MBE Advance Access originally published online on August 3, 2006
Molecular Biology and Evolution 2006 23(11):2081-2089; doi:10.1093/molbev/msl077
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Research Articles |
Genome Sequence Comparison Reveals Independent Inactivation of the Caspase-15 Gene in Different Evolutionary Lineages of Mammals
* Department of Dermatology, Medical University of Vienna, Vienna, Austria
Clinical Department for Farm Animals and Herd Management, University of Veterinary Medicine Vienna, Vienna, Austria
E-mail: leopold.eckhart{at}meduniwien.ac.at.
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Abstract |
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We have recently demonstrated that placental mammalian species such as pig and dog express a novel proapoptotic protease, caspase-15, whereas mouse and humans lack this enzyme. Here we investigated the evolutionary fate of the caspase-15 gene in different mammalian lineages by analyzing whole-genome shotgun sequences of 30 mammalian species for the presence of caspase-15 orthologs. Caspase-15 gene sequences were found in representatives of all major mammalian clades except for the superorders Afrotheria (tenrec, rock hyrax, and elephant) and Euarchontoglires (rodents, rabbit, tree shrew, and primates), which either lacked any caspase-15–like sequences or contained mutated remnants of the caspase-15 gene. Polymerase chain reaction screenings confirmed the results of the database searches and showed that the caspase-15 gene is expressed not only in various placental mammals but also in the marsupial, Monodelphis domestica. The observed species distribution implies that caspase-15 has originated in an early ancestor of modern mammals and has been conserved, over more than 180 Myr, in marsupials and many placental mammals, whereas it was independently lost in 2 phylogenetically distant clades of placental mammals, that is, Afrotheria and Euarchontoglires. Our data suggest that the inactivation of the caspase-15 gene was not counteracted by, and may even have been driven by, evolutionary constraints in these clades, and therefore, caution against the uncritical use of gene absence for the inference of phylogenetic relationships.
Key Words: caspase • gene deletion • Euarchontoglires • Afrotheria
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Caspase-15 is the newest member of the caspase family of cysteine proteases, which are implicated in apoptosis and inflammatory signaling (Degterev et al. 2003
; Martinon and Tschopp 2004; Eckhart et al. 2005). The physiological function of caspase-15 is not known at present. However, overexpression studies have shown that caspase-15, like other caspases, can induce programmed cell death in cultured cells (Eckhart et al. 2005). Caspase-15 is unique among mammalian caspases because of its prodomain that is predicted to fold into a pyrin domain, a structural motif implicated in the intermolecular binding of regulatory proteins in inflammation and apoptosis (Werts et al. 2006). The catalytic domain of caspase-15 is most similar in its amino acid sequence to caspase-14, a protease expressed in the epidermis of monotremes, marsupials, and placental mammals (Eckhart, Ban, et al. 2000; Eckhart, Declercq, et al. 2000; Alibardi et al. 2005). Expression of caspase-15 mRNA has been demonstrated in several organs of pig as well as in leukocytes of dog, cattle, sheep, goat, and horse (Eckhart et al. 2005). Analysis of genome sequences indicated that caspase-15 is absent from nonmammalian vertebrates including zebrafish, African clawed frog, and chicken (Eckhart et al. 2005) as well as from the mammalian species, mouse and humans.
The caspase-15–positive species described so far represent 3 orders (even-toed ungulates plus whales, odd-toed ungulates, and carnivores), which belong to the same clade of placental mammals, namely, Laurasiatheria (eulipotyphlan insectivores, bats, even-toed ungulates plus whales, odd-toed ungulates, carnivores, and pangolins) (Madsen et al. 2001; Murphy, Eizirik, Johnson, et al. 2001; Murphy, Eizirik, O'Brien, et al. 2001). By contrast, both mammalian species characterized as caspase-15–negative, that is, mouse and humans, belong to the superordinal clade Euarchontoglires (rodents, lagomorphs, tree shrews, flying lemurs, and primates). Therefore, 2 explanations for the observed distribution of the caspase-15 gene are possible: 1) the caspase-15 gene originated specifically within Laurasiatheria, or 2) caspase-15 originated before the split of Laurasiatheria and Euarchontoglires and was deleted in some or all Euarchontoglires. A clarification of this issue, which may have implications on comparative physiology (Garland et al. 2005), requires analysis of additional mammalian lineages in order to infer the ancestral state of the caspase-15 gene, that is, its absence or presence in the cenancestor of Laurasiatheria and Euarchontoglires. In this regard, representatives of the following clades are informative: monotremes and marsupials, which both diverged from the placental mammalian lineage more than 180 million years ago (MYA) (Springer et al. 2003) as well as the 2 placental mammalian superordinal clades Afrotheria (elephants, sirenians, hyraxes, aardvarks, tenrecs/golden moles and elephant shrews), and Xenarthra (anteaters, armadillos and sloths) (Madsen et al. 2001; Murphy, Eizirik, Johnson, et al. 2001; Murphy, Eizirik, O'Brien, et al. 2001; Kriegs et al. 2006). All other mammals are classified within the sister clades Laurasiatheria and Euarchontoglires and, accordingly, are phylogenetically close relatives of the known caspase-15–positive and caspase-15–negative species, respectively.
Mammalian species from diverse branches of the evolutionary tree have recently been selected for low-coverage genome sequencing (Margulies et al. 2005). In the course of the so-called mammalian genome project, the genomes of 16 mammals are being sequenced at a redundancy of twofold, which means that each nucleotide in the genome is covered, on average, by 2 sequence reads. Additional large-scale sequencing efforts have provided the finished genome sequences of humans and mouse, the nearly finished sequences of chimpanzee, rat, and dog, and low-coverage genome sequences of further mammals (table 1). As all mammalian genome sequences are open for Blast analysis on public domains, they can be used to search for gene orthologs among different groups of mammals.
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In the present study, we screened all mammalian genome sequences currently available for the presence of caspase-15 orthologs. Our findings clarify the fate of the caspase-15 gene during evolution of the main mammalian lineages and validate the use of low-coverage genome sequences for the phylogenetic analysis of mammalian genes.
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Materials and Methods |
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Sequence Queries and Alignments
Sequences were retrieved from the GenBank database, the trace archive at the National Center for Biotechnology Information (NCBI) (http://www.ncbi.nlm.nih.gov/Traces/) and the ENSEMBL genome browser (http://www.ensembl.org/index.html). The caspase-15 cDNA sequences of pig and dog were used as query sequences in discontiguous MEGA Blast searches in the NCBI trace archive. Amino acid and nucleotide sequence alignments were made with the Blast software package on the Web site of the NCBI (http://www.ncbi.nlm.nih.gov/BLAST/). Discontiguous Mega Blast (expect threshold, 100; other parameters default) was used for queries in the NCBI trace archive of whole-genome shotgun sequences. The coding sequence of the most similar gene paralog of caspase-15, that is, caspase-14 (Eckhart et al. 2005
), was used in parallel control queries, which confirmed that the screening algorithm could faithfully discriminate between these 2 genes. Additional nucleotide sequence alignments were made with the University of California Santa Cruz Genome Browser (http://www.genome.ucsc.edu/) and with the program LALIGN (http://www.ch.embnet.org/software/LALIGN_form.html).
Polymerase Chain Reactions and Sequence Analysis
Genomic DNA was prepared from animal tissues and from human HeLa cells according to a standard protocol. cDNA from kidney, liver, and skin of Monodelphis domestica was kindly provided by Jeannie Chan, Department of Genetics, Southwest Foundation for Biomedical Research, San Antonio, TX. Polymerase chain reactions (PCRs) were performed according to a published protocol with annealing temperatures between 50 and 55 °C (Eckhart et al. 1999). Opossum caspase-15 was amplified with the following primers: o15-s1 5'-CGCCAGGCAGCCAGGCAGT-3', o15-s2 5'-GTGTGAAGACTGGCAGACCAG-3', o15-a1 5'-TGTTTAGCCCCTGGTCTGCCA-3', and o15-a2 5'-ATAAAGTGGGAGGCACCGTGT-3'. The product of a PCR with primers o15-s1 and o15-a2 comprised the complete open reading frame of opossum caspase-15. The following primers were used for the amplification of conserved regions of the caspase-15 (C15) gene: C15-s1 5'-GCTGTTGCCTTGTTACTCTTATG-3', C15-a1 5'-ACCTCCTCTRCAGGCCTGGAT-3', C15-s2 5'-GTCCAGCACTTCAAGAGAAACC-3', and C15-a2 5'-GTGGGATADATGATGWARTAATCACTG-3'. As a positive control for the integrity of the genomic DNAs, the evolutionarily conserved prion protein (PRNP) gene (van Rheede et al. 2003) was amplified with the primers PRNP-s1 5'-GACTATGAGGACCGCTACTA-3' and PRNP-a1 5'-ACCACGCGCTCCATGATCTT-3'. The elephant homologs of caspase-15 exons 6 and 7 were amplified with the primer pairs El-C15-x6-s 5'-CCTGCTTCTGTACTCTCTGTAC-3', El-C15-x6-a 5'-TGCCAGGGACATCTCGTGGTC-3' and El-C15-x7-s 5'-GAGTTTACTGGGAGGCTTCTG-3', El-C15-x7-a 5'-GATGACAATCAGTACAATGCAAG-3', respectively. The elephant caspase-15 retropseudogene was amplified with the primers eps15-s 5'-GTAGATTTTCACAATGGGGCTAG-3' and eps15-a 5'- GAGAGGAGACATGCACGACTG-3'. PCR products were purified and sequenced according to standard protocols.
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Results |
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Cross-Species Comparison of Mammalian Genomes for Presence of the Caspase-15 Gene
Sequence stretches similar to the exons of caspase-15 were identified for platypus (Ornithorhynchus anatinus) (monotreme), gray short-tailed opossum (M. domestica), wallaby (Macropus eugenii) (marsupials), 9-banded armadillo (Dasypus novemcinctus), 2-toed sloth (Choloepus hoffmanni) (Xenarthra), and various representatives of Laurasiatheria such as European hedgehog (Erinaceus europaeus), common shrew (Sorex araneus), little brown bat (Myotis lucifugus), Malayan flying fox (Pteropus vampyrus), and cat (Felis catus). Blast searches with these caspase-15–like sequences confirmed that they were clearly more similar to caspase-15 than to any other gene, which strongly supported correct assignment as orthologs (Koonin 2005
). By contrast, no caspase-15–like sequences were identified by discontiguous Mega Blast among representatives of Euarchontoglires, that is, rabbit (Oryctolagus cuniculus), guinea pig (Cavia porcellus), ground squirrel (Spermophilus tridecemlineatus), mouse (Mus musculus), rat (Rattus norvegicus), tree shrew (Tupaia belangeri), bush baby (Otolemur garnetti), marmoset (Callithrix jacchus), rhesus monkey (Macaca mulatta), chimpanzee (Pan troglodytes), the Sumatran as well as the Bornean subspecies of orangutan (Pongo pygmaeus), and humans (Homo sapiens). As described below, supplementary genome analysis led to the identification of a sequence stretch similar to exon 1 of caspase-15 in the genomes of rhesus monkey, orangutan, chimpanzee, and humans (table 1). Among Afrotheria, the lesser hedgehog tenrec (Echinops telfairi) and the rock hyrax (Procavia capensis) lacked caspase-15–like sequence traces in their 2-fold coverage genome sequences, whereas caspase-15–like sequences were identified in the genome of the African savannah elephant (Loxodonta africana). The latter were investigated further as described below.
Identification of the Caspase-15 Gene in M. domestica
The detection of caspase-15–like sequences in a monotreme and 2 marsupial species suggested that caspase-15 originated in a common ancestor of all modern mammals. Because only a single exon highly similar to caspase-15 could be identified in the platypus genome, it remains presently uncertain whether monotremes contain functional caspase-15. By contrast, the complete caspase-15 gene could be identified by Blast search in the genome of M. domestica (GenBank accession number DQ213043). To test for active transcription of this gene, caspase-15 PCR was performed on cDNA from various opossum tissues. The complete caspase-15 open reading frame was amplified from opossum kidney, and expression was also detected in skin and liver (fig. 1A). The protein encoded by these cDNAs showed 54% and 57% amino acid sequence identity with pig and dog caspase-15, respectively (fig. 1B), and contained all residues critical for caspase catalytic activity as well as a prodomain homologous to the one identified in placental mammals (Eckhart et al. 2005). We concluded that M. domestica contained a functional caspase-15 gene.
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The caspase-15 cDNA sequences of opossum, dog, and cow were aligned to the respective genome sequences in order to determine the exon/intron structure of the caspase-15 genes. Seven exons flanked by bona fide splice sites (Breathnach and Chambon 1981
) were identified in all 3 species (fig. 1B). Exon 1 contained the start site of translation and, like the first exon of the pyrin domain protein genes, MEFV/pyrin and PYCARD/ASC, coded for the entire pyrin domain. Exons 2–7 were homologous in length and sequence to the coding exons of caspase-14 (Eckhart, Ban, et al. 2000). These data suggested that caspase-15 originated by fusion of 2 gene segments that were probably derived from more ancient genes encoding a pyrin domain protein and a caspase, respectively.
Cross-Species PCR Screening for Caspase-15 Genes in Mammals
Because only low-coverage genome sequences were available for most of the mammalian species subject to genome sequencing at the time of our analysis, we further probed for the potential presence of a caspase-15 by PCR with primers that annealed to conserved regions of the caspase-15 gene. With primers amplifying a portion of exon 4 (fig. 2A) and with a primer pair spanning the region from exon 4 to exon 5 (fig. 2B), caspase-15–like PCR products were obtained from opossum and 3 representatives of Laurasiatheria. PCRs were negative for tenrec (Afrotheria) and for representatives of 4 out of 5 orders of Euarchontoglires (fig. 2A and B), which supported the result of our in silico genome analysis, namely, that caspase-15 was absent or incomplete in these species. The validity of the PCR assay was confirmed by sequence analysis of amplification products and by confirmation of the integrity of caspase-15–negative DNAs by a control PCR (fig. 2C). From the genomic DNA of the African elephant, only the exon 4–exon 5 primer pair yielded a PCR product, which contained frameshift mutations and lacked intron 4, suggesting that it corresponded to a processed pseudogene (see below).
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Cross-Species Comparison of the Caspase-15 Gene Locus
Next we investigated the chromosomal environment of the caspase-15 gene and compared it with the homologous region in the genomes of caspase-15–negative species. Both in opossum and dog the caspase-15 gene was flanked, on the 5' side, by a gene encoding an ortholog of the human hypothetical protein FLJ20551 and, on the 3' side, by the ribosomal protein SA/laminin receptor 1 (LAMR1) gene (fig. 3A). By contrast, the orthologs of FLJ20551 and LAMR1 were adjacent to each other with no gene being located between them in the genomes of zebrafish (Danio rerio), African clawed frog (Xenopus tropicalis), and chicken (Gallus gallus) (fig. 3A). As it is very likely that the arrangement of the FLJ20551 and LAMR1 genes in fish, amphibia, and birds is identical to the one in the ancestors of mammals, the caspase-15 gene appears to have been inserted at this site during the evolution of mammals.
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In the genome assembly sequences of mouse, rat, chimpanzee, and humans, the FLJ20551 and LAMR1 genes were in close proximity. The distance between the 3' end of FLJ20551 and the 5' end of LAMR1 in these genomes was less than 3 kb in rodents and less than 10 kb in primates, whereas the caspase-15 genes of opossum and dog span more than 12 kb and 18 kb, respectively. When we scrutinized the human "caspase-15 locus" for sequences homologous to the open reading frame of dog caspase-15, we found a short sequence stretch of significant similarity to the start of the caspase-15–coding region (fig. 3B). However, the presence of 2 frameshift mutations in this region and the absence of exons 2–7 precluded the expression of a functional caspase-15 ortholog from the human caspase-15–like locus (fig. 3B). The region homologous to the start of the caspase-15–coding region was also found in the genomes of rhesus monkey, orangutan, and chimpanzee (table 1). In mouse and rat, a caspase-15 exon 1–like region could not be identified at the site corresponding to the ancient caspase-15 locus nor at any other site of the genome.
The caspase-15 gene locus was also analyzed in the low-coverage genome sequence assemblies of the lesser hedgehog tenrec and the African savannah elephant. No caspase-15–like sequences were found next to the tenrec orthologs of FLJ20551 and LAMR1, which, however, could not be attributed unambiguously to genuine absence of the gene because of a gap in the genome sequence assembly at this site (not shown). By contrast, an elephant sequence scaffold (L. africana ENSEMBL scaffold 26173) was identified, which contained the ortholog of LAMR1 and 3 exons of the caspase-15 gene (fig. 3A). Although the open reading frame of the exon 3–like region was intact, the homologs of exon 6 and 7 contained premature in-frame stop codons (not shown), which demonstrated that the elephant caspase-15 gene had undergone pseudogenization. The existence of frameshift mutations in caspase-15 exons 6 and 7 was confirmed by PCR amplification and sequencing of the corresponding regions from genomic DNA (GenBank accession number DQ285408).
Characterization of a Caspase-15 Retropseudogene in L. africana
In addition to the caspase-15 pseudogene at the ancient caspase-15 gene locus, the genome of the African savannah elephant contained a caspase-15 retropseudogene (DQ285409
[GenBank]
) identical in sequence to the product of one of the caspase-15 PCRs on elephant genomic DNA (fig. 2B). This retropseudogene corresponded to exons 4–7 of caspase-15, lacked introns, and contained frameshift mutations. It shared the lack of introns with caspase-15–like pseudogenes identified in 2 Xenarthrans, the 2-toed sloth, and the 9-banded armadillo (table 1). However, differences in sequence and chromosomal localization (the locus of the armadillo caspase-15–like pseudogene was homologous to the GNAI1 gene on human chromosome 7), indicated that the elephant caspase-15 retropseudogene had originated independently from the Xenarthran caspase-15 pseudogenes.
On the 5' side, at a distance of less than 1 kb, the elephant caspase-15 retropseudogene was flanked by a mutated remnant of a reverse transcriptase gene (greater than 45% sequence identity to Bos taurus reverse transcriptase–like protein, GenBank accession number CAA10770), which may have been involved in the retroposition event (fig. 4A). Alignment of the elephant genome scaffold containing the caspase-15 retropseudogene (L. africana ENSEMBL scaffold 17990) to the human genome, revealed that the retropseudogene locus corresponded to a region on the 5' side of the gene UNC5B on human chromosome 10 (GenBank accession number AL359832), which lacked both caspase-15 and reverse transcriptase–like sequences. Like the human genome, a contig of the tenrec genome sequence assembly (E. telfairi ENSEMBL contig 553134) comprised sequences similar to the flanking regions of elephant caspase-15 retropseudogene but did not contain a caspase-15 pseudogene. As compared with both the human and the elephant locus, the tenrec sequence contained a deletion of 6 kb at this site (fig. 4A). Analysis of the unassembled genome sequence of P. capensis, another afrotherian species, showed absence of caspase-15–like sequences in this genome but could not provide information on the organization of the chromosomal loci homologous to the caspase-15 pseudogenes in the elephant genome. These findings are compatible with 2 scenarios of the fate of the caspase-15 retropseudogene during the evolution of Afrotheria (fig. 4B). In scenario 1, the caspase-15 retroposition occurred in the elephant lineage after divergence from the tenrec lineage, and the caspase-15 gene was inactivated in both lineages. In scenario 2, the retropseudogene originated at the base of the afrotherian branch and was deleted, together with a flanking region, in the tenrec lineage. The original caspase-15 gene may have been inactivated before the evolutionary split of the elephant and the tenrec lineage (fig. 4B, 2 asterisks) or, independently, after divergence of the 2 lineages.
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C15) in the elephant genome. (B) Scenarios for the evolutionary history of r
). A caspase-15 pseudogene (Proposed Evolutionary History of the Caspase-15 Gene in Mammals
Our findings suggest that 1) the caspase-15 gene was inserted into an ancient chromosomal locus, defined by the genes FLJ20551 and LAMR1, 2) this insertion occurred after the divergence of the evolutionary lineage leading to diapsids (birds and others) and the lineage leading to synapsids (mammals), approximately, 310 MYA (Kumar and Hedges 1998
), and 3) the caspase-15 gene was mutated and/or partially deleted in ancestors of most or all members of Euarchontoglires as well as in ancestors of 3 orders of Afrotheria. Because Euarchontoglires is a sister group of caspase-15–positive Laurasiatheria but not of Afrotheria (Madsen et al. 2001; Murphy, Eizirik, Johnson, et al. 2001; Murphy, Eizirik, O'Brien, et al. 2001; Kriegs et al. 2006), it can be excluded that the lack of an intact caspase-15 gene in Afrotheria and Euarchontoglires is a trait derived from their last common ancestor. Rather, inactivation of caspase-15 appears to have occurred independently in these 2 lineages, and possibly, even independently in different branches of Afrotheria (as discussed above) and Euarchontoglires. The results of the phylogenetic analysis of the caspase-15 gene are summarized in figure 5.
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Discussion |
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Our data show that caspase-15 has evolved differently in various mammalian lineages. In several distant branches of the evolutionary tree, the caspase-15 gene and, in particular, the residues critical for enzyme activity have been conserved, which suggests that a functional caspase-15 gene has provided an evolutionary advantage to various species. By contrast, the caspase-15 gene has been inactivated in other clades, which indicates that caspase-15 has a function that is nonessential at least for some mammals or can also be fulfilled by an alternative enzyme. Studies on the physiological role of caspase-15 in the pig, which are underway in our laboratories, will provide the basis for the evaluation of these possibilities.
Another explanation for the inactivation of the caspase-15 gene during evolution is suggested by the "less is more" theory (Olson 1999), which states that gene loss can confer a selective advantage. Two recent studies have demonstrated that inactivation of another caspase gene, caspase-12 (Fischer et al. 2002), has been positively selected for in human evolution (Wang et al. 2006; Xue et al. 2006). Similar to the presumable selection factor of caspase-12 inactivation, that is, responsiveness to bacterial endotoxin (Saleh et al. 2004), the deletion of caspase-15 may have been advantageous by altering the organism's response to pathogens. Along this line of thinking, it is interesting to note that the structural motif of the caspase-15 prodomain, that is, the pyrin domain, is used as a binding motif of cellular and viral proteins that modulate inflammation and apoptosis (Johnston et al. 2005; Werts et al. 2006). Future studies on the potential involvement of caspase-15 in infectious animal diseases may provide clues as to possible mechanisms of positive selection for loss of caspase-15.
Deletions of genes or gene segments are considered rare genomic events in evolution and, accordingly, the presence of a common deletion in two or more systematic groups is regarded as reliable marker of close phylogenetic relationship (Rokas and Holland 2000). At the level of superordinal clades of placental mammals, deletions of nucleotide stretches within various genes have been reported as signatures specific for Afrotheria and Euarchontoglires (Madsen et al. 2001; Poux et al. 2002; de Jong et al. 2003). The present study extends this concept by showing that deletions do not only differentiate superordinal clades such as Laurasiatheria and Euarchontoglires at the DNA level but also may be associated with clade-specific alterations in the enzyme repertoire. However, because the inactivation of caspase-15 occurred independently in at least 2 phylogenetic groups, namely, in Euarchontoglires and Afrotheria and, possibly, even independently in different lineages within Euarchontoglires and Afrotheria (e.g., scenario 1 of the afrotherian caspase-15 evolutionary pattern), our results advise caution in the use of gene deficiency to infer phylogenetic relationships.
Besides delineating the species distribution and the gain and loss of caspase-15 during evolution, the present study establishes the usefulness of low-coverage whole-genome shotgun sequences for the evolutionary analysis of genes. When combined with analyses of the gene locus in complete or nearly complete genome sequences such as that of humans or mouse and, ideally, supplemented by PCR screenings, genome sequences with 2-fold coverage appear to be highly useful in the evaluation of the evolutionary persistence of a gene. The availability of 30 mammalian genome sequences and the knowledge of phylogenetic relationships of the species compensate for the incompleteness of some of these sequences. It is now possible to complement the characterization of mammalian genes by an in silico analysis of the evolutionary fate of the gene in diverse mammalian lineages. Conservation and deletion of genes are likely to correlate with physiological peculiarities specific for evolutionary lineages, and the multiple occurrences of gene inactivation events, as observed for caspase-15, may indicate that the activity of a gene has the potential to be disadvantageous to the organism under certain conditions of selection. We propose that, analogous to the investigation of the gene expression pattern in different tissues, the determination of the species distribution of a gene should become a standard part of gene characterization studies.
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Acknowledgements |
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The authors acknowledge the dedicated efforts of all teams that have provided mammalian DNA sequence data to the public databases at NCBI and ENSEMBL. We are grateful to Jeannie Chan (Department of Genetics, Southwest Foundation for Biomedical Research, San Antonio, TX), Anna-Karin Sundqvist (Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden), Heinz Kuenzle (Institute of Anatomy, Ludwig Maximilians-University, Munich, Germany), and Eberhard Fuchs (German Primate Center, Gottingen, Germany) for providing DNA and tissue samples. We thank Mark Springer (University of California, Riverside, CA) and Heinz Fischer (Medical University of Vienna, Austria) for helpful comments and Heidemarie Rossiter for critically reading the manuscript.
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Footnotes |
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Arndt von Haeseler, Associate Editor
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References |
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