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Seven Sycoryctine Fig Wasp Species (Chalcidoidea: Pteromalidae) Associated with Dioecious Ficus hirta Inhabiting South China and Southeast Asia

Seven Sycoryctine Fig Wasp Species (Chalcidoidea: Pteromalidae) Associated with Dioecious Ficus... biology Article Seven Sycoryctine Fig Wasp Species (Chalcidoidea: Pteromalidae) Associated with Dioecious Ficus hirta Inhabiting South China and Southeast Asia 1 , 2 , 3 1 , 2 , 3 1 , 2 , 3 , Da-Mien Wong , Songle Fan and Hui Yu * Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China; dmwong87@gmail.com (D.-M.W.); fansongle@scbg.ac.cn (S.F.) Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China Guangdong Provincial Key Laboratory of Digital Botanical Garden, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China * Correspondence: yuhui@scib.ac.cn Simple Summary: The non-pollinating fig wasps are essential components of fig wasp communities, negatively impacting mutualism. However, this group of fig wasps has received less taxonomic attention than pollinating fig wasps. This study presents seven new non-pollinating fig wasp species associated with Ficus hirta fig trees inhabiting South China and Southeast Asia. The presence of a long ovipositor sheath characterizes this group of fig wasps. An identification key is provided to distinguish between them, and the relationships with their host fig trees are discussed. The type specimens and examined materials are deposited in the South China Botanical Garden, Chinese Academy of Sciences, China. Abstract: Even though non-pollinating fig wasps are essential components in tropical and subtropical Citation: Wong, D.-M.; Fan, S.; Yu, H. habitats, yet they are poorly described in the Oriental communities. This study presented seven Seven Sycoryctine Fig Wasp Species new sycoryctine fig wasp species associated with Ficus hirta fig trees inhabiting South China and (Chalcidoidea: Pteromalidae) Southeast Asia. These new sycoryctine species belong to the genera Philotrypesis, Sycoryctes, and Associated with Dioecious Ficus hirta Sycoscapter. They can be easily distinguished by their adaptive morphologies such as face sculpture, Inhabiting South China and body-color, and ovipositors. An identification key is provided to differentiate between them, and Southeast Asia. Biology 2022, 11, 801. the relationships with their host fig trees are also discussed. The holotypes and paratypes are both https://doi.org/10.3390/ deposited in the South China Botanical Garden, Chinese Academy of Sciences, China. biology11060801 Academic Editor: Natraj Krishnan Keywords: inquilines; Indomalaya; non-pollinating fig wasps; parasitoids; Sycoryctinae Received: 1 May 2022 Accepted: 18 May 2022 Published: 24 May 2022 1. Introduction Publisher’s Note: MDPI stays neutral Fig wasps are exciting for ecological and evolutionary studies, particularly their with regard to jurisdictional claims in adaptive morphologies and co-speciation with their host fig trees [1,2]. Despite most of the published maps and institutional affil- early accounts of fig wasp focusing on pollinating species, there can be up to 30 diverse iations. non-pollinating species associated with a single host fig tree [3]. Although these tiny hymenopterans could play an important role in tropical- and sub-tropical ecology, the non-pollinating fig wasps are still poorly described in the Oriental realm [4]. Copyright: © 2022 by the authors. Sycoryctine fig wasps (Chalcidoidea: Pteromalidae) are non-pollinators of fig trees. Licensee MDPI, Basel, Switzerland. The taxonomy of sycoryctines has changed over the past ten years, and their phylogeny is This article is an open access article currently more defined due to the advancement of molecular techniques [5,6]. These fig distributed under the terms and wasps belong to the subfamily Sycoryctinae and are highly diversified and geographically conditions of the Creative Commons widespread [5]. Sycoryctines are associated with all six subgenera and at least 15 sections Attribution (CC BY) license (https:// in Ficus [7]. Surprisingly, an estimated 826 species (2.7 species per Ficus) are waiting creativecommons.org/licenses/by/ to be discovered in the Old World [5]. Two sycoryctine species have been described 4.0/). Biology 2022, 11, 801. https://doi.org/10.3390/biology11060801 https://www.mdpi.com/journal/biology Biology 2022, 11, 801 2 of 12 recently in Taiwan [8] and India [9], and hopefully more Oriental sycoryctines are going to be described. Sycoryctinae is currently divided into four tribes: (1) Apocryptini, comprising two genera: Apocrypta Coquerel, and Bouceka Kocak and Kemal; (2) Critogastrini, comprising only one genus: Critogaster Mayr; (3) Philotrypesini, comprising four genera: Dobunabaa Boucek, Philoverdance Priyadarsanan, Philotrypesis Forster, and Watshamiella Wiebes; and (4) Sycoryctini, comprising seven genera: Adiyodiella Priyadarsanan, Arachonia Joseph, Parasycobia Abdurahiman and Joseph, Sycorycteridea Abdurahiman and Joseph, Sycoryctes Mayr, Sycoscapter Saunders, and Sycoscapteridea Ashmead [5,10]. The sycoryctine fig wasps are considered host specificity conservatisms which originated about 49–64 million years ago [5]. The sycoryctine species are also believed to impact the fig–fig wasp mutualism significantly [11]. Female sycoryctines have remarkable long ovipositors that can penetrate the fig wall. They attack flowers containing other fig wasp larvae by consuming the host larvae or starving them by feeding on endosperm [12]. Their complicated trophic relationships make sycoryctines the ideal study species for the population dynamics in tropical and sub-tropical habitats [13]. A recent molecular study showed eight allopatric sycoryctine species associated with Ficus hirta Vahl in South China and Southeast Asia. The marked barcoding gaps ranged from 7.2% to 15.7% for the Cytb gene sequence in the same genus [14]. However, the morphological traits of these species remain unknown. This study compared their morphology and reported seven new species belonging to the genera Philotrypesis, Sycoryctes, and Sycoscapter. An identification key is provided to distinguish between them, and the relationships with their host fig trees are discussed. Like the non-pollinating fig wasps, sycoryctines often receive less research attention in the symbiosis of figs and fig wasps. Hence, this study is concerned with the taxonomy of the geographically widespread sycoryctine fig wasps associated with F. hirta. Our research and results provide new insights into the morphology and adaptation of these non-pollinating fig wasps. It contributes to our understanding of speciation and biodiversity in the Oriental fig–fig wasp communities. 2. Materials and Methods The specimens of sycoryctine fig wasps associated with F. hirta were collected in 23 sampling sites for Philotrypesis, 15 sites for Sycoscapter, and two sites for Sycoryctes during the years 2010 to 2018 are distributed from South China to Java (Table 1). The distribution of the species in each genus is allopatric except for two sites with two species in each genus co-occurred, QMS in Thailand and XI in China (Table 1). When figs close to ripening were dissected, the wasps emitted therein were collected. Two to twenty-four wasps in each site with one wasp exited from one natal fig were collected and stored in 75% ethanol. Later, the wasps were dehydrated through an ethanol series (80%, 90%, and 100%) and critical-point dried (LEICA EM CPD300, Leica Microsystems GmbH, Wetzlar, Germany) before being mounted on cards following Noyes (1982) [15]. Each photo was taken using a digital camera connected to a stereomicroscope (LEICA M205 FA, Leica Microsystem GmbH, Wetzlar, Germany). The images were processed using LAS X 3.08.19082 software to create a stacked image with increased focal depth [16]. Physical characteristics were measured using ImageJ 1.8.0_172 software (National Institutes of Health, Bethesda, MD, USA). Specimen measurements were taken with an accuracy of 0.001 mm and rounded to the nearest 0.01 mm. Specimens were mounted on brass stubs and sputter-coated with gold (LEICA EM ACE600, Leica Microsystem GmbH, Germany) before the observation and photographed using SEM (JEOL JSM-6360LV, JEOL Ltd., Tokyo, Japan). Morphological terminology follows Gibson (1997) and the Hymenoptera Anatomy Ontology (HAO) Portal [17,18]. The holotypes and a group of paratypes are deposited in the Plant Science Center, South China 0  0 Botanical Garden, Chinese Academy of Sciences (23 10 48” N; 113 21 8” E). Biology 2022, 11, 801 3 of 12 Table 1. Sampling sites for sycoryctine fig wasps associated with Ficus hirta. Wasp Species Country Site Latitude, Longitude Philotrypesis guangdongensis China Gui 25.077, 110.306 Huo 23.170, 113.373 DHS 23.166, 112.543 Xiang 22.424, 114.306 Nan 22.787, 108.389 Ding 19.697, 110.328 Wan 18.795, 110.391 Thailand QMS 18.809, 98.914 CH 12.774, 102.096 Wu 14.443, 105.273 HB 12.999, 108.230 ST 7.467, 99.639 P. yunnanensis China Sand 25.984, 107.874 XI 21.913, 101.264 Thailand QMS 18.809, 98.914 Tai 18.894, 98.858 CS 18.84, 99.47 P. fujianensis China Ning 26.664, 119.549 Sha 26.419, 117.818 Xia 24.742, 118.072 Sui 26.476, 114.239 Da 24.258, 116.806 Sycoryctes javaensis Indonesia CI 6.566, 106.706 JA 6.368, 106.830 Sycoscapter chinensis China Gui 25.077, 110.306 Huo 23.170, 113.373 DHS 23.166, 112.543 Xiang 22.424, 114.306 Sand 25.984, 107.874 Nan 22.787, 108.389 Ding 19.697, 110.328 Wan 18.795, 110.391 XI 21.913, 101.264 S. thaiensis Thailand CH 12.774, 102.096 Wu 14.443, 105.273 Tai 18.894, 98.858 CS 18.84, 99.47 QMS 18.809, 98.914 S. singaporensis Singapore SNP 1.312, 103.816 3. Results 3.1. Philotrypesis Forster, 1878 3.1.1. Philotrypesis Forster, 1878: 153–187. Type Species: Philotrypesis Longicaudata Mayr, 1906 Diagnosis: The female of this genus can be recognized by its lengthened seventh and eighth urotergites and its subquadrate pronotum. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Philotrypesis fig wasp species are known from Afrotropical realm: Eritrea, Guinea, Sierra Leone, South Africa, Zambia, Zimbabwe; Australasian realm: Australia, Indonesia; Nearctic realm: United States; Oriental realm: Indonesia, Japan, Mainland China, Malaysia, Philippines, Sri Lanka, Taiwan, Vietnam; and Palearctic realm: France, Israel, Italy. All described Philotrypesis fig wasp species are parasitoids or inquilines of other fig wasps associated with sections Conosycea, Ficus, Galoglychia, Sycidium, Sycocarpus, and Urostigma fig trees. The recorded host fig wasps of Philotrypesis included Blastophaga psenes Linnaeus, Ceratosolen dentifer Wiebes, Ceratosolen notus Baker, Ceratosolen solmsi Mayr, Eupristina verticillata Waterston, Kradibia brownii Ashmead, Kradibia gestroi Grandi, and Platyscapa quadraticeps Mayr. Biology 2022, 11, 801 4 of 12 Biology 2022, 11, x FOR PEER REVIEW 5 of 12 Philotrypesis guangdongensis Yu sp. n. (Figure 1a,d, Figure 2a,d and Figure 3a,d) Biology 2022, 11, x FOR PEER REVIEW 5 of 12 Figure 1. Habitus lateral of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp n.; (c) P. fu- Figure 1. Habitus lateral of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp. n.; (c) P. fu- jianensis sp. n. Mesosoma, dorsal view of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. Figure 1. Habitus lateral of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp n.; (c) P. fu- jianensis sp. n. Mesosoma, dorsal view of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. Noji ted that anensis sp. the n. blac Mes k band of osoma, doP. rsal yun vie nane w of ns (d is ) P on s . guangdonge cutellum ns is i is; ndi (e) P. stinct yun.nane Scal ne sis bars ; (f) P repr . fujies anen ent 250 sis. μm. Noted that the black band of P. yunnanensis on scutellum is indistinct. Scale bars represent 250 m. Noted that the black band of P. yunnanensis on scutellum is indistinct. Scale bars represent 250 μm. Figure 2. Head, dorsal view of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp n.; (c) P. Figure 2. Head, dorsal view of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp. n.; fujianensis sp. n. Head, ventral view of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. (c) P. fujianensis sp. n. Head, ventral view of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. Figure Noted 2. that Heathe d, do toru rsa li l of vie P.w gua ongdonge f (a) Philotrypes nsis are lois cat guangdonge ed below the nsis botto sp. m n. li;ne (b of comp ) P. yun oun nanens d eyes, is sp and n.; (c) P. the mouthpart of P. fujianensis extended below to the central of compound eyes. Noted fujianen that sis sp. the n. torHead, uli of P ventral . guangdongensis view of (ar d) eP. located guangdonge below ns the is; bottom (e) P. yun line nanen of compound sis; (f) P. fujia eyes, nens and is. Noted that the toruli of P. guangdongensis are located below the bottom line of compound eyes, and the mouthpart of P. fujianensis extended below to the central of compound eyes. the mouthpart of P. fujianensis extended below to the central of compound eyes. Biology 2022, 11, 801 5 of 12 Biology 2022, 11, x FOR PEER REVIEW 6 of 12 Figure 3. Mesosoma, dorsal view of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp n.; Figure 3. Mesosoma, dorsal view of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp. n.; (c) P. fujianensis sp. n. Hind leg of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. (c) P. fujianensis sp. n. Hind leg of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. Philotrypesis yunnanensisYu sp. n. Distribution: China (Guangdong, Guangxi, Hainan provinces, and Hong Kong SAR), (Figures 1b,e, 2b,e, and 3b,e) Thailand, Vietnam. Distribution: China (Guizhou and Yunnan Provinces), Thailand. 0  0 Types: Holotype, , CHINA: Guangzhou, 23 10 12.0” N, 113 22 22.8” E, 27 November 2015, Types: Holotype, ♀, CHINA: Yunnan, 21°26′49.2″ N, 101°34′04.8″ E, 4 July 2013, H. H. Yu. Paratypes, 4 , same locality and data as holotype. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.9–2.1 mm. Body color yellowish Description: Female. Color and Size. Body length 1.9–2.1 mm. Body color yellowish orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Ovipositor sheath length 2.5–3.0 mm. Ovipositor sheath length 2.5–2.9 mm. Head. Width 0.4–0.5 mm. Eye longer than gena. Antenna inserted below the bottom Head. Width 0.3–0.4 mm. Eye longer than gena. Antenna inserted below the bottom line of compound eye. Toruli apart, distance between toruli larger than diameter of one line of compound eye. Toruli apart, distance between toruli larger than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin flattened. margin flattened. Mesosoma. Length 2.0–2.2 mm. Wing length 1.3–1.5 mm and finely pubescent. Black Mesosoma. Length 2.0–2.2 mm. Wing length 1.3–1.4 mm and finely pubescent. Black band on scutellum distinct; black band on mesoscutum bifurcation. band on scutellum indistinct; black band on mesoscutum straight. Metasoma. Length 1.8–2.0 mm. Without petiole. Ovipositor sheath length 2 longer Metasoma. Length 1.6–2.0 mm. Without petiole. Ovipositor sheath length 2× longer than body. than body. Male. Unknown. Male. Unknown. Etymology: Named after the Guangdong province of China. Etymology: Named after the Yunnan province of China. Philotrypesis yunnanensis Yu sp. n. Philotrypesis fujianensis Yu sp. n. (Figure 1b,e, Figure 2b,e and Figure 3b,e) (Figures 1c,f, 2c,f and 3c,f) Distribution: China (Guizhou and Yunnan Provinces), Thailand. Distribution: China (Fujian, Guangdong, and Jiangxi Provinces). 0  0 Types: Holotype, , CHINA: Yunnan, 21 26 49.2” N, 101 34 04.8” E, 4 July 2013, H. Yu. Types: Holotype, ♀, CHINA: Fujian, 26°39′50.4″ N, 119°32′56.4″ E, 24 January 2016, Paratypes, 4 , same locality and data as holotype. H. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.9–2.1 mm. Body color yellowish Description: Female. Color and Size. Body length 1.9–2.3 mm. Body color yellowish orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Ovipositor sheath length 2.5–2.9 mm. Biology 2022, 11, 801 6 of 12 Head. Width 0.3–0.4 mm. Eye longer than gena. Antenna inserted below the bottom line of compound eye. Toruli apart, distance between toruli larger than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin flattened. Mesosoma. Length 2.0–2.2 mm. Wing length 1.3–1.4 mm and finely pubescent. Black band on scutellum indistinct; black band on mesoscutum straight. Metasoma. Length 1.6–2.0 mm. Without petiole. Ovipositor sheath length 2 longer than body. Male. Unknown. Etymology: Named after the Yunnan province of China. Philotrypesis fujianensis Yu sp. n. (Figure 1c,f, Figure 2c,f and Figure 3c,f) Distribution: China (Fujian, Guangdong, and Jiangxi Provinces). 0  0 Types: Holotype, , CHINA: Fujian, 26 39 50.4” N, 119 32 56.4” E, 24 January 2016, H. Yu. Paratypes, 4 , same locality and data as holotype. Description: Female. Color and Size. Body length 1.9–2.3 mm. Body color yellowish orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Ovipositor sheath length 2.6–2.9 mm. Head. Width 0.4–0.8 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli apart, distance between toruli larger than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin flattened. Mesosoma. Length 2.0–2.4 mm. Wing length 1.3–1.5 mm and finely pubescent. Black band on scutellum distinct; black band on mesoscutum straight. Metasoma. Length 1.8–2.1 mm. Without petiole. Ovipositor sheath length 1.5 longer than body. Male. Unknown. Etymology: Named after the Fujian province of China. 3.2. Sycoryctes Mayr, 1885 3.2.1. Sycoryctes Mayr, 1885: 153–187. Type Species: Sycoryctes Patellaris Mayr, 1885 Diagnosis: Stigmal knob not produced downwards. Dorso-apical spine on basitarsus short, not reaching end of second segment. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Sycoryctes fig wasp species are mainly known from the Afrotropical, Australasian, and Oriental realms. All described Sycoryctes fig wasp species are parasitoids or inquilines of other fig wasps. Sycoryctes javaensis Yu sp. n. (Figure 4) Distribution: Indonesia. 0  0 Types: Holotype, , INDONESIA: Java, 6 22 04.8”S, 106 49 48.0”E, 3 MAY 2014, H. Yu. Paratypes, 4 , same locality and data as holotype. Description: Female. Color and Size. Body length 1.2–1.6 mm. Body color metallic green with brownish reflection. Head and antennae metallic green. Mesosoma and meta- soma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.6–2.0 mm. Head. Width 0.2–0.5 mm. Eye longer than gena. Antenna inserted above the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin slightly protruded. Mesosoma. Length 1.1–1.5 mm. Wing length 1.2–1.4 mm and finely pubescent. Biology 2022, 11, x FOR PEER REVIEW 7 of 12 Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Ovipositor sheath length 2.6–2.9 mm. Head. Width 0.4–0.8 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli apart, distance between toruli larger than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin flattened. Mesosoma. Length 2.0–2.4 mm. Wing length 1.3–1.5 mm and finely pubescent. Black band on scutellum distinct; black band on mesoscutum straight. Metasoma. Length 1.8–2.1 mm. Without petiole. Ovipositor sheath length 1.5× longer than body. Male. Unknown. Etymology: Named after the Fujian province of China. 3.2. Sycoryctes Mayr, 1885 Sycoryctes Mayr, 1885: 153–187. Type Species: Sycoryctes Patellaris Mayr, 1885 Diagnosis: Stigmal knob not produced downwards. Dorso-apical spine on basitarsus short, not reaching end of second segment. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Sycoryctes fig wasp species are mainly known from the Afrotropical, Australasian, and Oriental realms. All described Sycoryctes fig wasp species are parasitoids or inquilines of other fig wasps. Sycoryctes javaensis Yu sp. n. (Figure 4) Distribution: Indonesia. Types: Holotype, ♀, INDONESIA: Java, 6°22′04.8″S, 106°49′48.0″E, 3 MAY 2014, H. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.2–1.6 mm. Body color metallic green with brownish reflection. Head and antennae metallic green. Mesosoma and meta- soma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.6–2.0 mm. Head. Width 0.2–0.5 mm. Eye longer than gena. Antenna inserted above the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of Biology 2022, 11, 801 7 of 12 one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epis- tomal margin slightly protruded. Mesosoma. Length 1.1–1.5 mm. Wing length 1.2–1.4 mm and finely pubescent. Metasoma. Length 1.0–1.4 mm. Without petiole. Ovipositor sheath length 3 longer Metasoma. Length 1.0–1.4 mm. Without petiole. Ovipositor sheath length 3× longer than body. than body. Male. Male. Unknown. Unknown. Etymology: Named after the Java Island of Indonesia. Etymology: Named after the Java Island of Indonesia. Figure 4. Sycoryctes javaensis sp. n. in (a) habitus lateral view; (b) head dorsal view; and (c) mesosoma Figure 4. Sycoryctes javaensis sp. n. in (a) habitus lateral view; (b) head dorsal view; and (c) mesosoma dorsal view. Scale bars on the stacked images are 250 μm. dorsal view. Scale bars on the stacked images are 250 m. 3.3. Sycoscapter Saunders, 1883 3.3.1. Sycoscapter Saunders, 1883: 29–47. Type Species: Sycoscapter Insignis Saunders, 1883 Diagnosis: Stigmal knob not produced downwards. Funicular segments symmetric. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Sycoscapter fig wasp species are mainly known from the Afrotropical, Australasian, and Oriental realms. All described Sycoscapter fig wasp species are parasitoids of other fig wasps. The recorded host fig wasps of Sycoscapter included Ceratosolen dentifer Wiebes, Eupristina delhiensis Abdurahiman and Joseph, Eupristina verticillata Waterston, and Kradibia gestroi Grandi. Sycoscapter chinensis Yu sp. n. (Figure 5a,b and Figure 6a) Distribution: China (Guangdong, Guangxi, Guizhou, Hainan, Yunnan Provinces, and Hong Kong SAR). 0  0 Types: Holotype, , CHINA: Guangzhou, 23 10 12.0” N, 113 22 22.8” E, 27 November 2015, H. Yu. Paratypes, 4 , same locality and data as holotype. Description: Female. Color and Size. Body length 1.6–2.0 mm. Body color metallic green. Head and antennae metallic green. Mesosoma and metasoma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.6–2.0 mm. Head. Width 0.3–0.5 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin slightly protruded. Mesosoma. Length 1.2–1.7 mm. Wing length 1.3–1.7 mm and finely pubescent. Metasoma. Length 1.2–1.6 mm. Without petiole. Ovipositor sheath length 3.5 longer than body. Male. Unknown. Etymology: Named after China. Sycoscapter thaiensis Yu sp. n. (Figure 5b,e and Figure 6b) Distribution: Thailand. 0  0 Types: Holotype, , THAILAND: Mueang Chiang Mai, 18 48 32.4” N, 98 54 50.4” E, 3 July 2014, H. Yu. Paratypes, 4 , same locality and data as holotype. Biology 2022, 11, x FOR PEER REVIEW 8 of 12 3.3. Sycoscapter Saunders, 1883 Sycoscapter Saunders, 1883: 29–47. Type Species: Sycoscapter Insignis Saunders, 1883 Diagnosis: Stigmal knob not produced downwards. Funicular segments symmetric. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Sycoscapter fig wasp species are mainly known from the Afrotropical, Australasian, and Oriental realms. All described Sycoscapter fig wasp species are parasitoids of other fig wasps. The recorded host fig wasps of Sycoscapter included Ceratosolen dentifer Wiebes, Eupristina delhiensis Abdurahiman and Joseph, Eupristina verticillata Waterston, and Kra- dibia gestroi Grandi. Sycoscapter chinensis Yu sp. n. (Figures 5a,b and 6a) Distribution: China (Guangdong, Guangxi, Guizhou, Hainan, Yunnan Provinces, and Hong Kong SAR). Types: Holotype, ♀, CHINA: Guangzhou, 23°10′12.0″ N, 113°22′22.8″ E, 27 Novem- ber 2015, H. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.6–2.0 mm. Body color metallic green. Head and antennae metallic green. Mesosoma and metasoma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.6–2.0 mm. Head. Width 0.3–0.5 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal Biology 2022, 11, 801 8 of 12 margin slightly protruded. Mesosoma. Length 1.2–1.7 mm. Wing length 1.3–1.7 mm and finely pubescent. Metasoma. Length 1.2–1.6 mm. Without petiole. Ovipositor sheath length 3.5× longer Description: Female. Color and Size. Body length 1.7–2.1 mm. Body color metallic than body. green with brownish reflection. Head and antennae metallic green. Mesosoma and meta- Male. Unknown. soma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.7–2.0 mm. Etymology: Named after China. Biology 2022, 11, x FOR PEER REVIEW 9 of 12 Figure 5. Habitus lateral view of (a) Sycoscapter chinensis sp. n.; (b) S. thaiensis sp. n.; (c) S. singaporensis Figure 5. Habitus lateral view of (a) Sycoscapter chinensis sp. n.; (b) S. thaiensis sp n.; (c) S. singaporensis sp. n. Head, dorsal of (d) S. chinensis; (e) S. thaiensis; (f) S. singaporensis. Noted that S. thaiensis and sp. n. Head, dorsal of (d) S. chinensis; (e) S. thaiensis; (f) S. singaporensis. Noted that S. thaiensis and S. singaporensis have deep face sculptures. Scale bars on the stacked images are 250 m. S. singaporensis have deep face sculptures. Scale bars on the stacked images are 250 μm. Figure 6. Mesosoma, dorsal view of (a) Sycoscapter chinensis sp. n.; (b) S. thaiensis sp n.; and (c) S. Figure 6. Mesosoma, dorsal view of (a) Sycoscapter chinensis sp. n.; (b) S. thaiensis sp. n.; and singaporensis sp. n. Noted that S. singaporensis has body color of metallic green with blue reflection. (c) S. singaporensis sp. n. Noted that S. singaporensis has body color of metallic green with blue Scale bars represent 250 μm. reflection. Scale bars represent 250 m. Sycoscapter thaiensis Yu sp. n. Head. Width 0.4–0.6 mm. Eye longer than gena. Antenna inserted at the bottom line (Figures 5b,e and 6b) of compound eye. Toruli approach, distance between toruli smaller than diameter of one Distribution: Thailand. torulus. Funicular segments slightly longer than wide. Face sculpture deep. Epistomal Types: Holotype, ♀, THAILAND: Mueang Chiang Mai, 18°48′32.4″ N, 98°54′50.4″ E, margin protruded. 3 July 2014, H. Yu. Paratypes, 4♀, same locality and data as holotype. Mesosoma. Length 1.3–1.7 mm. Wing length 1.3–1.5 mm and finely pubescent. Description: Female. Color and Size. Body length 1.7–2.1 mm. Body color metallic Metasoma. Length 1.4–1.6 mm. Without petiole. Ovipositor sheath length 3.5 longer green with brownish reflection. Head and antennae metallic green. Mesosoma and meta- than body. soma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.7–2.0 mm. Male. Unknown. Head. Width 0.4–0.6 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture deep. Epistomal margin protruded. Mesosoma. Length 1.3–1.7 mm. Wing length 1.3–1.5 mm and finely pubescent. Metasoma. Length 1.4–1.6 mm. Without petiole. Ovipositor sheath length 3.5× longer than body. Male. Unknown. Etymology: Named after Thailand. Sycoscapter singaporensis Yu sp. n. (Figures 5c,f and 6c) Distribution: Singapore. Types: Holotype, ♀, SINGAPORE: Tanglin, 1°18′43.2″ N, 103°48′57.6″ E, 19 August 2013, H. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.8–2.0 mm. Body color metallic green with blue reflection. Head and antennae metallic green. Mesosoma and metasoma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.8–2.2 mm. Head. Width 0.4–0.6 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture deep. Epistomal margin protruded. Mesosoma. Length 1.4–1.6 mm. Wing length 1.3–1.5 mm and finely pubescent. Metasoma. Length 1.4–1.5 mm. Without petiole. Ovipositor sheath length 4× longer than body. Male. Unknown. Biology 2022, 11, 801 9 of 12 Etymology: Named after Thailand. Sycoscapter singaporensis Yu sp. n. (Figure 5c,f and Figure 6c) Distribution: Singapore. 0  0 Types: Holotype, , SINGAPORE: Tanglin, 1 18 43.2” N, 103 48 57.6” E, 19 August 2013, H. Yu. Paratypes, 4 , same locality and data as holotype. Description: Female. Color and Size. Body length 1.8–2.0 mm. Body color metallic green with blue reflection. Head and antennae metallic green. Mesosoma and metasoma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.8–2.2 mm. Head. Width 0.4–0.6 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture deep. Epistomal margin protruded. Mesosoma. Length 1.4–1.6 mm. Wing length 1.3–1.5 mm and finely pubescent. Metasoma. Length 1.4–1.5 mm. Without petiole. Ovipositor sheath length 4 longer than body. Male. Unknown. Etymology: Named after Singapore. 3.4. Diagnoses of Female Sycoryctine Species Associated with Ficus Hirta The female of Philotrypesis guangdongensis is morphologically similar to P. yunnanensis and P. fujianensis; however, its toruli located slightly below the bottom line of compound eyes. The mouthpart of P. fujianensis is longer than F. guangdongensis and F. yunnanensis and it extended just below the central of the compound eyes. The black band of P. yunnanensis on scutellum is indistinct compared to P. guangdongensis and P. fujianensis, P. yunnanensis also has a non-bifurcated line on its mesoscutum. Both the females belong to the genus Sycoryctes and Sycoscapter have metallic green body color and a relatively long ovispositor; however, the knob of Sycoryctes on stigmal vein does not produce downward. Sycoscapter chinensis does not has deep face sculpture and an acute epistomal margin projection compared to S. thaiensis and S. singaporensis. 3.5. Key to Female Sycoryctine Species Associated with Ficus Hirta 1a. Toruli apart; gastral tail consists of two last tergites, ovipositor and its sheaths; stigmal vein without knob; body non-metallic gloss (Genus Philotrypesis Forster) . . . . . . . . . 2 1b. Toruli approach and located above the bottom line of compound eyes; gastral tail consists of a last tergites, ovipositor and its sheaths; stigmal vein with a knob; body with metallic gloss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 2a. Black band on scutellum indistinct (Figure 1b) . . . . . . . . . . . . . . . . P. yunnanensis sp. n. 2b. Black band on scutellum distinct . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3a. Toruli located below the bottom line of compound eyes (Figure 2a); black band on mesoscutum bifurcation (Figure 1d) . . . . . . . . . . . . . . . . . . . . . P. guangdongensis sp. n. 3b. Mouthpart extended below the central of compound eyes (Figure 2f); black band on mesoscutum does not bifurcate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. fujianensis sp. n. 4a. Epistomal margin without acute projection (Figure 4b); knob on stigmal vein does not elongate; wing pilosity strongly reduced . . . . . . . . . . . . . . . . Sycoryctes javaensis sp. n. 4b. Epistomal margin with an acute projection; fore wing with some long robust hairs below the marginal vein (Genus Sycoscapter Saunders) . . . . . . . . . . . . . . . . . . . . . . . . 5 5a. Face without deep sculpture (Figure 5d) . . . . . . . . . . . . . . . . . . . . . . . . S. chinensis sp. n. 5b. Face with deep sculpture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 6a. Metallic green body color with brownish reflection (Figure 6b) . . . . . . S. thaiensis sp. n. 6b. Metallic green body color with blue reflection (Figure 6c) . . . . . . . S. singaporensis sp. n. Biology 2022, 11, 801 10 of 12 4. Discussion This study confirmed that the dioecious F. hirta inhabiting Southeast Asia is associated with at least seven morphologically distinct sycoryctine fig wasp species. The seven syco- ryctine species associated with F. hirta can be distinguished morphologically by antennae, epistomal margin, face sculpture, body-color, and ovipositors. This study shows that the number of non-pollinating species on a dioecious fig tree across many geographical areas is higher than previously thought. The limited number of non-pollinating species is either due to the less sampling effort or may be due to the low dispersal ability of fig wasps in the dioecious fig community, which may promote the diversification of these sycoryctine fig wasps [14]. F. hirta is a shrub widely distributed in the tropics and subtropics from Java in the south to China in the north and westwards into northeast India [19]. It was initially thought to be symbiosis with one pollinating species and two non-pollinating species [20]. However, through our extensive geographical sampling and molecular sequencing analysis, the non- pollinating fig wasps in the genus of Philotrypesis and Sycoscapter, which have initially been considered one species, are divided into four and three species, respectively [14]. These non-pollinators are mainly allopatric distributed. The differences in barcode gaps among them in the same genus are no more than 15.7%. Compared with the same genus in other fig species [5], these species are closely related. Some cases have been found in other broadly distributed fig species, such as F. pumila [21], F. racemosa [22], and F. septica [23]. Those results suggest that fig wasps are more likely to differentiate into new species due to their relatively short generation time than their host figs. Although we have found more related species using molecular sequencing in both pollinating and non-pollinating fig wasps across wide geographical distribution within the same fig species [14,24], our identification of these non-pollinating fig wasps showed that they showed significant differentiation in morphology. Non-pollinating fig wasps of F. hirta lay eggs by inserting their long ovipositor through the fig wall. The fig wall within a single fig species varied largely under different environmental conditions [25]. For example, the fig wall thickness of F. hirta at the northern limit of China is thicker than that of south China. Accordingly, the ovipositor length of Philotrypesis fujianensis distributed there is also significantly longer. Exploring the speciation or host switching in the conservative sycoryctine phylogeny is pivotal to understanding the biological variability of non-pollinating fig wasps in the Old World. It is noteworthy that maritime Southeast Asia comprises thousands of tropical, segregated islands. The species richness across these habitats is consistently underesti- mated [26]. F. hirta is also distributed on some surrounding islands, such as Kalimantan. We may find more species if we identified the samples of non-pollinating fig wasps from more islands. Hence, additional sampling is necessary to establish a solid reference for further comparative studies, especially within mainland and maritime Southeast Asia. Author Contributions: Conceptualization, D.-M.W. and H.Y.; Data curation, D.-M.W. and H.Y.; Formal analysis, D.-M.W. and S.F.; Methodology, D.-M.W. and H.Y.; Validation, D.-M.W., S.F. and H.Y.; Writing—original draft, D.-M.W.; Writing—review and editing, D.-M.W., S.F. and H.Y. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by the Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0408), the Provincial Natural Science Foundation of Guangdong (Grant no. 20140500001306), the National Natural Science Foundation of China (Grant no. 31633008; 31971568; 32150410364), and the Chinese Academy of Sciences PIFI Fellowship for Visiting Scientists (2022VBA0002). Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: Not applicable. Biology 2022, 11, 801 11 of 12 Acknowledgments: The authors thank Po-An Chou from National Chung Hsing University for his valuable suggestion and discussion. The authors also thank Guangyi Dai and Xiaoying Hu from South China Botanical Garden for their professionally technical support. Conflicts of Interest: The authors declare no conflict of interest. References 1. Cook, J.M.; Rasplus, J.-Y. Mutualists with attitude: Coevolving fig wasps and figs. Trends Ecol. Evol. 2003, 18, 241–248. [CrossRef] 2. Jousselin, E.; Van Noort, S.; Greeff, J.M. Labile male morphology and intraspecific male polymorphism in the Philotrypesis fig wasps. Mol. Phylogenetics Evol. 2004, 33, 706–718. [CrossRef] [PubMed] 3. Hawkins, B.A.; Compton, S.G. African fig wasp communities: Undersaturation and latitudinal gradients in species richness. J. Anim. Ecol. 1992, 61, 361–372. Available online: https://www.jstor.org/stable/5328 (accessed on 9 July 2021). [CrossRef] 4. Van Noort, S.; Rasplus, J. 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Low sampling effort and high genetic isolation contribute to under-documented diversity in Philippine fig wasps. Philipp. J. Sci. 2020, 150, 173–180. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Biology Multidisciplinary Digital Publishing Institute

Seven Sycoryctine Fig Wasp Species (Chalcidoidea: Pteromalidae) Associated with Dioecious Ficus hirta Inhabiting South China and Southeast Asia

Wong, Da-Mien; Fan, Songle; Yu, Hui
Biology , Volume 11 (6) – May 24, 2022
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10.3390/biology11060801
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biology Article Seven Sycoryctine Fig Wasp Species (Chalcidoidea: Pteromalidae) Associated with Dioecious Ficus hirta Inhabiting South China and Southeast Asia 1 , 2 , 3 1 , 2 , 3 1 , 2 , 3 , Da-Mien Wong , Songle Fan and Hui Yu * Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China; dmwong87@gmail.com (D.-M.W.); fansongle@scbg.ac.cn (S.F.) Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China Guangdong Provincial Key Laboratory of Digital Botanical Garden, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China * Correspondence: yuhui@scib.ac.cn Simple Summary: The non-pollinating fig wasps are essential components of fig wasp communities, negatively impacting mutualism. However, this group of fig wasps has received less taxonomic attention than pollinating fig wasps. This study presents seven new non-pollinating fig wasp species associated with Ficus hirta fig trees inhabiting South China and Southeast Asia. The presence of a long ovipositor sheath characterizes this group of fig wasps. An identification key is provided to distinguish between them, and the relationships with their host fig trees are discussed. The type specimens and examined materials are deposited in the South China Botanical Garden, Chinese Academy of Sciences, China. Abstract: Even though non-pollinating fig wasps are essential components in tropical and subtropical Citation: Wong, D.-M.; Fan, S.; Yu, H. habitats, yet they are poorly described in the Oriental communities. This study presented seven Seven Sycoryctine Fig Wasp Species new sycoryctine fig wasp species associated with Ficus hirta fig trees inhabiting South China and (Chalcidoidea: Pteromalidae) Southeast Asia. These new sycoryctine species belong to the genera Philotrypesis, Sycoryctes, and Associated with Dioecious Ficus hirta Sycoscapter. They can be easily distinguished by their adaptive morphologies such as face sculpture, Inhabiting South China and body-color, and ovipositors. An identification key is provided to differentiate between them, and Southeast Asia. Biology 2022, 11, 801. the relationships with their host fig trees are also discussed. The holotypes and paratypes are both https://doi.org/10.3390/ deposited in the South China Botanical Garden, Chinese Academy of Sciences, China. biology11060801 Academic Editor: Natraj Krishnan Keywords: inquilines; Indomalaya; non-pollinating fig wasps; parasitoids; Sycoryctinae Received: 1 May 2022 Accepted: 18 May 2022 Published: 24 May 2022 1. Introduction Publisher’s Note: MDPI stays neutral Fig wasps are exciting for ecological and evolutionary studies, particularly their with regard to jurisdictional claims in adaptive morphologies and co-speciation with their host fig trees [1,2]. Despite most of the published maps and institutional affil- early accounts of fig wasp focusing on pollinating species, there can be up to 30 diverse iations. non-pollinating species associated with a single host fig tree [3]. Although these tiny hymenopterans could play an important role in tropical- and sub-tropical ecology, the non-pollinating fig wasps are still poorly described in the Oriental realm [4]. Copyright: © 2022 by the authors. Sycoryctine fig wasps (Chalcidoidea: Pteromalidae) are non-pollinators of fig trees. Licensee MDPI, Basel, Switzerland. The taxonomy of sycoryctines has changed over the past ten years, and their phylogeny is This article is an open access article currently more defined due to the advancement of molecular techniques [5,6]. These fig distributed under the terms and wasps belong to the subfamily Sycoryctinae and are highly diversified and geographically conditions of the Creative Commons widespread [5]. Sycoryctines are associated with all six subgenera and at least 15 sections Attribution (CC BY) license (https:// in Ficus [7]. Surprisingly, an estimated 826 species (2.7 species per Ficus) are waiting creativecommons.org/licenses/by/ to be discovered in the Old World [5]. Two sycoryctine species have been described 4.0/). Biology 2022, 11, 801. https://doi.org/10.3390/biology11060801 https://www.mdpi.com/journal/biology Biology 2022, 11, 801 2 of 12 recently in Taiwan [8] and India [9], and hopefully more Oriental sycoryctines are going to be described. Sycoryctinae is currently divided into four tribes: (1) Apocryptini, comprising two genera: Apocrypta Coquerel, and Bouceka Kocak and Kemal; (2) Critogastrini, comprising only one genus: Critogaster Mayr; (3) Philotrypesini, comprising four genera: Dobunabaa Boucek, Philoverdance Priyadarsanan, Philotrypesis Forster, and Watshamiella Wiebes; and (4) Sycoryctini, comprising seven genera: Adiyodiella Priyadarsanan, Arachonia Joseph, Parasycobia Abdurahiman and Joseph, Sycorycteridea Abdurahiman and Joseph, Sycoryctes Mayr, Sycoscapter Saunders, and Sycoscapteridea Ashmead [5,10]. The sycoryctine fig wasps are considered host specificity conservatisms which originated about 49–64 million years ago [5]. The sycoryctine species are also believed to impact the fig–fig wasp mutualism significantly [11]. Female sycoryctines have remarkable long ovipositors that can penetrate the fig wall. They attack flowers containing other fig wasp larvae by consuming the host larvae or starving them by feeding on endosperm [12]. Their complicated trophic relationships make sycoryctines the ideal study species for the population dynamics in tropical and sub-tropical habitats [13]. A recent molecular study showed eight allopatric sycoryctine species associated with Ficus hirta Vahl in South China and Southeast Asia. The marked barcoding gaps ranged from 7.2% to 15.7% for the Cytb gene sequence in the same genus [14]. However, the morphological traits of these species remain unknown. This study compared their morphology and reported seven new species belonging to the genera Philotrypesis, Sycoryctes, and Sycoscapter. An identification key is provided to distinguish between them, and the relationships with their host fig trees are discussed. Like the non-pollinating fig wasps, sycoryctines often receive less research attention in the symbiosis of figs and fig wasps. Hence, this study is concerned with the taxonomy of the geographically widespread sycoryctine fig wasps associated with F. hirta. Our research and results provide new insights into the morphology and adaptation of these non-pollinating fig wasps. It contributes to our understanding of speciation and biodiversity in the Oriental fig–fig wasp communities. 2. Materials and Methods The specimens of sycoryctine fig wasps associated with F. hirta were collected in 23 sampling sites for Philotrypesis, 15 sites for Sycoscapter, and two sites for Sycoryctes during the years 2010 to 2018 are distributed from South China to Java (Table 1). The distribution of the species in each genus is allopatric except for two sites with two species in each genus co-occurred, QMS in Thailand and XI in China (Table 1). When figs close to ripening were dissected, the wasps emitted therein were collected. Two to twenty-four wasps in each site with one wasp exited from one natal fig were collected and stored in 75% ethanol. Later, the wasps were dehydrated through an ethanol series (80%, 90%, and 100%) and critical-point dried (LEICA EM CPD300, Leica Microsystems GmbH, Wetzlar, Germany) before being mounted on cards following Noyes (1982) [15]. Each photo was taken using a digital camera connected to a stereomicroscope (LEICA M205 FA, Leica Microsystem GmbH, Wetzlar, Germany). The images were processed using LAS X 3.08.19082 software to create a stacked image with increased focal depth [16]. Physical characteristics were measured using ImageJ 1.8.0_172 software (National Institutes of Health, Bethesda, MD, USA). Specimen measurements were taken with an accuracy of 0.001 mm and rounded to the nearest 0.01 mm. Specimens were mounted on brass stubs and sputter-coated with gold (LEICA EM ACE600, Leica Microsystem GmbH, Germany) before the observation and photographed using SEM (JEOL JSM-6360LV, JEOL Ltd., Tokyo, Japan). Morphological terminology follows Gibson (1997) and the Hymenoptera Anatomy Ontology (HAO) Portal [17,18]. The holotypes and a group of paratypes are deposited in the Plant Science Center, South China 0  0 Botanical Garden, Chinese Academy of Sciences (23 10 48” N; 113 21 8” E). Biology 2022, 11, 801 3 of 12 Table 1. Sampling sites for sycoryctine fig wasps associated with Ficus hirta. Wasp Species Country Site Latitude, Longitude Philotrypesis guangdongensis China Gui 25.077, 110.306 Huo 23.170, 113.373 DHS 23.166, 112.543 Xiang 22.424, 114.306 Nan 22.787, 108.389 Ding 19.697, 110.328 Wan 18.795, 110.391 Thailand QMS 18.809, 98.914 CH 12.774, 102.096 Wu 14.443, 105.273 HB 12.999, 108.230 ST 7.467, 99.639 P. yunnanensis China Sand 25.984, 107.874 XI 21.913, 101.264 Thailand QMS 18.809, 98.914 Tai 18.894, 98.858 CS 18.84, 99.47 P. fujianensis China Ning 26.664, 119.549 Sha 26.419, 117.818 Xia 24.742, 118.072 Sui 26.476, 114.239 Da 24.258, 116.806 Sycoryctes javaensis Indonesia CI 6.566, 106.706 JA 6.368, 106.830 Sycoscapter chinensis China Gui 25.077, 110.306 Huo 23.170, 113.373 DHS 23.166, 112.543 Xiang 22.424, 114.306 Sand 25.984, 107.874 Nan 22.787, 108.389 Ding 19.697, 110.328 Wan 18.795, 110.391 XI 21.913, 101.264 S. thaiensis Thailand CH 12.774, 102.096 Wu 14.443, 105.273 Tai 18.894, 98.858 CS 18.84, 99.47 QMS 18.809, 98.914 S. singaporensis Singapore SNP 1.312, 103.816 3. Results 3.1. Philotrypesis Forster, 1878 3.1.1. Philotrypesis Forster, 1878: 153–187. Type Species: Philotrypesis Longicaudata Mayr, 1906 Diagnosis: The female of this genus can be recognized by its lengthened seventh and eighth urotergites and its subquadrate pronotum. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Philotrypesis fig wasp species are known from Afrotropical realm: Eritrea, Guinea, Sierra Leone, South Africa, Zambia, Zimbabwe; Australasian realm: Australia, Indonesia; Nearctic realm: United States; Oriental realm: Indonesia, Japan, Mainland China, Malaysia, Philippines, Sri Lanka, Taiwan, Vietnam; and Palearctic realm: France, Israel, Italy. All described Philotrypesis fig wasp species are parasitoids or inquilines of other fig wasps associated with sections Conosycea, Ficus, Galoglychia, Sycidium, Sycocarpus, and Urostigma fig trees. The recorded host fig wasps of Philotrypesis included Blastophaga psenes Linnaeus, Ceratosolen dentifer Wiebes, Ceratosolen notus Baker, Ceratosolen solmsi Mayr, Eupristina verticillata Waterston, Kradibia brownii Ashmead, Kradibia gestroi Grandi, and Platyscapa quadraticeps Mayr. Biology 2022, 11, 801 4 of 12 Biology 2022, 11, x FOR PEER REVIEW 5 of 12 Philotrypesis guangdongensis Yu sp. n. (Figure 1a,d, Figure 2a,d and Figure 3a,d) Biology 2022, 11, x FOR PEER REVIEW 5 of 12 Figure 1. Habitus lateral of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp n.; (c) P. fu- Figure 1. Habitus lateral of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp. n.; (c) P. fu- jianensis sp. n. Mesosoma, dorsal view of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. Figure 1. Habitus lateral of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp n.; (c) P. fu- jianensis sp. n. Mesosoma, dorsal view of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. Noji ted that anensis sp. the n. blac Mes k band of osoma, doP. rsal yun vie nane w of ns (d is ) P on s . guangdonge cutellum ns is i is; ndi (e) P. stinct yun.nane Scal ne sis bars ; (f) P repr . fujies anen ent 250 sis. μm. Noted that the black band of P. yunnanensis on scutellum is indistinct. Scale bars represent 250 m. Noted that the black band of P. yunnanensis on scutellum is indistinct. Scale bars represent 250 μm. Figure 2. Head, dorsal view of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp n.; (c) P. Figure 2. Head, dorsal view of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp. n.; fujianensis sp. n. Head, ventral view of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. (c) P. fujianensis sp. n. Head, ventral view of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. Figure Noted 2. that Heathe d, do toru rsa li l of vie P.w gua ongdonge f (a) Philotrypes nsis are lois cat guangdonge ed below the nsis botto sp. m n. li;ne (b of comp ) P. yun oun nanens d eyes, is sp and n.; (c) P. the mouthpart of P. fujianensis extended below to the central of compound eyes. Noted fujianen that sis sp. the n. torHead, uli of P ventral . guangdongensis view of (ar d) eP. located guangdonge below ns the is; bottom (e) P. yun line nanen of compound sis; (f) P. fujia eyes, nens and is. Noted that the toruli of P. guangdongensis are located below the bottom line of compound eyes, and the mouthpart of P. fujianensis extended below to the central of compound eyes. the mouthpart of P. fujianensis extended below to the central of compound eyes. Biology 2022, 11, 801 5 of 12 Biology 2022, 11, x FOR PEER REVIEW 6 of 12 Figure 3. Mesosoma, dorsal view of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp n.; Figure 3. Mesosoma, dorsal view of (a) Philotrypesis guangdongensis sp. n.; (b) P. yunnanensis sp. n.; (c) P. fujianensis sp. n. Hind leg of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. (c) P. fujianensis sp. n. Hind leg of (d) P. guangdongensis; (e) P. yunnanensis; (f) P. fujianensis. Philotrypesis yunnanensisYu sp. n. Distribution: China (Guangdong, Guangxi, Hainan provinces, and Hong Kong SAR), (Figures 1b,e, 2b,e, and 3b,e) Thailand, Vietnam. Distribution: China (Guizhou and Yunnan Provinces), Thailand. 0  0 Types: Holotype, , CHINA: Guangzhou, 23 10 12.0” N, 113 22 22.8” E, 27 November 2015, Types: Holotype, ♀, CHINA: Yunnan, 21°26′49.2″ N, 101°34′04.8″ E, 4 July 2013, H. H. Yu. Paratypes, 4 , same locality and data as holotype. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.9–2.1 mm. Body color yellowish Description: Female. Color and Size. Body length 1.9–2.1 mm. Body color yellowish orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Ovipositor sheath length 2.5–3.0 mm. Ovipositor sheath length 2.5–2.9 mm. Head. Width 0.4–0.5 mm. Eye longer than gena. Antenna inserted below the bottom Head. Width 0.3–0.4 mm. Eye longer than gena. Antenna inserted below the bottom line of compound eye. Toruli apart, distance between toruli larger than diameter of one line of compound eye. Toruli apart, distance between toruli larger than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin flattened. margin flattened. Mesosoma. Length 2.0–2.2 mm. Wing length 1.3–1.5 mm and finely pubescent. Black Mesosoma. Length 2.0–2.2 mm. Wing length 1.3–1.4 mm and finely pubescent. Black band on scutellum distinct; black band on mesoscutum bifurcation. band on scutellum indistinct; black band on mesoscutum straight. Metasoma. Length 1.8–2.0 mm. Without petiole. Ovipositor sheath length 2 longer Metasoma. Length 1.6–2.0 mm. Without petiole. Ovipositor sheath length 2× longer than body. than body. Male. Unknown. Male. Unknown. Etymology: Named after the Guangdong province of China. Etymology: Named after the Yunnan province of China. Philotrypesis yunnanensis Yu sp. n. Philotrypesis fujianensis Yu sp. n. (Figure 1b,e, Figure 2b,e and Figure 3b,e) (Figures 1c,f, 2c,f and 3c,f) Distribution: China (Guizhou and Yunnan Provinces), Thailand. Distribution: China (Fujian, Guangdong, and Jiangxi Provinces). 0  0 Types: Holotype, , CHINA: Yunnan, 21 26 49.2” N, 101 34 04.8” E, 4 July 2013, H. Yu. Types: Holotype, ♀, CHINA: Fujian, 26°39′50.4″ N, 119°32′56.4″ E, 24 January 2016, Paratypes, 4 , same locality and data as holotype. H. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.9–2.1 mm. Body color yellowish Description: Female. Color and Size. Body length 1.9–2.3 mm. Body color yellowish orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Ovipositor sheath length 2.5–2.9 mm. Biology 2022, 11, 801 6 of 12 Head. Width 0.3–0.4 mm. Eye longer than gena. Antenna inserted below the bottom line of compound eye. Toruli apart, distance between toruli larger than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin flattened. Mesosoma. Length 2.0–2.2 mm. Wing length 1.3–1.4 mm and finely pubescent. Black band on scutellum indistinct; black band on mesoscutum straight. Metasoma. Length 1.6–2.0 mm. Without petiole. Ovipositor sheath length 2 longer than body. Male. Unknown. Etymology: Named after the Yunnan province of China. Philotrypesis fujianensis Yu sp. n. (Figure 1c,f, Figure 2c,f and Figure 3c,f) Distribution: China (Fujian, Guangdong, and Jiangxi Provinces). 0  0 Types: Holotype, , CHINA: Fujian, 26 39 50.4” N, 119 32 56.4” E, 24 January 2016, H. Yu. Paratypes, 4 , same locality and data as holotype. Description: Female. Color and Size. Body length 1.9–2.3 mm. Body color yellowish orange. Head and antennae orange. Mesosoma and metasoma usually yellowish orange. Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Ovipositor sheath length 2.6–2.9 mm. Head. Width 0.4–0.8 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli apart, distance between toruli larger than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin flattened. Mesosoma. Length 2.0–2.4 mm. Wing length 1.3–1.5 mm and finely pubescent. Black band on scutellum distinct; black band on mesoscutum straight. Metasoma. Length 1.8–2.1 mm. Without petiole. Ovipositor sheath length 1.5 longer than body. Male. Unknown. Etymology: Named after the Fujian province of China. 3.2. Sycoryctes Mayr, 1885 3.2.1. Sycoryctes Mayr, 1885: 153–187. Type Species: Sycoryctes Patellaris Mayr, 1885 Diagnosis: Stigmal knob not produced downwards. Dorso-apical spine on basitarsus short, not reaching end of second segment. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Sycoryctes fig wasp species are mainly known from the Afrotropical, Australasian, and Oriental realms. All described Sycoryctes fig wasp species are parasitoids or inquilines of other fig wasps. Sycoryctes javaensis Yu sp. n. (Figure 4) Distribution: Indonesia. 0  0 Types: Holotype, , INDONESIA: Java, 6 22 04.8”S, 106 49 48.0”E, 3 MAY 2014, H. Yu. Paratypes, 4 , same locality and data as holotype. Description: Female. Color and Size. Body length 1.2–1.6 mm. Body color metallic green with brownish reflection. Head and antennae metallic green. Mesosoma and meta- soma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.6–2.0 mm. Head. Width 0.2–0.5 mm. Eye longer than gena. Antenna inserted above the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin slightly protruded. Mesosoma. Length 1.1–1.5 mm. Wing length 1.2–1.4 mm and finely pubescent. Biology 2022, 11, x FOR PEER REVIEW 7 of 12 Coxae concolorous with mesosoma. Wings hyaline. The 7th and 8th segment in ratio 4:1. Ovipositor sheath length 2.6–2.9 mm. Head. Width 0.4–0.8 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli apart, distance between toruli larger than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin flattened. Mesosoma. Length 2.0–2.4 mm. Wing length 1.3–1.5 mm and finely pubescent. Black band on scutellum distinct; black band on mesoscutum straight. Metasoma. Length 1.8–2.1 mm. Without petiole. Ovipositor sheath length 1.5× longer than body. Male. Unknown. Etymology: Named after the Fujian province of China. 3.2. Sycoryctes Mayr, 1885 Sycoryctes Mayr, 1885: 153–187. Type Species: Sycoryctes Patellaris Mayr, 1885 Diagnosis: Stigmal knob not produced downwards. Dorso-apical spine on basitarsus short, not reaching end of second segment. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Sycoryctes fig wasp species are mainly known from the Afrotropical, Australasian, and Oriental realms. All described Sycoryctes fig wasp species are parasitoids or inquilines of other fig wasps. Sycoryctes javaensis Yu sp. n. (Figure 4) Distribution: Indonesia. Types: Holotype, ♀, INDONESIA: Java, 6°22′04.8″S, 106°49′48.0″E, 3 MAY 2014, H. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.2–1.6 mm. Body color metallic green with brownish reflection. Head and antennae metallic green. Mesosoma and meta- soma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.6–2.0 mm. Head. Width 0.2–0.5 mm. Eye longer than gena. Antenna inserted above the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of Biology 2022, 11, 801 7 of 12 one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epis- tomal margin slightly protruded. Mesosoma. Length 1.1–1.5 mm. Wing length 1.2–1.4 mm and finely pubescent. Metasoma. Length 1.0–1.4 mm. Without petiole. Ovipositor sheath length 3 longer Metasoma. Length 1.0–1.4 mm. Without petiole. Ovipositor sheath length 3× longer than body. than body. Male. Male. Unknown. Unknown. Etymology: Named after the Java Island of Indonesia. Etymology: Named after the Java Island of Indonesia. Figure 4. Sycoryctes javaensis sp. n. in (a) habitus lateral view; (b) head dorsal view; and (c) mesosoma Figure 4. Sycoryctes javaensis sp. n. in (a) habitus lateral view; (b) head dorsal view; and (c) mesosoma dorsal view. Scale bars on the stacked images are 250 μm. dorsal view. Scale bars on the stacked images are 250 m. 3.3. Sycoscapter Saunders, 1883 3.3.1. Sycoscapter Saunders, 1883: 29–47. Type Species: Sycoscapter Insignis Saunders, 1883 Diagnosis: Stigmal knob not produced downwards. Funicular segments symmetric. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Sycoscapter fig wasp species are mainly known from the Afrotropical, Australasian, and Oriental realms. All described Sycoscapter fig wasp species are parasitoids of other fig wasps. The recorded host fig wasps of Sycoscapter included Ceratosolen dentifer Wiebes, Eupristina delhiensis Abdurahiman and Joseph, Eupristina verticillata Waterston, and Kradibia gestroi Grandi. Sycoscapter chinensis Yu sp. n. (Figure 5a,b and Figure 6a) Distribution: China (Guangdong, Guangxi, Guizhou, Hainan, Yunnan Provinces, and Hong Kong SAR). 0  0 Types: Holotype, , CHINA: Guangzhou, 23 10 12.0” N, 113 22 22.8” E, 27 November 2015, H. Yu. Paratypes, 4 , same locality and data as holotype. Description: Female. Color and Size. Body length 1.6–2.0 mm. Body color metallic green. Head and antennae metallic green. Mesosoma and metasoma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.6–2.0 mm. Head. Width 0.3–0.5 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal margin slightly protruded. Mesosoma. Length 1.2–1.7 mm. Wing length 1.3–1.7 mm and finely pubescent. Metasoma. Length 1.2–1.6 mm. Without petiole. Ovipositor sheath length 3.5 longer than body. Male. Unknown. Etymology: Named after China. Sycoscapter thaiensis Yu sp. n. (Figure 5b,e and Figure 6b) Distribution: Thailand. 0  0 Types: Holotype, , THAILAND: Mueang Chiang Mai, 18 48 32.4” N, 98 54 50.4” E, 3 July 2014, H. Yu. Paratypes, 4 , same locality and data as holotype. Biology 2022, 11, x FOR PEER REVIEW 8 of 12 3.3. Sycoscapter Saunders, 1883 Sycoscapter Saunders, 1883: 29–47. Type Species: Sycoscapter Insignis Saunders, 1883 Diagnosis: Stigmal knob not produced downwards. Funicular segments symmetric. Distribution and host relationships (from www.figweb.org, accessed on 9 July 2021): Sycoscapter fig wasp species are mainly known from the Afrotropical, Australasian, and Oriental realms. All described Sycoscapter fig wasp species are parasitoids of other fig wasps. The recorded host fig wasps of Sycoscapter included Ceratosolen dentifer Wiebes, Eupristina delhiensis Abdurahiman and Joseph, Eupristina verticillata Waterston, and Kra- dibia gestroi Grandi. Sycoscapter chinensis Yu sp. n. (Figures 5a,b and 6a) Distribution: China (Guangdong, Guangxi, Guizhou, Hainan, Yunnan Provinces, and Hong Kong SAR). Types: Holotype, ♀, CHINA: Guangzhou, 23°10′12.0″ N, 113°22′22.8″ E, 27 Novem- ber 2015, H. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.6–2.0 mm. Body color metallic green. Head and antennae metallic green. Mesosoma and metasoma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.6–2.0 mm. Head. Width 0.3–0.5 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture smooth. Epistomal Biology 2022, 11, 801 8 of 12 margin slightly protruded. Mesosoma. Length 1.2–1.7 mm. Wing length 1.3–1.7 mm and finely pubescent. Metasoma. Length 1.2–1.6 mm. Without petiole. Ovipositor sheath length 3.5× longer Description: Female. Color and Size. Body length 1.7–2.1 mm. Body color metallic than body. green with brownish reflection. Head and antennae metallic green. Mesosoma and meta- Male. Unknown. soma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.7–2.0 mm. Etymology: Named after China. Biology 2022, 11, x FOR PEER REVIEW 9 of 12 Figure 5. Habitus lateral view of (a) Sycoscapter chinensis sp. n.; (b) S. thaiensis sp. n.; (c) S. singaporensis Figure 5. Habitus lateral view of (a) Sycoscapter chinensis sp. n.; (b) S. thaiensis sp n.; (c) S. singaporensis sp. n. Head, dorsal of (d) S. chinensis; (e) S. thaiensis; (f) S. singaporensis. Noted that S. thaiensis and sp. n. Head, dorsal of (d) S. chinensis; (e) S. thaiensis; (f) S. singaporensis. Noted that S. thaiensis and S. singaporensis have deep face sculptures. Scale bars on the stacked images are 250 m. S. singaporensis have deep face sculptures. Scale bars on the stacked images are 250 μm. Figure 6. Mesosoma, dorsal view of (a) Sycoscapter chinensis sp. n.; (b) S. thaiensis sp n.; and (c) S. Figure 6. Mesosoma, dorsal view of (a) Sycoscapter chinensis sp. n.; (b) S. thaiensis sp. n.; and singaporensis sp. n. Noted that S. singaporensis has body color of metallic green with blue reflection. (c) S. singaporensis sp. n. Noted that S. singaporensis has body color of metallic green with blue Scale bars represent 250 μm. reflection. Scale bars represent 250 m. Sycoscapter thaiensis Yu sp. n. Head. Width 0.4–0.6 mm. Eye longer than gena. Antenna inserted at the bottom line (Figures 5b,e and 6b) of compound eye. Toruli approach, distance between toruli smaller than diameter of one Distribution: Thailand. torulus. Funicular segments slightly longer than wide. Face sculpture deep. Epistomal Types: Holotype, ♀, THAILAND: Mueang Chiang Mai, 18°48′32.4″ N, 98°54′50.4″ E, margin protruded. 3 July 2014, H. Yu. Paratypes, 4♀, same locality and data as holotype. Mesosoma. Length 1.3–1.7 mm. Wing length 1.3–1.5 mm and finely pubescent. Description: Female. Color and Size. Body length 1.7–2.1 mm. Body color metallic Metasoma. Length 1.4–1.6 mm. Without petiole. Ovipositor sheath length 3.5 longer green with brownish reflection. Head and antennae metallic green. Mesosoma and meta- than body. soma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.7–2.0 mm. Male. Unknown. Head. Width 0.4–0.6 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture deep. Epistomal margin protruded. Mesosoma. Length 1.3–1.7 mm. Wing length 1.3–1.5 mm and finely pubescent. Metasoma. Length 1.4–1.6 mm. Without petiole. Ovipositor sheath length 3.5× longer than body. Male. Unknown. Etymology: Named after Thailand. Sycoscapter singaporensis Yu sp. n. (Figures 5c,f and 6c) Distribution: Singapore. Types: Holotype, ♀, SINGAPORE: Tanglin, 1°18′43.2″ N, 103°48′57.6″ E, 19 August 2013, H. Yu. Paratypes, 4♀, same locality and data as holotype. Description: Female. Color and Size. Body length 1.8–2.0 mm. Body color metallic green with blue reflection. Head and antennae metallic green. Mesosoma and metasoma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.8–2.2 mm. Head. Width 0.4–0.6 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture deep. Epistomal margin protruded. Mesosoma. Length 1.4–1.6 mm. Wing length 1.3–1.5 mm and finely pubescent. Metasoma. Length 1.4–1.5 mm. Without petiole. Ovipositor sheath length 4× longer than body. Male. Unknown. Biology 2022, 11, 801 9 of 12 Etymology: Named after Thailand. Sycoscapter singaporensis Yu sp. n. (Figure 5c,f and Figure 6c) Distribution: Singapore. 0  0 Types: Holotype, , SINGAPORE: Tanglin, 1 18 43.2” N, 103 48 57.6” E, 19 August 2013, H. Yu. Paratypes, 4 , same locality and data as holotype. Description: Female. Color and Size. Body length 1.8–2.0 mm. Body color metallic green with blue reflection. Head and antennae metallic green. Mesosoma and metasoma metallic green. Coxae yellow. Wings hyaline. Ovipositor sheath length 1.8–2.2 mm. Head. Width 0.4–0.6 mm. Eye longer than gena. Antenna inserted at the bottom line of compound eye. Toruli approach, distance between toruli smaller than diameter of one torulus. Funicular segments slightly longer than wide. Face sculpture deep. Epistomal margin protruded. Mesosoma. Length 1.4–1.6 mm. Wing length 1.3–1.5 mm and finely pubescent. Metasoma. Length 1.4–1.5 mm. Without petiole. Ovipositor sheath length 4 longer than body. Male. Unknown. Etymology: Named after Singapore. 3.4. Diagnoses of Female Sycoryctine Species Associated with Ficus Hirta The female of Philotrypesis guangdongensis is morphologically similar to P. yunnanensis and P. fujianensis; however, its toruli located slightly below the bottom line of compound eyes. The mouthpart of P. fujianensis is longer than F. guangdongensis and F. yunnanensis and it extended just below the central of the compound eyes. The black band of P. yunnanensis on scutellum is indistinct compared to P. guangdongensis and P. fujianensis, P. yunnanensis also has a non-bifurcated line on its mesoscutum. Both the females belong to the genus Sycoryctes and Sycoscapter have metallic green body color and a relatively long ovispositor; however, the knob of Sycoryctes on stigmal vein does not produce downward. Sycoscapter chinensis does not has deep face sculpture and an acute epistomal margin projection compared to S. thaiensis and S. singaporensis. 3.5. Key to Female Sycoryctine Species Associated with Ficus Hirta 1a. Toruli apart; gastral tail consists of two last tergites, ovipositor and its sheaths; stigmal vein without knob; body non-metallic gloss (Genus Philotrypesis Forster) . . . . . . . . . 2 1b. Toruli approach and located above the bottom line of compound eyes; gastral tail consists of a last tergites, ovipositor and its sheaths; stigmal vein with a knob; body with metallic gloss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 2a. Black band on scutellum indistinct (Figure 1b) . . . . . . . . . . . . . . . . P. yunnanensis sp. n. 2b. Black band on scutellum distinct . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3a. Toruli located below the bottom line of compound eyes (Figure 2a); black band on mesoscutum bifurcation (Figure 1d) . . . . . . . . . . . . . . . . . . . . . P. guangdongensis sp. n. 3b. Mouthpart extended below the central of compound eyes (Figure 2f); black band on mesoscutum does not bifurcate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. fujianensis sp. n. 4a. Epistomal margin without acute projection (Figure 4b); knob on stigmal vein does not elongate; wing pilosity strongly reduced . . . . . . . . . . . . . . . . Sycoryctes javaensis sp. n. 4b. Epistomal margin with an acute projection; fore wing with some long robust hairs below the marginal vein (Genus Sycoscapter Saunders) . . . . . . . . . . . . . . . . . . . . . . . . 5 5a. Face without deep sculpture (Figure 5d) . . . . . . . . . . . . . . . . . . . . . . . . S. chinensis sp. n. 5b. Face with deep sculpture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 6a. Metallic green body color with brownish reflection (Figure 6b) . . . . . . S. thaiensis sp. n. 6b. Metallic green body color with blue reflection (Figure 6c) . . . . . . . S. singaporensis sp. n. Biology 2022, 11, 801 10 of 12 4. Discussion This study confirmed that the dioecious F. hirta inhabiting Southeast Asia is associated with at least seven morphologically distinct sycoryctine fig wasp species. The seven syco- ryctine species associated with F. hirta can be distinguished morphologically by antennae, epistomal margin, face sculpture, body-color, and ovipositors. This study shows that the number of non-pollinating species on a dioecious fig tree across many geographical areas is higher than previously thought. The limited number of non-pollinating species is either due to the less sampling effort or may be due to the low dispersal ability of fig wasps in the dioecious fig community, which may promote the diversification of these sycoryctine fig wasps [14]. F. hirta is a shrub widely distributed in the tropics and subtropics from Java in the south to China in the north and westwards into northeast India [19]. It was initially thought to be symbiosis with one pollinating species and two non-pollinating species [20]. However, through our extensive geographical sampling and molecular sequencing analysis, the non- pollinating fig wasps in the genus of Philotrypesis and Sycoscapter, which have initially been considered one species, are divided into four and three species, respectively [14]. These non-pollinators are mainly allopatric distributed. The differences in barcode gaps among them in the same genus are no more than 15.7%. Compared with the same genus in other fig species [5], these species are closely related. Some cases have been found in other broadly distributed fig species, such as F. pumila [21], F. racemosa [22], and F. septica [23]. Those results suggest that fig wasps are more likely to differentiate into new species due to their relatively short generation time than their host figs. Although we have found more related species using molecular sequencing in both pollinating and non-pollinating fig wasps across wide geographical distribution within the same fig species [14,24], our identification of these non-pollinating fig wasps showed that they showed significant differentiation in morphology. Non-pollinating fig wasps of F. hirta lay eggs by inserting their long ovipositor through the fig wall. The fig wall within a single fig species varied largely under different environmental conditions [25]. For example, the fig wall thickness of F. hirta at the northern limit of China is thicker than that of south China. Accordingly, the ovipositor length of Philotrypesis fujianensis distributed there is also significantly longer. Exploring the speciation or host switching in the conservative sycoryctine phylogeny is pivotal to understanding the biological variability of non-pollinating fig wasps in the Old World. It is noteworthy that maritime Southeast Asia comprises thousands of tropical, segregated islands. The species richness across these habitats is consistently underesti- mated [26]. F. hirta is also distributed on some surrounding islands, such as Kalimantan. We may find more species if we identified the samples of non-pollinating fig wasps from more islands. Hence, additional sampling is necessary to establish a solid reference for further comparative studies, especially within mainland and maritime Southeast Asia. Author Contributions: Conceptualization, D.-M.W. and H.Y.; Data curation, D.-M.W. and H.Y.; Formal analysis, D.-M.W. and S.F.; Methodology, D.-M.W. and H.Y.; Validation, D.-M.W., S.F. and H.Y.; Writing—original draft, D.-M.W.; Writing—review and editing, D.-M.W., S.F. and H.Y. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by the Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0408), the Provincial Natural Science Foundation of Guangdong (Grant no. 20140500001306), the National Natural Science Foundation of China (Grant no. 31633008; 31971568; 32150410364), and the Chinese Academy of Sciences PIFI Fellowship for Visiting Scientists (2022VBA0002). Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: Not applicable. 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Journal

Biology – Multidisciplinary Digital Publishing Institute

Published: May 24, 2022

Keywords: inquilines; Indomalaya; non-pollinating fig wasps; parasitoids; Sycoryctinae

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