A New Cryptic Species of the Chrysoperla Carnea Group (Neuroptera: Chrysopidae) from Western Asia: Parallel Speciation Without Ecological Adaptation
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Systematic Entomology (2014), 39, 380–393 A new cryptic species of the Chrysoperla carnea group (Neuroptera: Chrysopidae) from western Asia: parallel speciation without ecological adaptation CHARLES S. HENRY1, STEPHEN J. BROOKS2, JAMES B. JOHNSON3, ATSUSHI MOCHIZUKI4 andPETER DUELLI5 1Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT, U.S.A., 2Department of Entomology, The Natural History Museum, London, U.K., 3Division of Entomology, University of Idaho, Moscow, ID, U.S.A., 4National Institute for Agro-Environmental Sciences, Tsukuba City, Japan and 5Swiss Federal Research Institute WSL, Birmensdorf, Switzerland Abstract. Parallel (or convergent) evolution of vibrational mating songs between species confined to different continents has been found several times in the Chrysop- erla carnea species-group of cryptic (morphologically indistinguishable) green lacewings. Repeated parallel speciation resulting in taxa that differ in duetting songs but not in appearance or ecology suggests an atypical mode of speciation, one that need not involve ecological adaptation. Here we describe an additional example of convergent song phenotypes reflecting parallel nonadaptive speciation, between the common North American species Chrysoperla plorabunda (Fitch) and a newly discov- ered species that appears to be widespread in western Asia. To support the hypothesis of parallel evolution, we describe the song of the new species in detail, comparing it to that of C. plorabunda and demonstrate their acoustical similarity. Results of song playback trials are then presented, showing that the songs are also functionally (behaviourally) indistinguishable between individuals of both species and could not prevent hybridisation if the two species were sympatric. We demonstrate that the new species is very similar in morphology and ecology not only to C. plorabunda, but also to at least four other species in the carnea-group that co-occur with it in western Asia. To reject the alternative hypothesis that C. plorabunda and the new species are alike simply due to common ancestry, we show that they occupy relatively distant positions in a phylogenetic analysis of 4630 base pairs of protein-coding mitochondrial DNA. We then formally describe the new species as Chrysoperla heidarii sp.n., including with this description observations of its behaviour, ecology and life history. This published work has been registered in ZooBank, http://zoobank.org/urn: lsid:zoobank.org:pub:60C0FFC5-92B9-4C20-9FDF-561EB2764F16. Introduction to the role of ecology in speciation – that is, how disruptive natural selection acting upon populations of organisms can Speciation generates biodiversity, yet the process of speciation cause speciation through divergent evolutionary responses to remains poorly understood even after years of study (Otte & the biotic and abiotic environments (Schluter, 2000). This Endler, 1989; Howard & Berlocher, 1998; Coyne & Orr, 2004; process, known as ecological speciation (Rundle & Nosil, Butlin et al., 2012). Recently, attention has once again turned 2005; Nosil, 2012) or ‘adaptive speciation’ (Dieckmann et al., 2003), is thought by many to be the primary means by which Correspondence: Charles S. Henry, Department of Ecology & populations diverge, often in the presence of gene flow (Danley Evolutionary Biology, University of Connecticut, Unit 3043, 75 North & Kocher, 2001; Smadja & Butlin, 2011). According to this Eagleville Road, Storrs, CT 06269, U.S.A. E-mail: charles.henry@ uconn.edu view, ecological adaptation serves as the major driver of 380 © 2014 The Royal Entomological Society Chrysoperla heidarii, a new Eurasian species with an American song 381 reproductive isolation (Sobel et al., 2010), leading to ‘isolation and C. calocedrii Henry et al. from southern California sings by adaptation’ (IBA; Nosil et al., 2008). IBA incidentally like C. pallida Henry et al. from Europe (Henry et al., 2012). confers on new species distinctive ecological niches, such In these cases, allopatric distributions preclude hybridisation that their coexistence in the community is possible (Weissing and ‘de-speciation’ (Taylor et al., 2006; Webb et al., 2011) et al., 2011). Putative examples of ecological speciation have that would otherwise occur readily between parallel song been described in plants (Schulman et al., 2004; Friar et al., analogues (e.g. Henry, 1985; Henry et al., 2002b, 2012; Henry 2006; Hall & Willis, 2006; Levin, 2009), fish (Schluter, 1994; & Wells, 2010). More generally, very similar duetting songs Marchinko, 2009; Pavey et al., 2010), granivorous birds (Ryan are never found within single continental land masses, where et al., 2007; de Leon et al., 2010; Edelaar et al., 2012), lizards several widespread species co-exist in broad sympatry. Instead, (Richmond & Reeder, 2002; Rosenblum & Harmon, 2011) multiple sympatric species in the carnea-group partition the and many insects (Thomas et al., 2003; Nosil et al., 2006; acoustic signal space available in a geographic region and Arias et al., 2008; Stireman et al., 2008; Peccoud et al., 2009; occupy nonoverlapping song niches (Henry & Wells, 2010). Matsubayashi et al., 2010; Sullivan-Beckers & Cocroft, 2010; It is this lack of evidence for convergent duetting songs Funk et al., 2011). among sympatric species that argues against ecological selec- A related process – parallel speciation – lends powerful tion as the cause of parallel speciation in the carnea-group. support to any hypothesis of ecological speciation, because it Parallel adaptive responses should characterise the songs of demonstrates that a particular selective environment can repeat- sympatric and allopatric species equally, yet in sympatry two edly generate the same phenotype during speciation. In parallel lacewing species with replicated songs apparently cannot coex- speciation, a single species invading several new places gives ist (Henry et al., 2013). That is likely because the obvious rise to new species at each site that are phenotypically similar phenotypic differences between species-specific songs have between sites, presumably in response to similar ecological little or no ecological basis. Experiments comparing a conifer- imperatives. The best known example, the marine stickleback associated and a grass-associated lacewing species confirm that Gasterosteus aculeatus Linnaeus, has colonised several fresh- song phenotype is not explicitly adapted to the transmission water lakes, in each of which it has independently diverged into properties of the habitat: either song type functions equally a pair of ecologically and morphologically benthic and limnetic well, whether propagated through its own or the incorrect sub- taxa (Schluter & Nagel, 1995; Rundle et al., 2000; Turner, strate (Henry & Wells, 2004). Rather than natural selection, 2002; Hohenlohe et al., 2010). Similarly, two closely related sexual selection through mate choice and species recognition species of the stick insect Timema Scudder have independently is the more likely force that places each new species into an given rise to analogous pairs of populations on two host plants; available acoustical niche (Henry et al., 2013). Thus the cryp- in each species, one population is green and the other bears a tic species of the carnea-group present an anomalous case of white stripe, closely matching the foliage of the hosts (Nosil parallel speciation in the absence of clear ecological causation. et al., 2002). Truly parallel speciation is relatively uncom- Recently, a third species-pair exhibiting parallel song mon although increasingly recognised. It has thus far been evolution has been identified, once again comprising a North confirmed within Gasterosteus, Timema, Nesospiza Cabanis American species, C. plorabunda (Fitch), and a newly discov- finches (Ryan et al., 2007), Plestiodon skiltonianus (Baird & ered Asian species, ‘CcX-Asia’ (Henry et al., 2013). Here, we Girard) skinks (Richmond & Jockusch, 2007), Astyanax Baird describe the duetting song of this new species and compare it & Girard cave fish (Strecker et al., 2012), Littorina saxatilis to that of C. plorabunda. We show how the songs of these two (Olivi) marine snails (Galindo et al., 2009), Echinodera Wol- species have important differences in the frequency domain laston weevils (Astrin & Stuben, 2010), Inurois punctigera but are remarkably similar with respect to a critical temporal Prout winter moths (Yamamoto & Sota, 2012), and Hawaiian feature – volley period. Interspecific behavioural tests and Tetragnatha Latreille spiders (Blackledge & Gillespie, 2004). molecular sequence data are used to support the hypothesis that Green lacewings of the Chrysoperla carnea species-group C. plorabunda and ‘CcX-Asia’ have functionally equivalent also show strong evidence of parallel speciation. The 18 duetting songs but have not inherited their similar songs from recognised species in this globally distributed complex are a common ancestor. The new species is described formally as nearly indistinguishable from one another morphologically Chrysoperla heidarii sp.n., based on song phenotype, adult and exhibit only weak postzygotic barriers when forcibly and larval morphology, habitat association and ecophysiology. hybridised, but they achieve complete reproductive isolation in Implications of this new instance of parallel song evolution nature through species-specific substrate-borne duetting songs and speciation are discussed. (Henry, 1979; Wells & Henry, 1992a; Wells, 1993; Henry et al., 2013). However, there