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Heterozygosity, Heteromorphy, and Phylogenetic Trees in Asexual Eukaryotes

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Heterozygosity, Heteromorphy, and Phylogenetic Trees in Asexual Eukaryotes Copyright 0 1996 by the Genetics Society of America Heterozygosity, Heteromorphy, and Phylogenetic Trees in Asexual Eukaryotes C. William Birky, Jr. Department of Molecular Genetics, The Ohio State University, Columbus, Ohio 43210 Manuscript received September 18, 1995 Accepted for publication June 18, 1996 ABSTRACT Little attention has been paid to the consequences of long-term asexual reproduction for sequence evolution in diploid or polyploid eukaryotic organisms. Some elementary theory shows that the amount of neutral sequence divergence between two alleles of' a protein-coding gene in an asexual individual will be greater than that in a sexual species by a factor of Ztu, where t is the number of generations since sexual reproduction was lost and u is the mutation rate per generation in the asexual lineage. Phylogenetic trees based on only one allele from each of two or more species will show incorrect divergence times and, more often than not, incorrect topologies. This allele sequence divergence can be stopped temporarily by mitotic gene conversion, mitotic crossing-over, or ploidy reduction. If these convergence events are rare, ancient asexual lineages can be recognized by their high allele sequence divergence. At intermediate frequencies of convergence events, it will be impossible to reconstruct the correct phylogeny of an asexual clade from the sequences of protein coding genes. Convergence may be limited by allele sequence divergence and heterozygous chromosomal rearrangements which reduce the homology needed for recombination and result in aneuploidy after crossing-over or ploidy cycles. EGINNING with the pioneering studies of HUBBY ments resulting in heteromorphy (WHITE 1973). This B and LEWONTIN(1966) and-S (1966),popu- prediction has been verified by recent sequence analy- lation geneticists have analyzed the diversity of genes ses for some asexual species but not others. at the molecular level in populations, and heterozygos- Some basic theory presented here shows that neutral ity in individuals, in increasing detail ( reviewed by AWSE allele sequence divergence can accumulate to a high 1994). These studies initially used protein electropho- degree in asexual lineages. High levels of divergence resis to distinguish alleles, a method that detects much in a lineage are evidence that it has been asexual for a but not all of the actual sequence differences between very long time, and the numberof different alleles can alleles. The use of restriction analysis to detect restric- be used to determine the ploidy in eukaryotic microor- tion fragment polymorphism allowed the detection of ganisms where conventional cytological methods fail. some of the synonymous, as well as nonsynonymous, However, sequence divergence can be reducedor elimi- sequence differences between alleles. The logical exten- nated by gene conversion, mitotic crossing-over, or re- sion of these studies was the detection of all sequence duction of ploidy. These convergence processes can be variation in a sample of alleles byDNA sequencing identified if they occur infrequently and sufficiently ( KREITMAN 1983). This approach has been applied to many genes are examined. Allele sequence divergence a number of genes in Drosophila, a sexual diploid. Al- confounds phylogenetic analysis, causing gene trees to though the two alleles of a nuclear gene in a diploid depart drastically from species trees and making it dif- individual could show moderate sequence differences, ficult or impossible to recover the correct treetopology. no attempt has been made to sequence both alleles This has profound implications for the use of protein- from individual organisms, presumably because the dif- coding genes for phylogenetic reconstruction in evolu- ference between alleles in an individual will be similar tionary studies or to study epidemics of eukaryotic to that between alleles from any two randomly chosen pathogens. Testing theories about the evolutionary ad- organisms in a random matingsexual species. Only re- vantages and disadvantages of asexual reproduction of- cently has sequence analysis been extended to diploid ten requires knowing howlong asexual lineages survive or polyploid eukaryotes that reproduce strictly asexu- and theextent to which detrimental mutations accumu- ally.If asexual reproduction involvesonly mitotic late in diploids and polyploids, information that can be (equational) divisions, the two (or more) alleles of a obtained by studying all alleles in each clone. gene in an asexual lineage can show extremely high levels of heterozygosity; in addition, homologous chro- ALLELE SEQUENCEDIVERGENCE mosomes can acquire different chromosome rearrange- Alleles are alternate forms of a gene thatdiffer from Cmresponding uulhw: C. William Birky, Jr., Departmentof Molecular Genetics, The Ohio State University, 484 West 12th Ave., Columbus, each other in base sequence but code for the same OH 43210. E-mail: [email protected] polypeptide or RNA product when functional. They Genetics 144: 427-437 (September, 1996) 428 Birky usually occupy the same locus on a particular chromo- Now consider a sexual species in which a mutant some. In diploid (or polyploid) organisms, the two (or diploid individual gives rise to an asexual lineage. In the more) copies of a gene can be the same or different asexual lineage, the expected number of substitutions alleles, referred to as homozygosity and heterozygosity. between alleles within an individual will be increased Organisms that reproduce sexually at least occasionally to can produce offspring with new combinations of alleles, k = 4Nu 2tu = 2u(2N, t) (1) so no one lineage “owns” any pair of alleles (except + + in the case of obligate selfers ) . Although the alleles in where t is the number of generations since the origin a single individual may accumulate differentmutations, of the asexual lineage. most of the sequence divergence of those alleles has These relationships are illustrated in Figure 1, in been acquiredover manygenerations in many different which the total number of substitutions separating al- individuals. In contrast, organisms thatreproduce leles 3 and 4 in the asexual species Al, or alleles 5 and strictly asexually do not share alleles among lineages. 6 in asexual species A2, is 2 ( tl + b)u + 4Neu,compared The two (or more)alleles in an asexual lineage begin with 4N,u for alleles 1 and 2 in the sexual species S. to acquire different mutations from the moment that The difference is potentially very large; for example, if sexual reproduction is lost. If asexual reproduction con- 4N,u = 10 -‘(estimated by the nucleotide diversity T; tinues for a long time, the majority of the differences AWSE1994; MORIYAMAand POWELL1996), u = 5 X in sequence between alleles is acquired after sexual re- 10 mutations per base pair per generation ( LI et al. production was lost, and is unique to each lineage and 1985; WOLFEet al. 1989), there is one generation per each individual. I refer to the difference in sequence year, and tl + tr = 10 million years, then the expected between two or more alleles in an asexual cell as intra- number of substitutions between alleles is 0.01 in the cellular allele sequence divergence, hereafter ASD. sexual species and 0.11 in the asexual species. In fact, ASD can be detected by any of the molecular meth- 4N,u will be insignificant relative to 2 ( tl + b)u when ods normally used to distinguish between alleles. Se- sexual reproduction was lost >10 mya, as is true for a quencing provides the most detail, while restriction number ofcases (JUDSON and NORMARK1996). Al- analysis detects ASD in a sample of sites. Enzyme elec- though the alleles may be very different with respect to trophoresis can be used to detect heterozygosity of pro- base substitutions, especially in the third codon posi- tein-coding genes, butis basically qualitative rather than tion, they will continue to be recognizable as being quantitative because it fails to detect all synonymous the same gene and coding for proteins with the same substitutions and some nonsynonymous substitutions. function so long as selection favors individuals with two Strictly speaking, ASD refers to sequence differences functional copies of the gene. This is likely to be true among the alleles in a single cell. However, the alleles for many, if not all, genes in a diploid because inactiva- are normally isolated from a clone of cells or of multi- tion of one copy of a gene often causes detrimental cellular organisms. So long as the clone is young, the gene dosage effects. Note that these comments also alleles in the clone will be accurate copies of those in apply to dikaryotic organisms which have two different the single cell that gave rise to the clone. nuclei, usuallywith complete genomes, ineach cell (e.g., diplomonads such as Giardia and some fungi). NEUTRAL ASD Of course ASD will not increase indefinitely: the rate In asexually reproducing diploid species, population of increase will slow ast increases because multiple sub- genetic theory predicts, and observation confirms, that stitutions at the same site are not always detectable. the neutral sequence divergence between two alleles of Consequently the observed neutralsequence diver- a gene in a single individual will be low. In a random gence will asymptotically approach ’/+The true num- mating population, the expected number of substitu- ber of substitutions can be calculated from the observed tions between two different alleles is k = 4N,u differ- number by an appropriate method of correcting for ences per site where N, is the effective population size multiple hits ( LI et nl. 1985). and u is the mutation rate per site (base pair oramino Phylogenetic trees with two or more asexual species: acid) per generation. This is because the average time A second remarkable consequence of asexual reproduc- to the last common ancestor of two alleles, their coales- tion is that the two alleles in an individual may differ cent, is 2N, generations; since mutations accumulate from each other more than each does from an allele along both lineages after the coalescent, the total diver- in a related species or clone in the same asexual clade.
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