promote cooperation? , 2020, Biology Letters.

[6]  J. Wolf,et al.  Greenbeard Genes: Theory and Reality. , 2019, Trends in ecology & evolution.

[7]  S. West,et al.  Adaptation is maintained by the parliament of genes , 2019, Nature Communications.

[8]  A. Griffin,et al.  Honest signaling and the double counting of inclusive fitness , 2019, Evolution letters.

[9]  J. Strassmann,et al.  Evolutionary Conflict , 2018, Annual Review of Ecology, Evolution, and Systematics.

[10]  J. Field,et al.  Crozier’s Effect and the Acceptance of Intraspecific Brood Parasites , 2018, Current Biology.

[11]  S. West,et al.  Modeling relatedness and demography in social evolution , 2018, Evolution Letters.

[12]  J. Flanagan,et al.  The Integrative Review. , 2018, International journal of nursing knowledge.

[13]  R. Beynon,et al.  The Genetic Basis of Kin Recognition in a Cooperatively Breeding Mammal , 2015, Current Biology.

[14]  O. Gilbert Histocompatibility as Adaptive Response to Discriminatory Within-Organism Conflict: A Historical Model , 2015, The American Naturalist.

[15]  T. Linksvayer,et al.  Crozier’s paradox revisited: maintenance of genetic recognition systems by disassortative mating , 2013, BMC Evolutionary Biology.

[16]  A. Gardner,et al.  Adaptation and Inclusive Fitness , 2013, Current Biology.

[17]  Jonathan Wright,et al.  Bell miner provisioning calls are more similar among relatives and are used by helpers at the nest to bias their effort towards kin , 2011, Proceedings of the Royal Society B: Biological Sciences.

[18]  J. Strassmann,et al.  Kin discrimination and cooperation in microbes. , 2011, Annual review of microbiology.

[19]  D. Queller,et al.  Expanded social fitness and Hamilton's rule for kin, kith, and kind , 2011, Proceedings of the National Academy of Sciences.

[20]  Rafael D. Rosengarten,et al.  Model Systems of Invertebrate Allorecognition , 2011, Current Biology.

[21]  R. Beynon,et al.  Making progress in genetic kin recognition among vertebrates , 2010, Journal of biology.

[22]  S. Paterson,et al.  How effective is recognition of siblings on the basis of genotype? , 2009, Journal of evolutionary biology.

[23]  G. Shaulsky,et al.  Polymorphic Members of the lag Gene Family Mediate Kin Discrimination in Dictyostelium , 2009, Current Biology.

[24]  M. Salathé,et al.  The role of epistasis on the evolution of recombination in host-parasite coevolution. , 2009, Theoretical population biology.

[25]  Bruce Waldman,et al.  Self-referent MHC type matching in frog tadpoles , 2008, Proceedings of the Royal Society B: Biological Sciences.

[26]  M. Salathé,et al.  The Red Queen and the persistence of linkage-disequilibrium oscillations in finite and infinite populations , 2007, BMC Evolutionary Biology.

[27]  F. Rousset,et al.  CONSTRAINTS ON THE ORIGIN AND MAINTENANCE OF GENETIC KIN RECOGNITION , 2007, Evolution; international journal of organic evolution.

[28]  A. Gardner,et al.  Social Evolution: The Decline and Fall of Genetic Kin Recognition , 2007, Current Biology.

[29]  Susan A Dudley,et al.  Kin recognition in an annual plant , 2007, Biology Letters.

[30]  A. D. Peters,et al.  Short‐ and long‐term benefits and detriments to recombination under antagonistic coevolution , 2007, Journal of evolutionary biology.

[31]  M. Hossaert-McKey,et al.  Kin discrimination in juvenile mandrills, Mandrillus sphinx , 2007, Animal Behaviour.

[32]  Andy Gardner,et al.  The Relation between Multilocus Population Genetics and Social Evolution Theory , 2006, The American Naturalist.

[33]  G. Shaulsky,et al.  Social evolution: Kin preference in a social microbe , 2006, Nature.

[34]  V. Jansen,et al.  Altruism through beard chromodynamics , 2006, Nature.

[35]  M. Strand,et al.  Host resistance and the evolution of kin recognition in polyembryonic wasps , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  Ross A Hammond,et al.  ALTRUISM VIA KIN‐SELECTION STRATEGIES THAT RELY ON ARBITRARY TAGS WITH WHICH THEY COEVOLVE , 2004, Evolution; international journal of organic evolution.

[37]  S. Otto,et al.  Species Interactions and the Evolution of Sex , 2004, Science.

[38]  C. Lively,et al.  Modelling infection as a two-step process combining gene-for-gene and matching-allele genetics , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  A. D. Peters,et al.  The Red Queen and Fluctuating Epistasis: A Population Genetic Analysis of Antagonistic Coevolution , 1999, The American Naturalist.

[40]  S. Siller Foundations of Social Evolution , 1999, Heredity.

[41]  M. Grahn,et al.  MHC and kin discrimination in juvenile Arctic charr, Salvelinus alpinus (L.) , 1998, Animal Behaviour.

[42]  C. Lively,et al.  HOST‐PARASITE COEVOLUTION: EVIDENCE FOR RARE ADVANTAGE AND TIME‐LAGGED SELECTION IN A NATURAL POPULATION , 1998, Evolution; international journal of organic evolution.

[43]  M. Feldman,et al.  LONG-TERM EVOLUTION, SHORT-TERM EVOLUTION, AND POPULATION GENETIC THEORY , 1998 .

[44]  A. Solovy Theory and reality. , 1998, Hospitals & health networks.

[45]  P. Hammerstein Streetcar Theory and Long-Term Evolution , 1996, Science.

[46]  Steven A. Frank,et al.  Models of Parasite Virulence , 1996, The Quarterly Review of Biology.

[47]  N. Barton,et al.  A general model for the evolution of recombination. , 1995, Genetical research.

[48]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[49]  Jerram L. Brown,et al.  Kin Recognition and the Major Histocompatibility Complex: An Integrative Review , 1994, The American Naturalist.

[50]  S. Frank A kin selection model for the evolution of virulence , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  W. Potts,et al.  Communal nesting patterns in mice implicate MHC genes in kin recognition , 1992, Nature.

[52]  Peter D. Taylor,et al.  Inclusive fitness in a homogeneous environment , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[53]  P. Taylor Altruism in viscous populations — an inclusive fitness model , 1992, Evolutionary Ecology.

[54]  S. Frank,et al.  Models of plant-pathogen coevolution. , 1992, Trends in genetics : TIG.

[55]  D. Queller,et al.  A GENERAL MODEL FOR KIN SELECTION , 1992, Evolution; international journal of organic evolution.

[56]  W. Hamilton,et al.  Sexual reproduction as an adaptation to resist parasites (a review). , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[57]  A. Grafen Do animals really recognize kin? , 1990, Animal Behaviour.

[58]  R. Crozier GENETIC CLONAL RECOGNITION ABILITIES IN MARINE INVERTEBRATES MUST BE MAINTAINED BY SELECTION FOR SOMETHING ELSE , 1986, Evolution; international journal of organic evolution.

[59]  Alan Grafen,et al.  A geometric view of relatedness , 1985 .

[60]  W. Hamilton Sex versus non-sex versus parasite , 1980 .

[61]  W. Hamilton The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[62]  W. Hamilton The genetical evolution of social behaviour. II. , 1964, Journal of theoretical biology.

[63]  F. Rousset Genetic Structure and Selection in Subdivided Populations (MPB-40) , 2013 .

[64]  Mathieu Lihoreau,et al.  Kin recognition via cuticular hydrocarbons shapes cockroach social life , 2009 .

[65]  D. Queller,et al.  Genetic relatedness in viscous populations , 2005, Evolutionary Ecology.

[66]  D. Penn The scent of genetic compatibility: Sexual selection and the major histocompatibility complex , 2002 .

[67]  N. Barton,et al.  Genetic hitchhiking. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[68]  J. Haigh,et al.  The hitch-hiking effect of a favourable gene. , 1974, Genetical research.