Modeling the Multiple Facets of Speciation-with-Gene-Flow toward Inferring the Divergence History of Lake Whitefish Species Pairs (Coregonus clupeaformis)

Abstract

Parallel divergence across replicated species pairs occurring in similar environmental contrasts may arise through distinct evolutionary scenarios. Deciphering whether such parallelism actually reflects repeated parallel divergence driven by divergent selection or a single divergence event with subsequent gene flow needs to be ascertained. Reconstructing historical gene flow is therefore of fundamental interest to understand how demography and selection jointly shaped genomic divergence during speciation. Here, we use an extended modeling framework to explore the multiple facets of speciation-with-gene-flow with demo-genetic divergence models that capture both temporal and genomic variation in effective population size and migration rate. We investigate the divergence history of replicate sympatric species pairs of Lake Whitefish (normal benthic and dwarf limnetic) characterized by variable degrees of ecological divergence and reproductive isolation. Genome-wide SNPs were used to document the extent of genetic differentiation in each species pair, and 26 divergence models were fitted and compared with the unfolded joint allele frequency spectrum of each pair. We found evidence that a recent (circa 3,000–4,000 generations) asymmetrical secondary contact between expanding postglacial populations has accompanied Whitefish diversification. Our results suggest that heterogeneous genomic differentiation has emerged through the combined effects of linked selection generating variable rates of lineage sorting across the genome during geographical isolation, and heterogeneous introgression eroding divergence at different rates across the genome upon secondary contact. This study thus provides a new retrospective insight into the historical demographic and selective processes that shaped a continuum of divergence associated with ecological speciation.

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.…”

“…Coregonus clupeaformis samples were collected from Indian Lake and Cliff Lake, Maine (USA; Figure ), in 2010. These lakes are part of a well‐studied lake whitefish system (Bernatchez et al, ) and comprise the most divergent species‐pairs along the divergence continuum described in previous studies (Gagnaire, Pavey, et al, ; Renaut et al, ; Rougeux et al, ). In parallel, C. lavaretus individuals were sampled in two Scandinavian lakes in Norway (2014): Skrukkebukta, Langfjordvatn and two alpine lakes in Switzerland (2012): Zurich and Lucerne (Figure ).…”

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

“…Finally, only oriented loci (i.e. monomorphic loci in C. clupeaformis and polymorphic in C. lavaretus ) were kept after removing loci that were polymorphic in the outgroup (Rougeux et al., ; Tine et al., ). This resulted in 157,516, 136,499, 117,125 and 92,678 oriented SNPs (corresponding to a mean number of 8.9 SNPs/transcript for each lake, SD 0.49) for Langfjordvatn, Skrukkebukta, Lucerne and Zurich lakes, respectively, that were used to generate the unfolded JAFS of each lake, by projecting the data to 10 chromosomes (i.e.…”

“…Finally, we converted estimated parameter values using theta ( θ ) (Table ), by applying equations from Rougeux et al. ().…”

Genomic evidence for asymmetric introgression by sexual selection in the common wall lizard

“…In the second round, models were extended to consider heterogeneous migration across the genome. In order to quantify the mean effect of selection at specific sites, Tine et al., and Rougeux, Bernatchez, & Gagnaire, defined a Hill‐Robertson scaling factor (hrf), relating the effective population size of loci influenced by selection to that of neutral loci. Those parameters were implemented in the best‐fitting basic model (i.e., SC) in two different scenarios as SC2M‐1 and SC2M‐2.…”