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Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis.

ABSTRACT: Tephritid fruit flies belonging to the Rhagoletis pomonella sibling species complex are controversial because they have been proposed to diverge in sympatry (in the absence of geographic isolation) by shifting and adapting to new host plants. Here, we report evidence suggesting a surprising source of genetic variation contributing to sympatric host shifts for these flies. From DNA sequence data for three nuclear loci and mtDNA, we infer that an ancestral, hawthorn-infesting R. pomonella population became geographically subdivided into Mexican and North American isolates approximately 1.57 million years ago. Episodes of gene flow from Mexico subsequently infused the North American population with inversion polymorphism affecting key diapause traits, forming adaptive clines. Sometime later (perhaps +/-1 million years), diapause variation in the latitudinal clines appears to have aided North American flies in adapting to a variety of plants with differing fruiting times, helping to spawn several new taxa. Thus, important raw genetic material facilitating the adaptive radiation of R. pomonella originated in a different time and place than the proximate ecological host shifts triggering sympatric divergence.

SUBMITTER: Feder JL

PROVIDER: S-EPMC193558 | biostudies-literature | 2003 Sep

REPOSITORIES: biostudies-literature

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Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis.

Feder Jeffrey L JL Berlocher Stewart H SH Roethele Joseph B JB Dambroski Hattie H Smith James J JJ Perry William L WL Gavrilovic Vesna V Filchak Kenneth E KE Rull Juan J Aluja Martin M

Proceedings of the National Academy of Sciences of the United States of America 20030819 18

Tephritid fruit flies belonging to the Rhagoletis pomonella sibling species complex are controversial because they have been proposed to diverge in sympatry (in the absence of geographic isolation) by shifting and adapting to new host plants. Here, we report evidence suggesting a surprising source of genetic variation contributing to sympatric host shifts for these flies. From DNA sequence data for three nuclear loci and mtDNA, we infer that an ancestral, hawthorn-infesting R. pomonella populati ...[more]

PMID: 12928500

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Project description: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.

Project description:BackgroundSympatric speciation along ecological gradients has been studied repeatedly, in particular in freshwater fishes. Rapid post-glacial ecological divergence has resulted in numerous endemic species or ecologically distinct populations in lakes of the temperate zones. Here, we focus on the Baltic cisco (Coregonus albula) complex, to study the genetic similarity among two pairs of sympatric autumn- and spring-spawning populations from post-glacial German Lakes Stechlin and Breiter Luzin. For comparison, we included a similar pair of sympatric populations from the Swedish Lake Fegen. We wanted to explore potential genetic similarities between the three sympatric cisco population pairs in the three lakes, to evaluate whether the pairs may have emerged independently in the three lakes, or whether two different species may have colonized all three lakes independently. Furthermore, we considered allopatric C. albula populations from three Polish, three Finnish, and four Swedish locations, added one Siberian population of the sister species C. sardinella and a Swedish C. maraena (whitefish) population. By genotyping nine microsatellite markers in 655 individuals from these 18 populations, we wanted to elucidate how strongly the cisco populations differ across a larger geographical area within Europe. Finally, we compared the genetic differences between the spring- and autumn-spawning populations of ciscoes in the two German lakes to infer the potentially deteriorating effect of strong anthropogenic pressure on the lakes.ResultsDendrogram, Principal Coordinate Analysis and admixture analysis all indicated strong correspondence between population differentiation and geographical location for most cisco populations in Europe, including the Siberian population of C. sardinella. However, populations from some Swedish lakes deviated from this general pattern, by showing a distinct genetic structure. We found evidence for independent evolution of the three sympatric population pairs, because the populations co-occurring in the same lake were always most closely related. However, genetic differentiation was weak in the two German population pairs, but strong in the Swedish Lake Fegen, indicating that the weak differentiation in the German pairs reported earlier has eroded further.ConclusionsOur results suggest that the genetic differentiation at neutral genetic markers among populations of the Baltic cisco complex has evolved (and is maintained) by random genetic drift in isolated populations. However, earlier studies on the Swedish populations combining mitochondrial DNA and microsatellite data indicate that also post-glacial immigration from separate glacial refugia has shaped the present genetic population structure. The low neutral differentiation of the German sympatric pairs in contrast to the Swedish pair suggests that recent anthropogenic effects on the lakes in Germany may put the endemic spring-spawners at risk to extinction.

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Project description:The pattern of genetic differentiation between diverging species receives much attention as one of the key observable features of speciation. It has often been suggested that introgression between closely related species occurs commonly where their distributions overlap, leading to their becoming more morphologically and genetically similar, but there are a few opposite results. However, most of these studies have been carried out with animals and separate species; few have looked at intraspecific cases, especially in plants. Here, we conduct a comparative study on patterns of genetic differentiation among populations of two varieties of Oreocharis benthamii in allopatry and sympatry based on ISSR data for 754 individuals from 26 populations, in order to understand the processes leading to speciation. Contrary to expectations, the facultative xenogamy (mixed mating) species O. benthamii has a relatively low genetic diversity within populations (H = 0.1014, I = 0.1528) and high genetic differentiation among populations (G ST = 0.5867, ФST = 0.659), as is typically found for selfing species. Genetic variance between the two varieties in sympatric populations (44%, ФST = 0.444) is significantly more than that in allopatric populations (14%, ФST = 0.138). Consistent with the taxonomical delimitation of the two varieties, all sampled individuals of O. benthamii clustered into two genetic groups. Moreover, the genetic structures of populations of both varieties are correlated with their different geographical origins. Our studies show that significant divergence between sympatric populations of the two varieties could be attributed primarily to reinforcement by genetic divergent selection in sympatry where secondary contact had occurred. The major proportion of the genetic variation in outcrossing and mixed mating plants may exist among populations when the populations are distributed in fragmented habitats, due to the paucity of suitable habitat combined with inefficient seed dispersal mechanism and limited pollinator foraging area that may limit the gene flow.

Dataset Information

Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis.

Publications

Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis.

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