J. Crop Prot. 2021, 10 (1): 1-18______

Review Article Variation, plasticity and possible epigenetic influences in species belonging to the tribe (; ): A review

Seyed Hossein Hodjat and Alireza Saboori*

Jalal Afshar Zoological Museum, Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran.

Abstract: Environmental conditions can cause variation in morphology, behavior, and possibly epigenetic in the numerous species of the Gomphocerinae, especially in mountain habitats. Plasticity and changes in morphology in many of the species in this subfamily is caused by character segregation through the female choice of copulation that has produced various clines, sub-species or species groups. The variation and plasticity, as a result of environmental stress, besides morphology, affect physiology and of many species. Environmental stress and female assortative mating might be accompanied by hybridization in populations, resulting in character divergence and speciation after a long period of time. Contemporary evolution and/or epigenetic inheritance may be a reason for their variation in acoustic and morphology of Gomphocerinae and the main factor in the present situation of difficulty in their classification. We review possible effects of environmental stress on plasticity, hybridization, and speciation by the appearance of endemic species. About half of the insect pest species have reduced their impacts as pests under global warming. The present insect pest situation in Iran is discussed.

Keywords: Classification, Hybridization, Groups, Gomphocerini, Phenotype,

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1. Introduction12 2002; Mol et al., 2003; Tishechkin and Bukhvalova, 2009; Vedenina and Helversen, Geographical distribution of Gomphocerinae 2009; Şirin et al., 2010, 2014; Stillwell et al., species is the source for variation, plasticity, 2010; Vedenina and Mugue, 2011). Therefore and hybridization by environmental effects. morphology alone is not enough to define many Many endemic species and subspecies are species of Gomphocerini and taxonomists are created by acoustic divergence and sympatric using sound characteristics for identification. speciation. The degree and direction of a trait is studies of Gomphocerinae species related to and female choice are difficult due to a lack of knowledge for for copulation in (Robinson and Hall, accurately identifying them in Iran without recording their songs and considering other factors causing variation in their populations Handling Editor: Ali Asghar Talebi (Sultana et al., 2013; Hodjat et al., 2019). ______More than 81 species of Gomphocerini * Corresponding author: [email protected] Received: 16 September 2019, Accepted: 14 August 2020 are widely distributed in the world Published online: 03 October 2020 (Sergeev, 2011). In other words, Gomphocerini

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is an assemblage of several similar behavior regulated by corpora cardiac genera including , , secretion (Heinrich et al., 2012). , , Stauroderus, Populations in various species of and (Jago, 1971; Defaut, 2011, Gomphocerini may change their characteristics 2012, 2017). The genus Chorthippus has 229 by choosing different selection routes. species and is divided into 2 or 3 subgenera Differentially fixation of various characters on Chorthippus (Altichorthippus) (20 species), the population of a species may increase their Chorthippus (Chorthippus) (32 species), and for adaptation and survival chance. The process of various authors (including orthoptera species file divergence in colour, morphology, and song in OSF), Chorthippus (Glyptobothrus) (57 species). Pseudochorthippus parallelus (Zetterstedt) The other species of Chorthippus are not produces different traits by genetic classified into any subgenera. The Chorthippus polymorphism (Kohler et al., 2017). A long (Glyptobothrus) biguttulus group has 12 species separation of their population increases their and C. binotatus group has two species. The genetic distance, colour and morphological or genus Pseudochorthippus Defaut, 2012 with four acoustic diversification (Tregenza et al., 2000; species and two sub-species is closely related to Butlin and Hewitt, 2008; Vedenina and Mugue, Fischer and Fieber 2011; Monge, 2017). Subspecies and species (subtribe Stenobothrina). group formations are the results of genetic or Character changes in Gomphocerini species epigenetic changes in Gomphocerini (Smith and are a reaction to environmental factors that its Ritchie, 2013; Noguerales et al., 2016), through stress may have influenced their genetics, assortative mating and environmental epigenetics and external morphology (Laiolo et conditions (Klapper and Reinhold, 2003; al. 2013). Neurohormones regulate all life Burggren, 2017). processes in Gomphocerinae and insects in Rapid character divergence of grasshoppers general (Perica-mataruaga et al., 2006; Hodjat, in response to the male songs for copulation 2006). Juvenile hormones (JHs) and the and other environmental factors are influencing neurosecretory neurons (NSNs) secretions of taxonomists to clarify their classification. A corpora cardiac (CC), corpora allata (CA) and new line of research on sound production, the brain (CNS) release methylsulfonylmethane epigenetic, and stress has proved its influence (MSM) into the haemolymph. The gene on the Gomphocerinae species radiation expression is involved in C. biguttulus (L.) (Franzke and Reinhold, 2012). We refer to

Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 biogenic amines and chitin-binding. some publications of research on species Transcriptomic methods of profiling show radiations creating endemic forms by differential expression pattern in various stages phylogenetic, taxonomic, stress and genetic or of C. biguttulus life cycle and are described by epigenetic investigations (Pravdin, 1969; Mark, Berdan et al. (2017), and Tatsuta and Butlin 1983; Hodjat et al., 2018; Burggren, 2018; (2001). pattern in C. Riede, 2018). albonemus change when pastures have been overgrazed in cases of food shortage (Qin et al., 2. Phylogeny and classification difficulties 2017). The increased activity in locust is Orthoptera Species File (OSF) has provided a list initiated after adipokinetic neurohormones are of 20 tribes classified in the Gomphocerinae secreted (Hodjat, 2016). The reaction to subfamily. Gomphocerini Fieber, 1853 or acoustic communication in response to Chorthippini Shumakov, 1963 with 16 genera is environmental conditions has been studied in C. among the largest group of grasshoppers biguttulus (Klappert and Reinhold, 2003). (Cigliano et al., 2018). Some investigations have Species in the Chorthippus (Glyptopothrus) placed Gomphocerini, Chrysochraontini, group communicate by special male songs to Dociostaurini, and Arcypterini in the phylogenetic fend off competitors from the female, a structures of Gomphocerinae and included

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Omocestus, Myrmeleotettix, Stenobothrus, Shestakov (2014); Vedenina et al. (2001, Chorthippus and in their phylogenetic 2007b). Hybridization of C. albomarginatus tree (Vedenina and Mugue, 2011; Garcia-Navas et and C. oschei produces asymmetric populations al., 2017; Rohde et al., 2017). and reduces the hybrid viability (Vedenina et Considerable phenotypic plasticity is a major al., 2007a). The founder effect of the source of difficulty in developing a unique population with different songs can establish phylogenetic classification for Gomphocerini sibling species and new cline (Helversen and (Song, 2005; Zhang et al., 2013; Şirin et al., 2014; Helversen, 1997). The main driving force of Defaut, 2017). Morphological characters of a few speciation in this group of species is sexual species in Chrysochraontini, Arcypterini, selection by the female choice of courtship. Locustinae, , Melanoplinae, Calliptaminae and Cyrtacanthacridinae tribes or 2. 2. Chorthippus (Glyptobothrus) biguttulus subfamilies are close to Gomphocerinae or species group and subgroup overlapping in some morphological characters Habitat segregation, character diversification by (Defaut, 2017). The most common phylogenetic the female choice of copulation, and hybridization method of their separation is by the NADH are known to have established many similar (nicotine amid adenindinuclrotide phosphate) species in this group or subgroup of species mitochondrial analysis. Yet, with this method, the (Saldamando et al., 2005; Gottsberger 2007; Şirin relative time of appearance of Ramburiellini, et al., 2010; Gomez and Dyck, 2012). The Dociostaurini, and Arcypterini could not be complex C. biguttulus group is formed by a determined. However, it was estimated that the mixture of macropterous and brachypterous forms Gomphocerini and species in Stenobothrus, in occidental and central Europe (Ingrisch, 1995). Myrmeleotettix, Omocestus, Stenobothrus, and Many species in this group share habitat with C. Stauroderus genera are closely related (Defaut, binotatus binotatus (Charpentier) and are similar 2017). The acoustic and phylogenetic relations of to C. jacobsi (Harz), C. bornhalmi (Harz), C. various polyphyletic taxa in Gomphocerinae are ilkazi (Uvarov), C. miramae (Ramme) and C. comparable (Nattier et al., 2011; Vedenina and rubratibialis (Schmidt). Hybridization is reported Mugue, 2011). between these species in this group (Stumpner Integrating genomic and phylogenetic data and Helversen, 1994; Klapper and Reinhold, with molecular studies might result in species 2003; Helversen et al., 2004; Saldamando et al., delimitation and find how various traits 2005; Gottsberger, 2007; Franzke and Reinhold,

Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 produced the evolutionary radiation in 2012b). grasshoppers (Contreras and Chapco, 2006; Nattier et al., 2011; Via, 2012; Noguerales et 2. 3. Pseudochorthippus parallelus species al., 2018). The common species of group Gomphocerini in Europe and the Middle East Pseudochorthippus montanus (Charpentier), P. are C. albomarginatus, C. apricarius, C. curtipennis (Harris), P. tatrae (Harz), P. maritimus, C. brunneus, C. biguttulus and parallelus erythropus (Fieber, 1858), P. p. Pseudochorthippus parallelus (Harris, 1835), serbicus (Karanian, 1953), and P. p. tenuis the latter is classified as one of the P. parallelus (Brulle, 1832) are classified in this group. Hybrids subgroups (Sergeev, 2011). between the last two subspecies are formed Morphologically similar groups of because of cytoplasmic incompatibility as a result Gomphocerini species are as follows: of Wolbachiella infection (Bella et al., 2010). The differences in song and the hypothetical change of 2. 1. Chorthippus albomarginatus species group flight activity in separating flightless and winged Sound changes in this group of species is forms have been studied in this group (Ritchie, studied by Vedenina (2015); Vedenina and 1990; Tregenza et al. 2000; Butlin and Hewitt, Helversen (2003, 2009); Vedenina and 2008; Kohler et al., 2017) Morphological

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variations in P. parallelus from samples at 450- speciation or contemporary evolution i.e. the 2500 m elevation indicate that tegmina and body evolution of traits over a short period of time length of samples was decreased by ascending the (e.g. centuries rather than eons; Górür, 2005; mountain but morphology of pronotum is Whitman and Agrawal, 2009). Plasticity can unchanged. change individual, population or species epigenetic by environmental stress in insects 2. 4. Chorthippus (C.) dorsatus species group (Hoffmann and Parsons, 1991; Oxford Chorthippus loratus (Fischer von Waldheim) Research Group, 2015; Augustyniak et al., and C. dorsatus are sibling species in this group 2016; Burggren, 2018). of species. Songs in C. albomarginatus group Phenotypic plasticity reflects the “reaction represent an advanced development of the C. norm” of individuals to climate and other dorsatus group (Stumpner and Helversen 1994). environmental conditions (Laiolo et al., 2013). The complexity of the calling songs in these Reception of environmental stressful conditions two groups of grasshoppers is comparable (V. by CNS can cause variation and plasticity in parts Vedenina personal communication). of species population (Ronacher, 1989; Romer, 1993; Skinner, 2014). The genotype of an 2. 5. Chorthippus (Glyptobothrus) binotatus organism in the reaction norm may also be species group affected by life incidents. That is, plasticity Three subspecies of C. binotatus and three confers the capability of producing changes in subspecies of Chorthippus (G.) saulcyi (Krsuss) phenotype in response to environmental changes are classified in separate groups of species. The (Sgro et al., 2016). Final decision for direction of two groups are very similar and are usually movement towards a stimuli such as attraction to classified into one group. The genetic lineages the opposite sex in C. biguttulus, Gomphocerus between populations in this group of species sibiricus (L.), (L.) and living in the mountainous region of the border (Panzer, 1796) is taken by between France and Spain were studied by the brain signals that are involved to activate the Defaut (2011) and Noguerales et al. (2016, appropriate muscles (Helversen and Helversen, 2018). Isolation of populations living in 1997; Klapper and Reinhold, 2003). Therefore different mountain habitats may have been the plasticity is a broad term that can apply to the cause for species separation in this group genetic, epigenetic and contemporary evolution of (Noguerales et al., 2016). Gomphocerini response to the environment.

Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 3. Factors affecting classification of the 3. 1. 1. Plasticity and variation on insect pests Gomphocerinae Increasing plant defense against and 3. 1. Variation and Plasticity pathogens is related to DNA methylation and The definitions of phenotypic plasticity and its histone modification by the transgenerational relation to selection, coevolution, ecological defense. Changes in the phenotypic traits of speciation, genetic drift, phylogenetic inference, grasshoppers are also linked to their pleiotropy, reinforcement, sexual dimorphism performance and gene profile. Genes in C. and size constraints have been explicitly albonemus change expression pattern when described with examples of Gomphocerini pastures are overgrazed and in cases of food species (Whitman and Agrawal, 2009; Feng et shortage (Qin et al., 2017). The effects of al., 2015; Zinna et al., 2018). Plasticity is more ambient and optimal temperatures on 31 species liable to fix characters after insects acquire a of insect pests have been compared by new trait. Variations are temporary Lehmann et al., (2018). North Europe, South morphological character dissociation that may America, and Australia had fewer outbreaks of fix on a part of a population for several these pests compared to Asia and Africa. generations. Plasticity and variation may cause Aridity is an important factor in locust and

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grasshoppers to reach the outbreak point new traits in populations (Whitman and (Uvarov, 1957). Repeated insecticide treatments Agrawal, 2009). Such rapid phenotypic without considering the importance of natural adaptation to new environmental conditions enemies can cause pest outbreaks (Hodjat, reduces the strength of divergent selection 1967). A pest control project using modeling to (Sword, 2002, 2003; Smadja and Butlin, 2011). consider the efficiency of pest control methods Methylation of DNA through epigenetic for Iran is suggested by Hodjat (1974). regulation of the neural transcriptome occurs in Modares-Awal’s (2012) list of Orthoptera pests response to the stress of insects that become in Iran indicated that most species do not resistant to various toxins and escape unsuitable seriously damage crops and hardly reach to environmental conditions such as drought, heat outbreak position. Caution for not using and food restriction. In C. biguttulus DNA repeated insecticide treatments without pest breaking and its repair with new arrangements of management strategies has reduced pest amino acids is the result of environmental stress damage to crops (Hodjat, 1967). effects (Bijlsma and Loeschke, 2005; At present, the locust outbreaks are Augustyniak et al., 2006; Burggren, 2017; occasionally reported only after a rainy Lonsdale, 2018). Environmental stress and winter and revival of natural pastures in Iran. epigenetic inheritance are closely related to the Some pest species such as Eurygaster physiological change of organisms in reaction to integriceps Puton, Bemisia tabaci the inhabiting conditions that affect individual (Gennadius, 1889), Chilo suppressalis traits in the population (Skinner, 2014). (Walker) and occasionally other insect pests Methylation of DNA through epigenetic of crops and fruit trees need a continuous regulation of the neural transcriptome occurs in survey (Davatchi, 1954). However, locust response to environmental stress in insects. Most phase polymorphism, phenotypic plasticity, insects become resistant to various environmental including various mechanisms responsible for toxins and escape unsuitable living conditions the insurgence of aggressive biotypes, or such as drought, heat and food restriction. Food resistance to insecticides are the main factors shortages in crowded conditions of locust may behind the pest control problems (Song, increase cyclooxygenase, or COX stress enzymes. 2011; Augustyniak, 2016; Hodjat, 2016; Sgro The enzyme affects the metabolism of locust for a et al., 2016; Lehmann et al., 2018). few generations and the gregarious phase of the locust is produced (Rogers et al., 2003; Hodjat,

Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 3. 2. Epigenetic and stress influences 2006, 2016; Song, 2011). DNA breaking and its Various stressors trigger epigenetic repair with new arrangements of amino acids in modifications in and plants. C. biguttulus are the results of environmental Modifications allow gene transcription and stress effects (Bijlsma and Loeschke, 2005; remain in . Transgenerational Augustyniak et al., 2006; Burggren, 2017; epigenetic memory ensures plasticity and Lonsdale, 2018). genetic variation (Tricher, 2015). Gomphocerini The genes responsible for oxidative stress species may change colour, size, and activity in are expressed by superoxide dismutase (SOD) response to climatic conditions, and these (Bijlsma and Loeschcke, 2005; Glastad et al., changes are epigenetically inheritable (Rohde et 2011; O’Grady and Markow, 2012; Skinner, al. 2017). In fact, such polymorphisms are 2014; Burggren, 2017, 2018). common in Orthoptera (Wall, 1987; Mol et al., Transgenerational morphological and genetic 2003; Laws and Belovsky, 2010; Stillwell et characters are modified by stress-related levels al., 2010; Gomez et al., 2012; Nettle and of cytochrome oxidase. The toxin stress effects Bateson, 2015; Valverde and Schielzeth, 2015; on mitochondria and metabolism as a result of Lonsdale, 2018). Adaptive mutations by stress aging and zinc toxicity in insects are studied in in locust are non-directional but they may cause detail (Augustyniak et al., 2008, 2011, 2016;

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Skinner, 2014; Bultman, 2015; Lonsdale, changing their song loudness, resisting the 2018). Food shortages in crowded conditions of toxins in their surroundings or competing with locust may also increase COX stress enzymes. other males in copulation with females. Males After a few generations of crowding, metabolic of C. biguttulus resist the road noise by enzymes change appears in locust and may increasing the loudness of their song. Female change them to the gregarious phase (Rogers et selection of these males for copulation will al., 2003; Hodjat, 2006; Song, 2011). To increase the chance of progeny survival maintain plasticity, stress-induced epigenetic (Einhaupl et al., 2011; Lampe et al., 2012, modifications buffer against DNA sequence- 2014). A male of Omocestus viridulus sings based evolution (Tricker, 2015). shorter songs when other males are close by The epigenetic regulatory system of (Eiriksson, 1992). Various morphological forms neurosecretions allows reaction against stress of Glyptobothrus pullus (Philippi) appear as a effects (Smith and Ritchie, 2013; Tetreau, 2018). result of feeding on different host plants in Stressors with different intensity influence the Switzerland (Steiner, 2006). In C. biguttulus insect nervous secretions and hormones such as DNA breaking and its repair with new biogenic amines controlling carbohydrate or lipid arrangements of amino acids are the results of metabolism and causing variation in insect environmental stress effects (Bijlsma and behavior and morphology (Perić-Mataruga et al., Loeschke, 2005; Augustyniak et al., 2006; 2006). Insect pricking by injection wound Burggren, 2017; Lonsdale, 2018). produced antimicrobial phenoloxidase that In unfavorable environmental conditions, DNA masked the effect of lipopolysaccharide (LPS) damage or its partial modification may cause immune challenge (Monge, 2017).The phenotypic plasticity (Steiner, 2006; Gottsberger, embryogenesis in C. biguttulus by transcriptomic 2007; Dowle et al., 2014; Rohde et al., 2015a). The profiling at various stages of development shows genetic modification in the beet armyworm, that genes are upregulated in the imago of C. Spodoptera exigua (Hübner) is taking place after biguttulus and are mostly involved in aging and about 120 generations in multigenerational immunity (Berdan et al., 2017). In stressed microevolution. DNA damage by zinc treatment insects, changes in NF-kB (nuclear factor kapper- disrupted the development of C. brunneus, during light chain of activated B-cells) of proteins that diapause or induced embryonic disorders bind to DNA can decrease the antioxidant (Augustyniak et al., 2011). In stressed insects, activities in the Gluthathion redox system. Glutathione S-transferase (GSTs) and catalase

Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 Molecular and physiological effects of stress can (CAT) enzymes, important for metal defense impose novel trade-offs and character changes against intoxication, were reduced. The cycle of (Isaksson et al., 2011). Stress can produce protein digestion inside the cell and its effects on asymmetric forms in insect populations (Parsons, synthesizing antioxidant is reviewed by Isaksson et 1991, 1992; Møller and Swaddle, 1997; Jentzsch al., (2011). Common field grasshoppers usually et al., 2003; Hodjat, 2016) or asymmetric mate can adapt to metal-polluted habitats (Augustyniak choice in grasshoppers (Hochkirch and Lemke, et al., 2008, 2011). Zinc-induced effects are 2011). Multigenerational environmental stressors transferred to the embryonic DNA of C. brunneus on insects may last for a few generations by (Augustyniak et al., 2006, 2016). Chernobyl epigenetic effects but after the disappearance of radiation caused genetic damage and mutation on stress, populations can obtain the previous C. albomarginatus, as well as oxidative stress phenotypic form (Burggren, 2016). (Bonisoli-Alquati et al., 2018).

3. 3. Phenotypic plasticity in a noisy and 3. 4. Epigenetic modifications toxic environment So far the epigenetic influence on Environment and stressful conditions can morphological changes or character divergence change the phenotype of grasshoppers by of Chorthippus species is not known.

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Transgenerational defense induction and affecting maternal and paternal DNA epigenetic inheritance are cued by methylation methylation (Ernst et al., 2015; Burggren, signaling in the parental generation. The 2017). Some of the Gomphocerinae hybrid changes in the offspring genotype caused by species are produced after females choose to gene imprinting and neural fingerprints copulate with preferable males songs transcribe experiences of insects by affecting (Gottersberg, 2007). maternal and paternal DNA methylation (Norouzitallab et al., 2019; Ernst et al., 2015; 4. 1. Hybridization Burggren, 2017). Epigenetic modification is Hybridization and factors responsible for known to cause phenotypic changes by DNA character diversification may ultimately result methylation across insects (Bewick et al., in evolution and sympatric speciation. Many 2017). DNA methylation can regulate genome publications investigate factors responsible for at CG -sets on chromosomes. They can also the separation of population characters in regulate transcription at the CpG islands Gomphocerinae and their hybrids (Pravdin, (Deaton and Bird, 2011). The epigenetic 1969; Gottsberger, 2007; Vedenina et al., mechanisms can cause polymorphism, change 2007a; Smadja and Butlin, 2011; Frank and the locust phase, and act on caste formation of Reinhold, 2012b; Rhode, 2015; Job et al., social insects (Weiner, 2012; Ernst, et al., 2015; 2016). Positive selection in favor of increasing Mallon et al., 2016; Burggren, 2017; Lonsdale, flight ability is involved in some grasshopper 2018). Environmental epigenetic modification populations at high altitudes in the mountains of is closely related to the stress effects by stimuli- China (Li et al., 2018). The relative abundance response effects for defense on living of C. montanus and C. parallelus as specialist organisms. and generalist also produce hybrids that can trigger speciation (Rhode et al., 2015). Crosses 4. Hybridization and endemism of the following species can produce hybrids in Basic factors responsible for hybridization are Gomphocerinae species (Gottesberg, 2007; genomically influenced by genetics and Bella et al., 2010; Rhode, 2015; Vedenina, epigenetics. They influence cell division by 2015): cytoplasmic and genetic incompatibility C. brunneus X C. jacobsi; C. bigutulus X C. resulting in the presence of different brunneus; C.eisentrauti X C. brunneus; (Ishikawa and Kinoshita, 2009). Hybrid and C. biguttulus X C. mollis; C. albomarginatus X

Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 endemic species of Gomphocerinae are C. oschei; C. albomarginatus X; described in relation to asymmetry in female C. karelini; P. montanus X P. parallelus; preferences of male songs. Geographical Stenobothrus clavatus X S. rubicundus; distribution of Gomphocerinae species is the P. parallelus parallelus X P. parallelus source for variation, plasticity, and endemism erythropus. by environmental stress. Many endemic species In northeastern Ukraine, C. albomarginatus and subspecies are created by acoustic and C. oschei produce hybrid offspring. The two divergence and sympatric speciation in crossing species are morphologically very similar mountain regions. Hybridization and molecular except for their songs and organs for song evolution by mDNA sequencing are creating production. The differences in the song are caused new routes for investigating trait divergence in by leg movements and the type of pegs involved Gomphocerinae. Trans-generational defense on femur after hoppers change the angle of their induction and epigenetic inheritance are cued body (Vedenina et al., 2007b; Sardnick et al. by environmental signaling in the parental 2016). Courting males can produce more complex generation. The changes in the offspring sounds and are preferentially selected by the genotype caused by gene imprinting and neural female's inheritance. Duplicate loci controlled the fingerprints transcribe experiences of insects by homologous elements in the songs of the two

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copulating species of C. oschei from C. preferentially selected by the females. Inheritance albomarginatus (Vedenina and Helversen, 2003; implying duplicate loci that control the Vedenina et al., 2007b). C. karelini produced a homologous elements in the song of two closely song with two short elements alternating with a related species are involved in hybridization longer element. Even courtship songs of two between them such as hybrids between C. oschei males of C. karelini recorded from two different and C. albomarginatus (Vedenina and Helversen, localities in Ukraine produced different songs. 2003; Vedenina et al., 2007b). The songs from these localities had hybrid Even courtship songs of two males of C. characteristics of the two populations (Vedenina, karelini recorded from two different localities 2015). In the Picos district in the north Spain in Ukraine produced different songs. The songs hybridization between C. brunneus and C. jacobsi from these localities had a hybrid characteristic produced offspring with different numbers of of the two populations (Vedenina, 2015). stridulatory pegs in different localities. Various Asymmetry is observed in female preferences peg numbers produced different cline in the Picos between two closely related Stenobothrus region. The changes were significant from clavatus and S. rubicundus (Vedenina et al., populations approximately 30 km south of Picos 2014; Sardnick et al., 2016). In the Picos de Alps. The differences for wingless meadow district of north Spain, hybridization between grasshoppers, P. parallelus were measured by the C. brunneus and C. jacobsi has produced nested model for geographic variation. Mark and offspring with a different numbers of recapture methods for measuring the elation of stridulatory pegs in different localities. Various stridulatory pegs differences in various habitats peg numbers produced different clines in the have been applied to measure the extent of Picos region. The changes were significant differences (Bridle et al., 2001). Investigation of from populations approximately 30 km south of hybridization and molecular evolution by mDNA Picos de Europa Mountains. sequencing is creating new routes for finding Mark and recapture method is used for genetic or phylogeographic trait divergence in measuring the relation of stridulatory peg Gomphocerinae (Hewitt, 2001). Asymmetric numbers of C. brunneus living in different mate choice between the two closely related habitats in Santander mountain regions of north populations of Gomphocerini in the same locality Spain. The principal component analysis for mean is presumed to produce hybrid forms (Hochkirch peg scores against the distance from the fitted and Limke, 2011; Hochkirch, 2013). Asymmetry cline center shows that C. brunneus can be easily

Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 is recorded in female preferences between two distinguished from G. jacobsi by their peg closely related Stenobothrus clavatus and S. numbers. The hybrid forms are found within 30 rubicundus (Vedenina et al., 2014; Sardnick et al., km distance (Bridle et al., 2001). Similar studies 2016). Song of C. biguttulus changes of female choice of male song for copulation have characteristics in relation to male robustness and been conducted in other grasshopper species the attractiveness to females. The loudness of (Ritchie, 1989, 1990; Helversen and Helversen, songs also changes to neutralize noisy 1997; Bridle et al., 2001; Benediktov, 2005, 2014; surroundings (Gottsberger, 2007; Einhaupl et al., Einhaupl et al., 2011; Heinrich et al., 2012; Job et 2011; Lampe et al., 2014). al., 2016; Kohler et al., 2017). Hybrid sterility and mate preferences between two closely related species of Gomphocerini are 4. 2. Endemism related to many factors such as genetic Endemism is produced by divergence in incompatibility, gene flow between sympatric morphology and the song of Pseudochorthippus species, attractiveness to intermediate phenotypes parallelus (Zetterstedt) populations in and plasticity (Gootsberger, 2007; Hochkirch, mountains. Their populations by genetic 2013; Sgro et al., 2016). Courting males can polymorphism have chosen various traits. A produce more complex sounds and are long separation of population traits increased

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their genetic distance and caused morphological sibiricus, Omocestus viridulus (L.) and or acoustic diversification in various directions. Stenobothrus lineatus (Panzer, 1796) is not The variability in characters are signs for related to the number of pegs (Elsner, 1974; forming an endemic or sympatric species Saldamando et al., 2005; Perić-Mataruga et al., (Tregenza et al., 2000; Butlin and Hewitt, 2008; 2006). Stillwell et al., 2010; Vedenina and Mugue, Mating of female grasshoppers with a 2011; Monge, 2017). preferable male is because of their particular by feeding on various host song characteristics and can initiate sympatric plants produced plastic forms in Switzerland species for adapting to the prevailing (Steiner, 2006). Procedures for the appearance of conditions. Consequently, in large parts of endemic species in Chorthippus in Turkey (Mol et central Europe, hybrid populations and al., 2003) and the list of endemic sympatric species have originated (Hochkirch species of Iran (Hodjat et al., 2018) show the and Limke, 2011; Hochkirch, 2013; Rohde et reality of having endemic forms of grasshoppers. al., 2015b, 2017). The Euloryma Spearman, 2013 (Hemiacridinae; Chortoicetes terminifera song is changed by Acridinae) of the Cape Floristi region in South crowding conditions (Song, 2005, 2011; Africa produce endemic species in their narrow Chapuis et al., 2010; Ernst et al., 2015). The distribution area. Euloryma larsinorom and E. internal reaction to resist the road noise in lapollei are congeneric flightless hoppers males of C. biguttulus is causing an increase in distributed in natural shrub and heath vegetation. the loudness of their song. Female selection of E. umoja and E. ottei can tolerate vineyard and these males for copulation will also increase the agricultural environment (Adu-Acheampong et chance of progeny survival (Klappert and al., 2017). DNA methylation leading to epigenetic Reinhold, 2003; Einhaupl et al., 2011; Heinrich inheritance of the modified phenotype in endemic et al., 2012; Lampe et al., 2012). species of grasshoppers requires further Limited condition dependence of male body investigation (Nettle and Bateson, 2015). condition is likely to be correlated with male acoustic signals in C. biguttulus (Franzke and 5. Song and phenotypic variation Reinhold, 2012a). The embryogenesis in G. Sound in Gomphocerinae is produced by rubbing bigutullus by transcriptomic profiling at various the hind femora with a row of the stridulatory stages of development shows that gene expression pegs, up and down against the radial vein of the at various stages of the life cycle ranged from

Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 tegmina, which is more prominent than the other synthetic biogenic amines to chitin-binding. veins and is called the plectrum. The song of Genes upregulated in the imago of C. biguttulus males in C. dorsatus, C. dichrousand C. loratus were mostly involved in aging and immunity is also produced by movements of the hind (Berdan et al., 2017). In stressed insects, changes femur against the tegmina but differs in various in NF-kB (nuclear factor kapper-light chain of localities. The song character may change by the activated B-cells) of proteins that bind to DNA position of their upward body direction or the can decrease the antioxidant activities in the speed of rubbing the set of pegs. Detailed Gluthathion redox system. Molecular and registration of song characters differs between physiological effects of stress can impose novel Chorthippus (Glyptobothrus) bozdaghi trade-offs and character changes (Isaksson et al., (Uvarov), Chorthippus (Glyptobothrus) ilkazi 2011). Stress can produce asymmetric forms in (Uvarov) and Chorthippus (Glyptobothrus) insect populations (Parsons, 1991, 1992; Møller helverseni (Mol et al., 2003). Temporal features and Swaddle, 1997; Jentzsch et al., 2003; Hodjat, of the song in C. brunneus and C. jacobsi depend 2016) or asymmetric mate choice in grasshoppers on the neurological pattern that controls leg (Hochkirch and Lemke, 2011). Multigenerational movement. The neuromuscular activity during environmental stress on insects may last for a few stridulation of C. biguttulus, Gomphocerus generations by epigenetic effects but in some

9 Factors influencing the tribe Gomphocerini______J. Crop Prot.

cases after the disappearance of stress populations physiological changes, affecting insects due to can show phenotypic modification (Burggren, environmental conditions, are capable of being 2018). Pharmacologically induced stridulation epigenetically inherited through methylation. A had little effect on the courtship song and only new line of research is proposed for investigating changed one or two of the sound elements the relation of epigenetic changes to stress in (Vedenina et al., 2001). insects (Merritt and Bewick, 2017).

6. Conclusion Acknowledgments

Environmental and genetic factors have produced We thank Dr. Bernard Defaut (Quartier various endemic populations with new characters Babi,hameaud’Aynat, 09400 Bédeilhac-et- that may create endemic hybrid and sympatric Aynat, France) for taxonomic revision and species of grasshoppers (Hodjat et al., 2018). The reprints to improve the text. We acknowledge problem for taxonomists is to classify Orthoptera the help of Dr. Warren Burggren by considering their phylogenetic or ancestral (Developmental Investigative Biology relationship. In , mainly morphological Research, University of North Texas, Denton abrupt changes between taxa are the measure for USA) for many suggestions to improve the text. defining them but variation in morphological Dr. Varvara Vedenina (Russian Academy characters is the gradual results of gene flow into Science) for her suggestions, corrections, and the population. Morphological differentiation sending us the PDFs of her publications. despite gene flow is based on a selection of Dr. Klaus Riede, Zoologisches Forschungs phenotypes in the survived population as a result museum Alexander Koenig- Leibniz of the environmental stress (Dowle et al., 2014). It InstitutfürBiodiversität der Tierpe, Germany, is difficult to find the degree of morphological helped us with the manuscript. We thank Dr. character changes in each taxon. The Maria Augustyniak (Department of physiological trade-offs and diversifying Physiology and Eco-toxicology, University of characters of populations are known to affect the Silesia, Katowice, Poland). taxonomy and life history at various localities in animals (Zera and Harshman, 2001). In stressed References insects, changes in NF-kB (nuclear factor kapper- light chain of activated B-cells) proteins that bind Adu-Acheampong, S., Samways, M. J.,

Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 to DNA can decrease the antioxidant activities in Landmann, T., Kyerematen, R., Minkah, R., the Gluthathion redox system. Molecular and Mukundamago, M. and Moshobane, C. M. physiological effects of stress can impose novel 2017. Endemic grasshopper species trade-offs and character displacements (Isaksson distribution in an agro-natural landscape of et al., 2011). the Cape Floristic Region, South Africa. Phase polymorphism and variation in locust Ecological Engineering, 105: 133-140. morphometrics appear to be the result of Augustyniak, M., Babczynska, A. and environmental stress effects on their physiology Augustiniak, M. 2011. Oxidative stress in (Hodjat, 2016). Epigenetics in contemporary newly-hatched - the evolution separates the characters of the migratory effects of zinc treatment during diapauses, phase for several generations from the solitary depending on the female’s age and its phase (Mallon et al., 2016). This phenomenon can origins. Comparative Biochemistry and also affect other Gomphocerini species and Physiology–C. Toxicology and produce variation in their morphological Pharmacology, 154(3): 172-179. characters in response to environmental stress Augustyniak, M., Babczynska, A., (Parsons, 1992; Chapuis et al., 2010; Ketmaier et Kozlowski, M., Sawczyn, T. and al., 2010; Murren et al., 2015). Hormones and Augustiniak, M. 2008. Effects of zinc and

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Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021 Skinner, M. K. 2014. Environmental stress and Tatsuta, H. and Butlin, R. K. 2001. Amplified epigenetic transgenerational inheritance. fragment length polymorphism for the BMC Medicine, 12: 153. analysis of genetic structure in grasshopper Smadja, C. and Butlin, R. 2011. A framework populations. Journal of Orthoptera Research, for comparing processes of speciation in the 10(2): 203-207. presence of gene flow. Molecular Ecology, Tetreau, G. 2018. Interaction between insects, 20(24): 5123-5140. toxins, and bacteria: Have we been wrong so Smith, G. and Ritchie, M. G. 2013. How might far? Toxins, 10(7): 281-311. epigenetics contribute to ecological Tishechkin, D. Yu. and Bukhvalova M. A. speciation? Current Zoology, 59(5): 686-696. 2009. Acoustic communication in Song, H. 2005. Phylogenetic perspectives on grasshopper communities (Orthoptera: the revolution of locust phase Acrididae: Gomphocerinae): segregation of polymorphism. Journal of Orthoptera acoustic niches. Russian Entomological Research, 14(2): 235-245. Journal, 18(3): 165-188. Song, H. 2011. Density-dependent phase Tregenza, T., Prichard, V. L. and Butlin, P. K. polymorphism in nonmodel locusts: A mini 2000. Pattern of trait divergence between review. Psyche, 741769. populations of the meadow grasshopper

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17 Factors influencing the tribe Gomphocerini______J. Crop Prot.

ﻣﺮوري ﺑﺮ ﺗﺄﺛﯿﺮات ﺗﻐﯿﯿﺮ، اﻧﻌﻄﺎفﭘﺬﯾﺮي و اﭘﯽژﻧﺘﯿﮏ اﺣﺘﻤﺎﻟﯽ در ﮔﻮﻧﻪﻫﺎي ﻗﺒﯿﻠﻪ Gomphocerini (Orthoptera; Gomphocerinae)

ﺳﯿﺪﺣﺴﯿﻦ ﺣﺠﺖ و ﻋﻠﯿﺮﺿﺎ ﺻﺒﻮري*

ﻣﻮزه ﺟﺎﻧﻮرﺷﻨﺎﺳﯽ اﺳﺘﺎد ﺟﻼل اﻓﺸﺎر، ﮔﺮوه ﮔﯿﺎهﭘﺰﺷﮑﯽ، ﭘﺮدﯾﺲ ﮐﺸﺎورزي و ﻣﻨﺎﺑﻊ ﻃﺒﯿﻌﯽ داﻧﺸﮕﺎه ﺗﻬﺮان، ﮐﺮج، اﯾﺮان. ﭘﺴﺖ اﻟﮑﺘﺮوﻧﯿﮑﯽ ﻧﻮﯾﺴﻨﺪه ﻣﺴﺌﻮل ﻣﮑﺎﺗﺒﻪ: [email protected] درﯾﺎﻓﺖ: 25 ﺷﻬﺮﯾﻮر 1398؛ ﭘﺬﯾﺮش: 24 ﻣﺮداد 1399

ﭼﮑﯿﺪه: ﺷﺮاﯾﻂ ﻣﺤﯿﻄﯽ ﻣﻮﺟﺐ ﺗﻐﯿﯿﺮ در رﯾﺨﺖﺷﻨﺎﺳﯽ، رﻓﺘﺎر و اﺣﺘﻤﺎﻻً اﭘﯽژﻧﺘﯿﮏ در ﺑﺴﯿﺎري از ﮔﻮﻧﻪﻫﺎي زﯾﺮﺧﺎﻧﻮاده Gomphocerinae ﺑﻪوﯾﮋه در زﯾﺴﺘﮕﺎهﻫﺎي ﮐﻮﻫﺴﺘﺎﻧﯽ ﻣﯽﺷﻮد. اﻧﻌﻄـﺎف ﭘـﺬ ﯾﺮي و ﺗﻐﯿﯿـ ﺮات در رﯾﺨﺖﺷﻨﺎﺳﯽ ﺑﺴﯿﺎري از ﮔﻮﻧﻪﻫﺎ در اﯾﻦ زﯾﺮﺧﺎﻧﻮاده در اﺛﺮ ﺟﺪاﯾﯽ وﯾﮋﮔﯽﻫﺎ در ﻃـ ﯽ اﻧﺘﺨـﺎب ﻣـﺎده ﺑـﺮا ي ﺟﻔﺖﮔﯿﺮي اﯾﺠﺎد ﻣﯽﺷﻮد ﮐﻪ ﮐﺸﺎﻧﻪﻫﺎي ﻣﺨﺘﻠﻒ، ﮔﺮوهﻫﺎي زﯾﺮﮔﻮﻧﻪاي ﯾﺎ ﮔﻮﻧﻪاي ﺗﺸﮑﯿﻞ ﻣﯽدﻫﺪ. ﺗﻐﯿﯿﺮات و اﻧﻌﻄﺎفﭘﺬﯾﺮي در اﺛﺮ اﺳﺘﺮسﻫﺎي ﻣﺤﯿﻄﯽ اﻓﺰون ﺑﺮ رﯾﺨﺖﺷﻨﺎﺳﯽ، ﺑﺮ ﻓﯿﺰﯾﻮﻟﻮژي و اﭘﯽژﻧﺘﯿﮏ ﺑﺴﯿﺎري از ﮔﻮﻧﻪﻫﺎي ﺣﺸﺮات ﺗﺄﺛﯿﺮ ﻣﯽﮔﺬارد. اﺳﺘﺮسﻫﺎي ﻣﺤﯿﻄﯽ و ﺟﻔﺖﮔﯿﺮي ﺑﺎ ﻣﺎده ﻣﻨﺎﺳﺐ ﻣﻤﮑﻦ اﺳﺖ ﺑﺎ ﺗﻮﻟﯿﺪ دورگ در ﺟﻤﻌﯿﺖ ﻫﻤﺮاه ﺷﺪه و ﻣﻨﺠﺮ ﺑﻪ ﺟﺪاﯾﯽ ﺻﻔﺎت و ﮔﻮﻧﻪزاﯾﯽ در درازﻣﺪت ﺷﻮد. ﺗﮑﺎﻣﻞ ﻣﻌﺎﺻﺮ و ﯾﺎ وراﺛﺖ اﭘﯽژﻧﺘﯿﮏ ﻣﻤﮑﻦ اﺳﺖ دﻟﯿﻞ ﺑﺮ ﺗﻐﯿﯿﺮات در آوازﺧﻮاﻧﯽ و رﯾﺨﺖﺷﻨﺎﺳـ ﯽ Gomphocerinae ﺑـﻮده و ﻋﺎﻣﻞ اﺻﻠﯽ در ﻣﺸﮑﻼت ﮐﻨﻮﻧﯽ در ردهﺑﻨﺪي آﻧﻬﺎﺳﺖ. در اﯾﻦ ﻣﻘﺎﻟﻪ، اﺛﺮات اﺣﺘﻤﺎﻟﯽ اﺳﺘﺮسﻫﺎي ﻣﺤﯿﻄﯽ، دورگﮔﯿﺮي و ﮔﻮﻧﻪزاﯾﯽ ﺑﺎ ﻇﻬﻮر ﮔﻮﻧﻪﻫﺎي ﺑﻮﻣﯽ ﻣﺮور ﻣﯽﺷﻮد. ﺗﺄﺛﯿﺮ ﺣﺪود ﻧﯿﻤـ ﯽ از ﮔﻮﻧـﻪ ﻫـﺎ ي ﺣـﺸﺮات ﺑﻪﻋﻨﻮان آﻓﺖ در اﺛﺮ ﺗﻐﯿﯿﺮ در ﺷﺮاﯾﻂ ﻣﺤﯿﻄﯽ ﮐﻨﻮﻧﯽ ﮐﻢرﻧﮓ ﺷﺪه اﺳﺖ. وﺿﻌﯿﺖ ﮐﻨﻮﻧﯽ ﺣﺸﺮات آﻓﺖ در اﯾﺮان ﻣﻮرد ﺑﺤﺚ ﻗﺮار ﮔﺮﻓﺘﻪ اﺳﺖ.

واژﮔﺎن ﮐﻠﯿﺪي: ردهﺑﻨﺪي، دورگﮔﯿﺮي، Gomphocerini، ﻓﻨﻮﺗﺎﯾﭗ، آواز Downloaded from jcp.modares.ac.ir at 8:44 IRST on Saturday September 25th 2021

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