Erratic overdispersion of three molecular clocks: GPDH, SOD, and XDH

Rodrı́guez-Trelles, Francisco; Tarrı́o, Rosa; Ayala, Francisco J.

doi:10.1073/pnas.201392198

Cited by 61 publications

(32 citation statements)

References 45 publications

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“…1. The GenBank accession numbers for the corresponding Xdh nucleotide sequences are given elsewhere (20)(21)(22)(23)(24)(25), except for the cases of Anopheles gambiae, Danio rerio, Fugu rubripes, Ciona intestinalis, Caenorhabditis briggsae, Aspergillus fumigatus, Histoplasma capsulatum, Magnaporthe grisea, Dictyostelium discoideum, Oryza sativa, and Chlamydomonas reinhardtii, the hypothetical Xdh sequences of which were obtained by conducting BLAST searches with already-known Xdh amino acid sequences against their genome databases, and unambiguously corroborated by phylogenetic criterion. The data set includes 62 species of drosophilids, specially aimed to accomplish a dense phylogenetic sampling of all main lineages closely related to D. sucinea and D. capricorni (belonging to the bocainensis subgroup of the willistoni group), the two species containing intron A. Twelve of these species are named in Fig.…”

Section: Methodsmentioning

confidence: 99%

A new Drosophila spliceosomal intron position is common in plants

Tarrı́o¹,

Rodrı́guez-Trelles²,

Ayala³

2003

Proc. Natl. Acad. Sci. U.S.A.

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The 25-year-old debate about the origin of introns between proponents of ''introns early'' and ''introns late'' has yielded significant advances, yet important questions remain to be ascertained. One question concerns the density of introns in the last common ancestor of the three multicellular kingdoms. Approaches to this issue thus far have relied on counts of the numbers of identical intron positions across present-day taxa on the assumption that the introns at those sites are orthologous. However, dismissing parallel intron gain for those sites may be unwarranted, because various factors can potentially constrain the site of intron insertion. Demonstrating parallel intron gain is severely handicapped, because intron sequences often evolve exceedingly fast and intron phylogenetic distributions are usually ambiguous, such that alternative loss and gain scenarios cannot be clearly distinguished. We have identified an intron position that was gained independently in animals and plants in the xanthine dehydrogenase gene. The extremely disjointed phylogenetic distribution of the intron argues strongly for separate gain rather than recurrent loss. If the observed phylogenetic pattern had resulted from recurrent loss, all observational support previously gathered for the introns-late theory of intron origins based on the phylogenetic distribution of introns would be invalidated.S pliceosomal introns are one of the hallmarks of eukaryotic genomes, which are distinctively elusive at providing unmixed clues about their evolutionary origins. Yet, after 25 years of contention (see ref. 1 and references therein), the dispute about the origins of introns between ''introns-early'' (IE, alternatively known as the exon theory of genes) and ''introns-late'' (IL) advocates seems to be approaching a synthesis. It is now almost certain that, if the progenote had introns, those could be type II self-splicing introns but never spliceosomal introns (1, 2). Because of the presumably severe constraints imposed on intronic recombination by the role that self-splicing introns play in their own removal, the IE advocates claim that exon shuffling as a factor for the assemblage of primordial genes seems unlikely. However, recent findings in the deeply diverging, putative basal eukaryote Giardia strongly indicate that spliceosomal introns originated in the eukaryotic stem before the diversification of protists, considerably earlier than suggested initially by IL advocates (i.e., around the time of origin of multicellularity; ref.3). The IL notion that spliceosomal introns as well as the spliceosoma evolved through subfunctionalization of one or more self-splicing group II introns (2, 4, 5) has gained credit. Once released from the constraints of self-splicing, spliceosomal introns may have been instrumental in creating a profusion of new eukaryotic genes by exon shuffling (6). IE supporters now admit that intron insertion is an important process in the evolution of eukaryotic genes, although they persist in asserting that deletion of ancest...

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Section: Methodsmentioning

confidence: 99%

A new Drosophila spliceosomal intron position is common in plants

Tarrı́o¹,

Rodrı́guez-Trelles²,

Ayala³

2003

Proc. Natl. Acad. Sci. U.S.A.

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“…By assuming that mutation rates for protein coding loci are equal within the closely related L. rufiventris and C. seminitidus (Kimura 1983, but see Rodriguez-Trelles et al 2001), the relative reduction in N e of the former in comparisons to the latter can be represented as the following ratio:…”

Section: Data Analysesmentioning

confidence: 99%

Increased genetic differentiation in a specialist versus a generalist bee: implications for conservation

et al. 2006

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Oligolectic bees are specialists that collect pollen from one or a few closely related species of plants, while polylectic bees are generalists that collect pollen from both related and unrelated species of plants. Because of their more restricted range of floral hosts, it is expected that specialists persist in more isolated populations than do generalists. We present data on the population structure of two closely related bee species sampled from a super abundant floral host in the southern Atacama Desert. Pairwise comparisons of population subdivision over identical distances revealed that the specialist bee had significantly more differentiated populations in comparison to the generalist. Further, populations of the specialist had significantly less genetic variation, measured as observed and expected heterozgyosity, than those of the generalist. Our data support the hypothesis of decreased gene flow among populations of the specialist bee even at equivalent geographic distances. The resulting reductions in effective population size for specialists make them particularly prone to extinction due to both demographic and genetic reasons. Our findings have important implications for the conservation of bees and other specialist insects.

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“…Note, however, that (i) even if rate constancy holds, r R and r U represent different realizations of a stochastic process, subject to sampling variation such that they are not expected to be identical; indeed, the dispersion of the rate of molecular evolution has proved to be much larger than expected if the probability of change were constant (3,4,15,16); and (ii) because of its definition as a quotient of (often nonindependent, gamma-distributed) rates, time-since-divergence is an asymmetrically bounded random variate: constrained to be non-negative (i.e., the lower boundary is nonelastic) but unbounded above zero (i.e., elastic boundary). Equivalent random deviations around target times scale divisively forward (i.e., to the present), but multiplicatively backward (i.e., to the past) on their target times.…”

Section: -11 and 14)mentioning

confidence: 99%

A methodological bias toward overestimation of molecular evolutionary time scales

Rodrı́guez-Trelles

Tarrı́o

Ayala

2002

Proc. Natl. Acad. Sci. U.S.A.

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108

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There is presently a conflict between fossil-and molecular-based evolutionary time scales. Molecular approaches for dating the branches of the tree of life frequently lead to substantially deeper times of divergence than those inferred by paleontologists. The discrepancy between molecular and fossil estimates persists despite the booming growth of sequence data sets, which increasingly feeds the interpretation that molecular estimates are older than stratigraphic dates because of deficiencies in the fossil record. Here we show that molecular time estimates suffer from a methodological handicap, namely that they are asymmetrically bounded random variables, constrained by a nonelastic boundary at the lower end, but not at the higher end of the distribution. This introduces a bias toward an overestimation of time since divergence, which becomes greater as the length of the molecular sequence and the rate of evolution decrease.T he hypothesis of the molecular clock holds that the number of amino acid (or nucleotide) replacements in any given protein (or DNA) sequence changes linearly with time (1, 2). If constant, rates of molecular evolution can be extrapolated for dating past evolutionary events. Rates used for extrapolation have to be first calibrated by reference to absolute dates drawn from the fossil record. A notable feature of the hypothesis of the molecular clock is multiplicity: every one of the thousands of proteins or genes of an organism is an independent clock, each ticking at a different rate, but all measuring the same events (3-5). Molecular clock projections have ostensibly pushed back fossil-based dates in many studies (6). Prominent examples are the time of origin of the metazoan phyla, which has been placed as twice as old as determined by paleontologists (but see ref. 7), dating to more than 1,000 Myr ago (8-10); or the split of the three multicellular kingdoms, timed at about 1,600 Myr ago (9-11), some 400 Myr earlier than predicted from the fossil record.Two not mutually exclusive explanations have been adduced to account for molecular earlier than fossil dates: (i) incompleteness of the fossil record, such that paleontological data can provide only minimal divergence dates (6, 12, 13); and (ii) too few genes and proteins considered, which turns molecular dating methods inaccurate (6, 9). It has been proposed that discrepancies between fossil and molecular dates will fade away as new fossil findings continue to accumulate; but also, and more steeply, as the size of molecular data sets become increasingly larger, because averages across numerous estimates of the same date will converge toward more consistent estimates (6,9,10,14). Yet although data sets have become much larger and methods of analysis considerably more sophisticated, the discrepancy between fossil and molecular dates has not disappeared (reviewed in ref. 6). We now show that common molecular estimates are upwardly biased because of a fundamental f law in the molecular approach to dating.Suppose three orthologous protein sequenc...

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Erratic overdispersion of three molecular clocks: GPDH, SOD, and XDH

Cited by 61 publications

References 45 publications

A new Drosophila spliceosomal intron position is common in plants

A new Drosophila spliceosomal intron position is common in plants

Increased genetic differentiation in a specialist versus a generalist bee: implications for conservation

A methodological bias toward overestimation of molecular evolutionary time scales

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