Are Eurosta solidaginis on Solidago rugosa a divergent host-associated race?

  • Chandra E. MoffatEmail author
  • Mizuki K. Takahashi
  • Sarah L. Pease
  • Jonathan M. Brown
  • Stephen B. Heard
  • Warren G. Abrahamson
Original Paper


The ball-gall fly Eurosta solidaginis is considered a classic example of host-race formation in herbivorous insects, with host-associated races evolving at least twice, including the well-known pair on Solidago altissima and S. gigantea. Yet E. solidaginis has been occasionally observed galling other Solidago species. Here, we explore the origins of E. solidaginis on Solidago rugosa. We hypothesize that flies associated with S. rugosa are derived from the S. altissima host-race, and ask whether S. rugosa-associated flies have initiated host-race formation. We compared genetic variation among seventeen E. solidaginis populations collected from S. rugosa, S. altissima, and S. gigantea, in an adjacent COI/COII region of the mitochondrial genome. Across the study area, E. solidaginis flies from S. rugosa were as diverged from S. altissima-flies as they were from S. gigantea-flies (pairwise ΦPT 0.075 and 0.78 respectively) but S. altissima and S. gigantea-flies appeared considerably less diverged (0.002). This pattern was driven by the majority of flies, regardless of host-plant, sharing the same haplotype across the study area. However, we detected several site/region-specific haplotypes, not shared among host species. At the local site scale we were able to distinguish S. gigantea-associated fly haplotypes from either S. altissima or S. rugosa haplotypes, but the majority of S. altissima and S. rugosa-flies shared the same haplotype locally. These patterns of haplotype diversity support existing evidence of host-associated divergence in S. altissima- and S. gigantea-associated flies, and suggest that S. rugosa flies are either the same host-race as, or are recently derived from, S. altissima flies. Successful development on S. rugosa and the use of S. rugosa in the absence of use on sympatric S. altissima suggests that E. solidaginis either has a single oligophagous race using both S. altissima and S. rugosa or is in the earliest stages of host-associated differentiation.


Host-associated divergence Ecological speciation Sympatric speciation 



We thank J. Clark, M. Giasson, L. Harrington, J.H. Kim, J. Mlynarek, and Y. Schibel for field and/or lab assistance; J. Addison and S. Jordan for use of equipment; T. Einfeldt, R. Malefant, and S. Jordan for assistance with analyses; and L. Jesson and D. Quiring for useful suggestions on the manuscript.


Funding was provided by Bucknell University’s David Burpee Plant Genetics endowment and by the Natural Sciences and Engineering Research Council (Canada) via Discovery Grants to SBH and a Vanier Canada Graduate Scholarship to CEM.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10682_2018_9966_MOESM1_ESM.docx (39 kb)
Supplementary material 1 (DOCX 38 kb)


  1. Abrahamson WG, Blair CP (2008) Sequential radiation through host-race formation: herbivore diversity leads to diversity in natural enemies. In: Tilmon K (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 188–2002Google Scholar
  2. Abrahamson WG, Weis AE (1997) Evolutionary ecology across three trophic levels: goldenrods, gallmakers, and natural enemies. Princeton University Press, PrincetonGoogle Scholar
  3. Abrahamson WG, Sattler JF, McCrea KD, Weis AE (1989a) Variation in selection pressures on the goldenrod gall fly and the competitive interactions of its natural enemies. Oecologia 79:15–22CrossRefGoogle Scholar
  4. Abrahamson WG, McCrea KD, Anderson SS (1989b) Host preference and recognition by the goldenrod ball gallmaker Eurosta solidaginis (Diptera: Tephritidae). Am Midl Nat 121:322–330CrossRefGoogle Scholar
  5. Abrahamson WG, Brown JM, Roth SK, Sumerford DV, Horner JD, How ST, Craig TP, Packer RA, Itami JK (1994) Gallmaker speciation: an assessment of the roles of host-plant characters and phenology, gallmaker comopetition, and natural enemies. In: Price P, Mattson W, Baranchikov Y (eds) Gallforming insects. USDA Forest Service, North Central Experiment Station. General Technical Report NC-174, pp 208–222Google Scholar
  6. Abrahamson WG, Ball Dobley K, Houseknecht HR, Pecone CA (2005) Ecological divergence among five co-occurring species of old-field goldenrods. Plant Ecol 177:43–56CrossRefGoogle Scholar
  7. Batra L, Lichtwardt R (1963) Association of fungi with some insect galls. J Kansas Entomol Soc 336:262–278Google Scholar
  8. Beebe NW, Saul A (1995) Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction–restriction fragment length polymorphism analysis. Am J Trop Med Hyg 53(5):478–481CrossRefGoogle Scholar
  9. Berlocher SH, Feder JL (2003) Sympatric speciation in phytophagous insects: moving beyond controversy? Annu Rev Entomol 47:773–815CrossRefGoogle Scholar
  10. Brown JM, Abrahamson WG, Packer RA, Way PA (1995) The role of natural-enemy escape in a gallmaker host-plant shift. Oecologia 104:52–60CrossRefGoogle Scholar
  11. Brown JM, Abrahamson WG, Way PA (1996) Mitochondrial DNA phylogeography of host races of the goldenrod ball gallmaker, Eurosta solidaginis (Diptera: Tephritidae). Evolution 50:777–786CrossRefGoogle Scholar
  12. Bush GL (1969) Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera: Tephritidae). Evolution 23:237–251CrossRefGoogle Scholar
  13. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:165701659CrossRefGoogle Scholar
  14. Confer JL, Paicos P (1985) Downy woodpecker predation at goldenrod galls. J Field Ornithol 56:56–64Google Scholar
  15. Craig TP, Itami JK (2011) Divergence of Eurosta solidaginis in response to host plant variation and natural enemies. Evolution 65:802–817CrossRefGoogle Scholar
  16. Craig TP, Itami JK, Abrahamson WG, Horner JD (1993) Behavioural evidence for host-race formation in Eurosta solidaginis. Evolution 47:1696–1710CrossRefGoogle Scholar
  17. Craig TP, Itami JK, Ohgushi T, Ando Y, Utsumi S (2011) Bridges and barriers to host shifts resulting from host plant genotypic variation. J Plant Interact 6:141–145CrossRefGoogle Scholar
  18. Crespi BJ, Sandoval CP (2000) Phylogenetic evidence for the evolution of ecological specialization in Timema walking-sticks. J Evolut Biol 13:249–262CrossRefGoogle Scholar
  19. Cronin JT, Abrahamson WG (2001) Do parasitoids diversify in response to host-plant shifts by herbivorous insects? Ecol Entomol 26:347–355CrossRefGoogle Scholar
  20. Diehl SR, Bush GL (1984) An evolutionary and applied perspective of insect biotypes. Annu Rev Entomol 29:471–504CrossRefGoogle Scholar
  21. Dorchin NS, Jordan SD, Scott ER, Clarkin CE, Luongo MP, Abrahamson WG (2009) Behavioural, ecological and genetic evidence confirm the occurrence of host-associated differentiation in goldenrod gall midges. J Evol Biol 22:729–739CrossRefGoogle Scholar
  22. Dorchin NS, Joy JB, Hilke LK, Wise MJ, Abrahamson WG (2015) Taxonomy and phylogeny of the Ashondylia species (Diptera: Cedidomyiidae) on North American goldenrods: challenging morphology, complex host-associations, and cryptic speciation. Zool J Linn Soc 174:265–304CrossRefGoogle Scholar
  23. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  24. Felt EP (1917) Key to American insect galls. New York State Museum Bulletin 200, Albany, NYGoogle Scholar
  25. Felt EP (1940) Plant galls and gall makers. Comstock Publishing Company, Inc., IthacaGoogle Scholar
  26. Heard SB (2012) Use of host-plant trait space by phytophagous insects during host-associated differentiation: the gape-and-pinch model. Int J Ecol 192345:1–15CrossRefGoogle Scholar
  27. How ST, Abrahamson WG, Craig TP (1993) Role of host plant phenology in host use by Eurosta solidaginis (Diptera: Tephritidae) on Solidago (Compositae). Environ Entomol 22:388–396CrossRefGoogle Scholar
  28. Itami JK, Craig TP, Horner JD (1998) Factors affecting gene flow between the host races of Eurosta solidaginis. In: Genetic structure and local adaptation in natural insect populations. Springer US, Boston, pp 375–407Google Scholar
  29. Joy JB, Crespi BJ (2007) Adaptive radiation of gall-inducing insects within a single host-plant species. Evolution 61:784–795CrossRefGoogle Scholar
  30. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefGoogle Scholar
  31. Larsson S, Ekbom B (1995) Oviposition mistakes in herbivorous insects: confusion or a step towards a new host plant? Oikos 72:155–160CrossRefGoogle Scholar
  32. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  33. Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116CrossRefGoogle Scholar
  34. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  35. Matsubayashi KW, Ohshima I, Nosil P (2010) Ecological speciation in phytophagous insects. Entomol Exp Appl 134:1–27CrossRefGoogle Scholar
  36. Miller WE (1959) Natural history notes on the goldenrod ball gall fly, Eurosta solidaginis (Fitch) and on its parasites, Eurytoma obtusiventris Gahan and Eurytoma gigantea Walsh. J Tenn Acad Sci 34:246–251Google Scholar
  37. Ming Y (1989) A revision of the genus Eurosta Loew with a scanning microscopic study of taxonomic characters (Diptera: Tephritidae). M.S. thesis, Washington State University, Pullman, WAGoogle Scholar
  38. Mlynarek JJ, Heard SB (2018) Strong and complex host- and habitat-associated genetic differentiation in an apparently polyphagous leaf mining insect. Biol J Linn Soc 125:885–899CrossRefGoogle Scholar
  39. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  40. Novak JA, Foote BA (1980) Biology and immature stages of fruit flies: the genus Eurosta (Diptera: Tephritidae). J Kansas Entomol Soc 53:205–219Google Scholar
  41. Oksanen J, Blanchet FG, Friendly M, Kindt E, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagne H (2016) vegan: community ecology package version 2.4-0Google Scholar
  42. Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420CrossRefGoogle Scholar
  43. Peccoud JA, Oliver A, Plantegenest M, Simon J-C (2009) A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proc Natl Acad Sci USA 106:7495–7500CrossRefGoogle Scholar
  44. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  45. Schlichter L (1978) Winter predation by black capped chickadees and downy woodpeckers on inhabitants of the goldenrod ball gall. Can Field Nat 92:71–74Google Scholar
  46. Semple JC, Cook RE (2006) Solidago. In: Flora North America Editorial Committee (eds) Flora of North America. Vol. 20. Asteraceae, Part 2. Astereae and Senecioneae. Oxford University Press, pp 107–166Google Scholar
  47. Smith PT, Krager K, Cronin JT, Kambhampati S (2002) Mitochondrial DNA variation among host races of Eurosta solidaginis Fitch (Diptera: Tephritidae). Mol Phylogenet Evol 25:372–376CrossRefGoogle Scholar
  48. Smith PT, Krager K, Cronin JT, Kambhampati S (2003) Erratum to “Mitochondrial DNA variation among host races of Eurosta solidaginis Fitch (Diptera: Tephritidae)” [Mol. Phylogenet. Evol. 25:372–376]. Mol Phylogenet Evol 29:648CrossRefGoogle Scholar
  49. Sokal RR (1979) Testing statistical significance of geographic variation patterns. Syst Zool 28:227–232CrossRefGoogle Scholar
  50. Stireman JO, Nason JD, Heard SB (2005) Host-associated genetic differentiation in phytophagous insects: general phenomenon or isolated exceptions? Evidence from a goldenrod-insect community. Evolution 59:2573–2587CrossRefGoogle Scholar
  51. Stireman JO, Devlin H, Abbot P (2012) Rampant host-and defensive phenotype-associated diversification in a goldenrod gall midge. J Evol Biol 25:1991–2004CrossRefGoogle Scholar
  52. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. Genetics 132:619–633PubMedPubMedCentralGoogle Scholar
  53. Uhler L (1951) Biology and ecology of the goldenrod gall fly Eurosta solidaginis (Fitch). Cornell University Agricultural Experiment Station, IthacaGoogle Scholar
  54. Waring GL, Abrahamson WG, Howard DJ (1990) Genetic differentiation among host-associated populations of the gallmaker Eurosta solidaginis (Diptera: Tephritidae). Evolution 44:1648–1655CrossRefGoogle Scholar
  55. Wasbauer MS (1972) An annotated host catalog of the fruit flies of America north of Mexico (Diptera: Tephritidae). California Department of Agriculture, Bureau of Entomology Occasional Paper, vol 19, pp 1–172Google Scholar
  56. Whipple AV, Abrahamson WG, Khamiss MA, Heinrich PL, Urian AG, Northridge EM (2009) Host-race formation promoted by phenology, constrained by heritability. J Evol Biol 22:793–804CrossRefGoogle Scholar
  57. Whipple AV, Irwin JT, Heinrich PL, Abrahamson WG (2017) Distribution data support warm winter temperatures as a key limit on the range of a goldenrod gall fly host race. Northeastern Nat 24(Special Issue 7):B235–B250Google Scholar
  58. Xie X, Michel AP, Schwarz D, Rull J, Velez S, Forbes AA, Aluja MM, Feder JL (2008) Radiation and divergence in the Rhagoletis pomonella species complex: inferences from DNA sequence data. J Evol Biol 21:900–913CrossRefGoogle Scholar
  59. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134CrossRefGoogle Scholar
  60. Zhang B, Segraves KA, Xue HJ, Nie RE, Li WZ, Yang XK (2015) Adaptation to different host plant ages facilitates insect divergence without a host shift. Proc R Soc B Biol Sci 282:251–267CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BiologyUniversity of New BrunswickFrederictonCanada
  2. 2.Department of BiologyBucknell UniversityLewisburgUSA
  3. 3.Department of BiologyGrinnell CollegeGrinnellUSA
  4. 4.Agriculture and Agri-Food Canada, Summerland Research and Development CentreSummerlandCanada

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