Gene expression regulation and lineage evolution: the North and South tale of the hybrid polyploid Squalius alburnoides complex

Abstract

The evolution of hybrid polyploid vertebrates, their viability and their perpetuation over evolutionary time have always been questions of great interest. However, little is known about the impact of hybridization and polyploidization on the regulatory networks that guarantee the appropriate quantitative and qualitative gene expression programme. The Squalius alburnoides complex of hybrid fish is an attractive system to address these questions, as it includes a wide variety of diploid and polyploid forms, and intricate systems of genetic exchange. Through the study of genome-specific allele expression of seven housekeeping and tissue-specific genes, we found that a gene copy silencing mechanism of dosage compensation exists throughout the distribution range of the complex. Here we show that the allele-specific patterns of silencing vary within the complex, according to the geographical origin and the type of genome involved in the hybridization process. In southern populations, triploids of S. alburnoides show an overall tendency for silencing the allele from the minority genome, while northern population polyploids exhibit preferential biallelic gene expression patterns, irrespective of genomic composition. The present findings further suggest that gene copy silencing and variable expression of specific allele combinations may be important processes in vertebrate polyploid evolution.

Figure 1.

Distribution of S. alburnoides in the areas of sympatry with S. carolitertii (dark grey) and S. pyrenaicus (light grey). (a) The global composition of the populations of the complex in the two areas of sympatry are indicated, although local abundances can vary. (b) Samples collected in each location and reported frequencies of diploid (2N), triploid (3N) and tetraploid (4N) forms in Douro, Mondego and Tejo River basins.

Figure 2.

Relative expression (Ct) ratios between polyploid and diploid organ samples of individuals of the northern distribution of the complex, for the ef1a, gapdh, rpl8 and β-actin genes. Expected ratio of 1.5 in the case of no silencing 3n/2n (dashed line), expected ratio of 2, in the case of no silencing 4n/2n (dotted line) and expected ratio of 1 in the case of silencing (solid line). Observed 3n to 2n ratio (dark grey columns), observed 4n to 2n ratio (light grey columns), number of triploid and tetraploid triplicates analysed for each ratio calculation (N).