Cryptic species of fig-pollinating wasps: Implications for the evolution of the fig–wasp mutualism, sex allocation, and precision of adaptation

Fig-pollinating wasps have provided model systems for developing and testing theories of the evolution of mutualism, sex allocation, and precision of adaptation. With few exceptions, previous studies have assumed one species of pollinator wasp per host fig species. Here we report genetic data demonstrating the coexistence of previously undetected cryptic fig wasp species in at least half of the host fig species surveyed. The substantial mitochondrial sequence differences (4.2–6.1%) imply old divergences (≈1.5–5.1 million years ago) among these species. Furthermore, some cryptic species pairs seem to be sister taxa, whereas others clearly are not, indicating both long-term coexistence on shared hosts and the colonization of novel fig species. These findings undermine the prevalent notion of strict one-to-one specificity between cospeciating figs and their pollinators, thereby challenging existing theory concerning the evolution and stability of mutualisms. Moreover, the incorporation of the genetic information significantly improves the fit of the observed sex ratios to predictions of local mate-competition theory, further strengthening support for sex allocation theory and the precision of adaptation.

[1]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[2]  O. Pellmyr,et al.  Yuccas, yucca moths, and coevolution: A review , 2003 .

[3]  L. Keller,et al.  Species‐diagnostic microsatellite loci for the fig wasp genus Pegoscapus , 2002 .

[4]  J. Young,et al.  Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest , 2002, Molecular ecology.

[5]  J. Cook,et al.  Revision of the Australian species of Pleistodontes (Hymenoptera: Agaonidae) fig-pollinating wasps and their host-plant associations , 2002 .

[6]  G. Bush,et al.  Speciation in fig pollinators and parasites , 2002, Molecular ecology.

[7]  C. Simon,et al.  PHYLOGEOGRAPHY OF THE NEW ZEALAND CICADA MAORICICADA CAMPBELLI BASED ON MITOCHONDRIAL DNA SEQUENCES: ANCIENT CLADES ASSOCIATED WITH CENOZOIC ENVIRONMENTAL CHANGE , 2001, Evolution; international journal of organic evolution.

[8]  Elliott Sober,et al.  Adaptationism and Optimality , 2001 .

[9]  C. A. Machado,et al.  Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  Douglas W. Yu Parasites of mutualisms , 2001 .

[11]  Douglas W. Yu Regular ArticleParasites of mutualisms , 2001 .

[12]  G. Weiblen Phylogenetic relationships of fig wasps pollinating functionally dioecious Ficus based on mitochondrial DNA sequences and morphology. , 2001, Systematic biology.

[13]  Brian D. Farrell,et al.  Evolutionary assembly of the milkweed fauna: cytochrome oxidase I and the age of Tetraopes beetles. , 2001, Molecular phylogenetics and evolution.

[14]  A. Caccone,et al.  MOLECULAR BIOGEOGRAPHY OF CAVE LIFE: A STUDY USING MITOCHONDRIAL DNA FROM BATHYSCIINE BEETLES , 2001, Evolution; international journal of organic evolution.

[15]  A. Rodrigo,et al.  Likelihood-based tests of topologies in phylogenetics. , 2000, Systematic biology.

[16]  J. Zimmerman Tropical Forest Ecology , 2000 .

[17]  B. Charlesworth Levels of Selection in Evolution , 2000, Heredity.

[18]  K. Ganeshaiah,et al.  What fig wasp sex ratios may or may not , 1999 .

[19]  C. Kerdelhué,et al.  Molecular phylogeny of the Ceratosolen species pollinating Ficus of the subgenus Sycomorus sensu stricto: biogeographical history and origins of the species-specificity breakdown cases. , 1999, Molecular phylogenetics and evolution.

[20]  U. Mueller,et al.  The evolution of mutualisms: exploring the paths between conflict and cooperation. , 1999, Trends in ecology & evolution.

[21]  E. Herre,et al.  STABILIZING SELECTION AND VARIANCE IN FIG WASP SEX RATIOS , 1998, Evolution; international journal of organic evolution.

[22]  S. West,et al.  Conflict of interest in a mutualism: documenting the elusive fig wasp–seed trade–off , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  N. Knowlton,et al.  Landscape ecology of algal symbionts creates variation in episodes of coral bleaching , 1997, Nature.

[24]  C. A. Machado,et al.  Molecular phylogenies of figs and their pollinator wasps , 1996 .

[25]  M. Anstett,et al.  Resource allocation: a conflict in the fig/fig wasp mutualism? , 1996 .

[26]  S. Carrière,et al.  Exceptions to the one:one relationship between African fig trees and their fig wasp pollinators: possible evolutionary scenarios , 1996 .

[27]  J. Leebens-Mack,et al.  Non-mutualistic yucca moths and their evolutionary consequences , 1996, Nature.

[28]  Eörs Szathmáry,et al.  The Major Transitions in Evolution , 1997 .

[29]  A. Brower Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Clegg,et al.  The physiological significance of metabolite channeling: an idea whose time has come. , 1991, Journal of theoretical biology.

[31]  S. Compton,et al.  Studies of Ceratosolen galili, a Non-Pollinating Agaonid Fig Wasp' , 1991 .

[32]  E. Corner Wayside trees of Malaya , 1991 .

[33]  J. Bull,et al.  Distinguishing mechanisms for the evolution of co-operation. , 1991, Journal of theoretical biology.

[34]  H. Kishino,et al.  Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea , 1989, Journal of Molecular Evolution.

[35]  J. Bronstein,et al.  The fig/pollinator mutualism: A model system for comparative biology , 1989, Experientia.

[36]  C. C. Berg Classification and distribution ofFicus , 1989, Experientia.

[37]  E. Herre,et al.  Coevolution of reproductive characteristics in 12 species of New World figs and their pollinator wasps , 1989, Experientia.

[38]  E. Herre,et al.  Optimality, plasticity and selective regime in fig wasp sex ratios , 1987, Nature.

[39]  E. Herre,et al.  Sex Ratio Adjustment in Fig Wasps , 1985, Science.

[40]  W. Hamilton,et al.  The evolution of cooperation. , 1984, Science.

[41]  Daniel H. Janzen,et al.  How to be a Fig , 1979 .

[42]  J. T. Wiebes,et al.  CO-EVOLUTION OF FIGS AND THEIR INSECT POLLINATORS , 1979 .

[43]  M. Nei,et al.  Mathematical model for studying genetic variation in terms of restriction endonucleases. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[44]  W. Hamilton Extraordinary Sex Ratios , 1967 .

[45]  G. Weiblen How to be a fig wasp. , 2002, Annual review of entomology.

[46]  T. Yahara,et al.  Effects of time-dependent competition for oviposition sites on clutch sizes and offspring sex ratios in a fig wasp , 2002 .

[47]  L. Keller Levels of selection in evolution , 1999 .

[48]  F. Maytag Evolution , 1996, Arch. Mus. Informatics.

[49]  L. Maesen,et al.  The Biodiversity of African Plants , 1996, Springer Netherlands.

[50]  J. Wiebes,et al.  African fig trees and fig wasps , 1992 .

[51]  S. Compton A collapse of host specificity in some African fig wasps. , 1990 .

[52]  T. E. Moore,et al.  Sexual Selection and Reproductive Competition in Insects , 1979 .

[53]  B. Ramírez,et al.  Coevolution of Ficus and Agaonidae , 1974 .