Population differentiation in female sex pheromone and male preferences in a solitary bee

Population differentiation in female mating signals and associated male preferences can drive reproductive isolation among segregated populations. We tested this assumption by investigating intraspecific variation in female sex pheromone and associated male odour preferences among distant populations in the solitary bee Colletes cunicularius (L.) by using quantitative gas chromatography and by performing field bioassays with synthetic blends of key sex pheromone compounds. We found significant differences in sex pheromone blends among the bee populations, and the divergence in odour blends correlated positively with geographic distance, suggesting that genetic divergence among distant populations can affect sex pheromone chemistry. Our behavioural experiments, however, demonstrate that synthetic copies of allopatric female sex pheromones were cross-attractive to patrolling males from distant populations, making reproductive isolation by non-recognition of mating signals among populations unlikely. Our data also show that patrolling male bees from different populations preferred odour types from allopatric populations at the two sites of bioassays. These male preferences are not expected to select for changes in the female sex pheromone, but may influence the evolution of floral odour in sexually deceptive orchids of the genus Ophrys that are pollinated by C. cunicularius males.

[1]  M. Ayasse,et al.  Mating expenditures reduced via female sex pheromone modulation in the primitively eusocial halictine bee, Lasioglossum (Evylaeus) malachurum (Hymenoptera: Halictidae) , 1999, Behavioral Ecology and Sociobiology.

[2]  L. Simmons Kin recognition and its influence on mating preferences of the field cricket, Gryllus bimaculatus (de Geer) , 1989, Animal Behaviour.

[3]  J. Boughman How sensory drive can promote speciation , 2002 .

[4]  D S Jordan,et al.  THE ORIGIN OF SPECIES THROUGH ISOLATION. , 1905, Science.

[5]  W. Wcislo Attraction and learning in mate-finding by solitary bees, Lasioglossum (Dialictus) figueresi Wcislo and Nomia triangulifera Vachal (Hymenoptera : Halictidae) , 1992, Behavioral Ecology and Sociobiology.

[6]  W. Potts,et al.  Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. , 1993, Trends in genetics : TIG.

[7]  C. Löfstedt,et al.  Attraction of male turnip mothsAgrotis segetum (Lepidoptera: Noctuidae) to sex pheromone components and their mixtures at 11 sites in Europe, Asia, and Africa , 1992, Journal of Chemical Ecology.

[8]  William J. Bell,et al.  Chemical Ecology of Insects , 1985, Springer US.

[9]  N. Vereecken,et al.  Cuticular Hydrocarbons as Sex Pheromone of the Bee Colletes cunicularius and the Key to its Mimicry by the Sexually Deceptive Orchid, Ophrys exaltata , 2005, Journal of Chemical Ecology.

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

[11]  C. Boake Sexual Signaling and Speciation, a Microevolutionary Perspective , 2002, Genetica.

[12]  A. Matheson Forage for Bees in an Agricultural Landscape , 1994 .

[13]  F. Schiestl On the success of a swindle: pollination by deception in orchids , 2005, Naturwissenschaften.

[14]  T. Tscharntke,et al.  Plant-insect interactions in fragmented landscapes. , 2004, Annual review of entomology.

[15]  K. Dettner,et al.  CHEMICAL MIMICRY AND CAMOUFLAGE , 1994 .

[16]  O. Larsen,et al.  Vibration and sound communication in solitary bees and wasps , 1986 .

[17]  J. Antonovics The effects of a heterogeneous environment on the genetics of natural populations. , 1971, American Scientist.

[18]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[19]  F. Schiestl,et al.  Floral evolution and pollinator mate choice in a sexually deceptive orchid , 2003, Journal of evolutionary biology.

[20]  C. Löfstedt Moth Pheromone Genetics and Evolution , 1993 .

[21]  M. Breed,et al.  The Chemical Basis for Nestmate Recognition and Mate Discrimination in Social Insects , 1995 .

[22]  B. Smith,et al.  Kin-based male mating preferences in two species of halictine bee , 1987, Behavioral Ecology and Sociobiology.

[23]  T. Tregenza,et al.  Sexual selection and speciation. , 2001, Trends in ecology & evolution.

[24]  Achim Gathmann,et al.  Foraging ranges of solitary bees , 2002 .

[25]  A. Borg-Karlson,et al.  (S)-(+)-Linalool, a Mate Attractant Pheromone Component in the Bee Colletes cunicularius , 2004, Journal of Chemical Ecology.

[26]  DOES SELECTION ON FLORAL ODOR PROMOTE DIFFERENTIATION AMONG POPULATIONS AND SPECIES OF THE SEXUALLY DECEPTIVE ORCHID GENUS OPHRYS? , 2005, Evolution; international journal of organic evolution.

[27]  H. Noyes,et al.  Male sex pheromones and the phylogeographic structure of the Lutzomyia longipalpis species complex (Diptera: Psychodidae) from Brazil and Venezuela. , 2005, American Journal of Tropical Medicine and Hygiene.

[28]  J. Cane,et al.  Pheromonal cues direct mate-seeking behavior of maleColletes cunicularius (Hymenoptera: Colletidae) , 1981, Journal of Chemical Ecology.

[29]  P. Hedrick,et al.  Genetic Polymorphism in Heterogeneous Environments , 1976 .

[30]  F. Clarke,et al.  Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[31]  J. Neff,et al.  Floral Rewards: Alternatives to Pollen and Nectar , 1981 .

[32]  C. Löfstedt,et al.  Pheromone variation among eastern European and a western Asian population of the turnip mothAgrotis segetum , 1990, Journal of Chemical Ecology.

[33]  H. R. Koepfer SELECTION FOR SEXUAL ISOLATION BETWEEN GEOGRAPHIC FORMS OF DROSOPHILA MOJAVENSIS. II. EFFECTS OF SELECTION OF MATING PREFERENCE AND PROPENSITY , 1987, Evolution; international journal of organic evolution.

[34]  W. Roelofs,et al.  Individual variation in sex pheromone component ratios in two populations of the redbanded leafroller moth, Argyrotaenia velutinana. , 1980 .

[35]  John R. G. Turner,et al.  The Evolution of Mimicry: A Solution to the Problem of Punctuated Equilibrium , 1988, The American Naturalist.

[36]  J. David,et al.  VARIATIONS IN CUTICULAR HYDROCARBONS AMONG THE EIGHT SPECIES OF THE DROSOPHILA MELANOGASTER SUBGROUP , 1987, Evolution; international journal of organic evolution.

[37]  D. Liang,et al.  “You are what you eat”: Diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile , 2000, Naturwissenschaften.

[38]  C. Löfstedt,et al.  Pheromone dialects in European turnip moths Agrotis segetum , 1986 .

[39]  M. Breed Animal Signals.Oxford Series in Ecology and Evolution.ByJohn Maynard Smithand, David Harper.Oxford and New York: Oxford University Press. $99.50 (hardcover); $44.50 (paper). ix + 166 p; ill.; index. ISBN: 0–19–852684–9 (hc); 0–19–852685–7 (pb). 2003. , 2005 .

[40]  Eran Pichersky,et al.  Biology of floral scent , 2006 .

[41]  T. Markow,et al.  COURTSHIP BEHAVIOR AND CONTROL OF REPRODUCTIVE ISOLATION IN DROSOPHILA MOJAVENSIS , 1989, Evolution; international journal of organic evolution.

[42]  J. Knudsen,et al.  Floral scents-a checklist of volatile compounds isolated by head-space techniques , 1993 .

[43]  G. C. Eickwort,et al.  FORAGING AND MATING BEHAVIOR IN APOIDEA , 1980 .

[44]  D. Schluter,et al.  The Ecology of Adaptive Radiation , 2000 .

[45]  E. Pichersky,et al.  New Perspectives in Pollination Biology: Floral Fragrances. A day in the life of a linalool molecule: Chemical communication in a plant‐pollinator system. Part 1: Linalool biosynthesis in flowering plants , 1999 .

[46]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[47]  J. Tengö,et al.  The effects of temperature and body size on the mating pattern of a gregariously nesting bee, Colletes cunicularius (Hymenoptera: Colletidae) , 1989 .

[48]  M. Ayasse,et al.  Mating behavior and chemical communication in the order Hymenoptera. , 2001, Annual review of entomology.

[49]  J. Barker,et al.  Ecological and Evolutionary Genetics of Drosophila , 1990, Monographs in Evolutionary Biology.

[50]  J. Millar,et al.  GEOGRAPHIC VARIATION IN THE PHEROMONE SYSTEM OF THE SATURNIID MOTHHEMILEUCA EGLANTERINA , 2001 .

[51]  S. Wright,et al.  Isolation by Distance. , 1943, Genetics.

[52]  T. Markow,et al.  Temperature Effects on Epicuticular Hydrocarbons and Sexual Isolation in Drosophila mojavensis , 1990 .

[53]  K. C. Spencer,et al.  Chemical Mediation of Coevolution , 1990 .

[54]  J. Gershenzon,et al.  The Chemical Diversity of Floral Scent , 2020, Biology of Plant Volatiles.

[55]  S. Wakamura,et al.  Geographical variation in female sex pheromones of the rice leaffolder moth, Cnaphalocrocis medinalis: identification of pheromone components in Japan , 2000 .

[56]  J. Keogh,et al.  Mate recognition in a freshwater fish: geographical distance, genetic differentiation, and variation in female preference for local over foreign males , 2004, Journal of evolutionary biology.

[57]  R. Peakall,et al.  A mark-recapture study of male Colletes cunicularius bees: implications for pollination by sexual deception , 2004, Behavioral Ecology and Sociobiology.

[58]  T. Markow SEXUAL ISOLATION AMONG POPULATIONS OF DROSOPHILA MOJAVENSIS , 1991, Evolution; international journal of organic evolution.

[59]  W. Etges PREMATING ISOLATION IS DETERMINED BY LARVAL SUBSTRATES IN CACTOPHILIC DROSOPHILA MOJAVENSIS , 1992, Evolution; international journal of organic evolution.

[60]  W. Etges,et al.  Premating Isolation Is Determined by Larval‐Rearing Substrates in Cactophilic Drosophila mojavensis. V. Deep Geographic Variation in Epicuticular Hydrocarbons among Isolated Populations* , 2001, The American Naturalist.

[61]  J. Klun Insect sex pheromones: intraspecific pheromonal variability of Ostrinia nubilalis in North America and Europe. , 1975 .

[62]  U. Candolin The use of multiple cues in mate choice , 2003, Biological reviews of the Cambridge Philosophical Society.

[63]  M. Kohn You Are What You Eat , 1999, Science.

[64]  G. Bergström,et al.  Linalool in mandibular gland secretion ofColletes bees (Hymenoptera: Apoidea) , 1978, Journal of Chemical Ecology.

[65]  A. Rooney,et al.  Evolution of moth sex pheromones via ancestral genes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[66]  H. R. Koepfer SELECTION FOR SEXUAL ISOLATION BETWEEN GEOGRAPHIC FORMS OF DROSOPHILA MOJAVENSIS. I. INTERACTIONS BETWEEN THE SELECTED FORMS , 1987, Evolution; international journal of organic evolution.

[67]  W. Etges,et al.  Premating Isolation Is Determined by Larval Rearing Substrates in CactophilicDrosophila mojavensis. III. Epicuticular Hydrocarbon Variation Is Determined by Use of Different Host Plants inDrosophila mojavensis andDrosophila arizonae , 1997, Journal of Chemical Ecology.

[68]  M. Ayasse,et al.  Post-mating odor in females of the solitary bee, Andrena nigroaenea (Apoidea, Andrenidae), inhibits male mating behavior , 2000, Behavioral Ecology and Sociobiology.

[69]  R. Lande Models of speciation by sexual selection on polygenic traits. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[70]  M. Stowe CHAPTER 17 – Chemical Mimicry , 1988 .

[71]  S. Turillazzi,et al.  Cuticular Hydrocarbons of Polistes dominulus as a Biogeographic Tool: A Study of Populations from the Tuscan Archipelago and Surrounding Areas , 2004, Journal of Chemical Ecology.

[72]  M. West-Eberhard Sexual Selection, Social Competition, and Speciation , 1983, The Quarterly Review of Biology.

[73]  N. Mantel The detection of disease clustering and a generalized regression approach. , 1967, Cancer research.