Evidence for spatial clines and mixed geographic modes of speciation for North American cherry‐infesting Rhagoletis (Diptera: Tephritidae) flies. Issue 23 (28th October 2020)

• Record Type: Journal Article
• Authors: Doellman, Meredith M.; Saint Jean, Gilbert; Egan, Scott P.; Powell, Thomas H. Q.; Hood, Glen R.; Schuler, Hannes; Bruzzese, Daniel J.; Glover, Mary M.; Smith, James J.; Yee, Wee L.; Goughnour, Robert; Rull, Juan; Aluja, Martin; Feder, Jeffrey L.
• Is Part Of: Ecology and evolution. Volume 10:Issue 23(2020)
• Page Start: 12727
• Page End: 12744
• Publication Date: 2020-10-28
• Subjects: allopatry -- climate change -- isolation by distance -- microsatellites -- mtDNA -- range fragmentation -- Rhagoletis cingulata -- Rhagoletis indifferens -- wing spot; Ecology -- Periodicals; Evolution -- Periodicals; 577.05
• DOI: 10.1002/ece3.6667
• Languages: English
• ISSNs: 2045-7758

Abstract

Abstract: An important criterion for understanding speciation is the geographic context of population divergence. Three major modes of allopatric, parapatric, and sympatric speciation define the extent of spatial overlap and gene flow between diverging populations. However, mixed modes of speciation are also possible, whereby populations experience periods of allopatry, parapatry, and/or sympatry at different times as they diverge. Here, we report clinal patterns of variation for 21 nuclear‐encoded microsatellites and a wing spot phenotype for cherry‐infesting Rhagoletis (Diptera: Tephritidae) across North America consistent with these flies having initially diverged in parapatry followed by a period of allopatric differentiation in the early Holocene. However, mitochondrial DNA (mtDNA) displays a different pattern; cherry flies at the ends of the clines in the eastern USA and Pacific Northwest share identical haplotypes, while centrally located populations in the southwestern USA and Mexico possess a different haplotype. We hypothesize that the mitochondrial difference could be due to lineage sorting but more likely reflects a selective sweep of a favorable mtDNA variant or the spread of an endosymbiont. The estimated divergence time for mtDNA suggests possible past allopatry, secondary contact, and subsequent isolation between USA and Mexican fly populations initiated before the Wisconsin glaciation. Thus, the current genetics of cherry flies may involve different mixed modes of divergence occurring in different portions of the fly's range. We discuss the need for additional DNA sequencing and quantification of prezygotic and postzygotic reproductive isolation to verify the multiple mixed‐mode hypothesis for cherry flies and draw parallels from other systems to assess the generality that speciation may commonly involve complex biogeographies of varying combinations of allopatric, parapatric, and sympatric divergence. Abstract : Allopatry is often considered the null model for speciation, but there is often more than meets the eye for many seemingly straight‐forward stories of allopatric divergence. Here, we use patterns of genetic and morphological variation to demonstrate that two currently allopatric sibling species of cherry‐infesting flies likely diverged via a more complex mixed mode of speciation. Discordant nuclear and mitochondrial data suggest important roles for both biogeographic processes and endosymbionts in divergence. These complexities may have ramifications for understanding the evolution of reproductive isolation between populations leading to the formation of new species.