Evolution by polyploidy Dan Graur Polyploidy the addition

Evolution by polyploidy Dan Graur

Polyploidy = the addition of one or more complete sets of chromosomes to the original set. two copies of each autosome = diploid four copies of each autosome = tetraploid six copies of each autosome = hexaploid The gametes of diploids are haploid, those of tertraploids are diploid, those of hexaploid are triploid, and so on. Organisms with an odd number of autosomes, e. g. , the domestic banana plant (Musa acuminata), cannot undergo meiosis or reproduce sexually. Musa barbisiana (diploid) Musa acuminata (triploid)

Two main types of polyploidy: autopolyploidy (genome doubling) = the multiplication of one basic set of chromosomes allopolyploidy = the combination of genetically distinct, but similar chromosome sets. Autopolyploids are derived from within a single species; allopolyploids arise via hybridization between two species.

autopolyploidy 4

autopolyploidy Autopolyploidy may be common in plants, although its prevalence may be underestimated in the taxonomic literature. One species that is doubtlessly a true autopolyploid, rather than an allopolyploid derived from two very similar diploids, is the potato, Solanum tuberosum 5

autopolyploidy Advantage of autopolyploidy: 1. 2. 3. Much higher levels of heterozygosity than do their diploid progenitors due to polysomic inheritance Maintenance of more than two alleles per locus, allowing them to produce a larger variety of allozymes than diploids Larger effective population sizes than diploids, allowing selective processes to be much more effective relative to random genetic drift. 6

autopolyploidy Much higher levels of heterozygosity than do their diploid progenitors due to polysomic inheritance • Let us consider, for example, an autotetraploid (aabb) derived from a heterozygous diploid (ab). • Assuming simple tetrasomic inheritance, the genotype aabb is expected to produce diploid gametes in the ratio 1 aa: 4 ab: 1 bb. • In the progeny, the ratio of the genotypes will be 1 aaaa: 8 aaab: 18 aabb: 8 abbb: 1 bbbb. • That is, heterozygotes (aaab, aabb, abbb) are expected to outnumber homozygotes (aaaa, bbbb) 17 to 1. • In comparison, in diploids the heterozygote to homozygote ratio is 1: 1. 7

autopolyploidy Disadvantages of autopolyploidy: (1) prolongation of cell division time (2) increase in the volume of the nucleus (3) increase in the number of chromosome disjunctions during meiosis (4) genetic imbalances (5) interference with sexual differentiation when the sex of the organisms is determined by either the ratio between the number of sex chromosomes and the number of autosomes (as in Drosophila), or by degree of ploidy (as in Hymenoptera). 8

allopolyploidy 9

Allopolyploidy is much more common in nature than autopolyploidy. About 80% of all land plants may be allopolyploids. Red circles indicate instances of allopolyploidy. The blue circle indicates an instance of autopolyploidy. The green square indicates a putative triplication event before the divergence among dicotydelons. The two black ovals indicate an ancestral angiosperm genome duplication (190 -230 million years ago) and an ancestral seed-plant duplication (320 -350 million years ago).

Triticum urartu (AA) Aegilops speltoides (BB) T. turgidum (AABB) T. tauschii (DD) The common bread wheat (Triticum aestivum) is an allohexaploid containing three distinct sets of chromosomes derived from three different diploid species of goat-grass (Aegilops) through a tetraploid intermediary (durum wheat). T. aestivum (AABBDD) 11

In animals, allopolyploidy is rare. Allopolyploidy was found in insects, fish, reptiles, and amphibians. For example, Xenopus laevis, the African clawed frog of laboratory fame, is an allotetraploid. No cases of polyploidy have ever been found in birds. Two mammalian species are suspected tetraploids, the red vizcacha rat (Tympanoctomys barrerae) and the golden vizcacha rat (Pipanacoctomys aureus), however, some disagreement exists in the literature. 4 N = 100 + XY

Consequences of polyploidy At a phenotypic level, the effects of polyploidization are often mild. In many cases, polyploidy seem to have almost no effect on the phenotype. For example, diploid, autopolyploid, and allopolyploid Chrysanthemum species vary in chromosome number from 18 to 198, yet they are almost indistinguishable from one another. Similar observations have been made in roses (Rosa), leptodactylid toads (Odontophrynus), and goldfish (Carasius).

A tale of two daisies Haplopappus gracilis (yellow spiny daisy) = 4 chromosomes Senecio roberti-friesii (Robert & Friesi’s groundsel, belongs to the daisy family) = 90 chromosomes

Consequences of polyploidy Cell volume generally rises with increasing genome size, although the exact relationship between ploidy and cell volume varies among environments and among taxa. Although average cell size is larger in polyploids, the size of the adult polyploidy organism may not be altered. As a rough generalization, polyploidization is more likely to increase adult body size in plants and invertebrates than in vertebrates. The poor correlation between cell size and organismal size was even remarked upon by Albert Einstein, who stated: “Most peculiar for me is the fact that in spite of the enlarged single cell, the size of the animal is not correspondingly increased. ”

Following polyploidization, all genes become duplicated = OHNOLOGS

An important feature of many newly formed polyploids is that their genomes are unstable and undergo rapid repatterning and segmental loss. The rapidity of gene loss is illustrated by the bread wheat, Triticum aestivum, an allohexaploid that may have originated as early as 10, 000 years ago. In this very short time, many of the triplicated loci have been silenced. It has been estimated that the proportion of enzymes produced by triplicate, duplicate, and single loci in wheat is 57%, 25%, and 18%, respectively.

Sometimes duplicates persist for long periods of time ~8% of duplicated genes have remained in yeast about 100 million years following allotetraploidization. ~77% of ohnologs are still detectable in Xenopus laevis about 30 million years after allotetraploidization.

Consequences of polyploidy (continued) Transposable elements that had been repressed within each parent lineage may be activated in hybrids, and can facilitate the movement of genes and promote unequal crossing over. Polyploidy is an important factor in speciation. In particular, sexually reproducing autotetraploids are automatically isolated from their diploid progenitors because they produce diploid gametes; were these to combine with the haploid gametes of the diploids, they would give rise to triploid progeny.

Consequences of polyploidy (continued) Stebbins (1971) postulated that polyploids represent dead ends because of the inefficiency of selection when deleterious alleles can be masked by multiple copies. Mayrose et al. (2011) provided quantitative corroboration of the dead-end hypothesis by showing that speciation rates of polyploids are significantly lower than those of diploids, and their extinction rates are significantly higher. G. Ledyard Stebbins Sally Otto

• Diploidization is the evolutionary process whereby a tetraploid species “decays” to become a diploid with twice as many distinct chromosomes. • The key event in diploidization is the switch from having four chromosomes that form a quadrivalent at meiosis, to having two pairs of chromosomes each of which forms a bivalent. • In population-genetics terms, this is the switch from having four alleles at a single locus (tetrasomic inheritance) to having two alleles at each of two distinct loci (disomic inheritance).

A newly created polyploid = Neopolyploid Polyploid after diploidization = Paleopolyploid (diploid ancestors unknown or extinct) or Mesopolyploids (diploid ancestors known and extant) Cryptopolyploid (literally, a hidden polyploid) = an ancient polyploid that is no longer distinguishable from a diploid.

Distinguishing between gene duplication and genome duplication Most genomes contain gene duplications. They can either be the result of gene duplication or whole genome duplications. How can one distinguish between the two mechanisms?

Expectation: Following polyploidization, all the paralogous genes in the genome (ohnologs) should each yield the same tree (b). If, however, the paralogous genes yield alternative trees (c or d), then it is unlikely that all the gene duplications occurred at the same time. polyploidy

Regions of Double Synteny Two or more genomic regions containing paralogous arrays of genes.

Is Saccharomyces cerevisiae a cryptotetraploid? Wolfe and Shields (1997) searched the complete yeast proteome for regions of double synteny. The criteria used for defining two regions as duplicated were: (1) a sequence similarity between the two regions associated with a probability of less than 10– 18 of it being fortuitous (2) at least three protein-coding genes or open-reading frames in common, with intergenic distances of less than 50 Kb (3) conservation of gene order and orientation of the genes relative to the centromere.

54 nonoverlapping pairs of duplicated regions spanning about 50% of the yeast genome. ~900 of the ~5, 800 genes in the yeast genome, are paralogs located in duplicated chromosomal regions (blocks of doubly conserved synteny or 27 paralogons).

2 possible explanations: (1) the duplicated regions were formed independently by regional duplications occurring at different times. (2) the duplicated regions have been produced simultaneously by a single tetraploidization event, followed by genome rearrangement and loss of many redundant duplicates. 28

50/54 duplicated regions have maintained the same orientation with respect to the centromere. 54 independent regional duplications are expected to result in ~7 triplicated regions (i. e. , duplicates of duplicates), but none was observed. 29

Loss of 92% of the duplicate genes. Occurrence of 70 -100 map disruptions. 30

The expected genomic signature of whole genome duplication: Following duplication, sister regions would undergo gene loss by deletion; one or the other of the two paralogous copies of each gene would be lost in most cases, with both paralogs being retained only very rarely. Eventually, the only residual signature to show that two regions arose from ancestral duplication is the presence of a few paralogous genes in the same order and orientation scattered amidst a multitude of unrelated genes.

Close up to one example:

Vertebrate polyploidy? The 2 R hypothesis A simple expectation of the 2 R hypothesis: In the absence of any gene duplications prior, in between, or subsequent to the two rounds of genome duplication, the expectation is an (AB)(CD) topology, where A, B, C, and D are paralogous genes (a). Any other topology (b, c) may be interpreted as a refutation of the 2 R hypothesis.

Vertebrate polyploidy? The 2 R hypothesis Out of the 92 resolved phylogenetic topologies, only 22 topologies (24%) supported the 2 R hypothesis. Out of the 53 phylogenies in which all internal branches received statistically significant support, only 11 topologies (21%) supported the 2 R hypothesis, leading the authors to reject the hypothesis.

Vertebrate polyploidy? The 2 R hypothesis The previous test was very strict. If one selects only those human paralogs that have duplicated before divergence of tetrapods from the bonny fishes, the 2 R hypothesis cannot be rejected. Moreover, molecular clock analyses of all protein families in humans that have orthologs in Drosophila and C. elegans indicated that a burst of gene duplication activity (polyploidization? ) took place 350 – 650 million years ago.

A cryptooctoploid (Homo sapiens) and a cryptosedectoploids (Cyprinus carpio)? 36