Model‐based demographic inference of introgression history in European whitefish species pairs'

Abstract

Parallel phenotypic differentiation is generally attributed to parallel adaptive divergence as an evolutionary response to similar environmental contrasts. Such parallelism may actually originate from several evolutionary scenarios ranging from repeated parallel divergence caused by divergent selection to a unique divergence event followed by gene flow. Reconstructing the evolutionary history underlying parallel phenotypic differentiation is thus fundamental to understand the relative contribution of demography and selection on genomic divergence during speciation. In this study, we investigate the divergence history of replicate European whitefish (Coregonus lavaretus), limnetic and benthic species pairs from two lakes in Norway and two lakes in Switzerland. Demographic models accounting for semi‐permeability and linked selection were fitted to the unfolded joint allele frequency spectrum built from genome‐wide SNPs and compared to each other in each species pair. We found strong support for a model of asymmetrical post‐glacial secondary contact between glacial lineages in all four lakes. Moreover, our results suggest that heterogeneous genomic differentiation has been shaped by the joint action of linked selection accelerating lineage sorting during allopatry, and heterogeneous migration eroding divergence at different rates along the genome following secondary contact. Our analyses reveal how the interplay between demography, selection and historical contingency has influenced the levels of diversity observed in previous whitefish phylogeographic studies. This study thus provides new insights into the historical demographic and selective processes that shaped the divergence associated with ecological speciation in European whitefish.

Polygenic selection drives the evolution of convergent transcriptomic landscapes across continents within a Nearctic sister species complex

“…Yet, they maintained similar habitat preferences in cold freshwater lakes (Bernatchez & Dodson, ; Douglas et al, ; Østbye et al, , ), with a frequent occurrence of sympatric species‐pairs being, respectively, associated with benthic and limnetic ecological and trophic niches (Amundsen, Bøhn, & Våga, ; Häkli, Ostbye, Kahilainen, Amundsen, & Praebel, ; Kahilainen & Østbye, ; Landry, Vincent, & Bernatchez, ; Lu & Bernatchez, ). In both C. clupeaformis and C. lavaretus , historical demographic events and selective processes initiated species diversification (Rougeux et al, , ) and resulted in a repeated ecological specialization to limnetic and benthic habitats in each region. Here, the analysis of gene sequence divergence and differential expression in limnetic–benthic species has the potential to provide new insights into the genomic bases of parallel adaptation and parallel ecological speciation.…”

“…This system thus offers a valuable model to study the genomic and transcriptomic underpinnings of parallel differential adaptations leading to ecological speciation in independent lineages. The European whitefish species‐pairs appear to be the result of a secondary contact between glacial sublineages (Rougeux, Gagnaire, & Bernatchez, ), resulting in intralacustrine evolution of benthic and limnetic species across Scandinavian and Alpine lakes (Douglas, Brunner, & Bernatchez, ; Østbye et al, ; Østbye, Bernatchez, Naesje, Himberg, & Hindar, ). The North American lake whitefish sympatric species‐pairs are also the result of a postglacial secondary contact between two glacial sublineages during the late Pleistocene.…”

The role of genomic vs. epigenomic variation in shaping patterns of convergent transcriptomic variation across continents in a young species complex

“…In both lineages, diverging limnetic and benthic sympatric species pairs are associated with their respective trophic niches [53][54][55]. The repeated sympatric convergent phenotypic diversification occurred in several lakes where whitefish have undergone a secondary contact between diverged glacial lineages (i.e., sub-lineages that were formed in allopatry on each continent during the last glaciation event) [39,40]. In this study, whole transcriptome and epigenome data offered the opportunity to analyze both the level of DNA methylation and gene sequence divergence and combine these to the analysis of differential gene expression on representative sympatric pairs of limnetic-benthic whitefish species from two continents.…”

“…The Lake whitefish and the European whitefish (hereafter, lineages) evolved separately on both continents since they became geographically isolated ~500,000 years ago [33][34][35]. The limnetic-benthic species complex evolved independently on both continents in two separate glacial lineages during the last Pleistocene [33,[36][37][38][39], and on both continents, they result from a postglacial secondary contact which then colonized independent post-glacial lakes [39,40]. The limnetic species colonized the free limnetic ecological niche through an adaptive divergence with an associated phenotypic evolution that translated into slower growth, slender body, higher metabolic rate and more active swimming behaviour [41][42][43][44][45][46], that relied on convergent genetic and transcriptomic bases [8,[47][48][49], and are reproductively isolated from the sympatric benthic species [50].…”

Polygenic selection drives the evolution of convergent transcriptomic landscapes across continents within a Nearctic sister-species complex

“…This system thus offers a valuable model to study the genomic and transcriptomic underpinnings of parallel differential adaptations leading to ecological speciation in independent lineages. The European whitefish species-pairs appear to be the result of a secondary contact between glacial sub-lineages (Rougeux et al 2019), resulting in intra-lacustrine evolution of benthic and limnetic species across Scandinavian and Alpine lakes (Douglas et al 1999; Østbye et al 2005; 2006). The North American lake whitefish sympatric species-pairs are also the result of a post-glacial secondary-contact between two glacial sub-lineages during the late Pleistocene.…”