On the origin of species: insights from the ecological genomics of lake whitefish

Abstract

In contrast to the large amount of ecological information supporting the role of natural selection as a main cause of population divergence and speciation, an understanding of the genomic basis underlying those processes is in its infancy. In this paper, we review the main findings of a long-term research programme that we have been conducting on the ecological genomics of sympatric forms of whitefish (Coregonus spp.) engaged in the process of speciation. We present this system as an example of how applying a combination of approaches under the conceptual framework of the theory of adaptive radiation has yielded substantial insight into evolutionary processes in a non-model species. We also discuss how the joint use of recent biotechnological developments will provide a powerful means to address issues raised by observations made to date. Namely, we present data illustrating the potential offered by combining next generation sequencing technologies with other genomic approaches to reveal the genomic bases of adaptive divergence and reproductive isolation. Given increasing access to these new genomic tools, we argue that non-model species studied in their ecological context such as whitefish will play an increasingly important role in generalizing knowledge of speciation.

Transcriptome-wide signature of hybrid breakdown associated with intrinsic reproductive isolation in lake whitefish species pairs (Coregonus spp. Salmonidae)

“…Other minor incompatibilities could still exist, which would account for the differential expression of genes observed in the healthy backcross fish versus parental types. Along this line, we previously observed that a least one locus associated with embryonic mortality is also linked to a regulation (expression Quantitative Trait Locus, eQTL) hotspot and may harbor a major regulatory gene with strong pleiotropic effect on the expression of numerous genes (Bernatchez et al, 2010), thus representing a possible mechanism explaining the genome-wide disruption of regulation in hybrids.…”

“…Moreover, early in ontogeny, normal and dwarf fish are phenotypically and ecologically indistinguishable (Chouinard and Bernatchez, 1998;Bernatchez, 2004). At the same time, hybrid whitefish experience striking fitness consequences of genomic incompatibilities and ongoing reproductive isolation (increased mortality, disruption of hatching time and reduced sperm performance, Rogers and Bernatchez, 2006;Whiteley et al, 2009;Bernatchez et al, 2010).…”

“…Lake whitefish species pairs represent excellent model species to study the early onset of reproductive isolation and its effect on genomic divergence (Lu and Bernatchez, 1998;Rogers and Bernatchez, 2007;Bernatchez et al, 2010). Following the last glacier retreat (o15 000 years ago), secondary contact of lake whitefish (Coregonus clupeaformis) evolutionary lineages isolated during the Pleistocene (100 000-200 000 years ago) has led to the parallel evolution of two morphologically and ecologically divergent sympatric species in several lakes of northeastern North America: benthic normal and limnetic dwarf whitefish (Bernatchez 2004).…”

Genomic tools for new insights to variation, adaptation, and evolution in the salmonid fishes: a perspective for charr

“…These false positives lead us to conclude incorrectly about the genetic bases of the populations or phenotypes being studied. This is a central argument for leveraging the framework of parallel evolution (Bernatchez et al, 2010;Elmer & Meyer, 2011). Replicate Hydrobiologia (2016) 783:191-208 203 phenotypes in the parallel evolution framework are so called 'natural evolutionary experiments' (Doughty, 1996) used in comparative approaches as a way to tackle the challenges of evolutionary time scales and environmental stochasticity.…”

“…These morphotypes differ in a range of ecologically relevant traits such as body size, head shape, parasite load immunogenetics, growth rate, spawning timing and/or behaviour, and lipid content of the muscle (Skúlason et al 1996;Jonsson & Jonsson, 2001;Adams & Huntingford, 2004;Goetz et al, 2010Goetz et al, , 2014Gudbrandsson et al, 2015). Many of these traits are in fact archetypal of intralacustrine differentiation in other freshwater fishes, with similar components found from stickleback fishes (Schluter, 1993;Willacker et al, 2010) and coregonids [lake (Bernatchez et al, 2010) or European whitefish (Østbye et al, 2006)] in the northern hemisphere, to cichlid fishes in the Neotropics (Elmer et al, 2014) and Africa (Hulsey et al, 2013). However, among the northern fishes, charr are the species in which multiple sympatric morphs are found most abundantly (Klemetsen, 2010).…”