Molecular Biology and Evolution 17:1417-1424 (2000)
© 2000 Society for Molecular Biology and Evolution
ARTICLE |
Consistency of SINE Insertion Topology and Flanking Sequence Tree: Quantifying Relationships Among Cetartiodactyls
*Institute of Statistical Mathematics, Tokyo, Japan;
and
Tokyo Institute of Technology, Yokohama, Japan
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Abstract |
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 TOP Abstract IntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsliterature cited |
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Short interspersed nuclear elements (SINEs) have been used to generate unambiguous phylogenetic topologies relating eukaryotic taxa. The irreversible nature of SINE retroposition is supported by a large body of comparative genome data and is a fundamental assumption inherent in the value of this qualitative method of inference. Here, we assess the key assumption of unidirectional SINE insertion by comparing the SINE insertion–derived topology and the phylogenetic tree based on seven independent loci of five taxa in the order Cetartiodactyla (Cetacea + Artiodactyla). The data sets and analyses were largely independent, but the loci were, by definition, linked, and thus their consistency supported an irreversible pattern of SINE retroposition. Moreover, our analyses of the flanking sequences provided estimates of divergence times among cetartiodactyl lineages unavailable from SINE insertion analysis alone. Unexpected rate heterogeneity among sites of SINE-flanking sequences and other noncoding DNA sequences were observed. Sequence simulations suggest that this rate heterogeneity may be an artifact resulting from the inaccuracies of the substitution model used.
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsliterature cited |
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Analysis of the insertion patterns of SINEs to diagnose common ancestry among eukaryotic host genomes is emerging as a powerful new method of phylogenetic inference (Murata et al. 1993
; Shimamura et al. 1997
; Takahashi et al. 1998
; Nikaido, Rooney, and Okada 1999
; Shedlock and Okada 2000
). The putatively irreversible, independent nature of SINE retropositional events allows them to be employed as unambiguous, shared, derived characters for straightforward cladogram construction. Exploration of the limits of this new approach to molecular systematics invites further investigation (Hillis 1999
; Miyamoto 1999
; Shedlock, Milinkovitch, and Okada 2000
; Shedlock and Okada 2000
). Statistical evaluation of SINE data and their integration with conventional comparative DNA sequence analyses are particularly rich areas for the development of new methods.
Although SINE insertions allow one to construct tree topologies, they cannot be used reliably to calculate relative branch lengths without the ability to model amplification rates of SINE markers over time. It seems clear from well-studied systems such as mammalian MIR elements, human Alus, and the Hpa-I SINEs in fishes (Quentin 1988
; Deininger and Batzer 1993
; Takasaki et al. 1994
; Schmid 1996
) that assuming a constant rate of amplification across and within lineages is not justified and that establishing accurate historical amplification profiles for elements inserted at each independent locus analyzed is intractable. However, SINE-flanking sequences may potentially be used for dating historical retropositional events that diagnose common ancestry, because of the probable neutral nature of evolution in nonfunctional regions of the genome (Del Pozzo and Guardiola 1990
; Shedlock and Okada 2000
). The amount of divergence between nonfunctional SINE-flanking sequences at orthologous loci is proportional to elapsed time, and so analyses of these flanking sequences will provide branch lengths to the SINE topology. In contrast, if loci assumed to be orthologous are actually paralogous, we expect a lack of correspondence between the SINE insertion topology and the flanking-sequence tree. Thus, our evaluation of the consistency between the phylogenetic signal of the SINE insertion and flanking-sequence data is an explicit test of the assumption of orthology of loci.
Traditional morphological taxonomy groups the even-toed ungulates within the order Artiodactyla. Within this order are the three suborders Tylopoda (camels), Suiformes (pigs, peccaries, and hippopotamuses), and Ruminantia (deer, cows, giraffes, etc.) (Simpson 1984
). Cetacea (baleen and toothed whales) is considered a distinct order of probable ungulate origin (Dawson and Krishtalka 1984
). In contrast, molecular phylogenetics have described cetaceans as nested within the order Artiodactyla (Graur and Higgins 1994
; Shimamura et al. 1997
), often with whales and hippopotamuses as sister taxa (Sarich 1985
; Gatesy et al. 1996
; Ursing and Arnarson 1998
; Nikaido, Rooney, and Okada 1999
). A recent, inclusive analysis of DNA sequence data from Cetartiodactyla taxa supports these relationships and also identifies the camel as the root of Cetartiodactyla (Gatesy 1999
). Thus, molecular data view both the traditional order Artiodactyla and the suborder Suiformes as paraphyletic and argue for a revised order Cetartiodactyla (Cetacea + Artiodactyla).
In order to evaluate the orthologous nature of SINE insertion loci and to explore the feasibility of accurately estimating branch lengths for SINE cladograms, we analyzed the DNA sequences flanking seven SINE insertion sites, five of which were recently used to qualitatively define the relationships within the order Cetartiodactyla (Nikaido, Rooney, and Okada 1999
). We reasoned that if the SINE loci examined were orthologous and no misleading excision of elements had occurred, the relationships of the flanking sequences should mirror the SINE insertion topology. If the two data sets were found to be consistent, we then planned to use the sequence divergences to estimate branch lengths for the SINE insertion topology.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsliterature cited |
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DNA sequences from seven SINE insertion loci (APO, GPI, INO, KM14, LAC, M11, and PRO) were determined by previously described methods (Shimamura et al. 1997
; Nikaido, Rooney, and Okada 1999
). Sequences were aligned using ClustalX (Thompson et al. 1997
), and all ambiguously aligned regions and gap sites were removed. A total of 2,048 bases from at least one species representing five presumably monophyletic groups (Tylopoda, Hippopotamidae, Suidae, Cetacea, and Ruminantia) were analyzed (table 1
). Although our analyses were of unrooted trees, we implicitly assumed the root to Cetartiodactyla was to Tylopoda, as indicated by analyses of DNA sequences (Gatesy 1999
) and SINE insertions (Nikaido, Rooney, and Okada 1999
).
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The seven loci were analyzed individually and as concatenated sequences. The log-likelihoods of the 15 possible unrooted topologies relating the five taxa were calculated assuming a general reversible substitution model with a discrete gamma distribution of eight categories for the rate variation among sites (Yang 1994
) using the program baseML in the software package PAML, version 1.3A (Yang 1997
). The bootstrap support for nodes was estimated from the total data by the RELL method (Kishino, Miyata, and Hasegawa 1990
; Hasegawa and Kishino 1994
) using the program TotalML in MOLPHY, version 2.3 (Adachi and Hasegawa 1996a
). Divergence times were estimated from the concatenated sequences allowing the rate of evolution to vary among lineages (Thorne, Kishino, and Painter 1998
).
For each data set, the gamma parameter 
, which summarizes rate variation among sites, was estimated using the program baseML (Yang 1997
). To evaluate the distribution of the estimated values, two additional log-likelihoods were calculated from each data set by fixing to be first 1 and then 
. The log-likelihood value corresponding to the estimated was then compared with the values corresponding to = 1 and = using the likelihood ratio test. To further explore the estimation of , two data sets were simulated from the seven concatenated loci from five taxa using a version of PAML modified by one of us (H.S.). Each of these data sets consisted of 1,000 replicates of simulated sequences (5 x 2,048 bases) with fixed at either the value estimated from the original data or . Values of were then estimated from the two sets of 1,000 replicates.
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsliterature cited |
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The results of the maximum-likelihood analyses of the seven loci and the total data are shown in table 2 . Tree 1, (Tylopoda, Suidae, (Ruminantia, (Hippopotamidae, Cetacea))), is favored by the M11 locus and the total data analyses. For the total data analysis, tree 1 is favored over other topologies by at least 9.4 log-likelihood scores and has bootstrap support of 88%. Of the four other trees supported by at least one locus, the two with the strongest support are tree 4, (Tylopoda, Ruminantia (Suidae, (Hippopotamidae, Cetacea))), and tree 5, (Tylopoda, (Suidae, Ruminantia), (Hippopotamidae, Cetacea)), with 6% and 4% bootstrap support, respectively. Thus, 98% of bootstrap replicates support the pairing of the hippopotamus and the whale to the exclusion of other artiodactyls. Although tree 1 is not the maximum-likelihood tree for all loci, more importantly, it is not rejected by any locus. The total branch length, defined as the cumulative substitutions per site over tree 1 for the concatenated sequences, is 0.50 and is fairly uniform among loci (table 2 ).
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The estimates of the gamma shape parameter
for the tree 1 topology for the seven loci and five concatenated sequences are shown in table 3
. For each of the seven single-locus analyses, the maximum number of species available (total data) was used to estimate . For the M11 locus (estimated = 3.6), = 1 was rejected (P < 0.015), but not = (P > 0.13). Also included in table 3
for comparison are values of we estimated from intron sequences from salmon (GH1C and GH2C; Oakley and Phillips 1999
), carnivores (transthyretin intron I; Flynn and Nedbal 1998
), primates (IRBP intron1; Schneider et al. 1996
; Harris and Disotell 1998
), the 
-
-globin gene from primates (Koop et al. 1986
; Fitch et al. 1988
), and fourfold-degenerate sites from primate mtDNA (Horai et al. 1995
; Adachi and Hasegawa 1996b
). Figure 1B
shows that when data are simulated with fixed at 99 (infinity in PAML), 45% of the estimates of are lower, with a peak at = 10.
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Figure 2 shows the maximum-likelihood tree from the concatenated sequences with branch lengths proportional to the estimated number of substitutions. Bootstrap support for the nodes of this tree were calculated from the total data. As noted above, the grouping of hippopotamuses and Cetacea receives 98% bootstrap support, while the placement of ruminants as the most closely related taxa to this group receives 88% bootstrap support. The likelihood ratio test favors the nonclock model (fig. 2 ) over a clock model (P < 9.7 x 10-7), indicating rate variation among lineages. Although a molecular clock is rejected, divergence times may still be estimated by allowing the rates of evolution to evolve along lineages (Thorne, Kishino, and Painter 1998
). Figure 3
displays divergence times estimated in this manner. The variable molecular clock is calibrated by assuming the divergence of hippopotamuses and whales to be 52 MYA based on the primitive semiaquatic cetacean Pakicetus (Gingerich, Russell, and Ibrahim Shah 1983
).
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsliterature cited |
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One goal of this project was to evaluate the assumption of orthologous insertion inherent in the use of retroposons to diagnose clades. If any locus had experienced paralogous insertion or precise excision of a SINE element, we expected the sequences flanking that locus to strongly reject the SINE insertion topology. Analyses of the flanking sequences were further used to generate accurate branch lengths for SINE cladograms and thus provide additional insight into cetartiodactyl evolution. Our results are consistent with the original SINE analyses for these taxa (Shimamura et al. 1998
; Nikaido, Rooney, and Okada 1999
). Although tree 1 (Tylopoda, Suidae, (Ruminantia, (Hippopotamidae, Cetacea))) is not the maximum-likelihood tree for all loci, it is not rejected by any of the seven independent SINE loci examined and is the maximum-likelihood tree for all evidence considered simultaneously (table 2
). Although no outgroup to Cetartiodactyla is analyzed here, our unrooted phylogeny is completely consistent with the most recent SINE cladogram (Nikaido, Rooney, and Okada 1999
).
Figure 3
shows the divergence times estimated from the concatenated sequences allowing rates of evolution to evolve within lineages (Thorne, Kishino, and Painter 1998
). The radiation of the order Cetartiodactyla is estimated at 65 MYA, in general agreement with the appearance of large-bodied mammals in the fossil record (Dawson and Krishtalka 1984
). The split between ruminant and the sister taxa hippopotamuses and whales is estimated 60 MYA, indicating an earlier, and relatively rapid, divergence of the taxa Tylopoda and Suidae. These times are calibrated from a 52 MYA estimated divergence between hippopotamuses and whales. Pakicetus, an amphibious, but apparently not fully aquatic, ancestor of Cetacea (Gingerich, Russell, and Ibrahim Shah 1983
), is dated to 52 MYA, and presumably the ancestor of both Cetacea and Hippopotamus lived substantially prior to this time, making these divergence times minimum estimates.
A corollary of the divergence dates discussed above is estimates of the independent rates of evolution along each lineage. These relative rates of evolution are listed in table 4
, along with the body masses of each taxon. Since sequences from multiple cetaceans and ruminants are used here, an average body mass weighted by the number of bases from each species examined (table 1 ) is presented. Although it is unclear how long whales have been large, there are fossil skulls measuring 3.5 m dated to the Miocene (Dawson and Krishtalka 1984
). Similarly, it is uncertain when the other taxa examined attained their present size and life history characteristics, but surveys of extant species suggest that ruminants and suids have probably been the smallest artiodactyls over evolutionary time (Simpson 1984
). Note the inverse relationship between estimated substitution rate and body mass. The similarity of estimated evolutionary rates of ruminants and suids may reflect similar sizes and corresponding life histories. If evolution is neutral, as is probably the case for the SINE-flanking sequences, the substitution rate in evolution coincides with the mutation rate (Kimura 1983
). Body mass has been shown to be correlated with age of reproductive maturity, life span, and gestation period and inversely correlated with metabolic rate within mammalian taxa (Calder 1984
). We use body masses as estimators for these more interesting life history parameters because they are much easier to determine and are commonly available. The inverse relationship between estimated substitution rate and body mass is generally consistent with both the generation length (Wu and Li 1985
; Li, Tanimura, and Sharp 1987
) and the metabolic-rate hypothesis of molecular evolution (Martin, Naylor, and Palumbi 1992
). Further work focusing on the metabolic slowdown associated with deep-diving whales may be able to tease apart these correlated hypotheses.
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Since retroposons typically insert into nonfunctional regions dispersed throughout the eukaryotic genome (Weiner, Deininger, and Efstratiadis 1986
), one expects little rate heterogeneity among sites within flanking sequences. This expectation can be evaluated by examining the gamma shape parameter , which describes the mutation rate heterogeneity among sites. Theoretically, values of infinity result when all sites are free to vary with equal probability. In contrast, protein-coding sequences typically have values less than 1 due to the difference in constraints between the degenerate third position and the conservative, and sometimes nearly invariable, first and second positions within a codon (Hasegawa, Kishino, and Yano 1985
; Swofford et al. 1996
). The values of we observed for the SINE-flanking sequences ranged between 0.70 (PRO) and 3.90 (GPI) and were comparable with a wide range of other noncoding regions from a variety of taxa (table 3
). These data might seem to indicate that rate heterogeneity among sites is common even in the absence of functional constraints.
For each of the noncoding sequences, we calculated log-likelihood values for fixed values of 1 and in order to evaluate the shape of the likelihood surface. For the GPI locus and the two salmon introns (GH1C and GH2C), the likelihood surface was flat, with no significant variation with respect to values of ranging from 1 to . Values of for four of the other SINE-flanking loci (INO, KM14, LAC, and PRO), as well as IRBP intron 1 from primates, are not significantly different from 1. Interestingly, M11 is the only SINE-flanking sequence with an value not significantly different from .
In order to remove the potential effects of subtle biological sources of rate heterogeneity such as base composition, repeat motif instability, and regulatory constraints on the estimation of , a computer simulation was undertaken. Figure 1A
shows the estimates of from 1,000 data sets simulated from the seven concatenated loci with fixed at 2.01, the value estimated from the data (table 3
). The 1,000 values of have a mean of 2.2 and a standard deviation of 0.81. In contrast, figure 1B
shows the distribution of values estimated from data sets simulated with fixed at infinity. There are two modes to this distribution, with 55% of the values at 99 (infinity in PAML) and another peak at 10. These simulations indicate that rate heterogeneity may be inferred by chance even when = .
The unusual shape of the histogram (fig. 1B
) of the estimated values is caused by the parameterization of rate heterogeneity. In fact, the histogram is well approximated by the half-normal distribution if we use the natural parameterization 1/ instead of (fig. 4
). The following simplified model explains this:
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where xi and yi correspond to the relative rate and the observed pattern at site i, respectively. The variance 1/ of rates is estimated by
which is asymptotically distributed as the normal distribution, but with 0 representing all the negative values. The simulation results of Whelan and Goldman (1999)
and the argument of Ota et al. (2000)
confirm the above observation. Taking this into account, the P values of table 3
are calculated by the one-sided tests of 1/ = 1 against 1/ < 1, or 1/ = 0 against 1/ > 0.
Theoretically, the gamma parameter measures rate heterogeneity, but in practice, it may also compensate for other model parameters. For example, if there are aspects of the substitution process that are modeled unrealistically, then observed values of may confound rate heterogeneity and these hidden inaccuracies. The simulation results suggest that the rate heterogeneity observed in the SINE-flanking and other noncoding sequences may be an artifact of the substitution modeling process. Further work is in progress to explore this suggestion.
There are limits of SINE insertion analysis that require novel statistical approaches. These include the retention of ancestral polymorphisms and situations in which missing data or insufficient sampling of loci reduces confidence in hypothesis formation (Hillis 1999
; Miyamoto 1999
; Shedlock, Milinkovitch, and Okada 2000
; Shedlock and Okada 2000
). Also, methods used to assess the reliability of phylogenetic inference based on sequences, such as bootstrap resampling of data (Felsenstein 1985
), are not appropriate for small character sets. If the assumptions of irreversible and orthologous insertions are upheld, as in the present case, confidence in the character set defined by resampling of the data is not necessary (Sanderson 1995
; Shedlock, Milinkovitch, and Okada 2000
; Shedlock and Okada 2000
). Results from the present analyses represent an initial step toward confirming the assumptions fundamental to SINE character reliability. The integration of insertion data with nucleotide substitution information contained in nonfunctional flanking sequences provides a means for confirming the reliability and quantifying the phylogenetic results obtained qualitatively.
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Supplementary Material |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsliterature cited |
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The sequence alignment files used in the analyses are available on request. Accession numbers are AB028484–AB028488 and AB042892–AB042933.
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Acknowledgements |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSupplementary MaterialAcknowledgementsliterature cited |
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We thank the following individuals and organizations for providing samples: H. Kato (National Research Institute of Far Seas Fisheries, Shizuoka), M. Goto (Institute of Cetacean Research, Tokyo), I. Munechika (Chiba Zoological Park), Y. Mukai (Meat Hygiene Inspection Office, Nagano), and O. Ryder (Zoological Society of San Diego's Center for Reproduction of Endangered Species). We thank M. Fujiwara for assistance in implementing the software of J. Thorne. We would also like to thank the Japan Society for the Promotion of Science for postdoctoral support to J.K.L. (P97904) and A.M.S. (P98881) and the Ministry of Education, Science, Sports and Culture of Japan for research grants to M.H., N.O., and H.S.
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Footnotes |
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Dan Graur, Reviewing Editor
1 Keywords: SINE
DNA sequence
phylogeny
Cetartiodactyla
rate heterogeneity
mutation rate 
2 Address for correspondence and reprints: Masami Hasegawa, Institute of Statistical Mathematics, 4-6-7 Minami-Azabu, Minato-ku, Tokyo 106-8569, Japan. E-mail: hasegawa{at}ism.ac.jp
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Y.-H. Lin, P. A. McLenachan, A. R. Gore, M. J. Phillips, R. Ota, M. D. Hendy, and D. Penny Four New Mitochondrial Genomes and the Increased Stability of Evolutionary Trees of Mammals from Improved Taxon Sampling Mol. Biol. Evol., December 1, 2002; 19(12): 2060 - 2070. [Abstract] [Full Text] [PDF]
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 M. Nikaido, F. Matsuno, H. Hamilton, R. L. Brownell Jr., Y. Cao, W. Ding, Z. Zuoyan, A. M. Shedlock, R. E. Fordyce, M. Hasegawa, et al. Retroposon analysis of major cetacean lineages: The monophyly of toothed whales and the paraphyly of river dolphins PNAS, June 19, 2001; 98(13): 7384 - 7389. [Abstract] [Full Text] [PDF]
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 P. D. Gingerich, M. u. Haq, I. S. Zalmout, I. H. Khan, and M. S. Malkani Origin of Whales from Early Artiodactyls: Hands and Feet of Eocene Protocetidae from Pakistan Science, September 21, 2001; 293(5538): 2239 - 2242. [Abstract] [Full Text] [PDF]
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