Parapatric diversification after post‐glacial range expansion in the gall flyUrophora cardui(Tephritidae)

Abstract

Aim Primary and secondary genetic clines in post‐glacial colonized regions have different implications for biogeographic distributions and the origin of species. Primary clines arise in situ after colonization as adaptive responses to environmental gradients, while secondary clines are caused by contact between vicariant lineages. Here we analyse primary versus secondary origin of a genetic cline in the tephritid fly Urophora cardui in Jutland, Denmark, in a post‐glacial landscape. Location Western Palaearctic. Methods Phylogeographic and demographic analyses of U. cardui based on mitochondrial DNA (mtDNA) genealogies, hierarchical genetic variance tests based on allozymes and distribution analysis of a rare allele from the Jutland cline. Results There was no phylogeographic divergence between the Jutland population of U. cardui north of the cline and neighbouring western European regional populations, which all shared the common western European mtDNA haplotype H1. At nuclear loci, by contrast, the North Jutland population was diverged above the mean level of divergence among regional populations and had no loss of genetic variation. A rare allozyme allele that was frequent in the cline area (up to 45%) and was missing north of the cline also occurred at low frequency (0–14%) elsewhere in the sampling range. Shallow phylogeographic divergence was observed between Russian and western European populations and between English and continental populations. Main conclusions The genetic variation patterns support primary cline evolution and parapatric divergence in Jutland following a demographic expansion of a western European ancestral source population of U. cardui, and suggest cryptic refugia and/or selection in other European population assemblages. The patterns of intra‐specific regional divergence are discussed with respect to the interpretation of cryptic refugia in Europe after the most recent ice age.

Tracing the history and ecological context of Wolbachia double infection in a specialist host (Urophora cardui)—parasitoid (Eurytoma serratulae) system

“…DI in U. cardui was found in geographically and genetically separated populations with different intrataxon strains. As the phylogeographic differentiation in U. cardui is found both for mtDNA and nuclear genes (Johannesen et al, 2010), the present study provides evidence for sustained DI in U. cardui that is older than the current geographic distribution of the fly and which is not related to a selective sweep of infected mitochondrial haplotypes (Hurst & Jiggins, 2005). The genetic transition zone in U. cardui, which is defined by allelic variation of AAT, was not related to Wolbachia AAT.…”

“…Analysis was performed near exclusively on adults, N = 508 adults + 12 larvae = 520 specimens, with the purpose of avoiding the potential bias of parasitoid encapsulation in larvae that might impact estimates of infection. The frequency of single infections (SI) and double infections was compared among regional populations previously identified (Johannesen et al, 2010;Steinmetz et al, 2004) U. stylata and its specialist endoparasitoid E. compressa F. and its associated E. robusta were screened from individuals collected in Denmark and Germany in 2014 (Appendix S1). The endoparasitoids E. serratulae and E. compressa were analyzed as adults and treated as described above for U. cardui, whereas the three ectoparasitoid species were analyzed as both adults and larvae.…”

“…Nonparasitized fly larvae, by contrast, diapause as larvae and pupate shortly before emergence in spring ( Figure 1). The area of E. serratulae immigration harbors genetically distinct U. cardui populations, which are separated by a transition zone across the center of the peninsula (Johannesen, Drüeke, & Seitz, 2010;Steinmetz, Johannesen, & Seitz, 2004 area just south of the transition zone were not. Based on these findings, I speculated that U. cardui in the north had become infected with the parasitoid strain after immigration of the parasitoid and that the acquisition of double infection (DI) might impact the separation of U. cardui on either side of the transition zone (Riegler & Stauffer, 2002;Werren, 1998 This survey gave insights into whether the presence and/or absence of DI are unique to the immigration area but also assessed the age and stability of DI.…”

Characterisation of microsatellite and SNP markers from Miseq and genotyping-by-sequencing data among parapatricUrophora cardui(Tephritidae) populations

“…The study, based on allozyme loci, identified non-concordant clines at three loci and no clines at another four. Johannesen, Drüeke & Seitz (2010) reported dominance of the same mtDNA haplotype on both sides of the transition zone that belonged to a Western European lineage experiencing population expansion. This mix of allelic distributions across the transition area suggested an in situ origin of the parapatric divergence rather than one caused by secondary contact of two allopatrically evolved populations, i.e., by vicariance.…”

“…Urophora cardui L. (Diptera: Tephritidae) is a specialist gall maker associated with creeping thistle Cirsium arvense (L.) Scop (Asteraceae). Initially attracting attention as a biological control agent of C. arvense in Canada ( Zwölfer, Englert & Pattullo, 1970 ; Peschken & Harris, 1975 ), U. cardui has since been studied for a range of topics in its native Western Palearctic and introduced Canadian distribution ranges: biogeography, evolution of galls, interactions with parasitoids and for pest control (e.g., Peschken & Harris, 1975 ; Zwölfer, 1979 ; Eber & Brandl, 1997 ; Johannesen, Drüeke & Seitz, 2010 ; De Clerck-Floate & Cárcamo, 2011 ).…”