Anchored Hybrid Enrichment Provides New Insights Into the Phylogeny and Evolution of Longhorned Beetles (Cera
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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/319173521 Anchored hybrid enrichment provides new insights into the phylogeny and evolution of longhorned beetles (Cera.... Article in Systematic Entomology · August 2017 DOI: 10.1111/syen.12257 CITATIONS READS 2 878 9 authors, including: Seunggwan Shin Emily Moriarty Lemmon The University of Memphis Florida State University 17 PUBLICATIONS 96 CITATIONS 123 PUBLICATIONS 2,299 CITATIONS SEE PROFILE SEE PROFILE Brian D Farrell Adam Slipinski Harvard University The Commonwealth Scientific and Industrial … 172 PUBLICATIONS 5,715 CITATIONS 221 PUBLICATIONS 2,740 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: 4. Beyond Drosophila: Comparative transcriptomics of schizophoran flies to resolve a rapid radiation. NSF funded View project Phylogeny and diversification in the uniquely diverse beetle family Curculionidae (true weevils) View project All content following this page was uploaded by Seunggwan Shin on 04 January 2018. The user has requested enhancement of the downloaded file. Systematic Entomology (2018), 43, 68–89 DOI: 10.1111/syen.12257 Anchored hybrid enrichment provides new insights into the phylogeny and evolution of longhorned beetles (Cerambycidae) , STEPHANIE HADDAD1 *, SEUNGGWAN SHIN1,ALANR. LEMMON2, EMILY MORIARTY LEMMON3, PETR SVACHA4, BRIAN FARRELL5,ADAM SL´ I P I NS´ K I6, DONALD WINDSOR7 andDUANE D. MCKENNA1 1Department of Biological Sciences, University of Memphis, Memphis, TN, U.S.A., 2Department of Scientific Computing, Florida State University, Dirac Science Library, Tallahassee, FL, U.S.A., 3Department of Biological Science, Florida State University, Tallahassee, FL, U.S.A., 4Institute of Entomology, Biology Centre, Czech Academy of Sciences, Ceske Budejovice, Czech Republic, 5Museum of Comparative Zoology, Harvard University, Cambridge, MA, U.S.A., 6CSIRO, Australian National Insect Collection, Canberra, Australia and 7Smithsonian Tropical Research Institute, Ancon, Republic of Panama Abstract. Cerambycidae is a species-rich family of mostly wood-feeding (xylophagous) beetles containing nearly 35 000 known species. The higher-level phylogeny of Cerambycidae has never been robustly reconstructed using molecular phylogenetic data or a comprehensive sample of higher taxa, and its internal relation- ships and evolutionary history remain the subjects of ongoing debate. We reconstructed the higher-level phylogeny of Cerambycidae using phylogenomic data from 522 single copy nuclear genes, generated via anchored hybrid enrichment. Our taxon sample (31 Chrysomeloidea, four outgroup taxa: two Curculionoidea and two Cucujoidea) included exemplars of all families and 23 of 30 subfamilies of Chrysomeloidea (18 of 19 non-chrysomelid Chrysomeloidea), with a focus on the large family Cerambycidae. Our results reveal a monophyletic Cerambycidae s.s. in all but one analysis, and a polyphyletic Cerambycidae s.l. When monophyletic, Cerambycidae s.s. was sister to the family Disteniidae. Relationships among the subfamilies of Cerambycidae s.s. were also recovered with strong statistical support except for Cerambycinae being made paraphyletic by Dorcasomus Audinet-Serville (Dorcasominae) in the nucleotide (but not amino acid) trees. Most other chrysomeloid families represented by more than one terminal taxon – Chrysomelidae, Disteniidae, Vesperidae and Orsodacnidae – were monophyletic, but Megalopodidae was rendered paraphyletic by Cheloderus Gray (Oxypeltidae). Our study corroborates some relationships within Chrysomeloidea that were previously inferred from morphological data, while also reporting several novel relationships. The present work thus provides a robust framework for future, more deeply taxon-sampled, phylogenetic and evolutionary studies of the families and subfamilies of Cerambycidae s.l. and other Chrysomeloidea. Introduction Correspondence: Stephanie Haddad, Department of Biology, Rhodes College, 2000 North Parkway, Memphis, TN, 38112-1690, U.S.A. Longhorned beetles (family Cerambycidae Latreille) comprise E-mail: [email protected] and Seunggwan Shin, Department one of the most species-rich families of animals, with an of Biological Sciences, University of Memphis, 3700 Walker Avenue, estimated 4000 genera and 35 000 described extant species Memphis, TN, 38152, U.S.A. E-mail: [email protected] (Monné et al., 2009; Svacha & Lawrence, 2014). Cerambyci- ∗Present address: Department of Biology, Rhodes College, Memphis, dae s.s. (see Fig. 1 for representatives) is usually divided into TN, U.S.A. eight subfamilies: Lamiinae (>20 000 species), Cerambycinae 68 © 2017 The Royal Entomological Society Cerambycidae phylogeny 69 (∼11 000 species), Lepturinae (∼1500 species), Prioninae cones, bark, stems of herbs or flowers in Lamiinae), pollen (>1000 species), Dorcasominae (>300 species), Parandrinae and nectar (some Lepturinae, Necydalinae, Dorcasominae and (119 species), Spondylidinae (∼100 species) and Necydalinae Cerambycinae), sap (some Prioninae, Cerambycinae and Lep- (∼70 species) (Svacha & Lawrence, 2014). Cerambycidae s.s. turinae), fruit (e.g. various Cerambycinae and Lamiinae), and plus the families Disteniidae (>300 species), Oxypeltidae (three fungal spores or fruiting bodies (known in some Lepturinae and species) and Vesperidae (∼80 species) comprise the informal Lamiinae). grouping Cerambycidae s.l., equivalent to the Cerambycidae or Adult feeding usually has little impact on the environment Longicornia of most earlier authors, the Cerambycoidea of, for by itself, but some Lamiinae may transfer pathogens or para- example, Böving & Craighead (1931) or Svacha & Danilevsky sites such as the nematode Bursaphelenchus xylophilus (Steiner (1987), the cerambycid lineage/Cerambycidae s.l. of Reid and Buhrer) Nickle causing Pine Wilt Disease (e.g. Togashi (1995) or the cerambyciform assemblage of Svacha et al. (1997). & Shigesada, 2006). The extensive larval feeding makes cer- Cerambycidae s.l. occur worldwide but attain maximum ambycids an important component of both natural and man- species richness in the tropics, where Lamiinae, Cerambycinae, aged forest ecosystems. They are major recyclers of dead wood, and Prioninae typically dominate, although Dorcasominae is the and through their feeding activities they create access routes second largest subfamily in Madagascar (Berkov & Tavakilian, into wood for other decomposing agents, such as fungi, and 1999; Svacha & Lawrence, 2014). Cerambycidae s.l. belongs other invertebrates (Slipi´ nski´ & Escalona, 2013). However, lar- to the informal grouping Phytophaga, a clade of mostly phy- val feeding can also seriously damage or even kill the host plant, tophagous beetles consisting of the sister superfamilies Cur- either directly, or when the larval tunnels and adult emergence culionoidea Latreille (weevils s.l. including bark beetles) and holes provide access points for pathogenic fungi (e.g. Schowal- Chrysomeloidea Latreille (leaf beetles, longhorned beetles and ter, 2009). For instance, some Cerambycinae and Lamiinae are relatives). According to Slipi´ nski´ et al. (2011), the clade Phy- especially notorious pests of trees in urban, suburban and forest tophaga contains 125 237 described species (61 854 described ecosystems (Linsley, 1959). Some Cerambycinae are capable of species in Curculionoidea and 63 383 described species in infesting dry seasoned wood and may seriously damage struc- Chrysomeloidea). tural timber. Compared to the subfamilies Lepturinae, Prioni- The earliest fossil Cerambycidae s.l. (Wang et al., 2013; pos- nae and Parandrinae, whose larvae mostly develop in decaying sibly Yu et al., 2015) are from the Early Cretaceous. The earliest wood, species of Cerambycinae and Lamiinae also have higher known unambiguous fossil angiosperms (e.g. Friis et al., 2006) capacities for introduction in living or freshly dead plants or con- are also from that epoch. The diversity of Chrysomeloidea and struction wood and wood products (Cocquempot & Lindelöw, other phytophagous insects has been attributed by some to their 2010; Raje et al., 2016). For instance, the Asian longhorned bee- co-diversification with angiosperms (e.g. Farrell, 1998; Mitter & tle, Anoplophora glabripennis Motschulsky, has recently shown Farrell, 1991; McKenna & Farrell, 2006; McKenna et al., 2009; the potential to spread after introduction and cause significant McKenna, 2011). This seems only partially true for ceramby- ecological and economic damage (Nowak et al., 2001; Meng cids. Although they quite possibly pre-date angiosperms, whose et al., 2015; McKenna et al., 2016). Also, some terricolous root increasing diversity later contributed to cerambycid diversity, feeders (such as Philus Saunders or Migdolus Westwood of Ves- cerambycids (even at low taxonomic levels) are often highly peridae) may cause considerable damage to forest or agricultural polyphagous in the larval stage and some species may even feed plantations (Svacha et al., 1997; Machado & Habib, 2006). on both gymnospermous and angiospermous plants. There were As in other similarly extensive and diverse groups, it is often undoubtedly multiple host switches between gymnosperms and extremely difficult to even distinguish cerambycid higher taxa angiosperms in cerambycid evolution. on a worldwide scale based on classical adult characters. Lar- Larvae of Cerambycidae s.l. are mostly internal borers in val morphology appears more promising in this