Abstract

Taxa harboring high levels of standing variation may be more likely to adapt to rapid environmental shifts and experience ecological speciation. Here, we characterize geographic and host‐related differentiation for 10,241 single nucleotide polymorphisms in Rhagoletis pomonella fruit flies to infer whether standing genetic variation in adult eclosion time in the ancestral hawthorn (Crataegus spp.)‐infesting host race, as opposed to new mutations, contributed substantially to its recent shift to earlier fruiting apple (Malus domestica). Allele frequency differences associated with early vs. late eclosion time within each host race were significantly related to geographic genetic variation and host race differentiation across four sites, arrayed from north to south along a 430‐km transect, where the host races co‐occur in sympatry in the Midwest United States. Host fruiting phenology is clinal, with both apple and hawthorn trees fruiting earlier in the North and later in the South. Thus, we expected alleles associated with earlier eclosion to be at higher frequencies in northern populations. This pattern was observed in the hawthorn race across all four populations; however, allele frequency patterns in the apple race were more complex. Despite the generally earlier eclosion timing of apple flies and corresponding apple fruiting phenology, alleles on chromosomes 2 and 3 associated with earlier emergence were paradoxically at lower frequency in the apple than hawthorn host race across all four sympatric sites. However, loci on chromosome 1 did show higher frequencies of early eclosion‐associated alleles in the apple than hawthorn host race at the two southern sites, potentially accounting for their earlier eclosion phenotype. Thus, although extensive clinal genetic variation in the ancestral hawthorn race exists and contributed to the host shift to apple, further study is needed to resolve details of how this standing variation was selected to generate earlier eclosing apple fly populations in the North.

Highlights

  • The raw material for novel adaptation can come from new muta‐ tions or standing variation (Barrett & Schluter, 2008)

  • Large stores of standing genetic variation observed in some populations may be a product of complex evolutionary his‐ tories, including past gene flow coupled with ecological selection to maintain high levels of genetic variation resulting from tracking local, regional, or temporal differences in environmental or biotic condi‐ tions (Bergland, Tobler, González, Schmidt, & Petrov, 2016; Berner & Salzburger, 2015; Brawand et al, 2014; Feder, Berlocher, et al, 2003; Gompert, Fordyce, Forister, Shapiro, & Nice, 2006; Jeffery et al, 2017; Jones et al, 2012; Lamichhaney et al, 2015; Loh et al, 2013; Pease, Haak, Hahn, & Moyle, 2016; Roesti, Gavrilets, Hendry, Salzburger, & Berner, 2014; The Heliconius Genome Consortium, 2012)

  • We investigate genome‐wide patterns of differentia‐ tion in Rhagoletis pomonella (Diptera: Tephritidae) for 10,241 single nucleotide poly‐ morphism (SNP) by comparing results from the adult eclosion genome‐wide association study (GWAS) (Ragland et al, 2017) with a population survey of four sites distributed from north to south along a 430‐km transect across the Midwestern United States, where populations of hawthorn and apple flies co‐occur in sympatry (Figure 1)

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Summary

| INTRODUCTION

The raw material for novel adaptation can come from new muta‐ tions or standing variation (Barrett & Schluter, 2008). Clines can be in‐ dicative of more than just past progress toward speciation and be natural experiments in the speciation process itself, with gene flow providing an input of new material facilitating divergence (Abbott et al, 2013; Arnold, 1997; Endler, 1977; Gompert et al, 2014; Harrison & Larson, 2016; Hewitt, 1988; Mallet, 2007) In this regard, hybridization can create novel genotypes that may rapidly lead to differentiation from nearby parental taxa when hybrids oc‐ cupy underused niches or environments, via polyploid or homoploid mechanisms (Gompert et al, 2006; Kang, Schartl, Walter, & Meyer, 2013; Lamichhaney et al, 2018; Mavárez et al, 2006; Rieseberg & Willis, 2007; Salzburger, Baric, & Sturmbauer, 2002; Schwarz, Matta, Shakir‐Botteri, & McPheron, 2005; Yakimowski & Rieseberg, 2014). It spread through the Sierra Madre Oriental Mountains (SMO) of Mexico and into North America over the past ~1 million

G Apple and Hawthorn races G Hawthorn-infesting populations only
| MATERIALS AND METHODS
80 Urbana 75
| DISCUSSION
Findings
| CONCLUSION

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