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Testing the Role of Trait Reversal in Evolutionary Diversification Using Song Loss in Wild Crickets

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Testing the Role of Trait Reversal in Evolutionary Diversification Using Song Loss in Wild Crickets Testing the role of trait reversal in evolutionary diversification using song loss in wild crickets Nathan W. Baileya,1,2, Sonia Pascoalb,1, and Fernando Montealegre-Zc,2 aSchool of Biology, University of St. Andrews, St. Andrews KY16 9TH, United Kingdom; bDepartment of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom; and cSchool of Life Sciences, University of Lincoln, Lincoln LN6 7DL, United Kingdom Edited by Günter P. Wagner, Yale University, New Haven, CT, and approved March 6, 2019 (received for review November 19, 2018) The mechanisms underlying rapid macroevolution are controver- Male crickets produce calls by stridulating: They rub modified sial. One largely untested hypothesis that could inform this debate forewings together to generate mechanical vibrations (Fig. 1A). is that evolutionary reversals might release variation in vestigial An individual producing an advertisement, courtship, or ag- traits, which then facilitates subsequent diversification. We eval- gressive song will draw a thickened ridge of tissue (the scraper) uated this idea by testing key predictions about vestigial traits on one wing across a corrugated vein (the file) on the opposing arising from sexual trait reversal in wild field crickets. In Hawaiian wing. In many species, the resulting vibrations are amplified by Teleogryllus oceanicus, the recent genetic loss of sound-producing resonating membranes formed from modified wing cells. When and -amplifying structures on male wings eliminates their acoustic coupled with wing motor behaviors that repeat this movement signals. Silence protects these “flatwing” males from an acousti- in succession, the pulse rate, pattern, and carrier frequency of cally orienting parasitoid and appears to have evolved indepen- chirps can convey information about mate location, identity, dently more than once. Here, we report that flatwing males show quality, or aggressiveness. We studied the widely distributed enhanced variation in vestigial resonator morphology under var- Austro-Pacific cricket Teleogryllus oceanicus. Hawaiian pop- ied genetic backgrounds. Using laser Doppler vibrometry, we ulations of this species overlap with an acoustically orienting found that these vestigial sound-producing wing features reso- endoparasitoid fly (Ormia ochracea) that responds to male songs nate at highly variable acoustic frequencies well outside the nor- and infests them with destructive larvae. A mutation(s) showing mal range for this species. These results satisfy two important Mendelian segregation on the X chromosome appeared in a EVOLUTION criteria for a mechanism driving rapid evolutionary diversification: population on the island of Kauai approximately two decades Sexual signal loss was accompanied by a release of vestigial mor- ago, and it silences males by erasing or dramatically reducing the phological variants, and these could facilitate the rapid evolution stridulatory apparatus and sound resonators on their forewings of novel signal values. Widespread secondary trait losses have (15). Females have undifferentiated wings and do not sing. Males been inferred from fossil and phylogenetic evidence across numer- carrying the flatwing genotype develop wings resembling those of ous taxa, and our results suggest that such reversals could play a females, so are referred to as “flatwing males” (Fig. 1B). Flat- role in shaping historical patterns of diversification. wing males are protected against parasitoid infestation (15), and the flatwing phenotype rapidly spread and now appears on more acoustic communication | diversification | evolutionary rate | than one Hawaiian island (16, 17). In all cases investigated, sexual signal | trait loss flatwing segregates as a single-locus trait on the X chromosome (16, 18), but the degree to which affected male wings are feminized ne of the most contentious debates to have arisen in evo- Olutionary biology centers on the rate at which diversification Significance proceeds (1). In particular, the mechanisms responsible for driving rapid bursts of macroevolution remain unresolved de- Bursts of rapid evolutionary diversification are widely ob- – spite decades of study (2 4). Here, we evaluate an overlooked served, but their underlying causes are controversial. We mechanism that could cause rapid diversification: the release of tested whether secondary loss of sexual traits could play a role cryptic variation following secondary loss of a mate recognition in rapid diversification by releasing variation in vestigial sig- signal, which exposes a widened range of vestigial signaling struc- naling structures, which then facilitates the rapid evolution of tures to the action of selection. If novel or variable signal values novel signal values. We found evidence to support such an subsequently evolve, they could play a key role in speciation. evolutionary model in the field cricket Teleogryllus oceanicus, Secondary trait losses are common (5), and have been sug- which has recently lost the ability to sing. Trait reversals are gested to precede diversification in several studies, for example, widespread and may play an underappreciated role in de- in stick insects and plethodontid salamanders (6, 7). Loci in- termining the pattern and rate of macroevolutionary change. volved in functional traits important for diversification, such as spectral tuning of the visual system in cichlids, are known to be Author contributions: N.W.B. conceived the study; N.W.B., S.P., and F.M.-Z. designed the evolutionarily labile (8), and when such traits are lost, func- experiments; S.P. performed complementation and morphometric experiments; N.W.B. and F.M.-Z. performed laser Dopper vibrometry experiments; N.W.B., S.P., and F.M.-Z. tionless vestigial structures or behaviors are left behind, which analyzed data; and N.W.B. wrote the manuscript with input from S.P. and F.M.-Z. could facilitate the reevolution of new functions or trait values The authors declare no conflict of interest. (2, 9–11). Sexual traits involved in mate recognition systems are This article is a PNAS Direct Submission. particularly prone to reversal (12). Their reduction under pres- sure from countervailing natural selection is a central prediction Published under the PNAS license. Data deposition: Any data not presented in the supporting information for this article of sexual selection theory (13, 14), and widespread sexual trait have been archived in the St. Andrews Research database (https://doi.org/10.17630/ losses have been inferred phylogenetically (12). Acoustic signals a9885b35-fe5e-4800-a07c-df93c1350f6d). play a prominent role in speciation, communication, and many 1N.W.B. and S.P. contributed equally to this work. animal behaviors. Here, we tested how their evolutionary re- 2To whom correspondence may be addressed. Email: [email protected] or versal might predispose populations to diversification using a [email protected]. field cricket system in which the sexually selected male acoustic This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. signal has been recently, and abruptly, lost from multiple wild 1073/pnas.1818998116/-/DCSupplemental. populations (15, 16). www.pnas.org/cgi/doi/10.1073/pnas.1818998116 PNAS Latest Articles | 1of9 Downloaded by guest on September 26, 2021 A B posterior dorsal right left ventral anterior female normal-wing Kauai Oahu male flatwing flatwing male male C 12.7 kHz 25 kHz 10 kHz 1.7 kHz 5.0 kHz ? kHz ? kHz 2.9 kHz 2 3 5 1 4 6 7 8 Pholidoptera griseoaptera Tettigonia Teleogryllus oceanicus strepitans monaka pulkara pilkena fultoni viridissima Cyphoderris Gryllotalpa Riatina Riatina Oecanthus Prophal. Tettigoniidae Gryllotalpidae Gryllidae Fig. 1. Diversity of wing venation and acoustic signals in crickets and katydids. (A) Forewing stridulation in a normal-wing T. oceanicus male (anterior dorsal view with the cricket’s directions indicated), with the mirror, harp, and scraper highlighted in turquoise, purple, and yellow, respectively. The dashed black line indicates the stridulatory file present on the ventral surface of the upper (right) wing, and the solid gray line indicates the direction of forewing movements during singing. (B) Representative Hawaiian T. oceanicus forewings showing differences in the degree to which Kauai and Oahu flatwings are feminized. Resonators and corresponding vestigial structures are highlighted as above. Adapted from ref. 16. (C) Male forewings from exemplar orthopteran species (not to scale). Sampled clades are labeled on the phylogeny, and approximate carrier frequencies reported in the literature (“?” if unknown) are shown above species names. Prophal., Prophalangopsidae. Shaded regions of the wing visually illustrate taxonomic variation in sound resonator morphology across this group. In this simplified phylogeny adapted from ref. 30, branch lengths do not scale to divergence time. Thin branches represent groups that do not sing or are not represented here. Sources from which figures were drawn and carrier frequencies (Cf) obtained: 1[wing figure drawn from a photograph with permission from Geoffrey D. Ower (photographer); Cf data from ref. 69], 2[wing figure redrawn from Wikimedia Commons/Hans Schneider; Cf data from ref. 70], 3[wing figure redrawn from ref. 28 with permission from the Trustees of the Natural History Museum, London; Cf data from ref. 70], 4[wing figure redrawn from ref. 33 with permission from Daniel Otte; Cf data from ref. 33], 5[wing figure drawn from a photograph by the authors;
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