Polyploids — organisms that have multiple sets of chromosomes — are common in certain plant and animal taxa, and can be surprisingly stable. The evidence that has emerged from genome analyses also indicates that many other eukaryotic genomes have a polyploid ancestry, suggesting that both humans and most other eukaryotes have either benefited from or endured polyploidy. Studies of polyploids soon after their formation have revealed genetic and epigenetic interactions between redundant genes. These interactions can be related to the phenotypes and evolutionary fates of polyploids. Here, I consider the advantages and challenges of polyploidy, and its evolutionary potential.

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The advantages and disadvantages of being polyploid

Polyploid fish and shellfish: Production, biology and applications to aquaculture for performance improvement and genetic containment

Although polyploidy has been involved in speciation in both animals and plants, the general perception is often that it is too rare to have been a significant factor in animal evolution and its role in plant diversification has been questioned. These views have resulted in a bias towards explanations for what deters polyploidy, rather than the somewhat more interesting question of the mechanisms by which polyploidy arises and becomes established in both plants and animals. The evidence for and against some of the traditional views on polyploidy is reviewed, with an attempt to synthesize factors promoting evolution through genome duplication in both groups. It is predicted that polyploidy should be more common in temperate than in tropical breeders because environmental fluctuations may promote unreduced gamete formation, it should be most common in organisms with sufficient numbers of gametes that random meiotic problems can be overcome, and it should be more frequent when mechanisms to promote assortative mating are a direct byproduct of genome duplication. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 453‐466.

‘why polyploidy is rarer in animals than in plants’: myths and mechanisms

Whole genome duplication (leading to polyploidy) is widely accepted as an important evolutionary force in plants, but it is less recognized as a driver of animal diversification. Nevertheless, it occurs across a wide range of animals; this review investigates why it is particularly common in fish and amphibians, while rare among other vertebrates. We review the current geographic, ecological and phylogenetic distributions of sexually reproducing polyploid taxa before focusing more specifically on what factors drive polyploid formation and establishment. In summary, (1) polyploidy is phylogenetically restricted in both amphibians and fishes, although entire fish, but not amphibian, lineages are derived from polyploid ancestors. (2) Although mechanisms such as polyspermy are feasible, polyploid formation appears to occur principally through unreduced gamete formation, which can be experimentally induced by temperature or pressure shock in both groups. (3) External reproduction and fertilization in primarily temperate freshwater environments potentially exposes zygotes to temperature stress, which can promote increased production of unreduced gametes. (4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by shifts in mating system more than ploidy. However, insufficient data currently exist to provide rigorous tests of these hypotheses and we make a plea for zoologists to also consider polyploidy as a possibility in continuing taxonomic surveys.

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Genome duplication in amphibians and fish: an extended synthesis

A unisexual species is generally associated with polyploidy, and reproduced by a unisexual reproduction mode, such as gynogenesis, hybridogenesis or parthenogenesis. Compared with other unisexual and polyploid species, gibel carp (Carassius auratus gibelio) has a higher ploidy level of hexaploid. It has undergone several successive rounds of genome polyploidy, and experienced an additional, more recent genome duplication event. More significantly, the dual reproduction modes, including gynogenesis and sexual reproduction, have been demonstrated to coexist in the polyploid gibel carp. This article reviews the genetic basis concerning polyploidy origin, clonal diversity and dual reproduction modes, and outlines the progress in new variety breeding and gene identification involved in the reproduction and early development. The data suggests that gibel carp are under an evolutionary trajectory of diploidization. As a novel evolutionary developmental (Evo-Devo) biology model, this work highlights future perspectives about the functional divergence of duplicated genes and the sexual origin of vertebrate animals.

Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio

Green toads are common in the Palaearctic region, where they have differentiated into several taxa. The toads exist with variable amounts of ploidy, similar to other anuran species or reptiles. In vertebrate biology, the very rare occurrence of triploidy is coupled with infertility or unisexuality, or requires the coexistence of individuals of different ploidy in a reproductive community. The reproduction of naturally occurring triploids has been reported to occur only through parthenogenesis, gynogenesis or hybridogenesis. The bisexual reproduction of pure triploids has been considered to be impossible because of the problem of equally distributing three chromosome sets in meiosis. Here we report geographically isolated populations of green toads (Bufo viridis complex) that are all-triploid and reproduce bisexually.

Thomas Klapperstück

Papers

A bisexually reproducing all-triploid vertebrate