Convergence in form and function overcomes non-parallel evolutionary histories in a Holarctic fish

Abstract

<jats:title>Abstract</jats:title><jats:p>Understanding the extent to which evolution is predictable under multifarious selection is a longstanding question in evolutionary biology. However, the interplay of stochastic and contingent factors influencing the extent of parallelism in nature is not well understood. To test the predictability of evolution, we studied a ‘natural experiment’ on different organismal levels across lakes and evolutionary lineages of a freshwater salmonid fish, Arctic charr <jats:italic>(Salvelinus alpinus).</jats:italic> We identified significant phenotypic parallelism between Arctic charr ecotype pairs within a continuum of parallel evolution and highly parallel adaptive morphological traits. Variability in phenotypic predictability was explained by complex demographic histories, differing genomic backgrounds and genomic responses to selection, variable genetic associations with ecotype, and environmental variation. Remarkably, gene expression was highly similar across ecotype replicates, and explained the observed parallelism continuum. Our findings suggest that parallel evolution by non-parallel evolutionary routes is possible when the regulatory molecular phenotype compensates for divergent histories.</jats:p>

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

“…These results suggest a repression of expression of genes related to growth and developmental process in the limnetic species while genes associated with a higher metabolism and shorter cell cycle life are overexpressed in the limnetic species relatively to the benthic species. These observations at the epigenetic level corroborate those of previous studies at the transcriptomic and physiological levels performed on these populations and further supports the hypothesis of life history trade-offs between survival (limnetic) and growth (benthic) functions revealed in our previous transcriptomic studies [8,48,[66][67][68]. On the other hand, none of the convergent DMRs belong to a DEG, suggesting that methylation differentiation is not a major mechanism involved in the highest differential of gene expression associated to the divergence of limnetic and benthic species.…”

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

“…Consistent with results from the negative binomial glm, the RDA allowed identifying a parallel genetic basis of phenotypic and ecological divergence by revealing parallel DEGs between limnetic and benthic species. Moreover, we found that these DEGs are involved in several metabolic pathways belonging to energetic, growth, cell cycle metabolisms and transcription factor, regulating genes associated with energetic metabolism, as observed in Jacobs et al (). This approach also allowed detecting congruent expression signals at the integrated pathway scale, where the same effect on the selected phenotype can be achieved via regulation of different genes, because of the complexity and redundancy of the multigenic regulatory systems (Yeaman, ).…”

“…Consistent with results from the negative binomial glm, the RDA allowed identifying a parallel genetic basis of phenotypic and ecological divergence by revealing parallel DEGs between limnetic and benthic species. Moreover, we found that these DEGs are involved in several metabolic pathways belonging to energetic, growth, cell cycle metabolisms and transcription factor, regulating genes associated with energetic metabolism, as observed in Jacobs et al (2018).…”

Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

“…The morphs in Loch Stack (Adams et al 2008) and Loch Tay (Garduño-Paz et al 2012) are clearly of allopatric origin. A recent genome-wide study of sympatric charr in Scotland and Siberia is consistent with sympatric origins of charr morphs (Jacobs et al 2018). Ecological specialization can lead to differential growth, behavior and maturity that may influence both choice of spawning sites and timing of spawning.…”

“…Analyses of other scenarios, i.e. with changing migration rates or introgression would be most interesting (see for example Jacobs et al 2018). Considering the episodic nature of ice retreat and the high geological activity in the Þingvallavatn area during the formation of the lake (Saemundsson 1992;Norðdahl et al 2008) charr may have invaded the waters more than once, or experienced intromittent isolation of populations in rifts.…”