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Evolutionary Dynamics of Mitochondrial DNA Duplications in Parthenogenetic Geckos, Heteronotia Binoei

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Evolutionary Dynamics of Mitochondrial DNA Duplications in Parthenogenetic Geckos, Heteronotia Binoei Copyright 0 1991 by the Genetics Society of America Evolutionary Dynamics of Mitochondrial DNA Duplications in Parthenogenetic Geckos, Heteronotia binoei Craig Moritz Department of Zoology, University of Queensland, Brisbane, Queensland, Australia 4072 Manuscript received August 22, 1990 Accepted for publication May 1 1, 199 1 ABSTRACT Mitochondrial DNA (mtDNA) fromtriploid parthenogenetic geckos of the Heteronotia binoei complex varies in size from 17.2 to 27.6 kilobases (kb). Comparisons of long us. short genomes using restriction endonucleases revealed a series of tandem direct duplications rangingin size from 1.2 to 10.4 kb. This interpretationwas supported by transfer-hybridization experimentswhich also demon- strated that coding sequenceswere involved. Someof the duplications have been modifiedby deletion and restriction site changes, butno other rearrangements were detected. Analysis of the phylogenetic and geographic distribution of length variation suggests that duplications have arisen repeatedly within the parthenogenetic form of H. binoei. The parthenogens, and thus the duplications, areof recent origin; modificationsof the duplicated sequences, particularly by deletion, has therefore been rapid. The absence of duplications from the mtDNA of the diploid sexual populations of H. binoei reinforces the correlation between nuclear polyploidy and duplication of mtDNA sequences reported for other lizards. In comparison to the genomes of sexual H. binoei and of most other animals, the mtDNA of these parthenogenetic geckosis extraordinarily variablein length and organization. ONTRARY to previous assertions of extreme acting against thestrong geneticdrift of oocyte C economy and conservative organization (WAL- mtDNA, to maintainheteroplasmy (DENSMORE, LACE 1982; SEDEROEF1984; ATTARDI1985), there WRIGHT and BROWN1985; RAND and HARRISON have been several recent reports ofanimal mitochon- 1986; BUROKERet al. 1990). Analysis of segregation drial DNAs (mtDNAs) with large-scale size variation among the progenyof heteroplasmic females suggests attributableto repetitive sequences (Table 1). To- that smaller molecules may be at an advantage (RAND gether with numerous reports of intra-individual size and HARRISON1986), althoughin Drosophila the bias polymorphism (heteroplasmy, Table 1 and BIRMING- varies with the age of the female (SOLIGNACet al. HAM, LAMBand AVISE 1986) and variation in gene 1987). Comparisons among related species of lizards order (WOLSTENHOLMEet al. 1985; DUBIN,HSU-CHEN (DENSMORE,WRIGHT and BROWN 1985;DENSMORE et and TILLOTSEN1986; HAUCKEand GELLISSEN1988; al. 1989; MORITZ,WRIGHT and BROWN 1989),crick- GAREY andWOLSTENHOLME 1989; DESJARDINSand ets(RAND and HARRISON1989) and bark weevils MORAIS1990) these studies reveal a genome more (BOYCE,ZWICK and AQUADRO1989) revealed that plastic than previously supposed. It now seems that these noncoding tandem repeatsare often maintained the duplication and transposition of sequences is an through speciation events. Thus, any selection against importantmode of mtDNAevolution (MORITZ, large molecules must be balanced by recurrent muta- DOWLINGand BROWN1987; JACOBS et al. 1989; CAN- tion. TATORE et al. 1987). Most of the length variation that has been charac- A different form of length variation, involving the terized is due tovariation in the number of copies of tandemduplication of coding sequences, has been tandemlyrepeated noncoding sequences fromthe reported in mtDNAsfrom newts, nematodes, and control region (Table 1). Repeat units of this type lizards (Table 1). These duplications vary in size from vary in size from 64 base pairs (bp) in mtDNA from 1.1 to 8.0 kb and typically span or flank the control Cnemidophorus lizards (DENSMORE,WRIGHT and region. All known duplications of animal mtDNA BROWN 1985)to 2.0 kb in bark weevils (BOYCE,ZWICK coding sequences are tandem and direct,except in the and AQUADRO1989). In two groups with exception- nematode Romanomermis (HYMAN,BECK and WEISS ally large mtDNA, scallops (SNYDERet al. 1987; LA 1988) where there appears to be a partial, inverted ROCHEet al. 1990) and bark weevils, the additional copy disjunct from three tandem direct repeats. In DNA is largely due to these tandemly repeated se- contrastto the noncodingrepeats, duplications of quences. Several studies have suggested that copy coding sequencesare rarely heteroplasmicand appear number of the noncoding repeats changes rapidly, to beephemeral in that not one is sharedamong (knetics 129: 221-230 (September, 1991) 222 C. Moritz TABLE 1 Characteristics of repeated sequences (>20 bp) in animal mtDNA Shared between Location or Species Size species? Copy No. content Heteroplasmy Reference 1. Noncoding sequences Cnemidophorus spp. 64 bp Yes 3-9 Control region 15/92 DENSMORE,WRIGHK and BROWN(1 985) Acipens transmontanus 82 bp ? 1-4 Control region 521128 BUROKERet al. (1990) Gryllus spp. 206 bp Yes 2-7 Control region 1471319 RANDand HARRISON(1989) Drosophila spp. 470 pb Yes 2-6 Control region 17/92 SOLIGNACet al. (1986); HALEand SINGH(1 986) Pissodes spp. 0.8-2.0 kb Yes Control region 2191219 BOYCE,ZWICK and AQUADRO(1 989) Alosa sapidissma 1.5 kb ? 2-3 Control region 301244 BENTZEN,LEGGETT and BROWN(1 988) Placopecten magellias 1.4 kb 2-7 ? 181250 LA ROCHEet al. (1990) 2. Coding sequences Cnemidophurus spp. 1.5-8.0 kb No 2 Variable 1/43 MORITZand BROWN(1 987) Triturus 1.1-8.5 kb NO 2-3 Variable 213 WALLIS(1 987) Romanomermis 3.0 kb ? 3-5 ? None HYMAN,BECK and WEISS(1988) closely related species (Table 1) (MORITZ, DOWLING SEXUAL lcAsl S M6 and BROWN 1987). DIPLOID (0153) (0150) Previously reported duplications of mtDNA coding 9 sequences have been taxonomically or geographically isolated, offering little scope for analysis of their evo- CABISM6 PARTHENOGENETIC lutionary dynamics. In particular, thereis no evidence DIPLOID 7 (7) on the form and rate of sequence evolution within repeated mtDNAgenes. Is there selection for a return to small genome size? Doesthe presence of redundant sequences permitforms of sequence evolution (re- viewed in BROWN1985) not usually seen in animal mtDNA? J PARTHENOGENETIC ‘A’ ‘B + C’ This report concerns variation in the size and dis- TRIPLOIDS tribution of large tandem duplications of coding se- mlCA61SMB mlSM6lSM6 quences in mtDNA from parthenogenetic(all-female) (25154) (32133) FIGURE1 .-Evolutionary history of parthenogenetic H. binoei geckos of the Heteronotia binoei complex. These par- and their mtDNA (boxed). Analyses of chromosome and allozyme thenogens are triploid and arose via multiple inde- variants suggest thatthe parthenogens arose through multiple pendent hybridization events involving two chromo- hybridization events between the “CA6” and ”SM6” sexual races some races (“CA6” and “SM6”) of sexual H. binoei (MORITZ1984; MORITZet al. 1989). The predicted diploid-hybrid (Figure 1) (MORITZ 1983). The parthenogenetic line- intermediate has never been found despite intensive collecting and may no longer exist. The mtDNA of the parthenogens analyzed in ages are now distributed throughout most of the this reportare most similar to those from western Australian central and western deserts of Australia and, for a populations of the CA6 type (MORITZ 1991). The “A” and “B + C” parthenogenetic vertebrate, have extraordinarily high are designations for the two major chromosome classes of triploids genetic (allozymic and chromosomal) diversity within that are derived from different types of backcross. The frequency and between lineages (MORITZet al. 1989). There are of duplications in each type of lizard is given in parentheses. two major chromosome lineages that differ in the dosage of the parental genes and which are thought hybrid genome of the parthenogens, and the diploid to represent the result of different hybridizations (Fig- recombining nonhybrid backgroundof their maternal ure 1). In contrast to the variability of the nuclear sexual parents.Comparisons of mtDNAs in sexual genome, mtDNAs from the parthenogens have few and parthenogenetic lizards, and in different types of restriction site differences other than those due to parthenogenetic lineages may illuminate the processes length changes. These data suggest that the parthen- involved. In particular, thepresence in the partheno- ogens arose recently,ie., within the last few thousand gens of mtDNAs that differ only by length mutations years, from a small geographic area, probably in the provides a simple system for mapping and character- west (MORITZ 1991). izing the mutations. This paper presents an analysis The studies on the parthenogens provide ahistori- of the physical properties and the geographic and cal framework for interpreting changes in their mt- phylogenetic distributions of mtDNA duplications. DNAs. Similar mtDNAs occur in two very different This revealed a highly dynamic system of duplication nuclearbackgrounds; the triploidnon-recombining and deletion,which is in stark contrast to the stability Evolution of mtDNA Duplications 223 TABLE 2 kb s L1 L2L3L5 L7L7 02 Ls L11LS Localities sampled andresults obtained Sample Length Locality size variants" Aileron Stn., NT 1 Alice Springs, NT 9 70km W Alice Springs, NT 1 Bullabulling Stn., WA 4 3' Bullardoo Stn., WA 4 i Coondambo Stn., SA 3 Cunyu Stn.. WA 1 De Rose Hill Stn., SA 2 1 Faraheedy Stn., WA 2 Glenayle Stn., WA 1 Granite Downs Stn., SA 5 Granite Peak Stn., WA 1 Kathleen Valley, WA 2 Kirkalocka Stn., WA 1 FIGURE2.-Autoradiogram ofBg/lI-digested mtDNAs from par- Lake Violet Stn., WA 6 thenogenetic H. binoei showing the effects
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