Reproductive isolation between Pogonomyrmex rugosus and two lineages with genetic caste determination.

Hybrid speciation occurs when combination of two interspecific genomes results in individuals that are of high fitness but reproductively incompatible with the parental species. Although hybrid speciation is a relatively common source of new species in plants, it appears to be a much rarer occurrence in animal taxa. Here we report on reproductive isolation and range overlap between the rough harvester ant Pogonomyrmex rugosus and two lineages with hybrid genotypes (H 1 and H2). Both lineages obligately interbreed and produce genetically distinct queen and worker offspring, a phenomenon referred to as genetic caste determination (GCD). Diploid offspring produced by gametes of the same lineage develop only into queens, whereas diploid offspring derived from gametes of distinct lineages develop into workers. We investigated small-scale patterns of gene flow between the parent and the two H lineages by sampling along an 80-km transect between a pure P. rugosus population and a two-lineage population. Microsatellite and mitochondrial markers both indicated virtually no gene flow between the parent species and either lineage even at sites where parental and H-lineage colonies co-occurred. The geographic ranges of the parental species and the two-lineage population were essentially parapatric, with a surprisingly narrow band of overlap and evidence of spatial structuring even at microgeographic scales within the transition zone. This suggests that ecological competition with the parent species plays a significant role in determining the evolutionary persistence and current distribution of the hybrid lineages and the genetic caste system.

[1]  P. Nonacs Interspecific hybridization in ants: at the intersection of ecology, evolution, and behavior. , 2006, Ecology.

[2]  S. Cahan,et al.  Behavioral differences between Pogonomyrmex rugosus and dependent lineage (H1/H2) harvester ants. , 2006, Ecology.

[3]  G. Umphrey Sperm parasitism in ants: selection for interspecific mating and hybridization. , 2006, Ecology.

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

[5]  L. Keller,et al.  Genetic caste determination in Pogonomyrmex harvester ants imposes costs during colony founding , 2006, Journal of evolutionary biology.

[6]  M. Brian Studies of caste differentiation inMyrmica rubra L. , 1954, Insectes Sociaux.

[7]  D. Schwarz,et al.  Host shift to an invasive plant triggers rapid animal hybrid speciation , 2005, Nature.

[8]  L. Rieseberg,et al.  The ecological genetics of homoploid hybrid speciation. , 2005, The Journal of heredity.

[9]  P. Grant Population variation and hybridization: Comparison of finches from two archipelagos , 1994, Evolutionary Ecology.

[10]  M. Brian Studies of caste differentiation in «Myrmica Rubra» L , 1955, Insectes Sociaux.

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

[12]  A. Lowe,et al.  Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae) , 2004, Heredity.

[13]  J. Parker,et al.  A major evolutionary transition to more than two sexes? , 2004, Trends in ecology & evolution.

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

[15]  J. Oettler,et al.  Determinants of intracolonial relatedness in Pogonomyrmex rugosus (Hymenoptera; Formicidae): mating frequency and brood raids , 2003, Molecular ecology.

[16]  E. Louis,et al.  Hybrid Speciation in Experimental Populations of Yeast , 2002, Science.

[17]  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.

[18]  Deborah M. Gordon,et al.  Characterization of polymorphic microsatellite loci in the red harvester ant, Pogonomyrmex barbatus , 2002 .

[19]  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.

[20]  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.

[21]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[22]  Loren H Rieseberg,et al.  The likelihood of homoploid hybrid speciation , 2000, Heredity.

[23]  L. Rieseberg,et al.  Transgressive segregation, adaptation and speciation , 1999, Heredity.

[24]  R. Johnson Foundress survival and brood production in the desert seed-harvester ants Pogonomyrmex rugosus and P. barbatus (Hymenoptera, Formicidae) , 1998, Insectes Sociaux.

[25]  S. Rissing,et al.  An abrupt transition in colony founding behaviour in the ant Messor pergandei , 1998, Animal Behaviour.

[26]  P. David Heterozygosity–fitness correlations: new perspectives on old problems , 1998, Heredity.

[27]  T. Dowling,et al.  The role of hybridization and introgression in the diversification of animals , 1997 .

[28]  Loren H. Rieseberg,et al.  Hybrid Origins of Plant Species , 1997 .

[29]  D. Soltis,et al.  DISCORDANCE BETWEEN NUCLEAR AND CHLOROPLAST PHYLOGENIES IN THE HEUCHERA GROUP (SAXIFRAGACEAE) , 1995, Evolution; international journal of organic evolution.

[30]  R. Vrijenhoek Unisexual Fish: Model Systems for Studying Ecology and Evolution , 1994 .

[31]  M. Arnold,et al.  ECOLOGICAL AND GENETIC ASSOCIATIONS IN AN IRIS HYBRID ZONE , 1993, Evolution; international journal of organic evolution.

[32]  B. Tabashnik,et al.  Gene flow accelerates local adaptation among finite populations: simulating the evolution of insecti , 1992 .

[33]  A. Templeton MECHANISMS OF SPECIATION­ A POPULATION GENETIC APPROACH , 1981 .

[34]  M. Nei,et al.  Estimation of average heterozygosity and genetic distance from a small number of individuals. , 1978, Genetics.

[35]  V. Grant,et al.  POLLINATION SYSTEMS AS ISOLATING MECHANISMS IN ANGIOSPERMS , 1949, Evolution; international journal of organic evolution.