On the evolution of the tymbalian tymbal organ: Comment on “Planthopper bugs use a fast, cyclic elastic recoil mechanism for effective vibrational communication at small body size” by Davranoglou et al. 2019

In ihrer kürzlich erschienenen Arbeit (Davranoglou et al. 2019) untersuchten die Autoren an lebenden Exemplaren von Agalmatium bilobium (Issidae) mit modernsten Methoden (microCT) die Interaktionen zwischen Muskulatur und bestimmten Anteilen des Exoskeletts zur Vibrationserzeugung und beschreiben deren biomechanische Grundlage. Auf der Basis des morphologischen Vergleichs mit Museumsmaterial von Vertretern der meisten Taxa der Fulgoromorpha (Spitzkopfzikaden) im Familienrang postulieren Davranoglou et al. (2019), ein „neues und bisher übersehenes“ Organ entdeckt zu haben, das sie als „snapping organ“ bezeichnen und als charakteristisch für die Fulgoromorpha (mit Ausnahme der Delphacidae) interpretieren. Wir sehen diese Ergebnisse aus folgenden Gründen kritisch: 1. In ihrer umfassenden Übersicht zu den vibrationserzeugenden Organen der Hemiptera stellten Wessel et al. (2014) die Hypothese auf, dass sich alle bisher bekannten Strukturen zur Schall- und Vibrationserzeugung auf ein Organ zurückführen lassen, das mit hoher Wahrscheinlichkeit bei der Stammart aller Hemipteren oberhalb der Sternorrhyncha vorhanden war, und eine Synapomorphie dieses Taxons, der sog. Tymbalia (Wessel et al. 2014), darstellt. Da aufgrund der morphologischen Disparität des Organs in den einzelnen Taxa die Homologieverhältnisse schwierig zu beurteilen sind, stellten Wessel et al. (2014) Kriterien für das „Tymbal der Tymbalia“ auf. Das sogenannte „snapping organ“ erfüllt alle Kriterien dieses Tymbal-Organes. Die Einführung eines neuen Begriffes für eine bestimmte Struktur in einer langen und komplexen Kette evolutionärer Transformationen ist daher unnötig, wenn nicht sogar irreführend. Wir empfehlen daher dringend, in zukünftigen Arbeiten den Begriff „tymbalian tymbal organ with a snapping mechanism“ zu verwenden. 2. Die Grundannahme von Davranoglou et al. (2019), dass – im Gegensatz zum neu entdeckten „snapping organ“ der Fulgoromorpha – allen Cicadomorpha ein „tymbal-ähnliches Or-gan“ gemeinsam sei, ist zu stark vereinfacht und vernachlässigt die enorme Vielfalt der Ausprägungen des Tymbals bei Nicht-Singzikaden innerhalb der Cicadomorpha. In Anbetracht der verfügbaren Studien scheint es daher zweifelhaft, dass sich die vibrationserzeugenden Strukturen dreimal unabhängig voneinander entwickelt haben sollen, wie es die phylogenetische Interpretation bei Davranoglou et al. (2019: Abb. 3) suggeriert

Leafhopper males compensate for unclear directional cues in vibration-mediated mate localization

Abstract Ambient noise and transmission properties of the substrate pose challenges in vibrational signal-mediated mating behavior of arthropods, because vibrational signal production is energetically demanding. We explored implications of these challenges in the leafhopper Aphrodes makarovi (Insecta: Hemiptera: Cicadellidae) by exposing males to various kinds of vibrational noise on a natural substrate and challenging them to find the source of the female playback. Contrary to expectations, males exposed to noise were at least as efficient as control males on account of similar searching success with less signaling effort, while playing back male–female duets allowed the males to switch to satellite behavior and locate the target without signaling, as expected. We found altered mitochondrial structure in males with high signaling effort that likely indicate early damaging processes at the cellular level in tymbal muscle, but no relation between biochemical markers of oxidative stress and signaling effort. Analysis of signal transmission revealed ambiguous amplitude gradients, which might explain relatively low searching success, but it also indicates the existence of behavioral adaptations to complex vibrational environments. We conclude that the observed searching tactic, emphasizing speed rather than thorough evaluation of directional cues, may compensate for unclear stimuli when the target is near

The effect of delay of female reply on signalling and searching behaviour of <i>A</i>. <i>makarovi</i> males.

<p>(a) male advertisement call duration; (b) calling rate; (c) proportion of males searching for the source of female reply; (d) proportion of calling males locating the source; (e) proportion of searching males locating the source. (a, b) box and whisker plots show the median (black line), the 25–75% interquartile range (boxes), the lowest and the highest data points still within 1.5 of interquartile range (whiskers) and outliers (circles). Values obtained in the F₁₀ treatment are shown as median (thick white line) together with 95% confidence interval for median (gray area). *, ** and *** indicate significant difference from the F₁₀ treatment (Lme model followed by Dunnett’s multiple comparisons test, p < 0.05, p < 0.01 and p < 0.001, respectively). (c-e) determined proportion (black circle) together with 95% confidence interval for proportions is shown. Proportion obtained in the F₁₀ treatment (thick white line) is shown together with 95% confidence interval for proportions (gray area). *, ** and *** indicate values that are significantly lower than in the F₁₀ treatment (Regwq multiple comparisons test, p < 0.05, p < 0.01 and p < 0.001, respectively). N = number of males included in the analyses. F₁₀: N = 20 (a-d), N = 18 (e).</p

Experimental set-up.

<p>A schematic drawing of the experimental setup showing the initial position of the male on the top of the nettle plant and the positions of vibration exciters (not drawn to scale).</p

The effect of hidden female reply on signalling and searching behaviour of <i>A</i>. <i>makarovi</i> males.

<p>(a) male advertisement call duration; (b) calling rate; (c) proportion of males searching for the source of female reply; (d) proportion of calling males locating the source; (e) proportion of searching males locating the source. (a, b) box and whisker plots show the median (black line), the 25–75% interquartile range (boxes), the lowest and the highest data points still within 1.5 of interquartile range (whiskers) and outliers (circles). *, ** and *** indicate significant difference between treatments (Lme model followed by Tukey’s all pair comparisons test, p < 0.001). (c-e) determined proportion (black circle) together with 95% confidence interval for proportions is shown. * indicate values that are significantly lower than in the F5 treatment (one-tailed Fisher’s exact test, p < 0.05). Values obtained in the F₀ treatment (white circles) shown for comparison indicate the number of males changing their position during the trial (c) and the number of males arriving to the leaves (d, e) and were not included in statistical analyses.</p

Representative male-female duet in <i>A</i>. <i>makarovi</i>.

<p>Spectrogram (above) and waveform (below) are shown. Me0-Me3: species-specific elements as described in [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0139020#pone.0139020.ref025" target="_blank">25</a>].</p

The Effect of Timing of Female Vibrational Reply on Male Signalling and Searching Behaviour in the Leafhopper <i>Aphrodes makarovi</i>

<div><p>Sexual communication in animals often involves duetting characterized by a coordinated reciprocal exchange of acoustic signals. We used playback experiments to study the role of timing of a female reply in the species-specific duet structure in the leafhopper <i>Aphrodes makarovi</i> (Hemiptera: Cicadellidae). In leafhoppers, mate recognition and location is mediated exclusively by species- and sex-specific substrate-borne vibrational signals and a female signal emitted in reply to male advertisement calls is essential for recognition and successful location of the female. In <i>A</i>. <i>makarovi</i>, males have to initiate each exchange of vibrational signals between partners, and in a duet the beginning of a female reply overlaps the end of the male advertisement call. Results of playback treatments in which female replies were delayed and did not overlap with the male call revealed that in order to trigger an appropriate behavioural response of the male, female reply has to appear in a period less than 400 ms after the end of the initiating male call. Results also suggest that males are not able to detect a female reply while calling, since female reply that did not continue after the end of male call triggered male behaviour similar to behaviour observed in the absence of female reply. Together, our results show that vibrational duets are tightly coordinated and that the species-specific duet structure plays an important role in mate recognition in location processes.</p></div