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Report the Derived FOXP2 Variant of Modern Humans Was Shared with Neandertals Please cite this article in press as: Krause et al., The Derived FOXP2 Variant of Modern Humans Was Shared with Neander- tals, Current Biology (2007), doi:10.1016/j.cub.2007.10.008 Current Biology 17, 1–5, November 6, 2007 ª2007 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2007.10.008 Report The Derived FOXP2 Variant of Modern Humans Was Shared with Neandertals Johannes Krause,1,* Carles Lalueza-Fox,2 evolutionary changes in FOXP2, a gene that has been Ludovic Orlando,3,4 Wolfgang Enard,1 implicated in the development of speech and language. Richard E. Green,1 Herna´n A. Burbano,1 We furthermore find that in Neandertals, these changes Jean-Jacques Hublin,1 Catherine Ha¨nni,3,4 lie on the common modern human haplotype, which Javier Fortea,5 Marco de la Rasilla,5 previously was shown to have been subject to a selec- Jaume Bertranpetit,6 Antonio Rosas,7 tive sweep. These results suggest that these genetic and Svante Pa¨a¨bo1 changes and the selective sweep predate the common 1Max Planck Institute for Evolutionary Anthropology ancestor (which existed about 300,000–400,000 years Deutscher Platz 6 ago) of modern human and Neandertal populations. 04103 Leipzig This is in contrast to more recent age estimates of the Germany selective sweep based on extant human diversity data. 2Departament de Biologia Animal Thus, these results illustrate the usefulness of retriev- Facultat de Biologia ing direct genetic information from ancient remains for Universitat de Barcelona understanding recent human evolution. Avenida Diagonal 645 08028 Barcelona Results and Discussion Spain 3Pale´ oge´ ne´ tique et E´ volution Mole´ culaire One approach to understanding the origin and evolution Institut de Ge´ nomique Fonctionnelle de Lyon of language is to study the evolution of genes necessary Universite´ de Lyon for language acquisition. Although language and speech CNRS, INRA are clearly genetically complex phenomena, the only E´ cole Normale Supe´ rieure de Lyon, 46 Alle´ e d’Italie gene currently known that has a specific role in the de- 69364 Lyon, Cedex 07 velopment of language and speech is FOXP2 [1, 2]. France The inactivation of one FOXP2 copy leads primarily to 4Institut Fe´ de´ ratif Biosciences Gerland Lyon Sud deficits in orofacial movements and linguistic process- Universite´ Lyon 1 ing similar to those in individuals with adult-onset CNRS, INRA Broca’s aphasia [3]. Although FOXP2 is among the 5% E´ cole Normale Supe´ rieure de Lyon, 46 Alle´ e d’Italie most conserved proteins among mammals [4], two 69364 Lyon, Cedex 07 amino acid substitutions have fixed in the human lineage France since our split from the chimpanzee common ancestor. 5A´ rea de Prehistoria Departamento de Historia These amino acid substitutions are caused by nucleo- Universidad de Oviedo tide substitutions at positions 911 and 977 in exon 7 of Calle Teniente Alfonso Martı´nez s/n the FOXP2 gene and change threonine to aspartic acid 33011 Oviedo and arginine to serine residues, respectively. Coales- Spain cent simulations using extant human diversity data in 6Unitat de Biologia Evolutiva, CEXS the region around exon 7 suggested that a recent selec- Universitat Pompeu Fabra tive sweep occurred [4, 5] and ended within the last c. Dr. Aiguader 88 200,000 years [4]. Taken together, these results are 08003 Barcelona compatible with the notion that these two amino acid Spain substitutions are associated with the emergence of fully 7Departamento de Paleobiologı´a modern language ability [4, 5]. We have thus undertaken Museo Nacional de Ciencias Naturales (CSIC) a targeted approach to determine the genotype of Nean- Calle Jose´ Gutierrez Abascal 2 dertals at these FOXP2 positions. 28006 Madrid The retrieval of nuclear DNA sequences from ancient Spain remains by the polymerase chain reaction (PCR) is fraught with difficulty, primarily because most remains contain extremely low quantities of endogenous DNA. Summary An additional problem when Neandertal remains are studied is that modern human DNA is a frequent con- Although many animals communicate vocally, no ex- taminant of ancient remains and laboratory reagents [6] tant creature rivals modern humans in language ability. and that most human DNA sequences cannot be distin- Therefore, knowing when and under what evolutionary guished from Neandertal sequences [7]. Thus, in addi- pressures our capacity for language evolved is of great tion to designing six primers that in four combinations interest. Here, we find that our closest extinct relatives, amplify the nucleotide positions 911 and 977 (Figure 1), the Neandertals, share with modern humans two we designed three types of controls in order to as far as possible ensure the authenticity of our results. First, we analyzed the ratio of Neandertal to modern *Correspondence: [email protected] human mitochondrial (mt) DNA in an mtDNA segment Please cite this article in press as: Krause et al., The Derived FOXP2 Variant of Modern Humans Was Shared with Neander- tals, Current Biology (2007), doi:10.1016/j.cub.2007.10.008 Current Biology Vol 17 No 21 2 Figure 1. Sequence Alignment of Nucleotide Positions 880–1020 from the FOXP2 Gene The two nonsynonymous nucleotide substitutions on the human lineage are indicated by arrows. Identical positions in the alignment are given as dots. The three primer pairs used to retrieve the two substitutions from the El Sidro´ n Neandertals are indicated by arrows. where Neandertals and contemporary humans can be mixes and performed two-step multiplex PCRs [18]. All distinguished on the basis of several substitutions [8] primers were amplified for 30 cycles in a first PCR from fixed in each group. Among 46 DNA extracts prepared which aliquots were removed and then used to amplify from 22 Neandertal bones, we identified two bones each specific target individually in a second PCR. For where approximately 98%–99% of the hominid mtDNA each primer mix and individual, we also performed mock in the extracts are of the Neandertal type and where DNA amplifications containing no template DNA. None of 108 is abundant enough for PCR. Both bones originate from secondary PCRs from such negative controls yielded El Sidro´ n Cave in Asturias (north of Spain) [9]. These any specific product. The results for the two Neandertals bones (numbers 1253 and 1351c) were removed under are summarized in Figure 2. sterile conditions directly from the excavation in 2006, For the autosomal controls, nine out of 20 secondary immediately frozen, and transported to our clean room PCRs yielded the relevant products. The fact that not facility where extractions were performed. Because all primer pairs yield products shows that the extracts additional DNA sequences from the mtDNA hypervari- contain such small amounts of nuclear DNA that ampli- able region show that they stem from different individ- fication success is only sporadic and likely to often start uals (data not shown), they are referred to as the first from single-template molecules [10]. For two of the three and the second Neandertal, respectively, below. autosomal positions analyzed, both individuals carry the Second, we designed a number of additional controls ancestral allele. Out of the five products retrieved for the for detecting modern human nuclear DNA contamina- third autosomal position (A1, Table S1), both the ances- tion. To this end, we used genomic sequence data pro- tral and derived alleles are found in both El Sidro´ n Nean- duced from a 38,000-year-old Neandertal from Vindija dertals, suggesting that they were polymorphic at this Cave, Croatia [8] to identify seven sequence positions position. The second individual in addition carried an al- on autosomes and the X chromosome that are ancestral lele not seen in modern humans or chimpanzees. Given (i.e., identical to the chimpanzee sequence) in the Vindija that this sequence variant is a G to T substitution, not Neandertal but derived (i.e., different from the chimpan- a substitution commonly associated with ancient DNA zee sequence) and not known to vary among current hu- damage [10], it is likely to represent a genuine allele mans. We avoided C to T or G to A differences because present in the Neandertals. However, further work would these are common artifacts of ancient DNA sequences be necessary to verify this. Out of four X chromosomal [10–14]. We chose several control positions based on positions, only one yielded products in one individual. the Vindija Neandertal because it is not certain that It carried the ancestral state. Both Neandertals yielded any particular one would be shared with the El Sidro´ n products for Y chromosomal primer pairs, indicating Neandertals. Furthermore, given that most extracts con- that they were males. Strikingly, all 15 Y chromosomal tain very low amounts of Neandertal DNA, we expect products for the five assayed positions show the ances- only a fraction of amplifications of nuclear target se- tral allele. This includes two polymorphisms that define quences in any one experiment to yield products. the deepest split among current human Y chromosomes Third, we took advantage of the detailed modern hu- (Y2 and Y4, Figure S1) as well as two polymorphisms man Y chromosome phylogeny [15] and the fact that that cover less common African Y chromosomes (Y3 the time to the most recent common ancestor for mod- and Y5, Figure S1). These Y chromosome results must ern human Y chromosomes, approximately 90,000 years derive, then, either from Y chromosomes that fall out- ago [16], is more recent than the estimated population side the variation of modern humans or from the very split time with Neandertals [17]. A priori we therefore ex- rare African lineages not covered by the assay (Fig- pect Neandertal Y chromosomes to fall outside the var- ure S1). For our purposes, this result shows that neither iation of modern human Y chromosomes unless there the maternally inherited mtDNA nor the paternally in- was male gene flow from modern humans into Neander- herited Y chromosome shows evidence of gene flow tals.
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