Evidence for Historical Introgression Along a Contact Zone Between Two Species of Char (Pisces: Salmonidae) in Northwestern North America

Abstract

Phylogeographic analyses can yield valuable insights into the geographic and historical contexts of contact and hybridization between taxa. Two species of char (Salmonidae), Dolly Varden (Salvelinus malma) and bull trout (S. confluentus) have largely parapatric distributions in watersheds of northwestern North America. They are, however, sympatric in several localities and hybridization and some introgression occurs across a broad area of contact. We conducted a comparative phylogenetic analysis of Dolly Varden and bull trout to gain a historical perspective of hybridization between these species and to test for footprints of historical introgression. We resolved two major Dolly Varden mitochondrial DNA (mtDNA) clades (with 1.4-2.2% sequence divergence between haplotypes) that had different geographical distributions. Clade N is distributed across most of the range of Dolly Varden, from southern British Columbia through to the Kuril Islands in Asia. Clade S had a much more limited distribution, from Washington state, at the southern limit of the Dolly Varden range, to the middle of Vancouver Island. The distribution and inferred ages of the mtDNA clades suggested that Dolly Varden survived the Wisconsinan glaciation in a previously unsuspected refuge south of the ice sheet, and that Dolly Varden and bull trout were probably in continuous contact over most of the last 100,000 years. When bull trout were included in the phylogenetic analysis, however, the mtDNA of neither species was monophyletic: Clade S Dolly Varden clustered within the bull trout mtDNA clade. This pattern was discordant with two nuclear phylogenies produced (growth hormone 2 and rRNA internal transcribed sequence 1), in which Dolly Varden and bull trout were reciprocally monophyletic. This discordance between mtDNA- and nDNA-based phylogenies indicates that historical introgression of bull trout mtDNA into Dolly Varden occurred. Percent sequence divergence within these introgressed Dolly Varden (clade S) was 0.2-0.6%, implying that the introgression occurred prior to the most recent glaciation. Our analysis and other evidence of contact between divergent lineages in northwestern North America strongly suggests that the area may be the site of previously unsuspected suture zones of aquatic biotas.

Phylogeny and Phylogeography of the Liolaemus Darwinii Complex (Squamata: Liolaemidae): Evidence for Introgression and Incomplete Lineage Sorting

“…These phenomena have been reported in phylogenetic analyses of other vertebrates in regions or the Northern Hemisphere characterized by Pleistocene climatic changes, tectonic activity, and increased aridity, and general causative factors can sometimes be implicated (Dowling and Secor 1997;Grandjean and Souty-Grosset 2000;Alexandrino et al 2002;Redenbach and Taylor 2002;Sullivan et al 2002). Here we present the first evidence for introgression and incomplete lineage sorting in lizards (and possibly in any vertebrate) in temperate South America, which could also be related to Pleistocene climatic changes.…”

“…Lineage sorting eliminates ancestral polymorphism over time such that sister species eventually become reciprocally monophyletic with respect to mtDNA, but this is expected to be incomplete when the rate of lineage splitting or speciation exceeds the rate of stochastic sorting of allelic polymorphisms within lineages . In these cases the phylogeny of alleles sampled will differ from larger species phylogeny (Pamilo and Nei 1988;Moran and Kornfield 1993), and a single gene genealogy may be misleading (Moritz et al 1992;McMillan and Palumbi 1995;Redenbach and Taylor 2002). Under conditions of rapid speciation and maintenance of large effective population sizes, the effects of genetic drift are reduced and rates of lineage sorting slowed (Parker and Kornfield 1997).…”

“…A gene tree will not necessarily reflect a species tree (Pamilo and Nei 1988;Nichols 2001), and phylogeographic inferences within and between closely related species can be influenced (misled) by introgression and retention of ancestral polymorphism (Harrison 1991;Redenbach and Taylor 2002;Funk and Omland 2003). Recent studies have documented secondary contact and subsequent hybridization and introgression in previously isolated taxa (Soltis et al 1997;Pfenninger and Posada 2002), and others have shown that incomplete lineage sorting can produce gene trees that are incongruent with species trees (Moran and Kornfield 1993;Parker and Kornfield 1997).…”

“…Recent studies have documented secondary contact and subsequent hybridization and introgression in previously isolated taxa (Soltis et al 1997;Pfenninger and Posada 2002), and others have shown that incomplete lineage sorting can produce gene trees that are incongruent with species trees (Moran and Kornfield 1993;Parker and Kornfield 1997). Despite these limitations, a phylogeographic perspective can yield insights into the historical and geographical contexts of these processes (Butlin 1998;Rieseberg 1998;Redenbach and Taylor 2002).…”

Investigating the effects of Pleistocene events on genetic divergence within Richardsonius balteatus, a widely distributed western North American minnow

“…In northwestern North America, refugia are postulated to have occurred in several areas, including Beringia [22-25], the Chehalis River Valley [4,26-28], the lower Columbia River drainage [29-31], the Upper Columbia River drainage [32-36], Haida Gwaii (a.k.a., Queen Charlotte Islands: an archipelago off the Pacific Coast of British Columbia) [37-39], and the Klamath-Siskiyou region [5,36,40-42] (Figure 1). Additionally, some taxa have retained genetic signatures of survival in northern and southern refugia along the Pacific Coast [27,43,44]. …”