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Comparative Analysis of Male Calling Signals in Closely Related Species of Macropsis Lewis, 1836 (Homoptera: Auchenorrhyncha: Ci

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Comparative Analysis of Male Calling Signals in Closely Related Species of Macropsis Lewis, 1836 (Homoptera: Auchenorrhyncha: Ci Russian Entomol. J. 29(3): 247–260 © RUSSIAN ENTOMOLOGICAL JOURNAL, 2020 Comparative analysis of male calling signals in closely related species of Macropsis Lewis, 1836 (Homoptera: Auchenorrhyncha: Cicadellidae: Eurymelinae: Macropsini) reveals possible ways of evolution of the signal temporal pattern Ñðàâíèòåëüíûé àíàëèç ïðèçûâíûõ ñèãíàëîâ ñàìöîâ áëèçêîðîäñòâåííûõ âèäîâ Macropsis Lewis, 1836 (Homoptera: Auchenorrhyncha: Cicadellidae: Eurymelinae: Macropsini) ïîçâîëÿåò âûÿâèòü âîçìîæíûå ïóòè ýâîëþöèè âðåìåííî´ãî ðèñóíêà ñèãíàëîâ D.Yu. Tishechkin Ä.Þ. Òèøå÷êèí Department of Entomology, Faculty of Biology, M.V. Lomonosov Moscow State University, Vorobyevy Gory, Moscow 119234, Russia. E- mail: [email protected] Кафедра энтомологии Биологического факультета Московского государственного университета имени М.В. Ломоносова, Воробьёвы Горы, Москва 119234, Россия. KEY WORDS: Homoptera, Auchenorrhyncha, Cicadellidae, Macropsis, calling signals, variability, evolution. КЛЮЧЕВЫЕ СЛОВА: Homoptera, Auchenorrhyncha, Cicadellidae, Macropsis, призывные сигналы, изменчивость, эволюция. ABSTRACT. It is shown that, in some closely related РЕЗЮМЕ. Показано, что у некоторых близко- Macropsis species, male calling signals consist of similar родственных видов Macropsis призывные сигналы components but clearly differ in the duration of homolo- самцов состоят из сходных компонентов, но чётко gous parts, the shape of syllables, the presence/absence различаются по их длительности, форме серий, на- of additional components, or the presence/absence of личию/отсутствию дополнительных компонентов gaps between the signal parts. In some other leafhoppers, или наличию/отсутствию пауз между частями сиг- such differences are intraspecific and can be observed in нала. У ряда других видов Cicadellidae подобные the signals of males from the same population and even in различия представляют собой внутривидовые вари- the same male. Thus, in the considered Macropsis spe- ации, наблюдающиеся в сигналах самцов из одной cies, signals were apparently formed by fixing different популяции и даже у одного и того же самца. Это originally intraspecific variants in different phylogenetic позволяет предположить, что у рассмотренных ви- lineages in the course of their divergence. This suggests дов Macropsis сигналы сформировались за счёт фик- that intraspecific variability can become a basis for rapid сации разных изначально внутривидовых вариан- divergence of signal patterns if in different populations тов в разных филогенетических линиях в процессе different pattern variants gain a selective advantage. их дивергенции. Таким образом, внутривидовая из- Based on this, we can assume that male calling signals in менчивость может стать основой для быстрой ди- leafhoppers can evolve not only by a gradual change in вергенции структуры сигналов, если в разных попу- the quantitative parameters such as the signal parts dura- ляциях разные варианты сигнала получат селектив- tion but also through qualitative changes of temporal ное преимущество. При этом у цикадовых призыв- pattern due to adding new components, change of a ные сигналы могут эволюционировать не только в syllable shape, and splitting a single signal into several результате постепенного изменения количествен- parts. Since in closely related leafhopper species it is the ных параметров, например, длительности частей differences in signal patterns that provide reproductive сигнала, но и посредством качественных изменений isolation, such changes can result in rapid speciation. временно´го рисунка за счёт добавления новых ком- How to cite this article: Tishechkin D.Yu. 2020. Comparative analysis of male calling signals in closely related species of Macropsis Lewis, 1836 (Homoptera: Auchenorrhyncha: Cicadellidae: Eurymelinae: Macropsini) reveals possible ways of evolution of the signal temporal pattern // Russian Entomol. J. Vol.29. No.3. P.247–260. doi: 10.15298/rusentj.29.3.03 248 D.Yu. Tishechkin понентов, изменения формы серий или разделения described by Walker [1974]. The study of molecular, сигнала на несколько частей. Поскольку у близко- acoustic, and morphological differentiation in Gampso- родственных видов Cicadellidae репродуктивную cleis sedakovii (Fischer von Waldheim, 1846) (Ortho- изоляцию обеспечивают именно различия в струк- ptera: Tettigoniidae) from six localities in Inner Mon- туре сигналов, подобные изменения могут привести golia, China showed that the structure of acoustic sig- к быстрому видообразованию. nals is closely related to genetic differences between populations [Zhang et al., 2015]. Booij [1982] found Introduction evidence for geographic quantitative signal variation in Muellerianella (Homoptera: Delphacidae) in Western Europe. In many insect taxa, the male produces acoustic Sometimes not geographical isolation, but differ- calling signals for attracting a conspecific female. Pres- ences in host specialisation results in reproductive iso- ently, it is common knowledge that, in such taxa, differ- lation and acoustic divergence. N. lugens can feed on ences in calling signal patterns facilitate precopulatory cultivated and wild rices and on Leersia hexandra reproductive isolation between closely related species. Schwartz, 1788 (Poaceae), an abundant weed often Thus, the trigger of divergence and, as a consequence, growing along the edges of rice fields. Populations of N. of speciation in such taxa can be the changes in the lugens from rice and L. hexandra distinctly differ in mating signal pattern. pulse repetition frequency, under laboratory conditions In principle, speciation can occur by gradual change when given a choice always preferred a mate from the over long periods of time, or very rapidly or even own population, but can hybridize in no-choice crosses. instantaneously. In other words, it can occur through Hybrids show signal parameters intermediate between large-scale morphological and ecological divergence, parent populations but no obvious indications of hybrid or because of changes of single traits that directly affect non-viability. However, no males with “hybrid” signal reproductive isolation. Accordingly, in the genomes, it parameters were found in nature. This indicates a high may appear as a deep and large-scale changes or affect efficiency of the reproductive barrier between the two just a few loci. Polygenic control of mating signal traits host races and allowed to conclude that they have al- may suggest that signal patterns have diverged gradual- ready reached the level of different biological species ly, whereas single or few genes may imply that they can [Claridge et al., 1985b]. diverge more rapidly [Henry et al., 2002; Vedenina et Thus, the N. lugens species complex demonstrates al., 2006; Xu, Shaw, 2019]. examples of both allopatric (geographical) and sympa- Nilaparvata lugens (Stål, 1854) (Homoptera: Del- tric (due to host shift) speciation. Remarkably, that in phacidae) in the Pacific Region provides an example of both cases only quantitative signal parameters evolve. a gradual change in the quantitative parameters of the Similarly, in closely related species of planthoppers signal in the course of divergence. The general scheme from the genus Ribautodelphax Wagner, 1963 (Ho- of signal temporal pattern in this species remains con- moptera: Delphacidae) male calling signals have rather stant throughout its range. Populations differ only in complex, but similar temporal patterns so that signals of pulse repetition frequency and these differences reflect different species differ mostly in quantitative parame- genetic differentiation between them. The populations ters [den Bieman, 1986]. Male calling signals of cryptic from Philippines and Australia were most difficult to species of Enchenopa binotata (Say, 1824) complex hybridize in the laboratory and showed the greatest (Homoptera: Membracidae) also demonstrate only quan- differences in pulse repetition frequency. However, in titative differences. A carrier frequency of a signal is the those crosses which were successful, there were no most significant for conspecific mate recognition; dif- obvious indications of hybrid non-viability. Pulse repe- ferences in temporal patterns are less distinct and not so tition frequencies in hybrids showed values intermedi- much affect the choice of male by female [Cocroft et al., ate between and significantly different from both paren- 2008]. tal populations. Thus, differences in pulse repetition Under experimental conditions, quantitative signal frequency is the only reproductive barrier on the current parameters can change quite rapidly. Artificial bidirec- stage of divergence of these forms. This clearly indi- tional selection on pulse repetition frequency in female cates, that, first, the populations from Philippines and calls of Ribautodelphax imitans (Ribaut, 1953) (Ho- Australia represent an early stage of speciation process moptera: Delphacidae) resulted in complete divergence and, second, pre-mating ethological isolating mecha- in this parameter without overlap between two lines nisms have begun to evolve in advance of post-mating after only five generations. Male choice tests after 10 ones [Claridge et al., 1985a]. Similar situation exists in generations revealed significant preference of mates Gomphocerinae (Orthoptera: Acrididae), since some from the same line [de Winter, 1992]. grasshopper species producing different signals can be Under natural conditions, quantitative signal param- hybridised under laboratory conditions and hybrids are eters also can evolve during rather
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