BACKGROUND: Legless lizards, the slow worms of the genus Anguis, are forming secondary contact zones within their Europe-wide distribution. METHODS: We examined 35 populations of A. fragilis and A. colchica to identify the level of morphological and genetic divergence in Poland. We applied a conventional study approach using metric, meristic, and categorial (coloration) features for a phenotype analysis, and two standard molecular markers, a mitochondrial (NADH-ubiquinone oxidoreductase chain 2; ND2) and a nuclear (V(D)J recombination-activating protein 1; RAG1) one. RESULTS: We found clear differences between A. fragilis and A. colchica in molecular markers and phenotype-in meristic features, e.g., ear opening, number of scales rows around the body, and higher than so far known diversity in ND2 and RAG1 haplotypes. The presence of five hybrids was detected in three populations in the Polish part of the European contact zone. In all hybrids, homozygous alleles of RAG1 were detected, which suggests a back-crossing within the genus. CONCLUSIONS: The ability to produce fertile offspring by A. fragilis x A. colchica hybrids shows inefficient mechanisms of reproductive isolation of the two legless lizards. The hybrids were indistinguishable from parental species in head proportions (principal components and discriminant analyses) but more resembling A. colchica in meristic traits.

• Keywords
• Anguidae, Biogeography, Hybridization, Morphometrics, Speciation, Taxonomy,
• MeSH
• Phenotype MeSH
• Genetic Variation MeSH
• Haplotypes genetics   MeSH
• Lizards * genetics   anatomy & histology   MeSH
• Reproductive Isolation MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Geographicals
• Poland MeSH
• Names of Substances
• Homeodomain Proteins MeSH
• RAG-1 protein MeSH Browser

Hybridization and polyploidy are powerful evolutionary forces, inducing a range of phenotypic outcomes, including non-additive expression, subgenome dominance, deviations in genomic dosage, and transcriptome downsizing. The reasons for these patterns and whether they are universal adaptive responses to genome merging and doubling remain debated. To address this, we develop a thermodynamic model of gene expression based on transcription factor (TF)-promoter binding. Applied to hybridization between species with divergent gene expression levels, cell volumes, or euchromatic ratios, this model distinguishes the effects of hybridization from those of polyploidy. Our results align with empirical observations, suggesting that gene regulation patterns in hybrids and polyploids often stem from the constrained interplay between inherited diverged regulatory networks rather than from subsequent adaptive evolution. In addition, occurrence of certain phenotypic traits depend on specific assumptions about promoter-TF coevolution and their distribution within the hybrid's nucleoplasm, offering new research avenues to understand the underlying mechanisms. In summary, our model explains how the legacy of divergent species directly influences the phenotypic traits of hybrids and allopolyploids.

• MeSH
• Phenotype MeSH
• Gene Regulatory Networks MeSH
• Hybridization, Genetic * MeSH
• Models, Genetic MeSH
• Evolution, Molecular MeSH
• Polyploidy * MeSH
• Promoter Regions, Genetic * genetics   MeSH
• Gene Expression Regulation, Plant MeSH
• Transcription Factors * genetics   metabolism   MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Names of Substances
• Transcription Factors * MeSH

Hybridization and genome duplication have played crucial roles in the evolution of many animal and plant taxa. The subgenomes of parental species undergo considerable changes in hybrids and polyploids, which often selectively eliminate segments of one subgenome. However, the mechanisms underlying these changes are not well understood, particularly when the hybridization is linked with asexual reproduction that opens up unexpected evolutionary pathways. To elucidate this problem, we compared published cytogenetic and RNAseq data with exome sequences of asexual diploid and polyploid hybrids between three fish species; Cobitis elongatoides, C. taenia, and C. tanaitica. Clonal genomes remained generally static at chromosome-scale levels but their heterozygosity gradually deteriorated at the level of individual genes owing to allelic deletions and conversions. Interestingly, the impact of both processes varies among animals and genomic regions depending on ploidy level and the properties of affected genes. Namely, polyploids were more tolerant to deletions than diploid asexuals where conversions prevailed, and genomic restructuring events accumulated preferentially in genes characterized by high transcription levels and GC-content, strong purifying selection and specific functions like interacting with intracellular membranes. Although hybrids were phenotypically more similar to C. taenia, we found that they preferentially retained C. elongatoides alleles. This demonstrates that favored subgenome is not necessarily the transcriptionally dominant one. This study demonstrated that subgenomes in asexual hybrids and polyploids evolve under a complex interplay of selection and several molecular mechanisms whose efficiency depends on the organism's ploidy level, as well as functional properties and parental ancestry of the genomic region.

• Keywords
• asexual reproduction, gene conversions, hemizygous deletions, hybridization, loss of heterozygosity, polyploidy,
• MeSH
• Diploidy MeSH
• Genome, Plant MeSH
• Hybridization, Genetic MeSH
• Cypriniformes * genetics   MeSH
• Evolution, Molecular MeSH
• Polyploidy * MeSH
• Loss of Heterozygosity MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH

Despite its inherent costs, sexual reproduction is ubiquitous in nature, and the mechanisms to protect it from a competitive displacement by asexuality remain unclear. Popular mutation-based explanations, like the Muller's ratchet and the Kondrashov's hatchet, assume that purifying selection may not halt the accumulation of deleterious mutations in the nonrecombining genomes, ultimately leading to their degeneration. However, empirical evidence is scarce and it remains particularly unclear whether mutational degradation proceeds fast enough to ensure the decay of clonal organisms and to prevent them from outcompeting their sexual counterparts. To test this hypothesis, we jointly analysed the exome sequences and the fitness-related phenotypic traits of the sexually reproducing fish species and their clonal hybrids, whose evolutionary ages ranged from F1 generations to 300 ky. As expected, mutations tended to accumulate in the clonal genomes in a time-dependent manner. However, contrary to the predictions, we found no trend towards increased nonsynonymity of mutations acquired by clones, nor higher radicality of their amino acid substitutions. Moreover, there was no evidence for fitness degeneration in the old clones compared with that in the younger ones. In summary, although an efficacy of purifying selection may still be reduced in the asexual genomes, our data indicate that its efficiency is not drastically decreased. Even the oldest investigated clone was found to be too young to suffer fitness consequences from a mutation accumulation. This suggests that mechanisms other than mutation accumulation may be needed to explain the competitive advantage of sex in the short term.

• Keywords
• Muller’s ratchet, asexuality, clonal decay, exome capture, fitness, mutation load,
• MeSH
• Biological Evolution * MeSH
• Emotions MeSH
• Genome MeSH
• Models, Genetic MeSH
• Mutation MeSH
• Reproduction, Asexual genetics   MeSH
• Reproduction * genetics   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH

Hybrid sterility is a hallmark of speciation, but the underlying molecular mechanisms remain poorly understood. Here, we report that speciation may regularly proceed through a stage at which gene flow is completely interrupted, but hybrid sterility occurs only in male hybrids whereas female hybrids reproduce asexually. We analyzed gametogenic pathways in hybrids between the fish species Cobitis elongatoides and C. taenia, and revealed that male hybrids were sterile owing to extensive asynapsis and crossover reduction among heterospecific chromosomal pairs in their gametes, which was subsequently followed by apoptosis. We found that polyploidization allowed pairing between homologous chromosomes and therefore partially rescued the bivalent formation and crossover rates in triploid hybrid males. However, it was not sufficient to overcome sterility. In contrast, both diploid and triploid hybrid females exhibited premeiotic genome endoreplication, thereby ensuring proper bivalent formation between identical chromosomal copies. This endoreplication ultimately restored female fertility but it simultaneously resulted in the obligate production of clonal gametes, preventing any interspecific gene flow. In conclusion, we demonstrate that the emergence of asexuality can remedy hybrid sterility in a sex-specific manner and contributes to the speciation process.

• Keywords
• Cobitis, clonality, endoreplication, gynogenesis, hybridization, meiosis, polyploidy, speciation,
• MeSH
• Biological Evolution MeSH
• Chromosomes MeSH
• Hybrid Cells cytology   physiology   MeSH
• Infertility genetics   MeSH
• Meiosis * MeSH
• Parthenogenesis * MeSH
• Fishes genetics   physiology   MeSH
• Genetic Speciation * MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH