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Species Separation Within, and Preliminary Phylogeny For, The Species separation within, and preliminary phylogeny for, the leafhopper genus Anoscopus with particular reference to the putative British endemic Anoscopus duffieldi (Hemiptera: Cicadellidae) Article (Accepted Version) Redihough, Joanna, Russo, Isa-Rita M, Stewart, Alan J A, Malenovský, Igor, Stockdale, Jennifer E, Moorhouse-Gann, Rosemary J, Wilson, Michael R and Symondson, William O C (2020) Species separation within, and preliminary phylogeny for, the leafhopper genus Anoscopus with particular reference to the putative British endemic Anoscopus duffieldi (Hemiptera: Cicadellidae). Insects, 11 (11). a799 1-19. ISSN 2075-4450 This version is available from Sussex Research Online: http://sro.sussex.ac.uk/id/eprint/94927/ This document is made available in accordance with publisher policies and may differ from the published version or from the version of record. If you wish to cite this item you are advised to consult the publisher’s version. Please see the URL above for details on accessing the published version. Copyright and reuse: Sussex Research Online is a digital repository of the research output of the University. Copyright and all moral rights to the version of the paper presented here belong to the individual author(s) and/or other copyright owners. To the extent reasonable and practicable, the material made available in SRO has been checked for eligibility before being made available. Copies of full text items generally can be reproduced, displayed or performed and given to third parties in any format or medium for personal research or study, educational, or not-for-profit purposes without prior permission or charge, provided that the authors, title and full bibliographic details are credited, a hyperlink and/or URL is given for the original metadata page and the content is not changed in any way. http://sro.sussex.ac.uk 1 Species separation within, and preliminary 2 phylogeny for, the leafhopper genus Anoscopus with 3 particular reference to the putative British endemic 4 Anoscopus duffieldi (Hemiptera: Cicadellidae) 5 Joanna Redihough1, Isa-Rita M. Russo1, Alan J. A. Stewart2, Igor Malenovský3, Jennifer E. 6 Stockdale1, Rosemary J. Moorhouse-Gann1, Michael R. Wilson4 and William O. C. Symondson1* 7 1 Cardiff School of Biosciences, Sir Martin Evans Building, Museum Avenue, Cardiff C10 3AX, UK; 8 [email protected], [email protected] 9 2 School of Life Sciences, University of Sussex, Brighton BN1 9QG, East Sussex, U.K.; 10 [email protected] 11 3 Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic; 12 [email protected] 13 4 Department of Natural Sciences, National Museum of Wales, Cardiff, U.K.; 14 [email protected] 15 * Correspondence: [email protected] 16 Joanna Redihough now moved to Technovent, Bridgend; [email protected] 17 Rosemary Moorhouse-Gann now moved to Durrell Wildlife Conservation Trust, Bath; 18 [email protected] 19 Simple Summary. Anoscopus leafhoppers are a group of plant-feeding bugs that can be found in a 20 range of grassland habitats. There are seven recognized species in the UK, some of which are 21 difficult to tell apart. One species, Anoscopus duffieldi, has only been found at a single site, an RSPB 22 reserve at Dungeness in Kent. As Anoscopus leafhoppers can be quite variable in colour and pattern, 23 and in the structure of their genitalia, our aim was to establish, using DNA, whether this ‘species’ is 24 unique or whether it is simply a variant of one of the other species. If it is unique, found nowhere 25 else, it should be afforded special protection. Samples of all UK species, plus another from the Czech 26 Republic, were collected from the field and two genes were examined. The DNA sequences showed 27 that three species, A. duffieldi, A. albifrons and A. limicola were so closely related that they should 28 probably be considered to be a single species. However, A. duffieldi are distinctive in that they live 29 only in an area of vegetated shingle. We suggest that, until other evidence is forthcoming, A. duffieldi 30 could be considered to be a locally-adapted subspecies of scientific interest. 31 32 Abstract. The subfamily Aphrodinae (Hemiptera: Cicadellidae) contains ~33 species in Europe 33 within four genera. Species in two genera in particular, Aphrodes and Anoscopus, have proved to be 34 difficult to distinguish morphologically. Our aim was to determine the status of the putative species 35 Anoscopus duffieldi, found only on the RSPB Nature Reserve at Dungeness, Kent, a possible rare UK 36 endemic. DNA from samples of all seven UK Anoscopus species (plus A. alpinus from the Czech 37 Republic) were sequenced using parts of the mitochondrial cytochrome oxidase I and 16S rRNA 38 genes. Bayesian inference phylogenies were created. Specimens of each species clustered into 39 monophyletic groups, except for A. albifrons, A. duffieldi and A. limicola. Two A. albifrons specimens 40 grouped with A. duffieldi repeatedly with strong support and the remaining A. albifrons clustered 41 within A. limicola. Genetic distances suggest that A. albifrons and A. limicola are a single interbreeding 42 population (0% divergence) while A. albifrons and A. duffieldi diverged by only 0.28%. Shared 43 haplotypes between A. albifrons, A. limicola and A. duffieldi strongly suggest interbreeding although 44 mis-identification may also explain these topologies. However, all A. duffieldi clustered together in 45 the trees. A conservative approach might be to treat A. duffieldi, until other evidence is forthcoming, 46 as a possible endemic subspecies. Insects 2020, 11, x; doi: FOR PEER REVIEW www.mdpi.com/journal/insects Insects 2020, 11, x FOR PEER REVIEW 2 of 19 47 Keywords: Anoscopus duffieldi; Aphrodinae; Cicadellidae; genetic distance; molecular separation; 48 endemic species 49 50 1. Introduction 51 Conventional methods of species identification and separation rely on morphological features 52 to distinguish taxa [1]. Erroneous identification can undermine taxonomy, ecological research, 53 conservation efforts and ecosystem management [2-4]. Serious problems can arise when type 54 specimens are involved [5]. Differences between morphologically similar species, and their 55 phylogenetic relationships, can often be resolved using genetic evidence [6-9]. 56 The Auchenorrhyncha are within the fifth most diverse insect order, Hemiptera [10,11], and 57 comprises ~43,000 species worldwide including leafhoppers, planthoppers, treehoppers, froghoppers 58 (spittlebugs) and cicadas [12,13]. These herbivorous insects variously feed on xylem or phloem sap 59 or mesophyll contents [14]. Many leafhoppers are plant pathogen vectors [15,16], or are studied as 60 part of conservation efforts [14,17] or evaluation of community structure [18]. Species separation 61 within many leafhopper genera is seriously understudied and hampered by the presence of 62 morphologically cryptic species and biotypes. 63 The subfamily Aphrodinae (Hemiptera: Cicadellidae) contains 33 species in Europe within four 64 genera: Stroggylocephalus Flor, 1861, Planaphrodes Hamilton, 1975, Aphrodes Curtis, 1833 and Anoscopus 65 Kirschbaum, 1868 [19,20], of which 15 species and all genera occur in the UK [21]. Species in Aphrodes, 66 Planaphrodes and Anoscopus are morphologically similar, to the extent that all Anoscopus were 67 previously regarded as Aphrodes [22-25]. The current split between Anoscopus and Aphrodes dates back 68 to Hamilton [24}. External characters were used to distinguish between leafhopper species until the 69 late 1930s when the aedeagus became the primary discriminator [26]. Some Aphrodes and Anoscopus 70 species have proved difficult to distinguish morphologically, differences being mainly based upon 71 the details of the male aedeagus, such as its shape and positions of spines [9,20,27]. However, these 72 characters are subject to intraspecific variability and interspecific overlap, and females and nymphs 73 cannot be separated reliably [9]. More accurate morphological identification of male Aphrodes and 74 Anoscopus is generally possible using a combination of aedeagus and external morphometric 75 measurements [9,20,28]. 76 A possibly new species of ‘Aphrodes’ was reported by Duffield [29] from Dungeness, Kent. 77 Duffield noted banded elytra on three males, similar to Aphrodes assimilis (now Anoscopus assimilis 78 (Signoret, 1879)) which had not been recorded in Britain at the time. Additional morphological 79 characters of A. assimilis, published by Ribaut [22], supported Duffield’s initial identification. 80 Subsequently, Duffield sent specimens to Le Quesne, who established it as a new species, Aphrodes 81 duffieldi (now Anoscopus duffieldi (Le Quesne, 1964)), possibly confined to Kent, based upon aedeagus 82 characters [30]. Le Quesne [23] later considered A. duffieldi could be synonymous with Anoscopus 83 alpinus (Wagner, 1955), with this continental species regarded as conspecific with A. assimilis by Nast 84 [31], Hamilton [24] and, with question marks, Remane & Fröhlich [27]. Guglielmino & Buckle [20] 85 treated A. assimilis and A. alpinus as separate species, based on differences in the forewing shape, 86 colour and aedeagus size and structure. They also studied the morphology of nine male specimens 87 of A. duffieldi from the type locality and noticed a large variability in the aedeagus morphology and 88 external similarity to another species, A. albifrons (Linnaeus, 1758), suggesting that A. duffieldi 89 specimens
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