Reproductive isolation in a nascent species pair is associated with aneuploidy in hybrid offspring

Abstract

Speciation may occur when the genomes of two populations accumulate genetic incompatibilities and/or chromosomal rearrangements that prevent inter-breeding in nature. Chromosome stability is critical for survival and faithful transmission of the genome, and hybridization can compromise this. However, the role of chromosomal stability on hybrid incompatibilities has rarely been tested in recently diverged populations. Here, we test for chromosomal instability in hybrids between nascent species, the 'dwarf' and 'normal' lake whitefish (Coregonus clupeaformis). We examined chromosomes in pure embryos, and healthy and malformed backcross embryos. While pure individuals displayed chromosome numbers corresponding to the expected diploid number (2n ¼ 80), healthy backcrosses showed evidence of mitotic instability through an increased variance of chromosome numbers within an individual. In malformed backcrosses, extensive aneuploidy corresponding to multiples of the haploid number (1n ¼ 40, 2n ¼ 80, 3n ¼ 120) was found, suggesting meiotic breakdown in their F 1 parent. However, no detectable chromosome rearrangements between parental forms were identified. Genomic instability through aneuploidy thus appears to contribute to reproductive isolation between dwarf and normal lake whitefish, despite their very recent divergence (approx. 15 -20 000 generations). Our data suggest that genetic incompatibilities may accumulate early during speciation and limit hybridization between nascent species.

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

“…; Dion‐Côté et al . ). Yet substantial intrachromosomal polymorphism was identified, mainly involving labile or rapidly evolving structures associated with heterochromatin and repetitive DNA.…”

“…Lastly, we have found that aneuploidy, a severe form of genome instability that can promote chromosome rearrangements (Santaguida & Amon ), occurs in Lake Whitefish backcrosses (Dion‐Côté et al . ).…”

“…() with some modifications (Dion‐Côté et al . ). Between 0.2 and 2 mL of fresh blood was sampled with heparinized syringes and kept on ice for no more than 12 h. White blood cells were transferred to 5 mL of freshly prepared cell culture media [media 199 (Life technologies), 10% FBS (Sigma), 0.01% LPS (Sigma), 60 μg/mL kanamycin (Sigma), 18 μg/mL phytohemagglutinin (Sigma), 0.5× antibiotic antimycotic (Sigma) and 1.75 μL of 10% β‐mercaptoethanol per 100 mL of media].…”

“…Moreover, healthy and malformed backcrosses experience mitotic instability and meiotic breakdown respectively (Dion‐Côté et al . ), suggesting a role for a chromosomal component to reproductive isolation in Lake Whitefish. Nevertheless, it remains unknown whether chromosome rearrangements or structure changes occurred between normal and dwarf Lake Whitefish, nor is it known whether these potential changes played a role in reproductive isolation, given that only modest genetic differences have been documented between them.…”

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.…”