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Ancient Rapid Radiations of Insects: Challenges for Phylogenetic Analysis

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Ancient Rapid Radiations of Insects: Challenges for Phylogenetic Analysis ANRV330-EN53-23 ARI 2 November 2007 18:40 Ancient Rapid Radiations of Insects: Challenges for Phylogenetic Analysis James B. Whitfield1 and Karl M. Kjer2 1Department of Entomology, University of Illinois, Urbana, Illinois 61821; email: jwhitfi[email protected] 2Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, New Jersey 08901; email: [email protected] Annu. Rev. Entomol. 2008. 53:449–72 Key Words First published online as a Review in Advance on diversification, molecular evolution, Palaeoptera, Orthopteroidea, September 17, 2007 fossils The Annual Review of Entomology is online at ento.annualreviews.org Abstract by UNIVERSITY OF ILLINOIS on 12/18/07. For personal use only. This article’s doi: Phylogenies of major groups of insects based on both morphological 10.1146/annurev.ento.53.103106.093304 and molecular data have sometimes been contentious, often lacking Copyright c 2008 by Annual Reviews. the data to distinguish between alternative views of relationships. Annu. Rev. Entomol. 2008.53:449-472. Downloaded from arjournals.annualreviews.org All rights reserved This paucity of data is often due to real biological and historical 0066-4170/08/0107-0449$20.00 causes, such as shortness of time spans between divergences for evo- lution to occur and long time spans after divergences for subsequent evolutionary changes to obscure the earlier ones. Another reason for difficulty in resolving some of the relationships using molecu- lar data is the limited spectrum of genes so far developed for phy- logeny estimation. For this latter issue, there is cause for current optimism owing to rapid increases in our knowledge of comparative genomics. At least some historical patterns of divergence may, how- ever, continue to defy our attempts to completely reconstruct them with confidence, at least using current strategies. 449 ANRV330-EN53-23 ARI 2 November 2007 18:40 WHAT IS AN ANCIENT RAPID ABTime RADIATION? In this review, we focus on cases of diversifica- tion in which lineages of insects have diverged in rapid succession within a relatively short time span in the ancient past, generating pat- terns of molecular and morphological change that are difficult to discern phylogenetically. We refer to these patterns as ancient rapid ra- diations, with no implication that evolution- ary change has accelerated in these cases; in- stead, it is lineage splitting or diversification that has happened rapidly. While insects di- verged spectacularly in the Permian, and again in the Jurassic, and have been diverging ever since, “ancient” in this context refers not nec- essarily to a specific age, but to a high ratio between the amount of time that has elapsed since divergences occurred and the time span in which they occurred. These high ratios are of course more characteristic of divergences that are many millions of years old. THE PHYLOGENETIC SIGNATURE OF A RAPID Figure 1 RADIATION Diagrammatic representation of an ancient rapid Rokas et al. (103) have referred to the typical radiation, with the crucial short internal branches molecular phylogenetic pattern that charac- highlighted with a gray bar. terizes an ancient rapid radiation as its signa- ture. The signature can be described as the factors such as inadequate data, conflict within significantly closer temporal spacing (com- or among datasets, or loss of phylogenetic by UNIVERSITY OF ILLINOIS on 12/18/07. For personal use only. pression) of a number of cladogenetic or signal over time. Unfortunately, many in- lineage-splitting events in a phylogeny than sect datasets are plagued by short, ancient would be expected by either stochastic or rel- internodes, lineage-specific substitution rate Annu. Rev. Entomol. 2008.53:449-472. Downloaded from arjournals.annualreviews.org atively constant diversification. Figure 1 de- biases (substitutions accumulate at different picts a pattern of this sort. The only evidence rates among lineages), and lineage-specific of some relationships among the taxa we will base compositional biases (the nucleotides ever see must have accumulated on these short are sometimes found in different proportions horizontal branches (internodes) that link the among lineages, and among regions of the taxa together. All subsequent changes along genes). These problems frequently combine the branches may have an impact on how sim- with the inclusion of data whose substitution ilar taxa appear, but will not bear directly on rates are wildly inappropriate for the ques- their relationship. tions they are intended to address, to make Although such a phylogenetic pattern is insect phylogenetics a particularly challeng- to be expected from an ancient rapid radia- ing enterprise. We briefly review some meth- tion, its signature can be obscured by other ods for diagnosing confounding factors with 450 Whitfield · Kjer ANRV330-EN53-23 ARI 2 November 2007 18:40 ancient radiations—as more extensive recent ized, there may still be useful phylogenetic reviews are available (101, 129). signals in second codon sites or amino acids. Selection of genes is not always made ac- Split: a partition of cording to predictions of phylogenetic utility, COMPLICATIONS WITH the taxa in a but it is frequently based on ease of PCR, eco- phylogenetic tree ANALYZING ANCIENT RAPID nomics, and tradition. There are several dom- into two groups, RADIATIONS inant data sources in the insect systematics supported by a Phylogenetic studies of insects, especially toolbox. For inferring the deepest splits in the character or data pattern studies that address relationships among insect tree, nuclear rRNA, histone H3, elon- higher taxa, often exhibit a portion of the phy- gation factor-1α (EF-1α), and mitochondrial Long-branch attraction: the logeny with low support or resolution. When genes have been the most common sources of tendency of a large amount of data has been analyzed, a phylogenetic data. Each of these sources is dif- phylogenetic possible cause for the poor support is a rapid ferent in substitution rates, nucleotide com- methods to group radiation, because it would result in truly short position, and other analytical considerations, long but (in reality) interdivergence times for characters to accu- and can also be evaluated according to pre- nonadjacent branches mulate within. Unfortunately, such a signa- dicted phylogenetic utility when ancient in- ture of a rapid radiation can also result from, ternodes are short. For example, the most ob- or alternatively be obscured by, a variety of vious difference among genes apparent in our other causes related to data quality. It is thus neopteran example presented below is the ex- important to test whether the available data treme variation in tree lengths, resulting from are appropriate for resolving relationships at the differences in substitution rates among the hierarchical level being analyzed, and to genes. determine whether confounding biases in the One approach to solving a difficult phy- data are interfering with signal extraction. logenetic problem is to collect a lot of data. However, the effectiveness of this approach is linked directly to the branch lengths of the in- Are the Genes Appropriate? ternodes (which represent the time span upon The rates at which sites in a gene change which all evidence for relationship must accu- should be coordinated to the phylogenetic mulate) relative to the branch lengths of ter- question at hand. Just as one would not minal taxa. Fast-evolving sites are more likely measure continental drift with a stopwatch, to change on an ancient short internode, but some genes evolve too quickly to be useful for these changes are also more likely to be sub- some deep phylogenetic questions. In general sequently overwritten, especially if there is a by UNIVERSITY OF ILLINOIS on 12/18/07. For personal use only. different genes are appropriate for estimating lag in time between the first appearance of different divergence times. The time span a lineage and the origin of extant subgroups appropriate to some genes may be broad, from which we can sample today. Figures 2 Annu. Rev. Entomol. 2008.53:449-472. Downloaded from arjournals.annualreviews.org as is the case for nuclear ribosomal RNAs, and 3 illustrate this pattern. Slowly evolving which possess such a wide array of regionally sites are unlikely to change on short intern- variable substitution rates that portions of odes, but when they do, they are less likely to the data can be used to estimate relationships be overwritten. Extremes of slowly and fast- from within recently diverged genera (1, 138) evolving sites, at least with parsimony, would to relationships among arthropod classes and be expected to perform in opposite ways. Al- beyond (81, 119). Protein-coding genes may though it is widely understood that the phe- have regional rate variations that broaden nomenon of long-branch attraction (30) can their window of utility as well. Substitutions lead to phylogenetic error, what is often over- accumulate in different codon positions at dif- looked is the prediction that, when terminal ferent rates, and even if the synonymous nu- branches (undivided branches that start at the cleotide substitutions are essentially random- most recent node and lead to an extant species) www.annualreviews.org • Ancient Rapid Radiations of Insects 451 ANRV330-EN53-23 ARI 2 November 2007 18:40 Onychiurus yodai Podura aquatica Collembola Hypogastrura dolsana Diplura Campodea tillyardi P brevistylis Archaeognatha Hexapoda Lepisma sp. Tricholepidion gertschii Zygentoma Aeshna cyanea
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