*Department of Biochemistry, University of Nijmegen, Nijmegen, The Netherlands;
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam
Recent nuclear sequence analyses have provided evidence that primates and rodents are more closely related than previously believed (Madsen et al. 2001
; Murphy et al. 2001a,
2001b
). This proposal is difficult to reconcile with morphological insights (Liu et al. 2001
; Novacek 2001
) and is not generally supported by current mitochondrial sequence data (Reyes, Pesole, and Saccone 2000
; Nikaido et al. 2001
; Arnason et al. 2002
; Janke et al. 2002
). Moreover, the supporting data and analyses have been criticized on methodological grounds (Rosenberg and Kumar 2001
). Here we report deletions in two nuclear protein-coding genes that lend independent support to this contested grouping.
Some 18 orders of placental mammals are currently recognized, but their phylogenetic relationships remain highly controversial. Extensive sequence comparisons of mainly nuclear genes support a basal division into four major clades (Xenarthra, Afrotheria, Laurasiatheria, and Euarchontoglires), which has far-reaching implications for early mammalian biogeography and morphological diversification (Murphy et al. 2001b
). Euarchontoglires is composed of the orders Primates, Rodentia, Lagomorpha (rabbits, hares, and pikas), Scandentia (tree shrews), and Dermoptera (flying lemurs). In contrast, morphology groups Primates, Scandentia, and Dermoptera with Chiroptera (bats) in the clade Archonta, whereas Rodentia and Lagomorpha (jointly called Glires) are in a distant clade with Macroscelidea (elephant shrews) (Liu et al. 2001
; Novacek 2001
). Also, sequence data from 12 proteins encoded by the mitochondrial genome generally do not support Euarchontoglires (e.g., Nikaido et al. 2001
) or even maintain rodent polyphyly in many cases (Reyes, Pesole, and Saccone 2000
; Arnason et al. 2002
; Janke et al. 2002
). Only by excluding some taxa with high or atypical substitution rates (or both) can sound mitochondrial support be obtained (Waddell, Kishino, and Ota 2001
). Establishing the monophyly of the most speciose eutherian order, Rodentia, and finding its sister group has indeed been most difficult to solve on the basis of sequence evidence (e.g., Graur, Hide, and Li 1991
; Adkins et al. 2001
; Huchon et al. 2002
). As for the molecular data sets giving support to Euarchontoglires, it has been questioned whether these are actually able to resolve the relationship of rodents and primates or whether more genes and longer sequences are needed (Rosenberg and Kumar 2001
). Given, too, that Euarchontoglires is the least supported of the four major clades in some analyses (Madsen et al. 2001
), additional evidence for their monophyly is certainly needed. This could be provided by "rare genomic changes," such as insertions and deletions (indels) in proteins (Rokas and Holland 2000
). Indels in protein-coding DNA sequences require more complex mutational mechanisms and are generally more constrained than single base substitutions. Such indels can therefore be good indicators for monophyly, as demonstrated already for two of the other major clades, Xenarthra (van Dijk et al. 1999
) and Afrotheria (Madsen et al. 2001
), as well as in deeper vertebrate phylogeny (Venkatesh, Erdmann, and Brenner 2001
).
While studying genes involved in various neurodegenerative disorders, we noticed two deletions that might be informative for the naturalness of Euarchontoglires. One is a large deletion in exon 8 of the gene for spinocerebellar ataxia 1 (SCA1), resulting in an 18-residue deletion in the encoded protein (fig. 1 , top). The other is a 6-bp deletion at the 5' end of the intronless coding region of the prion protein gene (PRNP; fig. 1 , bottom). Both deletions perfectly distinguish Euarchontoglires from all other placentals and outgroup marsupials. Obviously, the most parsimonious interpretation is that these deletions originated once and independently in the SCA1 and PRNP genes of the last common ancestor of Euarchontoglires, thus supporting their monophyly. If the morphological or mitogenomic trees are true, both deletions must have originated at least twice in exactly the same lineages.
|
Acknowledgements
This work was supported by grants from the Netherlands Organisation for Scientific Research and the European Commission.
Footnotes
Rodney Honeycutt, Reviewing Editor
Keywords: insertions
deletions
phylogeny
Glires
primates
Euarchontoglires
Address for correspondence and reprints: Wilfried W. de Jong, Department of Biochemistry 161, University of Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands. w.dejong{at}ncmls.kun.nl
.
References
Adkins R. M., E. L. Gelke, D. Rowe, R. L. Honeycutt, 2001 Molecular phylogeny and divergence times for major rodent groups: evidence from multiple genes Mol. Biol. Evol 18:777-791
Arnason U., J. A. Adegoke, K. Bodin, E. W. Born, Y. B. Esa, A. Gullberg, M. Nilsson, R. V. Short, X. Xu, A. Janke, 2002 Mammalian mitogenomic relationships and the root of the Eutherian tree Proc. Natl. Acad. Sci. USA 99:81518156 .
Graur D., W. A. Hide, W.-H. Li, 1991 Is the guinea-pig a rodent? Nature 351:649-652[ISI][Medline]
Huchon D., O. Madsen, M. J. J. Sibbald, K. Ament, M. J. Stanhope, F. Catzeflis, W. W. de Jong, E. J. P. Douzery, 2002 Rodent phylogeny and a timescale for the evolution of Glires: evidence from an extensive taxon sampling using three nuclear genes Mol. Biol. Evol (in press)
Janke A., O. Magnell, G. Wieczorek, M. Westerman, U. Arnason, 2002 Phylogenetic analysis of 18S rRNA and the mitochondrial genomes of the wombat, Vombatus ursinus, and the spiny anteater, Tachyglossus aculeatus: increased support for the Marsupionta hypothesis J. Mol. Evol 54:71-80[ISI][Medline]
Liu F. G., M. M. Miyamoto, N. P. Freire, P. Q. Ong, M. R. Tennant, T. S. Young, K. F. Gugel, 2001 Molecular and morphological supertrees for eutherian (placental) mammals Science 291:1786-1789
Madsen O., M. Scally, C. J. Douady, D. J. Kao, R. W. DeBry, R. Adkins, H. M. Amrine, M. J. Stanhope, W. W. de Jong, M. S. Springer, 2001 Parallel adaptive radiations in two major clades of placental mammals Nature 409:610-614[ISI][Medline]
Murphy W. J., E. Eizirik, W. E. Johnson, Y. P. Zhang, O. A. Ryder, S. J. O'Brien, 2001a. Molecular phylogenetics and the origins of placental mammals Nature 409:614-618[ISI][Medline]
, , S. J. O'Brien, et al 2001b. Resolution of the early placental mammal radiation using Bayesian phylogenetics Science 294:2348-2351
Nikaido M., K. Kawai, Y. Cao, M. Harada, S. Tomita, N. Okada, M. Hasegawa, 2001 Maximum likelihood analysis of the complete mitochondrial genomes of eutherians and a reevaluation of the phylogeny of bats and insectivores J. Mol. Evol 53:508-516[ISI][Medline]
Novacek M. J., 2001 Mammalian phylogeny: genes and supertrees Curr. Biol 11:R573-R575[ISI][Medline]
Reyes A., G. Pesole, C. Saccone, 2000 Long-branch attraction phenomenon and the impact of among-site rate variation on rodent phylogeny Gene 259:177-187[ISI][Medline]
Rokas A., P. W. Holland, 2000 Rare genomic changes as a tool for phylogenetics Trends Ecol. Evol 15:454-459[ISI][Medline]
Rosenberg M. S., S. Kumar, 2001 Incomplete taxon sampling is not a problem for phylogenetic inference Proc. Natl. Acad. Sci. USA 98:10751-10756
van Dijk M. A. M., E. Paradis, F. Catzeflis, W. W. de Jong, 1999 The virtues of gaps: xenarthran (edentate) monophyly supported by a unique deletion in alpha-A-crystallin Syst. Biol 48:94-106[ISI][Medline]
Venkatesh B., M. V. Erdmann, S. Brenner, 2001 Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates Proc. Natl. Acad. Sci. USA 98:11382-11387
Waddell P. J., H. Kishino, R. Ota, 2001 A phylogenetic foundation for comparative mammalian genomics Genome Informatics 12:141-154
Wopfner F., G. Weidenhofer, R. Schneider, A. von Brunn, S. Gilch, T. F. Schwarz, T. Werner, H. M. Schatzl, 1999 Analysis of 27 mammalian and 9 avian PrPs reveals high conservation of flexible regions of the prion protein J. Mol. Biol 289:1163-1178[ISI][Medline]