The Legacy of Sexual Ancestors in Phenotypic Variability, Gene Expression, and Homoeolog Regulation of Asexual Hybrids and Polyploids

Abstract

Hybridization and polyploidization are important evolutionary processes whose impacts range from the alteration of gene expression and phenotypic variation to the triggering of asexual reproduction. We investigated fishes of the Cobitis taenia-elongatoides hybrid complex, which allowed us to disentangle the direct effects of both processes, due to the co-occurrence of parental species with their diploid and triploid hybrids. Employing morphological, ecological, and RNAseq approaches, we investigated the molecular determinants of hybrid and polyploid forms. In contrast with other studies, hybridization and polyploidy induced relatively very little transgressivity. Instead, Cobitis hybrids appeared intermediate with a clear effect of genomic dosing when triploids expressed higher similarity to the parent contributing two genome sets. This dosage effect was symmetric in the germline (oocyte gene expression), interestingly though, we observed an overall bias toward C. taenia in somatic tissues and traits. At the level of individual genes, expression-level dominance vastly prevailed over additivity or transgressivity. Also, trans-regulation of gene expression was less efficient in diploid hybrids than in triploids, where the expression modulation of homoeologs derived from the “haploid” parent was stronger than those derived from the “diploid” parent. Our findings suggest that the apparent intermediacy of hybrid phenotypes results from the combination of individual genes with dominant expression rather than from simple additivity. The efficiency of cross-talk between trans-regulatory elements further appears dosage dependent. Important effects of polyploidization may thus stem from changes in relative concentrations of trans-regulatory elements and their binding sites between hybridizing genomes. Links between gene regulation and asexuality are discussed.

No evidence for accumulation of deleterious mutations and fitness degradation in clonal fish hybrids: Abandoning sex without regrets

“…(2014) and Bartoš et al. (2019) documented niche segregation between the Cobitis forms, suggesting some role of ecological factors.…”

Are you more than the sum of your parents’ genes? Phenotypic plasticity in a clonal vertebrate and F1 hybrids of its parental species

“…Both cis ‐ and trans ‐regulatory networks show unique patterns of expression in hybrid species, especially when comparing diploid to triploid individuals (Bartoš et al. 2019). Thus, adaptation might proceed just by modifying the innate parental regulatory pathways or genes under relaxed selection.…”

Genome fractionation and loss of heterozygosity in hybrids and polyploids: mechanisms, consequences for selection, and link to gene function

“…We evaluated the effects of allele expression on LOH occurrence using recently published transcription profiles of livers and oocytes in sexual (C. elongatoides, C. taenia) and asexual (ET, EET, and ETT) females (Bartoš et al 2019). While Bartoš et al analyzed different individuals, they used the same reference transcriptome and thus we could investigate the transcription profiles of those genes which carried E-T diagnostic SNPs and were either LOH-positive (E-like or T-like LOH bearing), or LOH-negative, according to present exomecapture results.…”

“…Realizing their evolutionary significance and huge practical value to mankind (Mason and Batley 2015), research focused on hybridization and polyploidy intensified and revealed some prominent patterns. For instance, hybrid phenotypes may range from intermediate forms to transgressive expression of novel traits (Bell and Travis 2005;Yoo et al 2014; Bartoš et al 2019); however, often, one parental subgenome is more expressed than the other one, known as expression dominance (Yoo et al 2014;Alexander-Webber et al 2016;Cheng et al 2018). Hybrid and polyploid genomes evolve dynamically and often lose orthologous genes from one or the other parental species in processes referred to as loss of heterozygosity (LOH), genome fractionation, or rediploidization in polyploids (Yoo et al 2014;Lien et al 2016;Du et al 2020).…”

“…This study investigated the dynamics of diploid and polyploid clonal genomes on the finer scale of individual genes. To achieve this aim, we performed exome sequencing of the sexual parental species and their clonal hybrids and subsequently compared the data to recently published gene expression profiles (Bartoš et al 2019). This allowed us to identify mechanisms underlying fractionation and LOH in clonal genomes and to test how they relate to expression and function of the affected genes.…”