Ecological adaptation and reproductive isolation in sympatry: genetic and phenotypic evidence for native host races of Rhagoletis pomonella

Ecological speciation with gene flow may be an important mode of diversification for phytophagous insects. The recent shift of Rhagoletis pomonella from its native host downy hawthorn (Crataegus mollis) to introduced apple (Malus domestica) in the northeastern United States is a classic example of s...

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Published inMolecular ecology Vol. 23; no. 3; pp. 688 - 704
Main Authors Powell, Thomas H. Q, Forbes, Andrew A, Hood, Glen R, Feder, Jeffrey L
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.02.2014
Subjects
Adaptation
Adaptation, Physiological - genetics
allochronic isolation
Animal reproduction
Animals
Crataegus
Crataegus mollis
Crataegus viridis
DNA, Mitochondrial - genetics
eclosion
eclosion time
ecological divergence
Ecology
Fruit - chemistry
fruits
Gene Flow
Genetic diversity
Genetic Speciation
Genetic Variation
hosts
indigenous species
Insects
Louisiana
Malus
Malus domestica
Microsatellite Repeats
Mississippi
Phenology
Phenotype
phytophagous insects
races
Reproductive Isolation
Rhagoletis pomonella
speciation with gene flow
surveys
Sympatry
Tephritidae - genetics
Texas
Vaccinium
volatile compounds
Volatile Organic Compounds - chemistry
Louisiana
Mississippi
Texas
allochronic isolation
speciation with gene flow
Crataegus
eclosion time
ecological divergence
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Summary:Ecological speciation with gene flow may be an important mode of diversification for phytophagous insects. The recent shift of Rhagoletis pomonella from its native host downy hawthorn (Crataegus mollis) to introduced apple (Malus domestica) in the northeastern United States is a classic example of sympatric host race formation. Here, we test whether R. pomonella has similarly formed host races on four native Crataegus species in the southern United States: western mayhaw (C. opaca), blueberry hawthorn (C. brachyacantha), southern red hawthorn (C. mollis var. texana) and green hawthorn (C. viridis). These four southern hosts differ from each other in their fruiting phenology and in the volatile compounds emitted from the surface of their fruits. These two traits form the basis of ecological reproductive isolation between downy hawthorn and apple flies in the north. We report evidence from microsatellite population surveys and eclosion studies supporting the existence of genetically differentiated and partially reproductively isolated host races of southern hawthorn flies. The results provide an example of host shifting and ecological divergence involving native plants and imply that speciation with gene flow may be commonly initiated in Rhagoletis when ecological opportunity presents itself.
Bibliography:http://dx.doi.org/10.1111/mec.12635
Appendix S1 Methods. Table S1 Relative percentages of chemical compounds comprising the fruit volatile blends of the four southern hawthorn species (WMH = western mayhaw, GH = green hawthorn, BB = blueberry hawthorn, SR = southern red hawthorn) and the two northern R. pomonella hosts, apple (AP) and downy hawthorn (DH). Table S2 Information for mitochondrial sequence data used in Fig. 3. Table S3 List of 26 microsatellite markers used in this study. Table S4 Alleles included in one of two groups generated by Monte Carlo allele pooling method for each of 26 microsatellite loci across five chromosomes (Chr.). Table S5 Microsatellite allele frequencies for the 26 loci analysed in study for 16 field sites, including six green hawthorn, four western mayhaw, three blueberry hawthorn and three southern red hawthorn populations (uploaded to DRYAD). Table S6 Mean demic inbreeding coefficient (f) and standard deviation (σ) across all 26 loci for each of the 16 populations and sampling regime (S.R.) determined by host plant patch size as described above. Table S7 Results of GLM analyses of allele frequency for loci on chromosome 1. Table S8 Results of GLM analyses of allele frequency for loci on chromosome 2. Table S9 Results of GLM analyses of allele frequency for loci on chromosome 3. Table S10 Results of GLM analyses of allele frequency for loci on chromosome 4. Table S11 Results of GLM analyses of allele frequency for loci on chromosome 5. Table S12 Mean estimated Ln likelihood and standard deviation across five replicates of STRUCTURE analysis of paired local populations for K = 1 and K = 2, using a burn-in of 500 000 followed by 750 000 MCMC repetitions under a correlated allele frequency with admixture model.
NSF - No. 0614252
University of Notre Dame's GLOBES IGERT program
ArticleID:MEC12635
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content type line 23
ISSN:0962-1083
1365-294X
DOI:10.1111/mec.12635