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Modes of Chromosome Evolution Author(S): Anna Maryańska-Nadachowska, Valentina G Mediterranean Species of the Spittlebug Genus Philaenus: Modes of Chromosome Evolution Author(s): Anna Maryańska-Nadachowska, Valentina G. Kuznetsova, Dorota Lachowska and Sakis Drosopoulos Source: Journal of Insect Science, 12(54):1-17. 2012. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1673/031.012.5401 URL: http://www.bioone.org/doi/full/10.1673/031.012.5401 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Insect Science: Vol. 12 | Article 54 Maryańska-Nadachowska et al. Mediterranean species of the spittlebug genus Philaenus: Modes of chromosome evolution Anna Maryańska-Nadachowska1a*, Valentina G. Kuznetsova2b, Dorota Lachowska3c, Sakis Drosopoulos4d 1Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Poland 2Zoological Institute, Russian Academy of Sciences, Russia 3Department of Entomology, Institute of Zoology, Jagiellonian University, Poland 4Agricultural University, Athens, Greece Abstract The evolution of karyotypes and sex determination system of Philaenus Stål (Auchenorrhyncha: Aphrophoridae) species is studied here in detail. The most plausible scenario of chromosomal rearrangements accompanying phylogenetic differentiation in Philaenus is advanced. It is postulated that the ancestral karyotype of Philaenus was 2n = 24 + X0. Karyotype changes occurred several times independently in the genus. The karyotype of 2n = 22 + X0 (P. spumarius and P. tesselatus) originated from 2n = 24 + X0 by fusion between two autosomal pairs. The neo–XY system (P. arslani, P. loukasi, P. signatus, P. maghresignus, and P. tarifa) also originated from the 24 + X0 karyotype by means of independent fusions between autosomes and the original X chromosome. The neo–X1X2Y system (P. italosignus) evolved from the 2n = 22 + neo–XY karyotype by an additional fusion between the Y chromosome and one more autosomal pair. The neo–XnY system of P. italosignus is the first reported case of an evolutionarily fixed multiple sex chromosome system in Auchenorrhyncha. Keywords: cytogenetics, karyotype evolution, sex chromosome system Correspondence: a [email protected], b [email protected], c dorota.lachowska- [email protected], d [email protected], *Corresponding author Editor: Igor Sharakhov was Editor of this paper. Received: 16 June 2011, Accepted: 26 August 2011 Copyright : This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed. ISSN: 1536-2442 | Vol. 12, Number 54 Cite this paper as: Maryańska-Nadachowska A, Kuznetsova VG, Lachowska D, Drosopoulos S. 2012. Mediterranean species of the spittlebug genus Philaenus: Modes of chromosome evolution. Journal of Insect Science 12:54 available online: insectscience.org/12.54 Journal of Insect Science | www.insectscience.org 1 Journal of Insect Science: Vol. 12 | Article 54 Maryańska-Nadachowska et al. Introduction The Mediterranean species of Philaenus were shown to be sympatric with P. spumarius, The spittlebug genus Philaenus Stål while partly allopatric with each other. At (Auchenorrhyncha: Aphrophoridae) has long present, eight species are recognized in the attracted the particular interest of biologists genus Philaenus. The current taxonomy of due to its high color polymorphism. The this genus accepts a division of these species nature and origin of this polymorphism and its into two groups based on morphological possible contribution to the evolution of similarities in the male anal tube: the reproductive isolation and sympatric “spumarius” group (P. spumarius, P. speciation have been extensively documented tesselatus, P. loukasi,andP. arslani), and the for P. spumarius. This species is widely “signatus” group (P. signatus, P. italosignus, distributed, covering most of the Palaearctic P. maghresignus, and P. tarifa) (Drosopoulos region and extending into the Nearctic, as well and Remane 2000). According to larval food as most other temperate regions of the earth plant preferences, the genus is subclassified and many oceanic islands (Halkka and Halkka into the three groups developing: (1) on the 1990; Stewart and Lees 1996; Drosopoulos lily, Asphodelus aestivus (= A. microcarpus) 2003; Drosopoulos et al. 2010). Philaenus (P. signatus, P. italosignus, P. maghresignus, spumarius is a highly polyphagous insect, and and P. tarifa), (2) on xerophilic plants (P. has become a pest of fodder plants and loukasi and P. arslani), and (3) on various strawberries in areas where it is not a native dicotyledonous and monocotyledonous plants species (Halkka et al. 1967; Zając and Wilson (P. spumarius and P. tesselatus) (Drosopoulos 1984). Due to outstanding polymorphism in 2003). The results of a recent phylogenetic adult dorsal color/pattern, more than 50 study of Philaenus using nucleotide sequences synonyms have been given to P. spumarius from two mitochondrial (COI and CytB) (Nast 1972). Until the late 1980s, only three genes and one nuclear (ITS2) region is in species were recognized in the genus general agreement both with morphological Philaenus: the Holarctic P. spumarius, the and food plant preference classifications, with Mediterranean species P. signatus (which the exception of P. maghresignus, placed as a inhabits the Balkans and Middle East), and P. sister taxon to all remaining Philaenus species tesselatus (southern Iberia and Maghreb). (Maryańska-Nadachowska et al. 2010). Philaenus tesselatus was often treated as a subspecies (Wagner 1959) or a synonym of P. Over 90% of speciation events are suggested spumarius (Nast 1972). However, more recent to be accompanied with chromosomal studies suggested that it is a valid species rearrangements (White 1978). distinct from P. spumarius (Drosopoulos and Auchenorrhyncha possess holokinetic Quartau 2002). Since the 1990s, as a result of chromosomes; that is, their chromosomes do purposeful morphological studies on not have a primary constriction (the Philaenus in the Mediterranean region, five centromere) (Halkka 1959). Because of the further species have been described: P. absence of the centromere as a morphological loukasi (southern Balkans), P. arslani (Middle marker, and also because of the paucity of East), P. maghresignus (Maghreb and convenient differential techniques, the southern Spain), P. italosignus (southern Italy interchromosomal (particularly and Sicily), and P. tarifa (southern Iberia). intrachromosomal) rearrangements cannot be Journal of Insect Science | www.insectscience.org 2 Journal of Insect Science: Vol. 12 | Article 54 Maryańska-Nadachowska et al. detected in holokinetic chromosomes. These FISH mapping of genes, which are currently chromosomes have thus no distinctive features used in some economically important for individual identification in a karyotype, holokinetic organisms (Mandrioli et al. 2003; besides size differences, if present. In Mandrioli and Borsatti 2007; Marec et al. holokinetic chromosomes, a kinetochor plate 2010), are not yet developed or available for (to which the spindle microtubules attach) Auchenorrhyncha (Kuznetsova et al. 2010). covers all or the majority of the chromosome Over the past several decades, a number of surface (Wolf 1996). Theoretically, the large studies have used conventional banding kinetochor plate facilitates karyotype techniques (C-, AgNOR-, DAPI/CMA3- evolution by means of fusion and fission of banding) for the study of auchenorrhynchan holokinetic chromosomes, since on the one karyotypes (Noda and Tatewaki 1990; hand there is no risk of the formation of Perepelov et al. 2002; Kuznetsova et al. 2003, dicentric chromosomes and, on the other 2009a, 2009b, 2010; Maryańska- hand, even relatively small chromosome Nadachowska et al. 2006); however, these fragments can have a part of the kinetochore studies developed only a few chromosomal plate and thus be attached to the spindle. For markers. Additionally, their limited taxonomic the reasons mentioned above, these representation failed to provide rearrangements are conventionally accepted as comprehensive insight into the comparative the most common mechanisms of cytogenetics of the group (Kuznetsova et al. chromosome evolution in holokinetic groups. 2010). However, contrary to what may be expected, Auchenorrhyncha seem to be characterized by The family Aphrophoridae, to which the stable or only slightly variable karyotypes at genus Philaenus belongs, is a group with the levels of genera, tribes, and families fairly diversified karyotypes. In 29 studied (Halkka 1959; Kirillova 1986, 1988; species assigned to nine genera within Emeljanov and Kirillova 1989, 1991) Aphrophoridae,
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