Coleoptera: Cerambycidae), in Northeast Asia: Implications for Future Restoration in Korea
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insects Article Phylogeographic Investigation of an Endangered Longhorn Beetle, Callipogon relictus (Coleoptera: Cerambycidae), in Northeast Asia: Implications for Future Restoration in Korea Ji Hyoun Kang 1,† , Dae-Am Yi 2,†, Alexander V. Kuprin 3 , Changdo Han 4 and Yeon Jae Bae 5,* 1 Korean Entomological Institute, Korea University, Seoul 02841, Korea; [email protected] 2 Research Center of Natural Monument Insects, Yeongwol Insect Museum, Yeongwol 26210, Korea; [email protected] 3 Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, 690022 Vladivostok, Russia; [email protected] 4 Wildlife Research Center, Korea University, Ogawa-chô, Kodaira City, Tokyo 187-0032, Japan; [email protected] 5 Division of Environmental Science and Ecological Engineering, Korea University, Seoul 02841, Korea * Correspondence: [email protected]; Tel.: +82-0(2)-3290-3408 † These authors contributed equally to this work. Simple Summary: The critically endangered Callipogon relictus is one of the largest longhorn beetle species and also the only remnant species of the genus Callipogon found in the Palearctic region. Knowledge of the phylogeographic history and current conservational status is essential to un- derstand its unique distribution and to establish efficient conservation strategies. We studied the phylogeographical pattern and genetic diversity of C. relictus from almost its entire geographical range. The level of genetic diversity and divergence of C. relictus from the known distributions in four regions in Russia, China, North Korea, and South Korea using two mitochondrial markers (COI Citation: Kang, J.H.; Yi, D.-A.; and COII) revealed that genetic diversity lies within the range of intraspecific levels. Relatively Kuprin, A.V.; Han, C.; Bae, Y.J. Phylogeographic Investigation of an high genetic diversity with no distinct phylogeographic structures indicates that the wide range of Endangered Longhorn Beetle, current fragmented populations might be the remnant of genetically diverse populations in the past. Callipogon relictus (Coleoptera: The results of our phylogenetic and population genetic analyses suggest that C. relictus populations Cerambycidae), in Northeast Asia: surveyed in the present study can be used as a “source” for a future restoration and conservation Implications for Future Restoration in program. The findings of the genetic characteristics and phylogeographic history of C. relictus will Korea. Insects 2021, 12, 555. https:// help to establish effective conservation strategies for this endangered longhorn beetle species in doi.org/10.3390/insects12060555 Northeast Asia. Received: 12 April 2021 Abstract: The longhorn beetle, Callipogon (Eoxenus) relictus Semenov, is the only remnant species Accepted: 7 June 2021 found in the Palearctic region, while all other Callipogon species are distributed mainly in Central Published: 15 June 2021 America and partly in South America. This species has been placed in the first category (as ‘critically endangered’) of the Red Data Book in Russia and designated as one of the top-priority target species Publisher’s Note: MDPI stays neutral among all endangered invertebrate species for restoration in South Korea since 2006. Although with regard to jurisdictional claims in its restricted distribution in Northeast Asia with a high conservational value has been highlighted, published maps and institutional affil- iations. genetic features of C. relictus from different geographic regions remain unexplored. We first investi- gated the level of genetic diversity and phylogeographic patterns of C. relictus to evaluate the current conservational status and the feasibility of the implementation of a restoration program. The average genetic divergence of mitochondrial gene COI based on Kimura-2-parameter distance among the four regions in Russia, China, North Korea, and South Korea was 2.2%, which lies within the range Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. of intraspecific levels. However, two separate clades with 3.8% divergence were identified, despite This article is an open access article no geographical clustering of haplotypes. The linear pattern of the haplotype network with a high distributed under the terms and level of haplotype and nucleotide diversities suggests that the wide range of currently fragmented conditions of the Creative Commons populations might be the remnant of genetically diverse populations in the past. This study will Attribution (CC BY) license (https:// provide crucial information on the genetic characteristics and phylogeographic history of C. relictus, creativecommons.org/licenses/by/ which will help to establish conservation strategies for this cherished insect species in Northeast Asia. 4.0/). Insects 2021, 12, 555. https://doi.org/10.3390/insects12060555 https://www.mdpi.com/journal/insects Insects 2021, 12, 555 2 of 15 Keywords: COI; COII; endangered species; longhorn beetle; restoration; saproxylic insect Insects 2021, 12, x 1. Introduction 2 of 17 The critically endangered Callipogon relictus is one of the largest, most charismatic longhorn beetle species and also the only remnant species of genus Callipogon Audinet- Serville,of C. relictus 1832,, which found will in thehelp Palearctic to establish entomo-fauna conservation(Figure strategies1). for Other this Callipogoncherished insectspecies species in are distributed mainly in Central America and partly in South America [1–4]. In Asia, Northeast Asia. C. relictus is found only in the Siberian part of the Palearctic realm comprising far-east Russia, northeast China, North Korea, and the northern part of South Korea [5–8]. The boundariesKeywords: ofCOI the; COII known; endangered habitats encompassspecies; longhorn a distance beetle; of approximatelyrestoration; saproxylic 1400 km insect north to south and (app.) 1800 km east to west, covering almost eleven degrees of latitude (from 48◦370 N to 37◦440 N) and twelve degrees of longitude (from 135◦070 E to 123◦270 E) (Figure2) . Among the four countries, in both Russia and South Korea, C. relictus was placed1. Introduction in the first category of the Red Data Book and it is protected by law [7,9,10]. In SouthThe Korea, critically it is not onlyendangered listed as anCallipogon endangered relictus species is butone is of also the regarded largest, as most a national charismatic natural monument (no. 218); even the dead body of C. relictus is required to be registered longhorn beetle species and also the only remnant species of genus Callipogon Audinet- under the regulation of Cultural Properties Protection Law. Serville,Callipogon 1832, relictus found, ain saproxylic the Palearctic longhorn entomo-fauna beetle, inhabits (Figure mixed 1). and Other deciduous Callipogon forests species butare notdistributed temperate mainly coniferous in Central forests; America the beetles and feedpartly on in the South rotten America logs of ancient[1–4]. In or Asia, C. veteranrelictus broadleafis found only trees in such the as SiberianUlmus davidiana part of thevar. Palearcticjaponica (Ulmaceae), realm comprisingQuercus mongolica far-east Russia, (Fagaceae),northeast China,Quercus North aliena, Korea, Quercus and serrata, the northern Carpinus laxiflorapart of (Betulaceae),South Korea etc.[5–8]. [7, 10The,12 –boundaries17]. Theof the wood-boring known habitats larva isencompass a polyphagous a distance internal of approximately feeder, which goes 1400 through km north a five- to south to and seven-year(app.) 1800 developmental km east to west, period covering inside rotten almost timber eleven [15]. degrees Until the of beginning latitude of (from the 1950s, 48°37′ N to there37°44 were′ N) and two twelve major populations degrees of oflongitudeC. relictus (fromin South 135°07 Korea;′ E to one 123°27 in the′ E) Gwangneung (Figure 2). Among Forestthe four in Gyeonggi-docountries, in both (province) Russia and and the South other Korea, in Chuncheon C. relictus in was Gangwon-do, placed in whichthe first cate- isgory located of the 100 Red km Data to the Book east and of theit is Gwangneungprotected by Forest,law [7,9,10]. almost In in South the same Korea, latitude it is not only (37◦ N) [14]. Unfortunately, the Chuncheon site was destroyed during the Korean War listed as an endangered species but is also regarded as a national natural monument (no. (1950–1953) and then submerged by the immense Soyang Dam built in 1967. Recently, distribution218); even the of C. dead relictus bodyin theof C. Gwangneung relictus is required forest and to a be new registered location inunder Yangyang the regulation have of beenCultural reported Properties in Korea Protection during four Law. consecutive years from 2007 to 2017 [18]. FigureFigure 1. 1.Habitus Habitus of ofCallipogon Callipogon relictus relictus, male, male (left )(left and) femaleand female (right ()right (scale) 10(scale mm). 10 mm). Insects 2021, 12, 555 3 of 15 Figure 2. Sampling sites of C. relictus in the present study [11]. While a single adult female was found every year from 2014 to 2017 [18], no female C. relictus was found for almost 20 years in Gwangneung Forest during the period of 1986–2006 [14], and it was not until 2015 that another female was observed [18]. These observations might indicate that the population size in the remaining habitat in South Korea is extremely small. Although the population in Gwangneung Forest is not extinct and its new location is continuously reported, the risk of local extinction