Standing chromosomal variation in Lake Whitefish species pairs: the role of historical contingency and relevance for speciation

Abstract

The role of chromosome changes in speciation remains a debated topic, although demographic conditions associated with divergence should promote their appearance. We tested a potential relationship between chromosome changes and speciation by studying two Lake Whitefish (Coregonus clupeaformis) lineages that recently colonized postglacial lakes following allopatry. A dwarf limnetic species evolved repeatedly from the normal benthic species, becoming reproductively isolated. Lake Whitefish hybrids experience mitotic and meiotic instability, which may result from structurally divergent chromosomes. Motivated by this observation, we test the hypothesis that chromosome organization differs between Lake Whitefish species pairs using cytogenetics. While chromosome and fundamental numbers are conserved between the species (2n = 80, NF = 98), we observe extensive polymorphism of subtle karyotype traits. We describe intrachromosomal differences associated with heterochromatin and repetitive DNA, and test for parallelism among three sympatric species pairs. Multivariate analyses support the hypothesis that differentiation at the level of subchromosomal markers mostly appeared during allopatry. Yet we find no evidence for parallelism between species pairs among lakes, consistent with colonization effect or postcolonization differentiation. The reported intrachromosomal polymorphisms do not appear to play a central role in driving adaptive divergence between normal and dwarf Lake Whitefish. We discuss how chromosomal differentiation in the Lake Whitefish system may contribute to the destabilization of mitotic and meiotic chromosome segregation in hybrids, as documented previously. The chromosome structures detected here are still difficult to sequence and assemble, demonstrating the value of cytogenetics as a complementary approach to understand the genomic bases of speciation.

Allopatric and sympatric diversification within roach (Rutilus rutilus) of large pre‐alpine lakes

“…Given the abundances of perch and whitefish in Lake Brienz (Alexander et al., ; Doenz et al., ), the limited degree of diversification in roach could be a result of different factors: (a) Interspecific competition may have constrained roach from diversifying, (b) If the observed phenotypic differentiation (Figure ) is primarily due to phenotypic plasticity, the latter could have constrained diversification by shielding the genome from selection, thus decreasing the potential for genetic divergence (Ghalambor et al., ; Price et al., ), (c) The fundamental niche of roach may be narrower than that of whitefish, preventing roach to explore otherwise available niche space. For example, roach prefer warmer water and are therefore restricted to the shallow zones of lakes, whereas whitefish can tolerate colder water, allowing them to explore the deeper sections of lakes (Coutant, ; Kottelat & Freyhof, ), and (d) Recent genomic work suggests that adaptive diversification in stickleback and whitefish often occurs from standing genetic variation in genomic regions that show structural changes, including inversions (Jones et al., ; Marques et al., ) or chromosomal rearrangements (Dion‐Côté et al., ). Such structural genomic rearrangements may then facilitate diversification through coupling of co‐adapted alleles (Butlin & Smadja, ).…”

Beyond speciation genes: an overview of genome stability in evolution and speciation

“…Interestingly, hybridization also potentially led to speciation of a hybrid lineage in which chromosome rearrangements partially explain reproductive isolation with ancestral lineages [54]. Recently diverged populations of Lake Whitefish (<12–15,000 generations) show evidence of ongoing chromosomal divergence, and their hybrids suffer from extensive aneuploidy consistent with both meiotic and mitotic segregation errors [55,56]. Future efforts should aim in more systems to characterize genome organization comprehensively and to document the impact of chromosome rearrangements.…”

Introduction: integrative molecular ecology is rapidly advancing the study of adaptation and speciation

“…Dion‐Côté et al . () tested the possible role of chromosomal variation using the well‐characterized phylogeography of the Lake Whitefish ( Coregonus clupeaformis ), a species complex in which two lineages underwent geographical isolation ~60 000 ka (or ~15–20 000 generations ago) before colonizing newly formed postglacial lakes following the retreat of glacial ice 12 000 ka. Secondary contact was followed by the evolution of dwarfism in sympatry with the normal ecotype in limnetic and benthic niches of lakes, respectively.…”

“…Energy metabolism in the Lake Whitefish species complex (see Dion‐Côté et al . ) is key to local adaptation in white fish species pairs, but distinct genetic and transcriptomic changes often underlie phenotypic evolution. Dalziel et al .…”