Linkage Maps of thedwarfand Normal Lake Whitefish (Coregonus clupeaformis) Species Complex and Their Hybrids Reveal the Genetic Architecture of Population Divergence

Abstract

Elucidating the genetic architecture of population divergence may reveal the evolution of reproductive barriers and the genomic regions implicated in the process. We assembled genetic linkage maps for the dwarf and Normal lake whitefish species complex and their hybrids. A total of 877 AFLP loci and 30 microsatellites were positioned. The homology of mapped loci between families supported the existence of 34 linkage groups (of 40n expected) exhibiting 83% colinearity among linked loci between these two families. Classes of AFLP markers were not randomly distributed among linkage groups. Both AFLP and microsatellites exhibited deviations from Mendelian expectations, with 30.4% exhibiting significant segregation distortion across 28 linkage groups of the four linkage maps in both families (P , 0.00001). Eight loci distributed over seven homologous linkage groups were significantly distorted in both families and the level of distortion, when comparing homologous loci of the same phase between families, was correlated (Spearman R ¼ 0.378, P ¼ 0.0021). These results suggest that substantial divergence incurred during allopatric glacial separation and subsequent sympatric ecological specialization has resulted in several genomic regions that are no longer complementary between dwarf and Normal populations issued from different evolutionary glacial lineages. U NDERSTANDING the genetic consequences of population divergence is central to evolutionary biology (Edmands 2002;Coyne and Orr 2004;de Queiroz 2005). Namely, the ability to detect genetic regions implicated in this evolutionary process may provide insight into the genomic regions involved and the evolution of their role as potential barriers to gene flow. This remains challenging without knowledge of the genetic architecture, i.e., the number, location, and effect of genomic locations contributing to differentiation within and among populations or species (Rieseberg 1998;Orr and Turelli 2001). As genetic architecture may either promote or constrain divergence (Hawthorne and Via 2001), such genomewide perspectives are integral in working toward a complete understanding of the functional genomic response to the evolutionary processes incurred by populations as they diverge (Ting et al. 2001;Emelianov et al. 2004;Wu and Ting 2004).Genetic linkage mapping approaches have several advantages for addressing these issues (Rieseberg 1998). Such an approach has led to the detection of genomic regions resistant to introgression (e.g., Rieseberg et al. 1999;Rogers et al. 2001;Lexer et al. 2003), the identification of adaptive QTL, and the dissection of complex traits (e.g., Peichel et al. 2001;Saintagne et al. 2004) and has proven valuable for the mapping of gene expression profiles (expression QTL, e.g., Kirst et al. 2005). Comparative linkage mapping among species has also allowed inference about the types of genomic changes that may accompany divergence (e.g., Kuittinen et al. 2004, Lexer et al. 2005, Gharbi et al. 2006. Altogether, genetic mapping has provided an ...

A Hybrid Genetic Linkage Map of Two Ecologically and Morphologically Divergent Midas Cichlid Fishes (Amphilophusspp.) Obtained by Massively Parallel DNA Sequencing (ddRADSeq)

“…As the species are young and can be crossed easily, incompatible loci seems more probable than large genomic rearrangements (Moyle and Graham 2005). Genetic incompatibilities between species detected on the basis of segregation distortion have been suggested in many cases, including lake whitefish (Rogers and Bernatchez 2007; Rogers et al 2007), Drosophila (Phadnis and Orr 2009), Nasonia (Gadau et al 1999; Niehuis et al 2008), and some plant species (Foolad et al 1995; Whitkus 1998; Fishman et al 2001; Myburg et al 2004). …”

Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)

“…Several studies have reported high levels of segregation distortion, greater than 15% of loci at P  < 0.05, within hybrid maps across a variety of taxa, including interspecific crosses between Mimulus guttatus and M. nastutus [8], Lepomis cyanellus and L. megalotis [53], and Nasonia giraulti and N. vitripennis [54] and between intraspecific crosses of Salvelinus alpinus [55], M. guttatus [56], Ceratodon purpureus [57], Coregonus clupeaformis [58], and Tigriopus californicus [59]. Divergence time estimates between parental lineages used for several of these maps ranged from 0.1-0.2 MYA to 13–16 MYA [60-63].…”

Natural Selection and Neutral Evolution Jointly Drive Population Divergence between Alpine and Lowland Ecotypes of the Allopolyploid Plant Anemone multifida (Ranunculaceae)

“…The utilization of AFLP for genome scans has limitations. AFLP loci may be associated with a particular region of the genome, possibly missing section of the genome that are under natural selection [100]. In addition to the relatively few loci available for the genome scan, this concentration of restriction sites may account for the failure of AFLP to find outliers [101].…”