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Species Delineation Within the Euwallacea Fornicatus (Coleoptera: Curculionidae) Complex Revealed By Copyedited by: OUP Insect Systematics and Diversity, (2018) 2(6): 2; 1–11 doi: 10.1093/isd/ixy018 Taxonomy Research Article Species Delineation Within the Euwallacea fornicatus (Coleoptera: Curculionidae) Complex Revealed by Morphometric and Phylogenetic Analyses Downloaded from https://academic.oup.com/isd/article-abstract/2/6/2/5201072 by University of Florida user on 10 January 2019 Demian F. Gomez,1 James Skelton,1 M. Sedonia Steininger,2 Richard Stouthamer,3 Paul Rugman-Jones,3 Wisut Sittichaya,4 Robert J. Rabaglia,5 and Jiri Hulcr1,6,7 1School of Forest Resources and Conservation, University of Florida, 136 Newins-Ziegler Hall, Gainesville, FL 32611, 2Agricultural Research Service, USDA, 1600-1700 SW 23RD DRIVE, Gainesville, FL 32608, 3Department of Entomology, University of California, 3401 Watkins Drive, Riverside, CA 92521, 4Department of Entomology, Prince of Songkla University, 15 Karnjanavanich Road, Hat Yai, Songkhla 90110, Thailand, 5Forest Health Protection, USDA-Forest Service, 201 14 Street, SW, Washington, DC 20250, 6Entomology and Nematology Department, University of Florida,1881 Natural Area Drive, Gainesville, FL 32611, and 7Corresponding author, e-mail: [email protected] Subject Editor: Bjarte Jordal Received 24 May 2018; Editorial decision 22 October 2018 Abstract The ambrosia beetle Euwallacea fornicatus Eichhoff sensu lato is a complex of genetically divergent emerging pests responsible for damages to tree industries and ecosystems around the world. All lineages within the species complex are currently considered morphologically identical, presenting problems for their delineation and highlighting the shortcomings of species concepts based solely on type-specimen morphology.The objectives of this work were to 1) broaden the geographic sampling of the E. fornicatus complex in Asia, 2) reconstruct relationships between clades and populations, 3) find morphological characters or combinations of characters which are useful in delimiting the genetic lineages of the E. fornicatus species complex, and 4) propose taxonomic delimitation of species where morphology and phylogenetic identity correlate. Our integrated approach using molecular and morphological evidence suggests four clades that differ morphologically, but with overlap, therefore, cytochrome oxidase c subunit I (COI) barcoding remains necessary for assigning specimens to a clade. The following taxonomic changes are proposed: E. fornicatus (Eichhoff 1868) (= ‘Tea Shot Hole Borer Clade a’); E. fornicatior (Eggers 1923), stat. rev. (= ‘Tea Shot Hole Borer Clade b’); E. whitfordiodendrus (Schedl 1942), stat. rev. (= ‘Polyphagous Shot Hole Borer’); and E. kuroshio Gomez and Hulcr, sp. nov. (= ‘Kuroshio Shot Hole Borer’). This approach delivers a practical, evidence-based guidance for species delineation that can address overlapping variation in morphological characters of an emerging pest species complex. Key words: Ambrosia beetle, cryptic species, invasive species, morphology Species identity is foundational to all of biology. It becomes particu- Some of the most morphologically cryptic, economically damag- larly important in organisms whose biology defies the assumptions ing, and frequently intercepted pests are ambrosia beetles in the tribe of the standard species concepts, such as where barriers between Xyleborini (Coleoptera: Curculionidae: Scolytinae) (Haack 2001). biological species are porous, or in clonal organisms where vari- Of the 60 nonnative scolytines established in the United States ation does not transcend clones. The need to correctly delimit spe- (Haack and Rabaglia 2013), 30 are xyleborines (Atkinson 2017). cies is becoming increasingly important also for applied biology The haplodiploid mating system within this tribe, their small size and biosecurity research (Hurley et al. 2017). Unusual reproduct- (many species are <2 mm in length), their wood-boring habit, and ive strategies are overrepresented among invasive species, as clonal, their relationships with ambrosia fungi, make the ambrosia beetles inbred and otherwise unusually reproducing organisms are often highly successful invaders (Jordal et al. 2001). One of the most cost- more successful at colonizing new regions than regularly sexually effective options for the prevention of invasive scolytine establish- reproducing ones (Brockerhoff and Liebhold 2017), particularly ment is the enforcement of phytosanitary standards (Susaeta et al. when considering the many forest pests and pathogens that are 2016). However, a key issue in this approach is the ability to cor- morphologically cryptic. rectly identify the incoming invaders (Armstrong and Ball 2005). © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. 1 All rights reserved. For permissions, please e-mail: [email protected]. Version of Record, first published online November 28, 2018 with fixed content and layout in compliance with Art. 8.1.3.2 ICZN. Copyedited by: OUP 2 Insect Systematics and Diversity, 2018, Vol. 2, No. 6 One exceptionally successful invader is the xyleborine species Africa (Stouthamer et al. 2017, Paap et al. 2018). This last lineage Euwallacea fornicatus Eichhoff 1868 (Curculionidae: Scolytinae), has been given the common name Polyphagous Shot Hole Borer commonly called the Tea Shot Hole Borer (TSHB). This species (PSHB) in reference to its very broad host range. PSHB is associated impacts tea (Camelia sinensis) in at least 10 different countries (Li with several phytopathogenic Fusarium species and is causing sig- et al. 2015), including India and Sri Lanka where it is a major eco- nificant damage to avocado production, urban and natural vegeta- nomic pest (Danthanarayana 1968). Beetles matching the species tion (Eskalen et al. 2012, Boland 2016). Despite differences in fungal description for E. fornicatus were recently introduced into Israel, symbionts, geographic range, and host preference among these gen- where they inflict severe damage to several tree species (Mendel etic lineages of E. fornicatus, diagnostic morphological characters et al. 2012). Specimens from Israel were later found to be genet- have not yet been described. ically different from Sri Lankan beetles (O’Donnell et al. 2015, The objectives of this work were to 1) broaden the geographic Stouthamer et al. 2017). Specimens of E. fornicatus with the same sampling of the E. fornicatus complex in Asia, 2) reconstruct rela- Downloaded from https://academic.oup.com/isd/article-abstract/2/6/2/5201072 by University of Florida user on 10 January 2019 genetic identity as those from Israel were later confirmed as causing tionships between clades and populations, 3) find morphological damage to trees in California (United States) in 2012, where it was characters or combinations of characters which are useful in delimit- first recorded in 2003 (Eskalen et al. 2012). Specimens of E. for- ing the genetic lineages of the E. fornicatus cryptic species complex, nicatus which were genetically closer to Sri Lankan beetles were and 4) propose taxonomic delimitation of species where morph- also initially documented in Florida in 2002 with minor impacts ology and phylogenetic identity correlate. We tested the hypothesis on a few hosts (Rabaglia et al. 2006), and later on avocados in that there are quantifiable, diagnostic morphological differences 2012, with increasing levels of damage since then (Carrillo et al. between the three genetic lineages. Rather than using the traditional 2016). In addition to the genetic divergence of E. fornicatus beetles typological species concepts, we define putative species by the cor- in Israel and California from those in Florida and Sri Lanka, it was relation between variation in multiple morphological features and also reported that the fungal symbionts of the respective popula- phylogenetic placement, defined using multivariate analysis and tions were also morphologically and genetically distinct. Indeed, regression-based classification. Identifying and quantifying morpho- beetles from the Israel and California populations could not sur- logical differences may allow for the creation of an identification vive on the fungi of the pestiferous beetle species on tea (Freeman tool for use by researchers and agencies. Additionally, using histor- et al. 2012). However, the extent of such beetle-fungus specificity ical museum material, we tested whether the newly defined phe- is challenged by several studies showing that species of Euwallacea notypes fit any of the previously described species in or near the Hopkins, 1915 (Curculionidae: Scolytinae) switch or share symbi- E. fornicatus complex to clarify their taxonomic identity. onts (Kasson et al. 2013, O’Donnell et al. 2015, Dodge et al. 2017). The increasing damage caused by the E. fornicatus complex to Methods tree industries and ecosystems in the United States and abroad is of great importance to scientists, regulators and tree health practi- Specimens tioners (García-Avila et al. 2016). Individual populations, some of Eighty-nine specimens were measured and genotyped from 26 locali- which appear to cause greater damage than others, are currently ties in 11 countries (China, Hong Kong, Indonesia, Japan, Papua considered morphologically indistinguishable (Chen et al. 2016). New Guinea, American Samoa, Singapore, Taiwan, Thailand, United The confusion is compounded by the fact that the type specimen of States, and Vietnam). These populations were selected as represent- E. fornicatus, which was collected from
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