Are Eurosta solidaginis on Solidago rugosa a divergent host-associated race?
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.
KeywordsHost-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.
- 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
- Abrahamson WG, Weis AE (1997) Evolutionary ecology across three trophic levels: goldenrods, gallmakers, and natural enemies. Princeton University Press, PrincetonGoogle Scholar
- 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
- Batra L, Lichtwardt R (1963) Association of fungi with some insect galls. J Kansas Entomol Soc 336:262–278Google Scholar
- Confer JL, Paicos P (1985) Downy woodpecker predation at goldenrod galls. J Field Ornithol 56:56–64Google Scholar
- Felt EP (1917) Key to American insect galls. New York State Museum Bulletin 200, Albany, NYGoogle Scholar
- Felt EP (1940) Plant galls and gall makers. Comstock Publishing Company, Inc., IthacaGoogle Scholar
- 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
- Legendre P, Legendre L (1998) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
- 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
- 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
- Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
- 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
- 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
- R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- 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
- 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
- Uhler L (1951) Biology and ecology of the goldenrod gall fly Eurosta solidaginis (Fitch). Cornell University Agricultural Experiment Station, IthacaGoogle Scholar
- 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
- 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