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Fossil-Calibrated Molecular Phyiogenies Reveal That Leaf-Mining Moths Radiated Millions of Years After Their Host Plants

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Fossil-Calibrated Molecular Phyiogenies Reveal That Leaf-Mining Moths Radiated Millions of Years After Their Host Plants doi: 10.1111/j.1420-9101.2005.01070.x Fossil-calibrated molecular phyiogenies reveal that leaf-mining moths radiated millions of years after their host plants C. LOPEZ-VAAMONDE, N. WIKSTRÖr ,t C. LABANDEIRA4§ H. C. J. GODFRAY.t S. J. GOODMAN** & J. \/l. COOKU *INRA-Orkans. Laboratoire de Zoologie Forestière, Ardon, Olivet Cedex, France ^Department of Systematic Botany, Evolutionary Biology Centre, Uppsala University, Norbyvdgen, Sweden XDepartment of Paleobiology, Smithsonian Institution. National Museum of Natural History, Washington. DC, USA %Department of Entomology, University of Maryland, College Park, MD, USA ^Division of Biology and NERC Centre for Population Biology, Imperial College London. Silwood Park Campus, Ascot, Berkshire, UK **Institute of Integrative and Comparative Biology, University of Leeds, Leeds, UK Keywords: Abstract coevolution; Coevolution has been hypothesized as the main driving force for the cospeciation; remarkable diversity of insect-plant associations. Dating of insect and plant divergence times; phyiogenies allows us to test coevolutionary hypotheses and distinguish evolutionary rates; between the contemporaneous radiation of interacting lineages vs. insect 'host fossil record; tracking' of previously diversified plants. Here, we used nuclear DNA to host shift; reconstruct a molecular phytogeny for 100 species of Phyllonorycter leaf-mining leaf-mining moth; moths and 36 outgroup taxa. Ages for nodes in the moth phylogeny were penalized likelihood; estimated using a combination of a penalized likelihood method and a plant-insect interactions; Bayesian approach, which takes into account phylogenetic uncertainty. To sequential evolution. convert the relative ages of the moths into dates, we used an absolute calibration point from the fossil record. The age estimates of (a selection of) moth clades were then compared with fossil-based age estimates of their host plants. Our results show that the principal radiation of Phyllonorycter leaf- mining moths occurred well after the main radiation of their host plants and may represent the dominant associational mode in the fossil record. detect and understand macroevolutionary patterns in Introduction insect-plant associations (Farrell, 1998b, 2001; Sequeira The associations between vascular plants and insects or & Farrell, 2001; Percy et al, 2004; Kergoat et al, 2005). their early arthropodan relatives have a fossil record This research has received added impetus in recent years dating back to the first known terrestrial ecosystems of due to the increasing avaflability of molecular phyioge- the early Devonian, 415-400 Ma (Kevan et al, 1975; nies of speciose groups of plants and their herbivores. Labandeira, 2002). More recently, during the Cretaceous, There are now many estabfished examples of clades of from 145 to 65.5 Ma, flowering plants and their insect herbivores that have radiated on phylogenetically related herbivores have dominated terrestrial biomes and cur- groups of plants (e.g. FarreU, 1998a; Ronquist & Liljeblad, rently constitute a major fraction of the earth's biodiver- 2001; Weiblen & Bush, 2002). Less clear is the temporal sity, perhaps accounting for as much as 50% of all relationship between the plant and insect diversiflca- described species (excluding micro-organisms; Strong tions. At least three patterns are possible, but these et ai, 1984). Since the pioneering work of Ehrlich & should be seen as parts of a continuum rather than Raven (1964) on the coevolution of butterflies and their discrete categories. First, the insects might speciate host plants, there has been great interest in trying to contemporaneously with their host plants (cospeciation) so that their phyiogenies are congruent. Secondly, insect diversification may follow rapidly (in geochronological Correspondence: Dr Carlos Lopez-Vaamonde, INRA-Orleans, Laboratoire de Zoologie Forestière, BP 20619 Ardon, F- 45166 Olivet Cedex, France. terms) after plant diversification ('fast colonization hypo- Tel.: +33 2384 17861; lax: -^33 2384 17879; thesis'), but with the pattern of plant colonization e-mail: [email protected] influenced by some factors in addition to host-plant ©2006 THE AUTHORS 19 (2006) 1314-1326 1314 JOURNAL COMPILATION 2006 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY Asynchronous diversification of leaf miners and plants 1315 phylogeny, resulting in an insect radiation that is slightly mid-level taxonomic ranks to extant taxa (Labandeira younger and incongruent with that of the plants. Thirdly, et al, 1994). This facOitates the temporal calibration of colonization of plants may require an evolutionary the insect phylogeny, which is more difficult in other innovation and occur only when this arises, some time insect groups. after plant diversification ('delayed colonization hypo- In a previous study, we found no evidence for thesis'). Again, an imperfect match between the phylo- cospeciation between Phyllonorycter and their host plants genies is predicted, but now we also predict a time lag (Lopez-Vaamonde et al, 2003). However, Phyllonorycter before colonization. species from the same host-plant genus frequently form a Testing the above alternative scenarios ideally requires monophyletic clade. Closely related moth species often phytogenies of both taxa, along with fossil data for both feed on closely related plants, which we interpret as due groups, to provide absolute time calibrations. Recently, to host switching (colonization followed by speciation) Farrell (1998a) studied the evolution of host-plant use being more likely to happen amongst phylogenetically among herbivorous Phytophaga beetles (weevils, long- related plants. horned and leaf beetles), using phylogenetic and fossil The aim of this paper was to test whether the main data. He showed two bursts of beetle speciation: one diversification of Phyllonorycter moths occurred near- during the mid-Cretaceous (90 Ma) and the other in the contemporaneously (on a geochronological time scale) later-Cainozoic (10 Ma). This bimodal distribution may with that of their host plants, or after a significant time be attributable to three events: (1) a major spurt of lag. To do this we generated a molecular phylogeny of herbivore diversification coinciding with the mid-Creta- 100 species of Phyllonorycter leaf-mining moths using 28S ceous ecological expansion of angiosperms, (2) extinction rDNA sequence data. We then used a penalized likeli- of many specialized associations at the K/T boundary and hood method with a Bayesian approach to estimate (3) a gradual rebound to late-Cretaceous species diversity divergence times, a method that takes into account levels during the earUer Cainozoic (Wilf et al, 2001; phylogenetic uncertainty. We converted the relative ages Labandeira et al, 2002). of the moths into absolute dates using a calibration point More recently, Percy et al. (2004) compared fossil- from the fossil record. The absolute ages of the moths dated molecular phylogenies of both jumping plant-fice were then compared with fossil-based estimates of the (Psylloidea) and their legume host plants. They found dates of diversification of their host plants. that there was significant topological congruence of the phylogenies, but that the psyllids radiated after their Material and methods legume hosts, except in the geologicafiy recent Canary Islands where psylUds and genistoid legumes radiated Insect sampling contemporaneously. So far, attempts to time the diversifications of insect Moths were reared and collected as described by Lopez- and plant groups have focused mainly on external Vaamonde et al (2003). We used several other genera of feeders. Here, we explore this issue in a speciose genus gracillariids (from the subfamilies Gracillariinae and Phyl- of leaf-mining moths, Phyllonorycter (Lepidoptera: Gracil- locnistinae as well as the Lithocolletinae to which Phyl- lariidae). Radiations of internal feeders, such as leaf lonorycter belongs), one species of Bucculatricidae (in the miners, may differ from those of external feeders. For same suborder) and one species of Micropterigidae (a basal example, the larvae of leaf-mining moths have very group of lepidopterans) as outgroups (see Appendix SI). intimate associations with their host plants and this may mean that there are more host-imposed constraints on Data generation and laboratory procedures their ecology and evolution compared with externally feeding herbivores. Several authors have suggested that We estimated phylogenies using sequence data from an internal feeders show both greater host-plant specificity approximately 1000 bp fragment of the 28S nuclear and greater phylogenetic conservatism in colonizing new ribosomal subunit gene. We added 21 new outgroup species of plants (e.g. Powefi, 1980; Mitter & Farrefi, species and 22 new Phyllonorycter species to the published 1991; Lopez-Vaamonde et al, 2003). 28S rDNA phylogeny of 77 Phyllonorycter species in There are also some particular advantages to studying Lopez-Vaamonde et al. (2003). All new sequences have these issues with leaf-mining microlepidoptera. First, the been deposited in GenBank (accession numbers: earliest fossil evidence for leaf-mining moth clades AY521484-AY521528; see Appendix SI). We used the extends to at least 99 Myr, almost to the start of the polymerase chain reaction and sequencing procedures major explosion of angiosperm diversity during the described by Lopez-Vaamonde et al (2001). 28S Cretaceous (130-90 Myr; Powell, 1980; Powefi et al, sequences showed
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