Nature versus nurture in social insect caste differentiation.

Recent evidence for genetic effects on royal and worker caste differentiation from diverse social insect taxa has put an end to the view that these phenotypes stem solely from a developmental switch controlled by environmental factors. Instead, the relative influences of genotypic and environmental effects on caste vary among species, ranging from largely environmentally controlled phenotypes to almost purely genetic systems. Disentangling the selective forces that generate variation for caste predisposition will require characterizing the genetic mechanisms underlying this variation, and identifying particular life-history strategies and kin structures associated with strong genetic effects on caste.

[1]  L. Keller,et al.  Two alternate mechanisms contribute to the persistence of interdependent lineages in Pogonomyrmex harvester ants , 2007, Molecular ecology.

[2]  L. Keller,et al.  Genetic Compatibility Affects Queen and Worker Caste Determination , 2008, Science.

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

[4]  L. Keller,et al.  Clonal reproduction by males and females in the little fire ant , 2005, Nature.

[5]  L. Keller,et al.  Selfish genes: a green beard in the red fire ant , 1998, Nature.

[6]  J. Seger,et al.  Kinship and covariance. , 1981, Journal of theoretical biology.

[7]  D. Cassill Yoyo-bang: a risk-aversion investment strategy by a perennial insect society , 2002, Oecologia.

[8]  S. Vinson,et al.  Interspecific Hybridization and Caste Specificity of Protein in Fire Ant , 1977, Science.

[9]  U. Mueller,et al.  Thelytokous Parthenogenesis in the Fungus-Gardening Ant Mycocepurus smithii (Hymenoptera: Formicidae) , 2009, PloS one.

[10]  M. Haydak Larval Food and Development of Castes in the Honeybee , 1943 .

[11]  E. Hasegawa,et al.  Clonal reproduction by males of the ant Vollenhovia emeryi (Wheeler) , 2008 .

[12]  S. Higashi,et al.  Mating frequency, genetic structure, and sex ratio in the intermorphic female producing ant species Myrmecina nipponica , 2000 .

[13]  Laurent Keller,et al.  Maternal Effect on Female Caste Determination in a Social Insect , 2008, Current Biology.

[14]  Charles D. Michener,et al.  The Social Behavior of the Bees , 1974 .

[15]  J. Fewell,et al.  Modeling the Maintenance of a Dependent Lineage System: The Influence of Positive Frequency-Dependent Selection on Sex Ratio , 2009, Evolution; international journal of organic evolution.

[16]  L. Keller,et al.  Complex hybrid origin of genetic caste determination in harvester ants , 2003, Nature.

[17]  V. Imperatriz-Fonseca,et al.  Caste Development, Reproductive Strategies, and Control of Fertility in Honey Bees and Stingless Bees , 1990 .

[18]  S. Cahan,et al.  REPRODUCTIVE DIVISION OF LABOR BETWEEN HYBRID AND NONHYBRID OFFSPRING IN A FIRE ANT HYBRID ZONE , 2003, Evolution; international journal of organic evolution.

[19]  N. Franks,et al.  Social Evolution in Ants , 2019 .

[20]  W. E. Kerr EVOLUTION OF THE MECHANISM OF CASTE DETERMINATION IN THE GENUS MELIPONA , 1950 .

[21]  F. Ratnieks Heirs and spares: caste conflict and excess queen production in Melipona bees , 2001, Behavioral Ecology and Sociobiology.

[22]  Deborah M. Gordon,et al.  Genetic basis for queen–worker dimorphism in a social insect , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Steven W. Rissing,et al.  Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  R. Kucharski,et al.  Nutritional Control of Reproductive Status in Honeybees via DNA Methylation , 2008, Science.

[25]  John H. Werren,et al.  The role of selfish genetic elements in eukaryotic evolution , 2001, Nature Reviews Genetics.

[26]  N. Lo,et al.  Should Environmental Caste Determination Be Assumed for Termites? , 2009, The American Naturalist.

[27]  M. Wade,et al.  Genes with Social Effects are Expected to Harbor More Sequence Variation within and Between Species , 2009, Evolution; international journal of organic evolution.

[28]  L. Keller,et al.  Male reproductive success: paternity contribution to queens and workers in Formica ants , 1997, Behavioral Ecology and Sociobiology.

[29]  W. E. Kerr Genetic Determination of Castes in the Genus Melipona. , 1950, Genetics.

[30]  N. Weaver Effects of Larval Age on Dimorphic Differentiation of the Female Honey Bee , 1957 .

[31]  L. Keller,et al.  Sex Ratio Conflict and Worker Production in Eusocial Hymenoptera , 2001, The American Naturalist.

[32]  J. Cornuet,et al.  Sperm competition and last-male precedence in the honeybee , 2002, Animal Behaviour.

[33]  F. Ratnieks,et al.  Kin conflict over caste determination in social Hymenoptera , 1999, Behavioral Ecology and Sociobiology.

[34]  A. Buschinger,et al.  Genetically Mediated Queen Polymorphism and Caste Determination in the Slave-making Ant, Harpagoxenus sublaevis (Hymenoptera: Formicidae) , 1986 .

[35]  mith,et al.  The causes and consequences of genetic caste determination in ants (Hymenoptera: Formicidae) , 2008 .

[36]  K. Matsuura,et al.  Queen Succession Through Asexual Reproduction in Termites , 2009, Science.

[37]  H. Hepburn,et al.  Rare royal families in honeybees, Apis mellifera , 2005, Naturwissenschaften.

[38]  A. Estoup,et al.  Sex and clonality in the little fire ant. , 2007, Molecular biology and evolution.

[39]  Fachbereich Biologie-Zoologie DER POLYMORPHISMUS DER SKLAVENHALTENDEN AMEISE HARPAGOXENUS SUBLAEVIS (NYL.) , 1975 .

[40]  B. Oldroyd,et al.  Possible causes of reproductive dominance during emergency queen rearing by honeybees , 1999, Animal Behaviour.

[41]  A. Moczek,et al.  The basis of bee‐ing different: the role of gene silencing in plasticity , 2008, Evolution & development.

[42]  J. Heinze,et al.  Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi , 2006, Biology Letters.

[43]  L. Keller,et al.  Loss of Phenotypic Plasticity Generates Genotype-Caste Association in Harvester Ants , 2004, Current Biology.

[44]  W. Engels,et al.  Social Insects: An Evolutionary Approach to Castes and Reproduction , 2011 .

[45]  N. Lo,et al.  Sex-Linked Genetic Influence on Caste Determination in a Termite , 2007, Science.

[46]  S. Aron,et al.  Evolution: No-Male's Land for an Amazonian Ant , 2009, Current Biology.

[47]  J. Boomsma,et al.  Genetic royal cheats in leaf-cutting ant societies , 2008, Proceedings of the National Academy of Sciences.

[48]  T. Linksvayer DIRECT, MATERNAL, AND SIBSOCIAL GENETIC EFFECTS ON INDIVIDUAL AND COLONY TRAITS IN AN ANT , 2006, Evolution; international journal of organic evolution.

[49]  R. Crozier 6 – Genetics of Sociality , 1979 .

[50]  R. Crozier,et al.  Genetic Intrigues. (Book Reviews: Evolution of Social Insect Colonies. Sex Allocation and Kin Selection.) , 1997 .

[51]  K. Hartfelder,et al.  Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees , 2006 .

[52]  M. Asencot,et al.  The effect of sugars and juvenile hormone on the differentiation of the female honeybee larvae (Apis mellifera L.) to queens. , 1976, Life sciences.

[53]  C. Noirot,et al.  Caste differentiation in social insects. , 1985 .

[54]  J. Heinze Habitat structure, dispersal strategies and queen number in two boreal Leptothorax ants , 1993, Oecologia.

[55]  R. Shuel,et al.  The early establishment of dimorphism in the female honeybee,Apis mellifera L. , 1960, Insectes Sociaux.

[56]  Caste and ecology in the social insects , 1979 .

[57]  T. Wenseleers,et al.  Queen execution and caste conflict in the stingless bee Melipona beecheii , 2004 .

[58]  M. White,et al.  Animal cytology and evolution. , 1955 .

[59]  P. Kryger,et al.  Competition for royalty in bees , 1996, Nature.

[60]  S. Aron,et al.  Thelytokous parthenogenesis and its consequences on inbreeding in an ant , 2006, Heredity.

[61]  F. Ratnieks,et al.  Patriline differences in emergency queen rearing in the honey bee, Apis mellifera , 2003, Insectes Sociaux.

[62]  T. Seeley The honey bee colony as a superorganism. , 1989 .

[63]  A. Suarez,et al.  Caste Determination in a Polymorphic Social Insect: Nutritional, Social, and Genetic Factors , 2008, The American Naturalist.

[64]  G. Robinson,et al.  Genetic and genomic analyses of the division of labour in insect societies , 2008, Nature Reviews Genetics.

[65]  U. Winter,et al.  Der Polymorphismus der sklavenhaltenden AmeiseHarpagoxenus sublaevis (Nyl.) , 1975, Insectes Sociaux.

[66]  M. Wade,et al.  Genetic caste determination in harvester ants: possible origin and maintenance by cyto-nuclear epistasis. , 2006, Ecology.

[67]  D. Queller Models of kin selection on seed provisioning , 1984, Heredity.

[68]  S. Aron,et al.  Local resource competition and sex ratio in the ant Cataglyphis cursor , 2006 .

[69]  A. Saura,et al.  Cytology and evolution in parthenogenesis , 1987 .

[70]  M. Brian 5 – Caste Differentiation and Division of Labor , 1979 .

[71]  J. Strassmann,et al.  Caste totipotency and conflict in a large–colony social insect , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[72]  R. Crozier,et al.  Evolution of social insect colonies , 1996 .

[73]  J. Takahashi,et al.  Absence of reproductive conflict during queen rearing in Apis cerana , 2009, Insectes Sociaux.

[74]  Regulation of Reproduction , 1998 .

[75]  U. Mueller,et al.  No sex in fungus-farming ants or their crops , 2009, Proceedings of the Royal Society B: Biological Sciences.

[76]  F. Ratnieks,et al.  Tragedy of the commons in Melipona bees , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[77]  Jürgen Gadau,et al.  Genetic determination of the queen caste in an ant hybrid zone , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[78]  A. Buschinger,et al.  Queen polymorphism inLeptothorax spec. A: Its genetic and ecological background (Hymenoptera: Formicidae) , 1989, Insectes Sociaux.

[79]  L. Keller,et al.  Reproductive specialization in multiple-queen colonies of the ant Formica exsecta , 2007 .

[80]  L. Keller,et al.  Characterization and distribution of Pogonomyrmex harvester ant lineages with genetic caste determination , 2006, Molecular ecology.

[81]  J. Fewell,et al.  Distribution and evolution of genetic caste determination in Pogonomyrmex seed-harvester ants. , 2006, Ecology.

[82]  L. Keller,et al.  Conditional Use of Sex and Parthenogenesis for Worker and Queen Production in Ants , 2004, Science.

[83]  B. Oldroyd,et al.  Unequal subfamily proportions among honey bee queen and worker brood , 1997, Animal Behaviour.

[84]  Diana E. Wheeler,et al.  Developmental and Physiological Determinants of Caste in Social Hymenoptera: Evolutionary Implications , 1986, The American Naturalist.

[85]  J. Heinze,et al.  A heritable component in sex ratio and caste determination in a Cardiocondyla ant , 2009, Frontiers in Zoology.

[86]  M. Goodisman,et al.  Lack of conflict during queen production in the social wasp Vespula maculifrons , 2007, Molecular ecology.

[87]  K. Ross,et al.  Regulation of Reproduction in Eusocial Hymenoptera , 1985 .

[88]  Jean-Marie Cornuet,et al.  Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[89]  M W Bruford,et al.  Parentage, reproductive skew and queen turnover in a multiple–queen ant analysed with microsatellites , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.