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The Y Chromosome As a Storyteller Jaume Bertranpetit* Facultat De Cie`Ncies De La Salut I De La Vida, Universitat Pompeu Fabra, Barcelona, Catalonia, Spain

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The Y Chromosome As a Storyteller Jaume Bertranpetit* Facultat De Cie`Ncies De La Salut I De La Vida, Universitat Pompeu Fabra, Barcelona, Catalonia, Spain Commentary Genome, diversity, and origins: The Y chromosome as a storyteller Jaume Bertranpetit* Facultat de Cie`ncies de la Salut i de la Vida, Universitat Pompeu Fabra, Barcelona, Catalonia, Spain nalysis of human genome variation concerning the accuracy of our knowledge tion. The new analysis (2) on the same Amay focus on one of two possible goals: of genome dynamics, worries concerning chromosome gives only one-third of the understanding the genome region under the ability and power to detect specific pro- time. It is thus an interesting new proposal study or solving historical and evolutionary cesses and disentangle cases where more not only in human evolution but also in questions specific to the population(s) ana- than one mechanism may have produced human evolutionary genetics. It could mean lyzed. Understanding of variation of a given similar genetic patterns, and worries con- that a population with modern characteris- genome region has a genetic interest be- cerning the appropriateness of evolutionary tics had to exist in Africa 50,000 ya and cause it is a consequence of the dynamics of models needed for the inference. And fi- spread later to Eurasia and the rest of the the genome and thus the evolutionary forces nally there have been worries from anthro- world. Besides the concordance of this pro- (mutation, selection in its varieties, drift, pologists who do not perceive the interface posal with archaeological evidence, there recombination, . ) may be understood. It between the evolutionary biology of a spe- are more strictly genetic issues to be dis- is thus a way to understand the mechanisms cies and that of tiny fragments of DNA, cussed, namely the limitations of the theory that produce variation in the genome. On usually in noncoding regions, worries sur- and of the genetic data, the interpretation of the other hand, when genetic variation is rounding a fast-developing field, heir to the variation, and possible specific proper- being analyzed, random individuals from classical population genetics, with brilliant ties unique to the Y chromosome. specific populations offer the possibility to novelties but also eager to get headlines. New ideas coming from genetics in hu- trace back their origin beyond the limitation In this context, two related papers in man evolution have had very different fates, of the genome region sampled. The goal this issue (1, 2) analyze an ample set of and some cases are remembered for having then may be the evolutionary reconstitution sequences of the Y chromosome to ad- proposed a paradigm shift strongly attacked of specific populations or, for a global sam- dress the issue of human origins. Their by paleoanthropologists but later shown to pling, the origin of our species. The under- main objective is to propose a novelty: the be correct. This was the case for the time lying idea is very simple: if we are able to common origin of present humans is not depth of the hominid branch, as a separate COMMENTARY trace back the coalescence of genomic re- as old as previously believed, but should group from our close relatives, the chim- gions from an ample worldwide sample, we be much more recent, around 50,000 years panzee and the bonobo. In most cases the can infer the phylogeny of humans. The ago (ya), the age of coalescence of the Y process either to acceptance or rejection rationale can be sketched as follows: chromosomes surveyed (2) and in congru- goes with a lively debate in which scholars (i) The evolutionary dynamics of the ge- ence with an onset of expansion of around from very different disciplines enter the fray nome region is known in pattern and tempo. 30,000 ya (1). Moreover, both studies cor- with non-mutually intelligible languages. A (ii) From the extant variation the past roborate the existence of a substantial (or proposal like the present one (1, 2), stem- can be inferred and the coalescence pro- exponential) population growth and an ming from genetics, has implications in sev- cess reconstructed; in some cases just part African origin for modern humans, in eral fields, from which specific clarifications of the genetic information is being used, accord with most other genetic data. may be asked: and analyses do not fully exploit the in- The newly proposed age is much younger (i) Evolutionary genetics: Are conclu- formation contained in the data. than dates consistent with nuclear and mi- sions about population fully supported or (iii) Translate the genetic process into a tochondrial DNA (mtDNA) (see references may there be a bias due to the genomic process of individuals that reproduce (the in ref. 2), where the minimum coalescent region under study? Does all of the ge- population), and the time and place of the age was obtained for mtDNA at around nome tell the same story? ancestral individual (carrying the ances- 150,000 years and much older for nuclear (ii) Mathematical genetics: May the tral genome) may be recognized. genes, except for the present case. Similar models used be safely applied to the real (iv) If the geographic distribution of results have been obtained through other world, apart from their theoretical ele- derivative genetic stages is known, the genetic approaches, such as short tandem gance? What are the implications of vio- expansion process may be dissected as repeat (STR, also called microsatellite) vari- lation of the theoretical assumptions? migratory waves and events. ation (3), where a figure of 156,000 years for (iii) Human paleontology: Is the evolu- (v) The structure of the genetic variation the deepest split in human phylogeny was tionary history of humans as interpreted may reveal demographic characteristics such obtained, or Alu insertions (4), with a pro- from the hard evidence (the fossils) com- as population size and subdivision as well as posed age of 137,000 years for the time of patible with the new genetic proposals? ancient dynamics, such as expansions. separation of African versus non-African (iv) Archaeology and Paleodemogra- This simple pathway is not easy. Infer- populations. phy: Since cultural innovations are at the ences from molecules to populations are not What seems more surprising is the dis- base of population expansions, are time straightforward, and there have been recur- crepancy with the results of nine diallelic and mode of cultural change correlated rent worries on what was being analyzed, polymorphic sites on the Y chromosome either the genes or genomic regions on one (5), where the analysis with the same meth- hand or the individuals, populations, or spe- ods as those in ref. 2 gave a figure of around See companion articles on pages 7354 and 7360. cies on the other. There have been worries 150,000 ya for the coalescence of the varia- *E-mail: [email protected]. PNAS ͉ June 20, 2000 ͉ vol. 97 ͉ no. 13 ͉ 6927–6929 Downloaded by guest on September 26, 2021 Table 1. Observed nucleotide diversity in coding and noncoding regions of autosomes that it is a footprint of a population expan- and X and Y chromosomes and values predicted for the Y chromosome by correcting sion, other phenomena could be involved, the values for autosomes and the X chromosome for the population size, assuming that such as a selective sweep or an uneven male and female effective population sizes are equal mutation rate along the nucleotides. Thus Diversity ϫ 10Ϫ4 genomic factors and population factors mimic each other in shaping genetic varia- Observed Predicted for Y tion, and only accurate and comparative Regions Autosomes X Y By autosomes By X analyses may solve ambiguities. There is still another alternative that Coding 2.91 1.96 0.52 0.73 0.65 could account for a discordance of results Noncoding 6.18 3.92 1.11 1.54 1.31 between Y chromosome age and other ge- netic results, as the history of the Y chro- mosome may be different from the history with their demographic consequences re- selection has not been important in hu- of the autosomes and mtDNA. Conflicting trieved through genetic data? man history, what is at the base of the patterns in the structure of genetic variation differentiation of populations is drift. To have been found between Y chromosome To Understand the Genome or the Popula- what extent can drift alone explain levels and mtDNA, that is, between paternal and tion? Take two good papers on evolution- of differentiation found among Y chro- maternal lineages (8, 9), which have been ary genetics, one on Drosophila and the mosomes in humans? For STRs (6) it was interpreted as a sex-specific migratory pat- other on humans. As an average, there is shown that differentiation between popu- tern, with higher mobility for females than a striking difference: while the Drosophila lations (as measured by Fst, a measure of males. Could a sex-specific characteristic paper tends to focus on the understanding genetic distance) and gene diversity within account for discrepancies in coalescence? A of the genomic region and the forces act- populations were comparable to those of possible explanation could be a lower effec- tive size for Y chromosomes than for ing on it, keeping demography and history autosomal STRs when corrections for the mtDNA and for autosomes. The latter is at a second level, the human paper tends smaller effective population size of the Y much less likely, as differences should be to address specific population questions, chromosome were taken into account. dramatic to show their effect, as autosomes considering that the mechanisms of ge- Nothing else was needed to explain the are in both males and females. But even for nome change are sufficiently well known 4-fold difference in the value of Fst be- mtDNA, differences do not seem to have for the purpose.
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