Near Intron Positions Are Reliable Phylogenetic Markers: An Application to Holometabolous Insects

Abstract

Today, the reconstruction of the organismal evolutionary tree is based mainly on molecular sequence data. However, sequence data are sometimes insufficient to reliably resolve in particular deep branches. Thus, it is highly desirable to find novel, more reliable types of phylogenetic markers that can be derived from the wealth of genomic data. Here, we consider the gain of introns close to older preexisting ones. Because correct splicing is impeded by very small exons, nearby pairs of introns very rarely coexist, that is, the gain of the new intron is nearly always associated with the loss of the old intron. Both events may even be directly connected as in cases of intron migration. Therefore, it should be possible to identify one of the introns as ancient (plesiomorphic) and the other as novel (derived or apomorphic). To test the suitability of such near intron pairs (NIPs) as a marker class for phylogenetic analysis, we undertook an analysis of the evolutionary positions of bees and wasps (Hymenoptera) and beetles (Coleoptera) in relation to moths (Lepidoptera) and dipterans (Diptera) using recently completed genome project data. By scanning 758 putatively orthologous gene structures of Apis mellifera (Hymenoptera) and Tribolium castaneum (Coleoptera), we identified 189 pairs of introns, one from each species, which are located less than 50 nt from each other. A comparison with genes from 5 other holometabolan and 9 metazoan outgroup genomes resulted in 22 shared derived intron positions found in beetle as well as in butterflies and/or dipterans. This strongly supports a basal position of hymenopterans in the holometabolous insect tree. In addition, we found 31 and 12 intron positions apomorphic for A. mellifera and T. castaneum, respectively, which seem to represent changes inside these branches. Another 12 intron pairs indicate parallel intron gains or extraordinarily small exons. In conclusion, we show here that the analysis of phylogenetically nested, nearby intron pairs is suitable to identify evolutionarily younger intron positions and to determine their relative age, which should be of equal importance for the understanding of intron evolution and the reconstruction of the eukaryotic tree.

Phylogenetic relationships among insect orders based on three nuclear protein-coding gene sequences

“…Subsequent analyses based on the secondary structure of the 18S rRNA gene (Misof et al, 2007), the gain and loss of introns (Krauss et al, 2008), and the nucleotide sequences of nuclear genes (Wiegmann et al, 2009;Longhorn et al, 2010) support the results of this genome-scale analysis. Our present analyses based on amino acid sequences of three nuclear protein-coding genes from specimens representing all orders of Holometabola strongly suggest that the order Hymenoptera is the sister group to all the other holometabolous orders (Fig.…”

Molecular phylogeny of bark and ambrosia beetles (Curculionidae: Scolytinae) based on 18 molecular markers

“…Even if a deep knowledge of insect genomes in a comparative perspective is currently rather limited (Krauss et al, 2008), a higher number of introns seem to be present in beetles than in other insect groups (Dolezelova et al, 2006, Wild and. In our study, the sequences of the amplified genes showed large variability in the number and length of introns ( Figure 3).…”

Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell

“…To alleviate this issue at least in part, Near Intron Positions (NIPs) have been proposed (Krauss et al, 2008) as a relatively homoplasy-free marker. Since exons separating two introns need to have a minimum length, two very close introns cannot coexist in the same sequence so that one has to be lost before the other is inserted, thus establishing a temporal ordering.…”