Cyprinidae

Polyploid evolution in Cyprinidae View in CoL .

The achievement of evolutionary novelty is challenging due to the multitude of evolutionary pressures and the lengthy process of mutation and selection. On rare occasions, species hybridisation may result in fertile hybrids that exhibit an ecological benefit from the novel combination of genes and the subsequent morphological, physiological, and behavioural characteristics. However, hybrids of very different species may encounter difficulties due to the distinctiveness of their genomes, which may prevent the normal meiotic process essential for the formation of gametes (egg and sperm). Such hybrids are often sterile and unable to transmit their novel character combination to the next generation. Numerous hybrids between different species in Cyprinidae and Leuciscidae are known, and it is assumed that hybridisation, even between distantly related fish species, has occurred frequently for millions of years.

In exceptional cases, a hybrid may exhibit a doubling of chromosomes inherited from each parent, restoring meiotic pairing and fertility. This process, known as polyploidisation, results in a transition from a diploid, sterile hybrid to a tetraploid, fertile hybrid. Additionally, fish can duplicate their genome during their ontogenetic development, resulting in a doubling of the number of chromosomes inherited from the same parental species. This phenomenon, known as auto-polyploidisation, occurs independently of hybridisation. In a further pathway, a hybrid between species produces clonal, full-genomic gametes with two sets of chromosomes, as in all other body cells. This is an accidental occurrence in the gamete-tissue. In such a diploid, the clonal egg is fertilised by a haploid sperm, resulting in triploid offspring. Triploid individuals, which are usually females, experience difficulties in producing gametes via meiosis and are once again sterile. Except in the case in which the female may again produce clonal eggs, now with three sets of chromosomes (as in many Carassius ), the offspring will be tetraploid (with four copies of each chromosome) if a haploid sperm of the parental species fertilise these. These hybrids are viable and fertile and may have a double-size genome, with four sets of chromosomes from each parental species. This represents one pathway in the process of allo-polyploidisation. Other pathways include F1 hybrids producing clonal, diploid eggs and sperm. In all cases, the fish overcomes the sterility associated with hybrids as soon as an even (4 n, 6 n) chromosome number has been re-established with even numbers of chromosomes from each parental species.

In evolutionary terms, polyploidisation is rare in vertebrates, occurring only in a few fish groups, including sturgeons and some cypriniforms. Many of the polyploidisation events in Cyprinidae are ancient, having happened at the base of large radiations that are recognised at the generic or subfamily level today. One example is an allo-tetraploidisation event at the root of all barbels (Barbini), which are all tetraploid. The allo-tetraploidisation event at the root of Cyprinini (carps and goldfish) is believed to have occurred approximately 12 million years ago, at the end of the middle Miocene. The hybridisation event leading to the hexaploid genus Capoeta occurred more recently, during the late Miocene. As previously discussed in the context of Capoeta , identifying the parental species associated with allo-polyploidisation events is of interest. In the case of Cyprinini , one species of Barbini or Acrossocheilini was potentially the maternal contributor. In contrast, a species closely related to or included within Labeonini was potentially the paternal source. These can be identified as each polyploid fish possesses each gene four times (if tetraploid), with two copies originating from the mother and two from the father. As both parental species may have been only distantly related, the phylogeny of the polyploid fish has two roots. It does not follow the “tree-like” evolutionary pathway often seen in textbooks. This phenomenon makes it difficult to reconstruct the phylogeny of cyprinid fishes, which is why we still have a poor understanding of the relationships of different groups of Cyprinids. It is noteworthy that maternal subgenomes frequently predominate in the genomes, a phenomenon that introduces an additional layer of complexity.

One might inquire why polyploidy is so uncommon in fishes compared to plants. Polyploid animals appear to encounter significant challenges in coping with genomic and developmental chaos from merging two genomes. A fish cannot organise its functions from its new genome, as conflicting recipes exist for the same transcriptional challenges. Fish employ diverse strategies to balance dynamic subgenomic diversification during continuous re-diploidisation. They regain functional diploidy over time by eliminating certain parts of their genome, potentially those that disrupt transcription. Originally, polyploid fishes became functional diploids again through this process. This phenomenon is observed in numerous species within the Cyprinidae family.

Further reading. Otto & Whitton 2000 (evolution); Mable 2013 (ecological benefits of polyploids and hybrids); Yang et al. 2015 (phylogeny of Cyprinidae ); Ma et al. 2014 (timing of polyploidisations in Cyprinini ); Luo et al. 2020 (diploidisation); Xu et al. 2023 (subgenomic differentiation).