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Distinctive but Functionally Convergent Song Phenotypes

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Distinctive but Functionally Convergent Song Phenotypes JOURNAL OF NATURAL HISTORY, 2018 VOL. 52, NOS. 25–26, 1603–1635 https://doi.org/10.1080/00222933.2018.1478011 Distinctive but functionally convergent song phenotypes characterize two new allopatric species of the Chrysoperla carnea-group in Asia, Chrysoperla shahrudensis sp.nov.and Chrysoperla bolti sp.nov.(Neuroptera:Chrysopidae) Charles S. Henrya, Stephen J. Brooksb, James B. Johnsonc, Atsushi Mochizukid, Alinaghi Mirmoayedie and Peter Duellif aEcology and Evolutionary Biology, University of Connecticut, Storrs, CT, USA; bDepartment of Life Sciences, The Natural History Museum, London, UK; cDivision of Entomology, University of Idaho, Moscow, ID, USA; dEntomology Department, Institute for Agro-Environmental Sciences NARO, Tsukuba City, Japan; eDepartment of Plant Protection of Razi University, Kermanshah, Iran; fBiodiversity and Conservation Biology, WSL Swiss Federal Research Institute, Birmensdorf, Switzerland Chrysoperla shahrudensis sp.nov.isdiscoveredinnorthernIran, ARTICLE HISTORY co-occurring with at least five other cryptic species of the Received 29 November 2017 Chrysoperla carnea-group. It is distinguished by the volley period Accepted 9 May 2018 and tonality of its courtship duetting song. Another Asian species KEYWORDS from alpine meadows of northern Kyrgyzstan, previously Convergent evolution; C. ‘adamsi-K’ but here named Chrysoperla bolti sp. nov., has a courtship song; duetting; song distinct from but convergent with both C. shahrudensis and Eurasia; parallel speciation; North American Chrysoperla adamsi. Coordinated duets can be sibling species; systematics; established in the laboratory between individuals of vibration C. shahrudensis and recorded songs of either C. bolti or C. adamsi. Such functional song equivalence in distinct allopatric species suggests that repeated episodes of parallel speciation can drive the origin of cryptic species diversity in lacewings. Morphology, life history, and ecology of larvae and adults of C. shahrudensis and C. bolti are then formally described. Adding C. shahrudensis to a large mitochondrial DNA data set for ≈ 21 species shows it to be similar to neither C. adamsi nor C. bolti, further supporting independent, convergent evolution of song rather than song similarity due to relationship. Although C. bolti and C. shahrudensis are both from Asia and share some basic temporal song features, the two taxa are distinct, allopatric bio- logical species. www.zoobank.org/urn:lsid:zoobank.org:pub:D9B7BDC9-6C09-468B-A6B-D378628EC557 Introduction The green lacewing species Chrysoperla carnea (Stephens) was once thought to be distributed across the entire North Temperate Zone (Tjeder 1960; Tauber and Tauber 1986). However, it is now understood that the original taxon comprises at least 21 distinct but morphologically cryptic sibling species, reproductively isolated from each CONTACT Charles S. Henry [email protected] © 2018 Informa UK Limited, trading as Taylor & Francis Group Published online 29 Jun 2018 1604 C.S. HENRY ET AL. other by complex species-specific, substrate-borne vibrational duetting songs (Henry et al. 2013). These species, collectively assigned to the ‘carnea’ species-group of Chrysoperla (Brooks 1994), generally exhibit large, often extensively overlapping geo- graphic distributions. Throughout its range, each species retains its distinctive courtship signal, including in regions where it might be sympatric or even syntopic with other members of the carnea-group (e.g. compare the song of Chrysoperla agilis Henry et al. in Switzerland, the Azores, or Fairbanks, Alaska – see Henry et al. 2003, 2011). Wherever there is geographic heterogeneity, cryptic species diversity is high in the carnea-group. For example, at least five of the eight carnea-group species recognized in North America are largely syntopic in the far western mountains of that continent (Henry et al. 2013). In Eurasia, the known complement of sibling species is 12 (Henry et al. 2013), and at least five of these at a time can be found living together in close association in mountainous regions (Duelli et al. 2015). Asia is relatively under-collected and its carnea- group fauna is poorly understood (e.g. see Mirmoayedi et al. 2014), except in the south and Far East (Henry et al. 2010, 2015). Recent opportunities to collect in Iran and the Kyrgyz Republic therefore presented a chance to sample the carnea-group from western and central Asia, respectively. The recent trip to Iran included authors P. Duelli and A. Mirmoayedi and their colleague D. Bolt (MTM Consulting, Switzerland) and took place during August 2014. This trip, plus earlier collecting in Iran by Dr H. Heidari (Centre for Sustainable Development, Iran) in July 2002 (Henry et al. 2014), revealed the presence in that country of five described species: Chrysoperla carnea (Stephens), Chrysoperla pallida Henry et al., C. agilis Henry et al., Chrysoperla heidarii Henry et al., and Chrysoperla zastrowi sillemi (Esben-Petersen). Two additional widespread species, Chrysoperla medi- terranea (Hölzel) and Chrysoperla lucasina (Lacroix), occur in nearby Armenia and Georgia (Henry et al. 2014; Duelli et al. 2015) and are probably also present in Iran, although song-confirmed specimens have not yet been found there (but see Mirmoayedi and Thierry 2002, who nevertheless included C. lucasina in the lacewing fauna of Iran based on morphology). Also collected during the 2014 trip were six gravid females of a new ‘song species’ of the carnea-group, from which more than 20 offspring were reared to adulthood. We describe here the external appearance of all life stages of this Iranian species, naming it Chrysoperla shahrudensis sp. nov. for the collecting site of the holotype (Shahrud). Its species-specific vibrational courtship songs and duets are also described for both sexes, including song features that distinguish the taxon from all other cryptic species in the carnea-group. Comparative ecological and song playback observations of C. shahrudensis are included, and its phylogenetic affinities within the carnea-group are inferred using p-distances and branching topology calculated from mitochondrial DNA sequences. Another recent collecting trip of P. Duelli and D. Bolt was to Kyrgyzstan in central Asia during June and July 2016. Three distinct but undescribed song species were collected there, all of which had been found by P. Duelli on a previous trip to that country in May and June, 1995 (Aspöck et al. 1996). One of these species, informally known as C. ‘adamsi KR’ or ‘adamsi-K’ (Wells and Henry 1998; Henry, Wells et al. 1999), exhibits some intriguing acoustic similarities to C. shahrudensis. Thus, parallel speciation (Schluter and Nagel 1995) due to convergent evolution of courtship songs in species having non-overlapping geographic ranges is once again shown to be an important theme JOURNAL OF NATURAL HISTORY 1605 underlying evolution and speciation in the carnea-group (Wells and Henry 1998; Henry et al. 2012, 2014). Given these apparent song similarities between C. ‘adamsi-K’ and C. shahrudensis, we present here a formal description and comparative diagnosis of this central Asian species as Chrysoperla bolti sp. nov., named in honour of our colleague and collector, Daniel Bolt. Included are comprehensive acoustic and morphological data pertaining to all its life stages, ecological and song playback observations, and phylo- genetic inferences from mitochondrial DNA. Materials and methods Collecting, rearing and identification Chrysoperla shahrudensis sp. nov.: Six gravid adult females of this species were collected in the Islamic Republic of Iran between 1200 and 2300 m elevation during August 2014 by P. Duelli, A. Mirmoayedi and D. Bolt. Collecting data are shown in Table 1. Each individual was isolated in a 250-ml clear-plastic arena, placed under long-day photo- period (17 : 7 h light : dark), and provided with water and a Wheast-based diet (Hagen and Tassan 1970). Because field-mated females will not sing (Henry and Busher 1987), it was necessary to rear progeny of mated individuals to determine species identity. Eggs were therefore collected and the larvae were raised individually in 28-ml clear-plastic cups at 20–26°C on sterile Ephestia kuehniella (Zeller) moth eggs plus locally available species of Aphidae. Newly spun cocoons were shipped (in compliance with USDA APHIS- PPQ permit P526P-07–06006) to Storrs, CT, USA, where songs were recorded from quarantined virgin adults 3–5 days after eclosion (see below). We were able to obtain living adult offspring from all six females. Song-identified individuals were preserved either as dried specimens or in 96% ethanol for molecular systematic studies (Price et al. 2015). Several first-, second-, and third-instar larvae were taken from rearing stocks and preserved in alcohol for morphological study. Voucher specimens were deposited in (i) the University of Connecticut Invertebrate Collection, Storrs, CT, USA (UCMS); (ii) the Natural History Museum, London (BMNH); (iii) the collection of Peter Duelli, Zürich, Table 1. Collecting sites for living Chrysoperla shahrudensis sp. nov. in Iran (western Asia) and Chrysoperla bolti sp. nov. in Kyrgyzstan (central Asia). Locality Elevation GPS coordinates Date collected Specimens tested for song Pass Qazvin to Alamut Valley, Iran 2267 36.38°N, 50.21°E 5 August 2014 4 ♀,1♂ progeny of 1 field (Populus, Alnus) C. shahrudensis Shahrud, Iran (agricultural: 1296 36.37°N, 54.99°E 7 August 2014 7 ♀,6♂ progeny of 3 field vegetable crops; pistachio) C. shahrudensis Shahrud, Iran (alfalfa) 1286 36.60°N, 54.98°E 7 August 2014 1 ♀,3♂ progeny of 2 field C. shahrudensis S Kara Balta, Kyrgyzstan (high- 1700 42.60°N, 73.85°E 27 May 1995 1 ♀,1♂ progeny of 2 field grass meadows) C. bolti Chichkan Valley, Kyrgyzstan (high- 1750 42.12°N, 72.80°E 1 June 1995 7 ♀,5♂ progeny of 2 field grass meadows) C. bolti N Kyzyl-Unkyur, Kyrgyzstan (high- 1350 41.48°N, 73.05°E 11 June 1995 2 ♀,2♂ progeny of 4 field grass meadows) C. bolti Alamüdün District, Kyrgyz. (high- 1950–2056 42.58°N, 74.48°E 25 June 2016; 12 8 ♀,15♂ progeny of 5 field grass meadows) July 2016 C. bolti Elevation is in metres, geographic coordinates are in decimal format, and each specimen tested for its song (i.e.
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