Population Differentiation and Genetic Variation in Performance on Eight Hosts in the Pea Aphid Complex

Abstract Phytophagous insects frequently use multiple host-plant species leading to the evolution of specialized host-adapted populations and sometimes eventually to speciation. Some insects are confronted with a large number of host-plant species, which may provide complex routes of gene flow between host-adapted populations. The pea aphid (Acyrthosiphon pisum) attacks a broad range of plants in the Fabaceae and it is known that populations on Trifolium pratense and Medicago sativa can be highly specialized at exploiting these species. To find out whether adaptation to a broad range of co-occurring hosts has occurred, we tested the performance of pea aphid clones collected from eight host-plant genera on all of these plants in a reciprocal transfer experiment. We provide evidence for pervasive host-plant specialization. The high performance of all aphid clones on Vicia faba suggests that this host plant could be a site of gene flow between different populations that could limit further host-associated divergence. The genetic variance in host-plant usage was partitioned into within- and among-population components, which represent different levels of host adaptation. Little evidence of within-population trade-offs in performance on different plant species was found.

[1]  J. R. Ott,et al.  Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. , 2007, Ecology.

[2]  Timothy P. Craig,et al.  HOST PLANT GENOTYPE INFLUENCES SURVIVAL OF HYBRIDS BETWEEN EUROSTA SOLIDAGINIS HOST RACES , 2007, Evolution; international journal of organic evolution.

[3]  H. Godfray,et al.  Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids , 2007, Oecologia.

[4]  R. Harrington,et al.  Aphids as crop pests , 2007 .

[5]  H. Godfray,et al.  POPULATION DIFFERENTIATION AND GENETIC VARIATION IN HOST CHOICE AMONG PEA APHIDS FROM EIGHT HOST PLANT GENERA , 2006, Evolution; international journal of organic evolution.

[6]  B. Crespi,et al.  Experimental evidence that predation promotes divergence in adaptive radiation. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Plantegenest,et al.  Ecological specialization correlates with genotypic differentiation in sympatric host‐populations of the pea aphid , 2006, Journal of evolutionary biology.

[8]  H. Godfray,et al.  Aphid Protected from Pathogen by Endosymbiont , 2005, Science.

[9]  J. Nason,et al.  HOST‐ASSOCIATED GENETIC DIFFERENTIATION IN PHYTOPHAGOUS INSECTS: GENERAL PHENOMENON OR ISOLATED EXCEPTIONS? EVIDENCE FROM A GOLDENROD‐INSECT COMMUNITY , 2005, Evolution; international journal of organic evolution.

[10]  J. Scheirs,et al.  Have Genetic Trade-Offs in Host Use been Overlooked in Arthropods? , 2005, Evolutionary Ecology.

[11]  N. Moran,et al.  Evolutionary Relationships of Three New Species of Enterobacteriaceae Living as Symbionts of Aphids and Other Insects , 2005, Applied and Environmental Microbiology.

[12]  H. Rundle,et al.  Ecological speciation: Ecological speciation , 2005 .

[13]  H. Godfray,et al.  The maintenance of intraspecific biodiversity: the interplay of selection on resource use and on natural enemy resistance in the pea aphid , 2005, Ecological Research.

[14]  A. Joshi,et al.  Trade-offs and the evolution of host specialization , 2005, Evolutionary Ecology.

[15]  T. Kawecki,et al.  Conceptual issues in local adaptation , 2004 .

[16]  P. Nosil Reproductive isolation caused by visual predation on migrants between divergent environments , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  Teresa E. Leonardo Removal of a specialization‐associated symbiont does not affect aphid fitness , 2004 .

[18]  T. Fukatsu,et al.  Host Plant Specialization Governed by Facultative Symbiont , 2004, Science.

[19]  H. Godfray,et al.  Linking the bacterial community in pea aphids with host‐plant use and natural enemy resistance , 2004 .

[20]  P. Barbosa,et al.  Generalized plant defense: effects on multiple species , 1991, Oecologia.

[21]  R. Prokopy,et al.  Behavioral evidence for host races in Rhagoletis pomonella flies , 1988, Oecologia.

[22]  W. B. Watt,et al.  Individual variation in oviposition preference in the butterfly, Colias eurytheme , 1981, Oecologia.

[23]  D. J. Funk,et al.  Herbivorous Insects: Model Systems for the Comparative Study of Speciation Ecology , 2004, Genetica.

[24]  Teresa E. Leonardo,et al.  Facultative symbionts are associated with host plant specialization in pea aphid populations , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  I. Yao,et al.  Genetic architecture for normal and novel host‐plant use in two local populations of the herbivorous ladybird beetle, Epilachna pustulosa , 2003, Journal of evolutionary biology.

[26]  B. Sabater-Muñoz,et al.  Host–based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  N. Moran,et al.  Side‐stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea , 2003, Molecular ecology.

[28]  J. Bossart Covariance of preference and performance on normal and novel hosts in a locally monophagous and locally polyphagous butterfly population , 2003, Oecologia.

[29]  J. Mallet,et al.  Host choice promotes reproductive isolation between host races of the larch budmoth Zeiraphera diniana , 2003, Journal of evolutionary biology.

[30]  H. Godfray,et al.  Resistance to a fungal pathogen and host plant specialization in the pea aphid , 2003 .

[31]  N. Moran,et al.  Facultative bacterial symbionts in aphids confer resistance to parasitic wasps , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  H. Shibao,et al.  Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum , 2002, Molecular ecology.

[33]  A. Hendry,et al.  ADAPTIVE DIVERGENCE AND THE BALANCE BETWEEN SELECTION AND GENE FLOW: LAKE AND STREAM STICKLEBACK IN THE MISTY SYSTEM , 2002, Evolution; international journal of organic evolution.

[34]  J. Mallet,et al.  Host races in plant-feeding insects and their importance in sympatric speciation. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  A. Maxmen,et al.  Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress , 2002 .

[36]  J. Feder,et al.  Sympatric speciation in phytophagous insects: moving beyond controversy? , 2002, Annual review of entomology.

[37]  David J. Hawthorne,et al.  Genetic linkage of ecological specialization and reproductive isolation in pea aphids , 2001, Nature.

[38]  S. Via,et al.  Sympatric speciation in animals: the ugly duckling grows up. , 2001, Trends in ecology & evolution.

[39]  D. Schluter Ecology and the origin of species. , 2001, Trends in ecology & evolution.

[40]  G. Turner The Ecology of Adaptive Radiation , 2001, Heredity.

[41]  S. Via,et al.  Specialized Feeding Behavior Influences Both Ecological Specialization and Assortative Mating in Sympatric Host Races of Pea Aphids , 2000, The American Naturalist.

[42]  S. Via,et al.  REPRODUCTIVE ISOLATION BETWEEN DIVERGENT RACES OF PEA APHIDS ON TWO HOSTS. II. SELECTION AGAINST MIGRANTS AND HYBRIDS IN THE PARENTAL ENVIRONMENTS , 2000, Evolution; international journal of organic evolution.

[43]  S. Via REPRODUCTIVE ISOLATION BETWEEN SYMPATRIC RACES OF PEA APHIDS. I. GENE FLOW RESTRICTION AND HABITAT CHOICE , 1999, Evolution; international journal of organic evolution.

[44]  T. Kawecki Sympatric speciation driven by beneficial mutations , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[45]  J. D. Fry The Evolution of Host Specialization: Are Trade-Offs Overrated? , 1996, The American Naturalist.

[46]  J. Sandström Temporal changes in host adaptation in the pea aphid, Acyrthosiphon pisum , 1996 .

[47]  A. Mackenzie A TRADE‐OFF FOR HOST PLANT UTILIZATION IN THE BLACK BEAN APHID, APHIS FABAE , 1996, Evolution; international journal of organic evolution.

[48]  D. Simberloff,et al.  LOCAL ADAPTATION AND AGENTS OF SELECTION IN A MOBILE INSECT , 1995, Evolution; international journal of organic evolution.

[49]  J. Feder The Effects of Parasitoids on Sympatric Host Races of Rhagoletis Pomonella (Diptera: Tephritidae) , 1995 .

[50]  J. Thompson,et al.  The Coevolutionary Process , 1994 .

[51]  J. Sandström,et al.  Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance , 1994 .

[52]  J. Feder,et al.  Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Timothy P. Craig,et al.  BEHAVIORAL EVIDENCE FOR HOST‐RACE FORMATION IN EUROSTA SOLIDAGINIS , 1993, Evolution; international journal of organic evolution.

[54]  J. D. Fry THE “GENERAL VIGOR” PROBLEM: CAN ANTAGONISTIC PLEIOTROPY BE DETECTED WHEN GENETIC COVARIANCES ARE POSITIVE? , 1993, Evolution; international journal of organic evolution.

[55]  R. Julkunen‐Tiitto,et al.  HOST PREFERENCE AND ALLOZYME DIFFERENTIATION IN SHOOT GALLING SAWFLY, EUURA ATRA , 1993, Evolution; international journal of organic evolution.

[56]  Scott P Carroll,et al.  HOST RACE RADIATION IN THE SOAPBERRY BUG: NATURAL HISTORY WITH THE HISTORY , 1992, Evolution; international journal of organic evolution.

[57]  S. Via SPECIALIZED HOST PLANT PERFORMANCE OF PEA APHID CLONES IS NOT ALTERED BY EXPERIENCE , 1991 .

[58]  S. Via THE GENETIC STRUCTURE OF HOST PLANT ADAPTATION IN A SPATIAL PATCHWORK: DEMOGRAPHIC VARIABILITY AMONG RECIPROCALLY TRANSPLANTED PEA APHID CLONES , 1991, Evolution; international journal of organic evolution.

[59]  D. Houle GENETIC COVARIANCE OF FITNESS CORRELATES: WHAT GENETIC CORRELATIONS ARE MADE OF AND WHY IT MATTERS , 1991, Evolution; international journal of organic evolution.

[60]  D. Karowe PREDICTING HOST RANGE EVOLUTION: COLONIZATION OF CORONILLA VARIA BY COLIAS PHILODICE (LEPIDOPTERA: PIERIDAE) , 1990, Evolution; international journal of organic evolution.

[61]  B. Charlesworth OPTIMIZATION MODELS, QUANTITATIVE GENETICS, AND MUTATION , 1990, Evolution; international journal of organic evolution.

[62]  R. Denno,et al.  Role of Enemy‐Free Space and Plant Quality in Host‐Plant Selection by Willow Beetles , 1990 .

[63]  J. Jaenike Host Specialization in Phytophagous Insects , 1990 .

[64]  S. Via,et al.  Ecological genetics and host adaptation in herbivorous insects: the experimental study of evolution in natural and agricultural systems. , 1990, Annual review of entomology.

[65]  M. Rausher Is Coevolution Dead , 1988 .

[66]  E. Bernays,et al.  On the Evolution of Host Specificity in Phytophagous Arthropods , 1988 .

[67]  D. Futuyma,et al.  The Evolution of Ecological Specialization , 1988 .

[68]  D. Futuyma,et al.  GENETIC VARIATION AND COVARIATION IN RESPONSES TO HOST PLANTS BY ALSOPHILA POMETARIA (LEPIDOPTERA: GEOMETRIDAE) , 1987, Evolution; international journal of organic evolution.

[69]  J. Daniel Hare,et al.  GENETIC VARIATION IN PLANT‐INSECT ASSOCIATIONS: SURVIVAL OF LEPTINOTARSA DECEMLINEATA POPULATIONS ON SOLANUM CAROLINENSE , 1986, Evolution; international journal of organic evolution.

[70]  M. Rausher TRADEOFFS IN PERFORMANCE ON DIFFERENT HOSTS: EVIDENCE FROM WITHIN‐ AND BETWEEN‐SITE VARIATION IN THE BEETLE DELOYALA GUTTATA , 1984, Evolution; international journal of organic evolution.

[71]  D. Futuyma,et al.  Adaptation to Host Plants in the Fall Cankerworm (Alsophila pometaria) and Its Bearing on the Evolution of Host Affiliation in Phytophagous Insects , 1984, The American Naturalist.

[72]  O. Heie The Aphidoidea (Hemiptera) of Fennoscandia and Denmark, Volume 1. General Part. The Families Mindaridae, Hormaphididae, Thelaxidae, Anoeciidae, and Pemphigidae , 1980 .

[73]  Fred Gould,et al.  Associations of Plants and Insects in Deciduous Forest , 1979 .

[74]  J. Felsenstein The theoretical population genetics of variable selection and migration. , 1976, Annual review of genetics.

[75]  M. Slatkin Gene flow and selection in a cline. , 1973, Genetics.

[76]  V. Eastop Keys for the identification of Acyrthosiphon (Hemiptera: Aphididae) , 1971 .

[77]  G. Bush SYMPATRIC HOST RACE FORMATION AND SPECIATION IN FRUGIVOROUS FLIES OF THE GENUS RHAGOLETIS (DIPTERA, TEPHRITIDAE) , 1969, Evolution; international journal of organic evolution.

[78]  P. Raven,et al.  BUTTERFLIES AND PLANTS: A STUDY IN COEVOLUTION , 1964 .