Resolution of a deep animal divergence by the pattern of intron conservation

Abstract

The relationship between three biologically important groups, arthropods, nematodes, and deuterostomes, remains unresolved. It is unknown whether arthropods are more closely related to nematodes (consistent with the ''ecdysozoa'' hypothesis) or to deuterostomes (consistent with ''coelomata''). We present a method in which we use the pattern of spliceosomal intron conservation to develop a series of inequalities that characterize each possible relationship. We find that only the ecdysozoa grouping satisfies these predictions, with P < 10 ؊6 . Simulations show that our method, unlike some previous methods, is largely insensitive to rate variation between branches.coelomata ͉ ecdyosozoa ͉ intron evolution ͉ phylogenetics T he traditional ''coelomata'' phylogeny joining deuterostomes with arthropods to the exclusion of nematodes has been questioned by analyses of molecular data sets (1-6). The alternative ''ecdysozoa'' hypothesis joins arthropods and nematodes with deuterostomes as the outgroup. Morphological (7-10) and molecular (1)(2)(3)(4)(5)(6)(11)(12)(13)(14) analyses have lent support to both sides. Molecular many-taxa studies have tended to support ecdysozoa (2-6), whereas many-gene analyses have tended toward coelomata (11-13). The result has been a web of studies and reviews of opposite conclusions. At the heart of the uncertainty lies a dearth of characters slowevolving enough to guide in reconstruction of such deep divergences and the potential failure of many phylogenetic methods in cases of rate variations between lineages (e.g., see discussion in refs. 15-17).A promising class of elements for resolving such deep divergences is spliceosomal intron positions (18,19). Introns have a very slow rate of insertion and loss with intron turnover estimates ranging from around 10 Ϫ9 per year for flies (20,21) and worms (21, 22) to 10 Ϫ11 per year for mammals (23) and with a large fraction of introns persisting for very long periods (18,24,25), presumably allowing them to retain phylogenetic signal long after nucleic acid and many protein sequences have saturated. In addition, intron loss is presumably virtually irreversible (once lost, an intron is quite unlikely to be subsequently gained at the exact site), thus evading the problems of back mutation endemic to sequence-based methods.Previous studies have used one or a few shared nuclear or mitochondrial introns to try to determine various groupings (18,(26)(27)(28)(29). However, such anecdotal evidence ignores the possibility of (multiple) intron loss and must therefore be treated with caution except in groups with extremely low rates of intron loss [e.g., vertebrates (18)]. Other studies finding that the same intron has been lost multiple times independently along different lineages have led some to conclude that introns are not useful as phylogenetic characters. Cho et al. (30) found that the same intron had been lost multiple times in separate Caenorhabditis lineages and thus concluded that introns are not good phylogenetic criteria. Rogozin et al. (24) fo...

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“…phosphatase in Fig. 4) suggest that ancient protein domains were composed of many exons (or contained many introns), which has also been proposed in other studies [22,36,38]. The current study suggest a minimum exon length around 4 nucleotides, similar to modern minimum reported exon lengths (see [39] for exon sizes).…”

In silico characterization and comparative genomic analysis of the Culex quinquefasciatus glutathione S-transferase (GST) supergene family

“…Intron positions have been used successfully to delineate the deep phylogenetic relationships (Rogozin et al 2005). Roy and Gilbert used pattern of intron conservation to resolve the deep phylogenetic relationship between the arthropods, nematodes, and deuterostomes (Roy and Gilbert 2005), suggesting that intron positions could be considered as informative phylogenetic marker. Following which, others have used introns as an informative marker to resolve phylogenetic relationships (Krauss et al 2008;Rokas and Holland 2000;Zheng et al 2007).…”

Likely Scenarios of Intron Evolution

“…We note in passing that there is some ongoing debate [20][21][22][23] as to whether the phylogenetic tree of Fig. 2 is correct, namely, whether Ecdysozoa are monophyletic.…”

“…Philippe et al [22] argue that they are, and that support for other hypotheses are due to long branch attraction phenomena. Roy and Gilbert [21] also argue for an ecdysozoan clade, based on the intron data set of [4]. We consider only one phylogenetic tree, and leave further analysis to a more complete version of this abstract.…”