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Obligatory Duetting Behaviour in the Chrysoperla Carneagroup of Cryptic

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Obligatory Duetting Behaviour in the Chrysoperla Carneagroup of Cryptic Biol. Rev. (2013), 88, pp. 787–808. 787 doi: 10.1111/brv.12027 Obligatory duetting behaviour in the Chrysoperla carnea-group of cryptic species (Neuroptera: Chrysopidae): its role in shaping evolutionary history Charles S. Henry1,∗, Stephen J. Brooks2, Peter Duelli3, James B. Johnson4, Marta M. Wells5 and Atsushi Mochizuki6 1 Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut CT 06269, U.S.A. 2 Department of Entomology, The Natural History Museum, London, SW7 5BD, U.K. 3Swiss Federal Research Institute WSL, Birmensdorf, CH-8903, Switzerland 4Division of Entomology, University of Idaho, Moscow, Idaho, ID 83844, U.S.A. 5Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, CT 06520, U.S.A. 6National Institute for Agro-Environmental Sciences, Tsukuba City, Ibaraki, 305 8604, Japan ABSTRACT An unusual system of communication has evolved in green lacewings of the Chrysoperla carnea-group, triggering rapid proliferation of numerous cryptic species across all of the Northern Hemisphere and large portions of Africa. The system is based on sexually monomorphic, substrate-borne vibrational signals, produced by abdominal oscillation. These low-frequency signals are exchanged between courting individuals in a precise duetting format. The song of each of the more than 20 described species exhibits a unique acoustical phenotype that reproductively isolates the taxon from all other species with which it might come into contact. Here, we review what is known about duetting behaviour in the carnea-group, emphasizing the dominant role that duetting has played in the evolution, ecology, and speciation of the complex. Included are descriptions and discussions of song diversity and its impact on reproductive isolation among species, the genetic basis of interspecific song differences, partitioning of acoustic space among sympatric species, parallel song evolution in allopatric species pairs, and modes of speciation within the complex. We also emphasize the importance of correctly identifying by song all species of the carnea-group that are to be used either in experimental studies or programs of biological control, while acknowledging the continuing relevance of morphology to carnea-group systematics. Key words: songs, speciation, insects, taxonomy, convergent evolution, parallel evolution, sibling species, sexual monomorphism. CONTENTS I. Introduction ................................................................................................ 788 II. The Chrysoperla carnea (Stephens) species-group ............................................................. 789 III. Sexual signalling and the duetting songs of thecarnea-group ................................................ 789 (1) Song production in insects ............................................................................. 789 (2) Communication between the sexes .................................................................... 790 (3) Sexually monomorphic duetting songs ................................................................. 790 (4) Multimodal sexual signalling ........................................................................... 791 * Author for correspondence (Tel: ++86 04 864450; E-mail: [email protected]). Biological Reviews 88 (2013) 787–808 © 2013 The Authors. Biological Reviews © 2013 Cambridge Philosophical Society 788 Charles S. Henry and others IV. Diversity of duetting song phenotypes in the carnea-group .................................................. 791 V. song variation within species ............................................................................... 793 (1) Geographic variation .................................................................................. 793 (2) Phenotypic plasticity ................................................................................... 795 VI. reproductive isolation ...................................................................................... 796 (1) Premating, prezygotic isolation ........................................................................ 796 (2) Postmating, postzygotic isolation ....................................................................... 796 VII. Acoustic space and song evolution .......................................................................... 797 (1) Parallel evolution ...................................................................................... 798 (2) Movement between continents ......................................................................... 798 VIII. Duetting and speciation .................................................................................... 799 (1) Three critical properties of the clade ................................................................... 799 (a) Duets enforce reproductive isolation ................................................................ 799 (b) The genetic basis of song differences is simple ...................................................... 799 (c) Cryptic phenotypes have cryptic genotypes ......................................................... 800 (2) Mode of speciation ..................................................................................... 800 (3) Ecology and speciation ................................................................................. 800 (4) Does reinforcement complete speciation? .............................................................. 801 IX. The importance of morphology ............................................................................ 802 X. Denying song-delineated species: studies from the literature ............................................... 803 XI. Cryptic species, systematics, and biological control ......................................................... 804 XII. Future directions ........................................................................................... 804 XIII. Conclusions ................................................................................................ 804 XIV. Acknowledgements ......................................................................................... 805 XV. References .................................................................................................. 805 of cryptic species, each with a species-specific duetting ‘When they came near each other, both the males and the song (Henry, 1983a). This complex is the focus of our females began to jerk the abdomen upward and downward, review. First, we present the classification of the carnea- an act which is generally seen before copulation.’ group. Because of the cryptic nature of these species, the fast-evolving duetting signals are the most reliable (Smith, 1922, pp. 1331–1332) taxonomic characters in the clade; therefore, we summarize sexual signalling and song diversity, highlighting the features I. INTRODUCTION that make the song of each species unique. We describe intraspecific variation in duetting behaviour, parsing the Written 90 years ago, these words record the observations relative contributions of genetic versus environmental effects made in 1916 by Dr Roger C. Smith of Cornell University and reviewing the results of single-species experiments on concerning behaviour he had seen in a common North sex recognition and intrasexual competition. The impact of American insect species, Chrysopa oculata Say. In publishing duetting songs on premating reproductive isolation between this paper, Smith became the first scientist to describe otherwise interfertile cryptic species is then described and courtship and mating in a green lacewing (Order Neuroptera, its implications discussed, especially within the context of Family Chrysopidae). More significantly, his account is the relatively weak postmating, postzygotic isolation across the first to identify the essential elements of a remarkable system carnea-group. Because duetting songs occupy distinct regions of duetting behaviour in lacewings, one that is based on of acoustical space, we explore the physical and biotic nature substrate-borne signals or ‘songs’ produced by the vibrating of this space, the importance of species-specific regions abdomen of sexually active individuals. of space, and the impact of available acoustic space on It would be another 40 years before Smith’s observations parallel (or convergent) song evolution in species that will not were confirmed and extended to other species and genera encounter each other because of their allopatric distributions. within the Chrysopidae (Toschi, 1965; Riek, 1967; Ickert, One likely consequence of ongoing song divergence in the 1968; Sheldon & MacLeod, 1974; Brooks, 1987). Even so, carnea-group is recent, rapid speciation, so we examine some and despite a growing body of literature (see references in newer ideas about song-mediated cladogenesis in lacewings. Henry & Wells, 2010), the nature of duetting behaviour and Throughout the review, we emphasize the necessity of using its impact on the evolution, speciation, and classification an accurate taxonomy of carnea-group lacewings based on of lacewings are not familiar to many biologists. One song-delineated species, in which morphology and ecology particular clade of lacewings, the carnea-group of the are accorded secondary rather than primary taxonomic genus Chrysoperla Steinmann, has radiated rapidly and importance. We show how the identification of cryptic species recently into an especially large and important complex can sometimes be achieved even using dead specimens,
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