Laboratorio de Fisiología y Biología Molecular, Facultad de Ciencias Exactas y Naturales, Departamento de Ciencias Biológicas, Pabellón II, Buenos Aires, Argentina;
Department of Biological Sciences, Idaho State University;
Laboratorio de Evolución, Facultad de Ciencias, Montevideo, Uruguay
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Abstract |
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Introduction |
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A number of investigations have focused on the molecular properties and the chromosomal locations of the sequences involved in these rearrangements. Recently, two satellite DNAs (satDNAs) had been shown to be involved in Rb translocations in mice (Garagna et al. 2001)
and muntjac deer (Li et al. 2000)
. Another means of testing of ideas concerning the role of satDNA in chromosomal change would involve the assessment of the correlated evolution of chromosomal and genomic change through the evolutionary history of a clade. Such an approach would require the documentation of satellite DNA in a chromosomally diverse clade. In this paper, we characterize the evolutionary history of amplifications and deletions of a particular satDNA identified in the highly polymorphic tuco-tucos (genus Ctenomys). These subterranean rodents form one of the most karyotypically diverse clades of mammals known, with chromosomal diploid numbers ranging from 10 to 70 (Cook, Anderson, and Yates 1990
; Gallardo 1991
; Reig et al. 1992
; Ortells 1995
). Tuco-tucos belong to the family Octodontidae and are distributed throughout the southern cone of South America with more than 56 described species (Reig et al. 1990
). Another member of this family, Tympanoctomys barrerae, has 102 chromosomes and apparently is the first tetraploid mammal known (Gallardo et al. 1999
). This tremendous range in diploid numbers in a single mammalian clade has attracted speculation regarding the mechanisms that promoted high diversification (Nevo 1999
). Reig and Kiblisky (1969)
first proposed that tuco-tucos were a prime example of chromosomal speciation. Diversification may have been facilitated by the isolation of small demes that characterize population structure in most species (Reig et al. 1990
) and extensive chromosomal rearrangements (Reig and Kiblisky 1969
; Cook 1990
; Gallardo 1991
; Ortells 1995
). The apparent relationship between high karyotypic diversity and elevated rates of speciation in subterranean rodents has been explored by a number of investigators (White 1978
; Reig 1989
; Nevo 1999
; Steinberg and Patton 2000
).
The major satDNA sequence characterized for tuco-tucos (named RPCS) varies in copy number among species (Rossi, Reig, and Zorzópulos 1990, 1993
; Rossi et al. 1995b
). RPCS has been located in chromosomal regions with positive C-heterochromatic bands in most species (Rossi et al. 1995b
). The repetitive unit of RPCS shows high sequence and structural identity with the long terminal repeat (LTR) of retroviruses (Rossi et al. 1993
; Pesce et al. 1994
). This particular satDNA may promote chromosomal rearrangements by virtue of its capacity for amplification and movement through the genome. In turn, amplification is thought to facilitate rapid chromosomal evolution associated with speciation (Rossi et al. 1995a, 1995b
).
We used an expanded phylogenetic framework based on complete cytochrome b sequences for Ctenomys to explore the evolution of the satellite RPCS. These phylogenies encompassed Bolivian, Chilean, Uruguayan, and Argentinean tuco-tucos from throughout the distribution of the genus and included representatives of the three named subgenera.
To further investigate the role of RPCS in chromosomal evolution in Ctenomys, we performed quantitative dot-blots of RPCS. We analyzed the copy number of the repetitive unit of RPCS in each species and inferred these values for the ancestral nodes to provide an assessment of the amplification/deletion process across the genus.
Because tuco-tucos have been considered an exemplary case of chromosomal speciation in mammals (Reig et al. 1990
), we examined this clade as a case study of the role of satDNA in chromosomal change. We did this by (1) providing an expanded molecular phylogeny based on complete sequences of the mitochondrial cytochrome b gene, (2) estimating RPCS copy numbers in the genomes of the species represented in the phylogeny, and (3) using phylogeny-based methods to examine the relationship between the stability of the copy number of the RPCS satellite and the stability of chromosome numbers through the evolutionary history of the clade.
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Materials and Methods |
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For dot-blot experiments, 10, 100, and 1,000 ng of genomic DNA were fixed to a nylon membrane using a Bio-Dot microfiltration unit (Bio-Rad) and hybridized to 32P-labeled RPCS under low-stringency conditions (6 x SSC, 60°C). Autoradiographs were scanned, and the density of dots was measured using NIH Image v1.62. RPCS copy number per genome was computed using pRPCS (Rossi, Reig, and Zorzópulos 1990
) as standard.
Sequence and Phylogenetic Analysis
Alignment of DNA sequences was performed using the program Sequence Navigator, version 1.01 (Applied Biosystems). Nucleotide composition was computed with MEGA 1.02 (Kumar, Tamura, and Nei 1993
). MacClade 3.0 (Maddison and Maddison 1992
) was used to compute numbers of transitions, transversions, and changes per codon position. Genetic distances among all pairs of taxa were obtained with PAUP 4.0 beta (Swofford 1998
). Phylogenetic signal was evaluated with the g1 value derived from 10,000 random trees (Hillis and Huelsenbeck 1992
). All phylogenetic analyses used O. degus, O. gliroides, and T. barrerae as outgroups.
Maximum-parsimony (MP) trees were obtained using PAUP 4.0 beta (Swofford 1998
). Fifty replicates of heuristic searches (with random addition of sequences) were performed using the weighting scheme 2, 5, and 1 for first, second, and third codon positions, respectively, and a stepmatrix giving a transition/transversion (Ts/Tv) ratio of 6. These parameters fit with biases associated with the molecular evolution of cytochrome b as analyzed here and elsewhere (Lessa and Cook 1998
). Support for each clade was assessed by performing bootstrap analysis with 1,000 replicas (each repeated five times with random addition of sequences).
Maximum-likelihood (ML) analysis used PAUP 4.0 beta (Swofford 1998
). The model that best fitted our data set was the general time reversible (GTR) model of evolution, whose parameters were calculated following the routine proposed by Sullivan, Markert, and Kilpatrick (1997)
. The proportion of sites assumed to be invariable was 0.44795, and the shape parameter of the gamma distribution was 0.94708. We performed a total of 10 runs with random addition of sequences.
Neighbor-joining (NJ) trees were constructed with PAUP 4.0 beta (Swofford 1998
) using the same model and parameters used in the ML analysis. One thousand bootstrap replicas were performed to assess the robustness of the topology.
The ancestral condition of RPCS content was reconstructed by estimating the haploid copy number of RPCS at internal nodes using the program ANCML (Schluter et al. 1997
). This analysis was based on an ML tree computed under the GTR model assuming a molecular clock.
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Results and Discussion |
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To facilitate computationally intensive analyses, only one individual of each taxon was retained in phylogenetic searches, except for those taxa exhibiting values of intraspecific divergences higher than 1.5%. The g1 value, -2.887236, computed from 10,000 random trees was highly significant (P < 0.01), indicating that this data matrix has strong phylogenetic signal (Hillis and Huelsenbeck 1992
).
The 50% majority-rule consensus of 80 equally parsimonious trees, as well as the corresponding bootstrap support values, reveals a polytomy at the base of the tuco-tuco radiation (fig. 1
). This basal polytomy of cytochrome bbased trees of ctenomyine evolution has been observed in previous analyses (Lessa and Cook 1998
; D'Elía, Lessa, and Cook 1999
; Mascheretti et al. 2000
). The persistence of this polytomy, even with our larger sample size, provides additional support for an early burst of cladogenesis in the evolution of the genus (Lessa and Cook 1998
). The molecular signature of a rapid cladogenetic event corresponds to the burst of speciation found in the fossil record, recently reviewed by Cook, Lessa, and Hadly (2000)
. The phylogenetic relationships of the well-supported clades of tuco-tucos are discussed below.
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Another well-characterized clade is composed of C. opimus and C. fulvus. These species have similar standard (2n = 26 and FN = 48) and C-banded karyotypes (Gallardo 1991
). The close phylogenetic relationship based on cytochrome b between these two northern species from the highland deserts of Chile, together with their karyologic similarities, indicate that these two taxa may be conspecific (Gallardo 1979
; Reig et al. 1992
).
The monophyly of C. mendocinus, C. porteousi, C. australis, and Ctenomys azarae (not included here) of central and western areas of Argentina, referred to as the mendocinus group, has been noted since their karyotypes were first described (Massarini et al. 1991
). Other investigations supported the inclusion of C. flamarioni and C. rionegrensis in this group (D'Elía, Lessa, and Cook 1999
). Ctenomys rionegrensis also showed a strong association with the mendocinus group in our MP (fig. 1A and B
) and NJ analyses. The relationship between this last group and C. pearsoni is suggested but not strongly supported (fig. 1B
). Finally, C. talarum is possibly related to this clade. Ctenomys talarum shares its chromosomal number with species of the mendocinus group (Massarini et al. 1991
), although differences in G-banding patterns and morphological characters have been noted (Ortells and Barrantes 1994
).
This analysis extends previous assessments of the mendocinus group (Rossi, Reig, and Zorzópulos 1990, 1993
) that supported the monophyly of the clade and suggested a close association with C. rionegrensis (D'Elía, Lessa, and Cook 1999
). Our three specimens of C. mendocinus do not form a monophyletic group (figs. 13
). Ctenomys mendocinus 3 exhibited a closer relationship with other species of the group than with the two other specimens of C. mendocinus. It is possible that some of the numerous tuco-tuco populations that have been assigned to C. mendocinus represent distinct but closely related forms (C. Borghi, personal communication). The northern Argentine C. tucumanus, C. argentinus, and C. latro form a monophyletic group in all analyses (figs. 1B, 2, and 3
).
Ctenomys haigi, C. coyhaiquensis, and C. magellanicus are all distributed in southern Argentina and Chile and form a well-supported clade (figs. 1B, 2, and 3
). These species all have asymmetric sperm morphology and may be closely related (Kelt and Gallardo 1994
). This southern clade is distinct from the mendocinus group, which is the other major clade with asymmetric sperm, indicating that the derived sperm morphology (Vitullo and Cook 1991
) may have evolved twice in the history of the genus, as suggested by D'Elía, Lessa, and Cook (1999)
. The position of C. maulinus, which also has this type of sperm, cannot be determined with certainty because this taxon collapsed to the basal polytomy (fig. 1B
). Further analysis of several new species from Patagonia (southern Argentina and Chile) may resolve the position of C. maulinus.
Evolution of RPCS Copy Number
Dramatic differences in RPCS copy numbers among species were previously demonstrated in a group of Argentine species (Rossi, Reig, and Zorzópulos 1993
). We extended these analyses to Uruguayan, Bolivian, Chilean, and additional Argentinean species. Quantitative dot-blots, displayed together with the ML tree (fig. 2
), showed species with high, medium, low, and undetectable RPCS copies. In C. opimus, C. fulvus, C. magellanicus, C. tucumanus, and C. maulinus, RPCS is virtually absent. Other species and forms, like C. steinbachi, C. minut, Ctenomys sp. ITA, Ctenomys sp. MONTE, C. argentinus, C. latro, and C. tuconax, range from low to medium copy numbers of RPCS. In the remaining species, RPCS seemed to be present in high numbers. Ctenomys haigi, a species from Argentinean Patagonia, displayed the highest RPCS content (6.60 x 106 copies), as did the species of the mendocinus group, with 3.3 x 106 to 4.69 x 106 copies.
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Recently, a phylogenetic approach was successfully employed to analyze chromosomal number evolution in muntjac deers (Wang and Lan 2000)
. However, a comprehensive integration of a phylogenetic framework with chromosomal evolution, as well as copy number assessments of satDNA data, has been lacking.
In the present work, we considered RPCS copy number as a continuous character and inferred ancestral values by using an ML approach. MP-based methods, which produce estimates requiring the smallest number of changes through time, are among the most popular for inferring ancestral character states (Maddison and Maddison 1992
; Schluter et al. 1997
). When characters evolve rapidly and the probabilities of gains and loses are unequal, however, MP-based methods may be problematic (Cunningham, Omland, and Oakley 1998
). Inevitably, uncertainties of ancestral-state estimation appear when stochastic elements are present in the evolutionary process (Schluter et al. 1997
).
New approaches for reconstructing ancestral states based on ML algorithms have been developed for discrete (Schluter 1995
) and continuous traits (Schluter et al. 1997
). The advantages and weaknesses of ML-based methods are detailed in Schluter et al. (1997)
and reviewed by Cunningham, Omland, and Oakley (1998)
. An important feature of ML-based methods is that they provide an opportunity to quantify uncertainty. The substantial degree of variation in RPCS content suggests high rates of change in this trait. Therefore, we chose an ML approach to infer RPCS copy number for internal nodes of the ctenomyine radiation (fig. 2 ), an approach that required branch lengths to be proportional to time. We used the DNAMLK program (Felsenstein 1993
) but had to assume a molecular clock due to constraints imposed by this program, even though cytochrome b does not fit constant rates of evolution in this group (Cook and Lessa l998
). It is worth noting that the molecular-clock assumption affects only branch lengths, and not the topology of the ML tree (fig. 2 ), which was obtained without that constraint. Finally, errors associated with ancestral nodes were high, but they were lower than the range of variation of the values in the tips (see fig. 2 ). This relationship contrasts with values of the examples studied by Schluter et al. (1997)
, indicating that this method should provide a reasonable overview of the evolutionary history of RPCS.
We used our ML phylogenetic hypothesis, in combination with RPCS copy number (a continuous character), to estimate changes in RPCS through the evolutionary history of the ctenomyine. Our ML reconstruction of the history of RPCS contrasts the relatively high copy numbers found in the deep branches of the ctenomyine radiation with the comparatively low copy numbers among the octodontines (fig. 2 ). The ML tree also suggests that RPCS remained relatively stable (at ca. 1,500 x 103 copies) along most other basal branches of the tuco-tuco clade. Although this is an area of poor phylogenetic resolution, it appears that little variation in RPCS took place along these branches. Subsequently, substantial increases in the number of copies of RPCS are suggested along the branch leading to the mendocinus group, followed by relatively constant values along most of the terminal branches. Ctenomys talarum may be related to the mendocinus group (fig. 1 ); therefore, we cannot rule out the possibility that a single amplification accounts for greater copy numbers in these taxa.
Deletions also occurred throughout internal branches. For example, the ancestor of the C. opimusC. fulvus clade is inferred to have experienced a 17-fold reduction in RPCS copy number. Low amounts of RPCS were conserved along the terminal branches.
In contrast, several well-defined clades show substantial variation internally in RPCS copy numbers, implying relatively recent and rapid changes. Specifically,
The broadened comparative framework provided by these analyses suggests that the history of the RPCS repeat has been extremely complex, with multiple events of gains and losses in copy number.
Evolution of RPCS Copy Number and Chromosomes in Tuco-tucos
Amplification and movement of satDNA is well documented (e.g., Hamilton, Honeycutt, and Baker 1990
; Modi 1993
) and has been suspected to play a role in karyotypic evolution (Wichman et al. 1991
; Hamilton, Hong, and Wichman 1992
; Bradley and Wichman 1994
; Garagna et al. 1997, 2001
; Yang et al. 1997
). These processes may have dramatic consequences for chromosome architecture. For example, Garagna et al. (2001)
elucidated the organization of a satDNA at fusion points involved in Rb translocations in mouse chromosomes. Li et al. (2000)
demonstrated the involvement of two satDNAs of the muntjac deer genome in tandem fusions of chromosomes; these fusions resulted in drastic reduction in diploid numbers. These studies are in agreement with an early hypothesis of Wichman et al. (1991)
that suggests that intragenomic movements of repetitive sequences (studied by in situ hybridization in ancestral and derived karyotypes) promote rapid chromosomal evolution. This hypothesis was consistent with several cases of chromosomal evolution, including Microtus (Modi 1993
), Reithrodontomys (Hamilton, Honeycutt, and Baker 1990
), Peromyscus (Hamilton, Hong, and Wichman 1992
), and Equus (Bradley and Wichman 1994
). A phylogenetic context provides an opportunity to investigate the impact of satDNA dynamics on chromosomal evolution.
The ctenomyine radiation has been recognized as an exceptional model for investigating the dynamics of chromosome rearrangements (Reig et al. 1990
). RPCS, a retroviral satDNA present in the genome of these rodents (Rossi et al. 199
3; Pesce et al. 1994
), was proposed to be associated with the extreme chromosomal variability documented for the group (Rossi et al. 1995a
).
Analysis of the evolution of RPCS copy number together with chromosomal variability in lineages of Ctenomys showed two distinctive patterns. One pattern was characterized by high variability in copy numbers between closely related lineages, accompanied by substantial chromosomal variability. The other pattern consisted of rather stable copy numbers of RPCS within karyotypically stable clades. The first pattern was mirrored by three well-defined clades. RPCS copy number in the clade formed by C. tucumanus, C. latro, and C. argentinus (figs. 13 ) exhibited deletions, particularly conspicuous in the terminal branch leading to C. tucumanus (fig. 2 ). Many rearrangements differentiate the karyotype of C. tucumanus (2n = 28) from that of C. latro (2n = 4042) and C. argentinus (2n = 44).
More impressive is the case of a clade of species from Patagonia Argentina composed of C. haigi, C. coyhaiquensis, and C. magellanicus (figs. 13
). Both large amplifications and large deletions occurred within this group. Ctenomys haigi experienced a 2.5-fold amplification, whereas C. magellanicus and C. coyhaiquensis underwent 91- and 17-fold deletions, respectively (fig. 2
). Once again, these amplifications and deletions were accompanied by high levels of chromosomal evolution. In this case, a largely bi-armed karyotype of low chromosomal number (C. coyhaiquensis, 2n = 28) (Kelt and Gallardo 1994
) evolved into primarily uni-armed karyotypes with higher chromosomal numbers (C. haigi, 2n = 50) (Gallardo 1991
). These rearrangements would have been primarily fissions and would have been accompanied by significant RPCS expansion (fig. 2
). Conversely, a hypothesis implying the loss of RPCS and a series of chromosomal fusion events in the lineage leading to C. coyhaiquensis is also plausible.
Although the close relationship between C. steinbachi (2n = 10) and the group formed by Ctenomys sp. ROBO, C. goodfellowi, and C. boliviensis is not strongly supported (figs. 1 and 2
), previous studies (Cook and Yates 1994
; Cook and Lessa 1998
) indicate that these species are related. Ctenomys steinbachi is thought to have undergone rapid and extensive chromosomal evolution from karyotypes of higher diploid numbers (Lessa and Cook 1998
). This dramatic chromosomal evolution is associated with a 46-fold RPCS deletion (fig. 2
).
Stasis in copy number associated with karyotype stability characterized the second pattern of RPCS evolution and was observed in the mendocinus group and in the C. opimusC. fulvus clade. RPCS content is uniformly high in all members of the mendocinus group. Ancestral character state analysis suggested that significant amplification in RPCS occurred in the ancestor of this group, followed by stasis throughout subsequent branches (fig. 2
). The clade containing C. opimus and C. fulvus also displayed chromosomal and RPCS stability. Both species have 2n = 26, as well as similar C-banded karyotypes (Reig and Kiblisky 1969
; Gallardo 1979, 1991
) and almost undetectable amounts of RPCS. The inferred RPCS value for the base of this clade is large (85,000 copies; fig. 2
), and it is therefore possible that a larger deletion occurred prior to this node, maintaining the RPCS low copy number constant throughout all of the branches of this clade (fig. 2
). However, the high ancestral value for the clade may be overestimated because the method estimates ancestor state as a weighted average of the neighboring tips (Schluter et al. 1997
).
Finally, the clade composed of C. frater, C. lewisi, Ctenomys sp. LLATHU, and C. conoveri shows relatively stable amounts of RPCS (except in Ctenomys sp. LLATHU). Diploid numbers are also fairly constant (52 for C. frater, 56 for C. lewisi, and 4850 for C. conoveri), but a comprehensive picture of this clade is lacking because Ctenomys sp. LLATHU has not been karyotyped.
Several models relating chromosomal evolution to amounts of heterochromatin have been proposed for the distinctive patterns that have been described. For example, Patton and Sherwood (1982)
investigated the patterns of heterochromatin variation in rodents of the genus Thomomys and argued that large amounts of heterochromatin do not appear to promote rearrangements, as proposed by Hatch et al. (1976)
for kangaroo rats (genus Dipodomys). Other investigators have suggested that heterochromatic differences might cause reproductive isolation (Yunis and Yasmineh 1971
), although Patton and Sherwood (1982)
and others (Rice and Straus 1973
; Dev et al. 1975
; John and Miklos 1979
and papers therein) provided examples in which this does not occur. We found that clades that exhibited karyotypic stability contained high, as well as low, RPCS content. On the other extreme, the clade from Corrientes Province with high chromosomal variability showed few C-bands (Reig et al. 1992
). The existence of many different scenarios of satDNA and chromosome variation seems to indicate that the influence of repetitive DNA on chromosomal evolution does not rely simply on copy number. Rather, our analyses of tuco-tucos suggest an association between changes in karyotypes and changes in RPCS copy number (either increase or decrease). Conversely, we found that the stability of RPCS copy number was tied to chromosomal stability. We speculate that only satDNA that is actively involved in processes of expansion, contraction, and mobilization is likely to promote changes in karyotype morphology. If so, an "active" satDNA could promote chromosomal change even if it is present at a low copy number. Thus, the molecular nature of each particular type of satDNA probably determines its potential for promoting chromosomal rearrangements. The potential distinction between active and stabilized satDNA and their differing roles in relation to chromosomal change is, as noted, speculative. Further analyses should include both detailed reconstructions of actual chromosomal events (using chromosome banding or in situ methods) and more detailed characterization of the status of satDNA.
We have shown that a phylogenetic perspective has improved our understanding of not only chromosomal evolution, but also the related and complex history of RPCS across this diverse mammalian clade. Indeed, inferences concerning radical changes (or stability) across the phylogeny were key to assessing the relationship between amplifications and/or deletions of RPCS and chromosomal evolution in tuco-tucos. Clearly, further phylogenetic work is needed to explore uncertainty at or near the base of the tuco-tuco tree, which could not be resolved by cytochrome b sequences. Other markers should be incorporated to test the clades proposed by these analyses and to investigate the early evolutionary history of this chromosomally diverse clade.
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Acknowledgements |
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Footnotes |
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1 Keywords: satellite DNA
chromosomal evolution
cytochrome b
phylogenetics
2 Address for correspondence and reprints: M. Susana Rossi, Laboratorio de Fisiología y Biología Molecular, Facultad de Ciencias Exactas y Naturales, Departamento de Ciencias Biológicas, Pabellón II, Ciudad Universitaria, C1428EHA, Buenos Aires, Argentina. srossi{at}bg.fcen.uba.ar
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