Smithsonian Tropical Research Institute, Balboa, Panamá
Department of Biology, University of Maryland
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Abstract |
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Introduction |
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The publication of the first complete avian mitochondrial genome revealed that the mitochondrial gene order of the chicken (Gallus gallus) differs from the arrangement prevalent in nonavian vertebrates (Desjardins and Morais 1990
). In most vertebrates, the gene order near the control region is NADH dehydrogenase 6/tRNAGlu/cytochrome b/tRNAThr/tRNAPro/control region/tRNAPhe, while in the chicken, NADH dehydrogenase 6 (ND6) and tRNAGlu are found between tRNAPro and the control region (see fig. 1
). While this unique gene order is shared by most avian lineages and appears to be ancestral (we shall term it the "typical" bird gene order), Mindell, Sorenson, and Dimcheff (1998)
recently reported a second gene order (the "novel" gene order) that appears to have evolved independently in several distantly related avian lineages. In the novel arrangement, the control region is located between tRNAThr and tRNAPro, and a second noncoding region (NC) is found in the position typically occupied by the control region (fig. 1
). This NC region varied in length in the taxa sampled by Mindell, Sorenson, and Dimcheff (1998)
and in some cases resembled the control region (up to 82% sequence similarity for a section of the NC in Smithornis sharpei).
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A similar pattern of gradual degeneration and loss has been observed in duplicated tRNAs of two Cucumaria sea cucumbers (Arndt and Smith 1998
); the cattle tick, Boophilus microplus (Campbell and Barker 1999
); and the akamata snake, Dinodon semicarinatus (Kumazawa et al. 1998
). While these observations of duplication and subsequent degeneration and loss are consistent with the idea of selection for compact mitochondria, some of these same taxa appear to have fully duplicated control regions that show no signs of degeneration. In the case of the sea cucumbers, for example, the two control region sequences differ by only 3% (Arndt and Smith 1998
), while in the akamata snake they are identical (Kumazawa et al. 1998
). Furthermore, metastriate ticks possess two nearly identical control regions (Black and Roehrdanz 1998
; Campbell and Barker 1999
), and the Western rattlesnake (Crotalus viridis) and the himehabu viper (Ovophis okinavensis) have duplicate control regions that differ at only one nucleotide position (Kumazawa et al. 1996
). At present, it remains uncertain why these widely divergent taxa should maintain two nondegenerate copies of a duplicated control region while the vast majority of taxa have only a single control region.
Here, we present results from a study of Amazona parrots and a Pionus parrot outgroup, showing that these taxa also exhibit the novel avian gene order first identified by Mindell, Sorensen, and Dimcheff (1998)
. However, in contrast to previous studies of birds, the duplicate control regions show a high degree of sequence similarity, and several conserved sequence features typically found in avian control regions are present in both control regions of these parrots. A phylogenetic analysis of homologous sequences from the two control region copies demonstrates a pattern of concerted evolution consistent with occasional gene conversion events at a frequency higher than the rate of speciation in these parrots.
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Materials and Methods |
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To identify the order of genes in the area surrounding the control region duplication, and to verify that neither copy was nuclear in origin, we amplified the entire segment from the middle of cytochrome b to the middle of 12S in large (13 kb) overlapping sections followed by selected reamplification of nested fragments as necessary for sequencing (see table 2
for primer sequences and figure 1
for primer locations). PCR was performed in 25-µl reactions with a final concentration of 1 x Taq Extender 10 x buffer, 0.2 mM of each dNTP, 0.6 µM of each primer, 1.5 U Taq polymerase (Sigma-Aldrich), 1.5 U Taq Extender (Stratagene), and 1 µl of template. We performed 30 PCR cycles with annealing temperatures ranging from 50°C to 55°C. All gene order PCR and sequencing was performed at UMD. We constructed consensus sequences for one individual each of Amazona ochrocephala oratrix, Amazona ochrocephala auropalliata, and Amazona farinosa for the entire segment from cytochrome b to 12S using overlapping sequences aligned in Sequencher 3.1 (Gene Codes Corporation). These sequences were aligned with those for the appropriate coding genes and tRNAs of the chicken (G. gallus) using the Clustal routine in Megalign 1.1 (DNASTAR). Sequence length limitations in Megalign forced us to align these 5.3-kb sequences in two 2.6-kb sections, which were then combined. Further alignments of the parrot sequences with conserved sequence blocks from published control region sequences were performed using Sequencher 3.1 and by eye. The parrot sequences are deposited in GenBank (accession numbers AF338819AF338821), and the alignment of the sequences with the chicken gene sequences is available as supplementary material. Secondary structures and their thermodynamic properties were found using M. Zucker's DNA mfold (SantaLucia 1998
) using the A. o. auropalliata sequence.
To examine patterns of evolution in the duplicated control regions, we sequenced portions of both duplicate control regions (fragments CR1* and CR2*; see fig.1 ) for 21 individuals representing six subspecies of the A. ochrocephala complex, three other species of Amazona (A. autumnalis, A. farinosa, and A. amazonica), and Pionus chalcopterus, a species from a closely related genus. We amplified these segments using either LThr (for CR1*) or LGlu (for CR2*) paired with CR522Rb (fig 1 ). PCR was performed in 25-µl reactions with a final concentration of 1 x PCR buffer, 2 mM MgCl2, 0.2 mM of each dNTP, 0.5 µM of each primer, 1.25 U of Taq (Perkin Elmer AmpliTaq at STRI or Sigma Taq at UMD), and 1 µl template. At UMD, all sequences were amplified for 35 cycles with an annealing temperature of 54°C. The same PCR profile was used for CR1* sequences at STRI, while CR2* sequences were amplified using five cycles with 50°C annealing temperatures followed by 30 cycles at 56°C. Both strands of these products were sequenced as detailed above using the amplifying primers. For each species, at least one individual was sequenced at STRI and one was sequenced at UMD with the exception of P. chalcopterus; table 1 lists the sequencing location for each sample. We aligned 550-bp of the 42 resulting sequences using Sequencher 3.1 and used this alignment for subsequent phylogenetic analyses. These sequences are deposited in GenBank (accession numbers AF338277AF338318).
We conducted phylogenetic analyses of the aligned CR1* and CR2* sequences using both maximum-likelihood and parsimony algorithms in PAUP, version 4.0b3 (Swofford 1999
). Since the 5' end of CR1* includes two degenerate pseudogenes (see Results), only the 550 bases homologous to the CR2* sequence and belonging to the control region sensu stricto were included in further analyses unless specifically noted. Optimal parameters for maximum-likelihood searches were obtained with Modeltest, version 3.0 (Posada and Crandall 1998
). Both the hierarchical likelihood ratio tests and the Akaike information criterion selected the Hasegawa-Kishino-Yano model with the following parameters: empirical base frequencies (A = 0.29, C = 0.25, G = 0.15, T = 0.31), transition/transversion ratio = 7.0, gamma distribution shape = 3.7, and proportion of invariable sites = 0.32. For maximum-parsimony searches, we set all characters to be unordered and of equal weight, with gaps treated as fifth bases and multistate characters treated as uncertainties. For both optimality criteria we obtained starting trees via stepwise addition and used the tree bisection-reconnection branch-swapping algorithm. We ran bootstrap searches of 30 replicates for maximum likelihood and 5,000 replicates for parsimony. CR1* and CR2* sequences from P. chalcopterus served as outgroups in all searches.
Estimates of the rate of gene conversion between the duplicated control regions were obtained using the Kimura two-parameter distances between the alignable portions of the CR1* and CR2* sequences for each individual. Distance to the last common ancestor was assumed to represent the conversion of one gene to another and was estimated as half the distance between the two sequences. The time since last conversion for each individual was estimated by assuming a constant mutation rate of 20%/Myr for the control region, which was found for the snow goose, Anser caerulescens, using Kimura-corrected distances (Quinn 1992
). Quinn's (1992)
estimate was based on Shields and Wilson's (1987)
fossil-based calibration of 2%/Myr for the mitochondrial genome and the observation that sequences from the first domain of the control region of the snow goose evolve approximately 10 times as fast as the mitochondrial genome as a whole (Quinn 1992
). A similar 10-fold faster substitution rate in the first domain of the control region has been observed in parrots (unpublished data), so in the absence of parrot fossil data with which to obtain a parrot-specific rate calibration, we used that of Quinn (1992)
. Although the mutation rate of the first domain of the control region in geese may differ from that in parrots, any error in the clock calibration would only affect the absolute time estimates, and not the relative rates of gene conversion.
We compared the rates of evolution in the CR1* and CR2* sequences in two ways. First, to evaluate whether one copy of the control region evolves more quickly than the other, we separately calculated uncorrected p distances between P. chalcopterus and each of the Amazona samples for the alignable portions of the CR1* and CR2* sequences. The CR1* distances were then compared with the CR2* distances using a paired t-test to determine whether one of the fragments tended to yield greater distance estimates. A t-test was also used to compare the rates of evolution in two different portions of the CR1*. t-tests were performed with StatView, version 4.1 (Abacus Concepts).
Second, to examine the pattern of variability along the two control regions, we compared the numbers of changes observed within nonoverlapping 25-nt windows along the CR1* and CR2* sequences. The CR1* and CR2* sequences were analyzed separately, and for each taxon pair, the numbers of mismatched sites were counted within 25-nt windows. The numbers of differences from all pairwise comparisons were then summed for each window. The patterns of variation in CR1* and CR2* were compared using a 2 test in StatView. We excluded window 16 from this analysis because the observed number of changes was zero for both CR1* and CR2*.
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Results and Discussion |
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In the following sections, we describe and compare the structures of the CR1 and CR2 regions. Although the two differ somewhat in length, both contain structural elements that have been identified in avian control regions. In contrast to previous studies of mitochondrial genome rearrangements in birds, we found no signs of degeneration in either control region copy. Instead, the paralogous copies are evolving in parallel, as we show in a phylogenetic analysis of homologous portions of the two control regions. In the final section, we discuss the maintenance of duplicate control regions in parrots and in other animals and mention some possible mechanisms responsible for their concerted evolution.
Comparison of CR1 and CR2
While both CR1 and CR2 contain many of the conserved features typically identified in avian control regions, an alignment of CR1 with CR2 highlights some differences between the two regions. For any given individual, CR1 and CR2 can be aligned starting at approximately nucleotide 150 of CR1 and nucleotide 4 of CR2. From that point, a span of about 1,296 nt can be easily aligned with few, if any, indels. This alignable section encompasses all of the conserved sequence blocks, TASs, and secondary structures described below.
The first 156 nt of CR1 do not have a corresponding analog in CR2 and do not appear to belong to the control region sensu stricto. The first 137 nt at the 5' end of CR1 can be aligned to the parrot tRNAGlu and adjacent ND6 sequence with 63% sequence similarity. The chicken tRNAGlu can also be aligned with the 5' end of CR1, but the similarity is only 50%, which is lower than the 66% match between the chicken tRNAGlu and the presumably functional parrot tRNAGlu adjoining the 5' end of CR2. The parrot tRNAGlu sequence can be folded into the expected cloverleaf structure, while the tRNAGlu-like sequence from the 5' end of CR1 cannot (fig. 2
). Furthermore, we found an accelerated rate of sequence evolution relative to the outgroup in the 156 nt at the 5' end of CR1* when compared with the adjacent 550 nt portion of CR1* that could be aligned to CR2* (t-test; N = 20, t = -13.567, P < 0.0001) (fig. 3
). The lack of functional structure in the tRNAGlu-like sequence, coupled with the accelerated rate of change in this section, suggests that the 5' portion of CR1 contains two pseudogenes corresponding to degenerating copies of ND6 and tRNAGlu. Degenerating copies of ND6 and tRNAGlu at this location are predicted by the rearrangement model described by Bensch and Härlid (2000)
for the control region duplication in Phylloscopus warblers. For clarity, we will continue to use CR1 and CR2 to refer to the sections bounded by functional tRNAs, as shown in figure 1
; "control region" will be used sensu stricto, referring to the sections between pseudo-tRNAGlu and tRNAPro in CR1 and between tRNAGlu and tRNAPhe in CR2.
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Structure of the Control Regions
If the boundaries of the two control regions are defined by pseudo-tRNAGlu and tRNAPro in CR1 and tRNAGlu and tRNAPhe in CR2 (fig. 4
), then the duplicate control regions differ in size, with the first control region in the three species ranging in length from 1,553 to 1,713 nt, and the second ranging from 1,457 to 1,868 nt. The lengths of the longest of these control region sequences are minimum estimates because the presence of long stretches of tandem repeats in these sequences prevented complete sequencing of overlapping strands. Even the shortest of the control regions sequenced here (1,457 nt) is longer than control regions previously described for other birds, which are in turn longer than those of most vertebrates (Baker and Marshall 1997
). As is the case for most avian control regions (Baker and Marshall 1997
), both parrot control regions can be divided into three subsections that differ in levels of sequence variation: a highly variable domain I closest to tRNAGlu in the typical avian gene order; a central conserved domain II that contains the F, D, and C boxes; and a moderately variable domain III closest to tRNAPhe in the typical gene order.
Both control region copies in Amazona parrots show many of the features typically found in the functional control regions of birds and other vertebrates. The first domain of both paralogs (approximately positions 469890 in fig. 4
) includes several features that have been identified in the control regions of other animals. Both parrot control regions have a C-rich sequence near the 5' end, corresponding to the "goose hairpin" (Quinn and Wilson 1993
), which has been found in similar locations in other bird species (Baker and Marshall 1997
; Marshall and Baker 1997
; Randi and Lucchini 1998
; Bensch and Härlid 2000
). Conserved extended termination-associated sequences (ETASs) have been identified in domain I of some mammal control regions (Sbisà et al. 1997
) and are thought to indicate the 3' end of the nascent H-strand in the three-strand D-loop structure. The consensus mammalian ETAS1 and ETAS2 can be aligned to domain I of the parrot control regions with approximately 50% sequence agreement. In some partridges, the sequence corresponding to ETAS2 can form a stem-and-loop structure (Randi and Lucchini 1998
); the same is true for the parrot control region sequences (fig. 4
), which form hairpin loops (
G = -4.13 kcal/mol). Another sequence capable of forming a stem-and-loop structure is found approximately 40 nt upstream of the F box (
G = -3.80 kcal/mol).
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In all animals studied to date, the origin of heavy-strand replication (OH) has been found in the third domain, located immediately next to or within CSB1 (Sbisà et al. 1997
). As in partridges (Randi and Lucchini 1998
), a polyC sequence that resembles the mammalian OH is located 20 nt upstream of the parrot CSB1 in both parrot control regions. The chicken's bidirectional transcription promoter sequence (L'Abbé et al. 1991
) does not align with any part of the parrot control regions with better than 50% similarity. Since this promoter is associated with a stem-and-loop structure, we examined the parrot control regions downstream of CSB1 for inverted repeats that could form such structures. One such sequence (
G = -1.93 kcal/mol) was located approximately 65 nt downstream of CSB1 (fig. 4
).
Both parrot control regions contain one or more series of tandem repeats in the third domain downstream of the conserved features described above. These repeat motifs are short microsatellite-like sequences that are tandemly repeated up to 50 times (e.g., the 5'-TTCATTCG-3' motif in CR2 of A. o. auropalliata). Both the repeat motif and the number of these repeats differ among the three taxa examined and between the two control region copies within each taxon (table 3
). Only the first seven or eight repeats (a TTTG motif) are alignable between the two control region copies of any one individual; the remaining stretch of tandem repeats does not align well. This variation in repeat number accounts for much of the observed variation in length of the control regions. Such repeat regions have been found to be highly variable in length in a range of vertebrate species (Baker and Marshall 1997
; Wilkinson et al. 1997
). There is also some evidence of heteroplasmy in the first control region of A. o. auropalliata, where consistent double peaks were observed in the primary sequence of the repeat section of CR1. Such heteroplasmy may be due to slippage during replication of the short tandem sequences. Heteroplasmy due to replication errors of tandemly repeated sequences is found in a number of species (Wilkinson et al. 1997
).
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Phylogenetic Analysis of CR1* and CR2* Sequences
We performed phylogenetic analyses on CR1* and CR2* sequences from 21 individuals representing four species of the genus Amazona and P. chalcopterus. Both parsimony and maximum likelihood gave well-supported phylogenies that showed a similar branching pattern in which both control region copies of an individual in general were more closely related to each other than to corresponding segments of other individuals (fig. 5
). The solid boxes in figure 5
indicate the three exceptions to this general pattern, all of which occur within subspecies of A. ochrocephala. In no case are sequences for a particular copy most closely related to the same segment in another species, as would be predicted by a scenario of independent evolution of the two copies following an ancient duplication event in the common ancestor of these species. The average sequence difference of the paralogous control regions (CR1* vs. CR2* within individuals) was 1.4%, versus a mean value of 4.1% between control region orthologs representing nearest phylogenetic neighbors. The CR1* and CR2* sequences show complete identity within an individual in only three cases: those of the two A. farinosa samples and that of the P. chalcopterus individual.
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The phylogenetic analysis suggests that the two control region copies are evolving in concert at the level of subspecies and above, but with some degree of independence within subspecies. One mechanism that could give rise to this pattern is occasional gene conversion events that occur sporadically. We estimated the frequency of such events based on the sequence data from CR1* and CR2*. Averaged across all samples, the time between conversion events was estimated to be 34,670 ± 18,400 years (table 4 ).
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The presence of nondegenerate duplicate control regions has previously been described in only a few, diverse taxa: several snakes (Kumazawa et al. 1996, 1998
), metastriate ticks (Black and Roehrdanz 1998
; Campbell and Barker 1999
), and sea cucumbers (Arndt and Smith 1998
). The concerted evolution of the two parrot control regions, as shown by the phylogenetic analysis of CR1* and CR2* sequences, is very similar to the pattern suggested by the limited phylogenetic analysis of metastriate tick control region sequences (Black and Roehrdanz 1998
). In both cases, two control region copies within an individual appear to evolve independently to some degree, but convergently over the long term. The tick pattern differs somewhat from that of the duplicate control regions found in several distantly related snake species, in which the two copies are identical to each other (or differ at only one nucleotide position) (Kumazawa et al. 1996, 1998
).
The concerted evolution of the two control region copies in parrots differs from the pattern observed in both metastriate ticks and snakes in that it does not involve the entire control region, but rather only those portions that are believed to be functional. This observation suggests three alternative, but not necessarily exclusive, hypotheses for the maintenance of high sequence similarity between these regions: (1) a mechanism of gene conversion involving only the convergent portions, (2) gene conversion involving the entire control region with subsequent extremely rapid evolution of nonfunctional portions, and (3) parallel selection to maintain functionality of both regions.
A hypothetical gene conversion mechanism that could be responsible for concerted evolution of most of the "alignable" portions of the two control regions involves the three-strand D-loop structure. In the D-loop, the parental H strand is displaced by a nascent H strand (Clayton 1982
), which originates at the OH and extends to the TASs near the 5' end of the control region (Sbisà et al. 1997
). The nascent H strand can become disassociated by brief exposure to denaturing conditions or if one of the parental strands is nicked (Clayton 1982
). In a genome with duplicate control regions, the nascent H strand fragment from one D-loop could dissociate and recombine with the parent H strand of the other control region. This recombination process would tend to homogenize the section between the OH and the TASs but would not explain the observed similarity between the putative OH and the beginning of the tandem repeats. This latter section corresponds to avian domain II of the control region, which tends to be highly conserved in most bird species (Baker and Marshall 1997
). The relatively high level of conservatism in this section implies that it is of functional importance, so the similarity between these portions of CR1 and CR2 could result from an independent process of stabilizing selection.
A second hypothesis is that the entire control regions are sporadically homogenized, and during the intervals between homogenization events, the 3' portions of CR1 and CR2 (which contain tandem repeats) evolve more rapidly than the 5' sections. Kumazawa et al. (1998)
proposed two possible mechanisms for the concerted evolution of entire duplicate control regions in the snake. One of these models involves tandem duplication during replication, and the other involves frequent gene conversion due to crossing over of nicked strands between two control regions followed by replacement of one of the control region sequences via repair of the resulting heteroduplex DNA intermediate (Kumazawa et al. 1998
). In parrots, our phylogenetic analysis suggests that these homogenization events might occur relatively infrequently, and in the interim, the portions of CR1 and CR2 containing tandem repeats could evolve rapidly, perhaps through replication slippage (Madsen, Ghivizzani, and Hauswirth 1993
). Such rapid evolution of tandem repeats is widespread in the nuclear genome (Charlesworth, Sniegowski, and Stephan 1994
) and is thought to account for heteroplasmy in the control regions of a range of bat species (Wilkinson and Chapman 1991
; Wilkinson et al. 1997
).
A possible alternative to gene conversion is selection that works in parallel on functional areas of the two control regions. One source for such selection could be provided by nuclear gene products that bind onto the nascent H strand fragment during replication (Albring, Griffith, and Attardi 1977
). Mutations in this nuclear product could exert parallel selection on the two copies of the control region if both functioned in this manner, and could maintain a high degree of similarity between the two copies within an individual. However, the fact that avian domain I sequences typically evolve very rapidly implies that mutations at many sites in this domain are selectively neutral. Thus, it seems unlikely that selective constraints imposed by nuclear gene products would account for the degree of concerted evolution observed in Amazona.
When duplications occur within the mitochondrial genome, one of the copies usually degenerates and eventually disappears, as expected given the apparent selection for compact size of the genome (Rand and Harrison 1986
). This has been shown to occur in a number of studies that have documented tRNA duplications followed by degeneration of one of the duplicates (Arndt and Smith 1998
; Kumazawa et al. 1998
; Mindell, Sorenson, and Dimcheff 1998
; Campbell and Barker 1999
; Bensch and Härlid 2000
). In previously reported examples of control region duplication in birds, the copy corresponding to the parrot CR1 is maintained as a functional control region, while the section corresponding to the parrot CR2 has degenerated (Mindell, Sorenson, and Dimcheff 1998
; Bensch and Härlid 2000
). In Amazona parrots, there is no evidence that either copy is degenerate or in any way nonfunctional. If only one copy were functional and gene conversion were directional, such that the functional copy always converted the nonfunctional copy, the nonfunctional copy still would be expected to accumulate changes more quickly between conversion events. However, all comparisons for these parrots show that the two copies are accumulating changes at approximately the same rate. This pattern would be expected if both of the parrot control regions were functional.
Taken together with previously published work on mitochondrial genome rearrangements and gene duplications, our results demonstrate an emergent pattern. Observations of gene duplication followed by degeneration of duplicate copies are consistent with the idea that mitochondrial genomes are under selection for compactness. Gene duplications have been documented in a number of organisms, and the copies are usually degenerate (Arndt and Smith 1998
; Kumazawa et al. 1998
; Mindell, Sorenson, and Dimcheff 1998
; Campbell and Barker 1999
; Bensch and Härlid 2000
) or short-lived on an evolutionary timescale (Moritz and Brown 1986, 1987
).
In some cases, however, duplicate control regions may persist without any apparent loss of functionality (Kumazawa et al. 1996
; Black and Roehrdanz 1998
; Campbell and Barker 1999
). Along with our findings, these results suggest that in some cases, the presence of two control regions may be advantageous and thus be maintained over evolutionary time, either through stabilizing selection or through occasional gene conversion. Alternatively, duplicate control regions may persist only if the duplication event gives rise to complete, functional copies; otherwise, the incomplete duplicate will degenerate and eventually be lost.
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Supplementary Material |
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Acknowledgements |
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Footnotes |
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1 Present address: Macaulay Library of Natural Sounds, Cornell Laboratory of Ornithology, Ithaca, New York.
1 Keywords: Amazona
control region
mitochondrial DNA
parrots
concerted evolution
gene duplication
genomic rearrangement
2 Address for correspondence and reprints: Jessica R. Eberhard, Macaulay Library of Natural Sounds, Cornell Laboratory of Ornithology, 159 Sapsucker Woods Road, Ithaca, New York 14850. E-mail: jre24{at}cornell.edu
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