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Copulatory courtship by bushcricket genital titillators revealed by functional morphology, μCT scanning for 3D reconstruction and female sense structures.

Published on Jul 1, 2015in Arthropod Structure & Development 1.84
· DOI :10.1016/j.asd.2015.05.001
Nadja C. Wulff3
Estimated H-index: 3
(Humboldt University of Berlin),
Arne W. Lehmann13
Estimated H-index: 13
+ 1 AuthorsGerlind U. C. Lehmann14
Estimated H-index: 14
(Humboldt University of Berlin)
Cite
Abstract
Abstract Genitalia are rapidly evolving morphological structures most likely under sexual selection. Due to their internal nature they are often hidden inside the body, thus morpho-functional studies of animal genitalia are broadly lacking. Males of some bushcricket taxa bear paired genital appendices called titillators, the exact function of which is unknown since they are obscured inside the female body during pairing. To investigate titillator morphology and possible function during copulation, we studied the bushcricket Metrioptera roeselii (Hagenbach, 1822) using a novel combination of independent, yet complementary, techniques. Copulating pairs were snap-frozen and scanned by X-ray micro-computed tomography (μCT) to visualize the coupling of male and female genitalia in situ . Video recordings of copulating pairs also showed rhythmical insertion of male titillators into the female's genital chamber, where they percuss a softened structure on the female's subgenital plate. Movements did not induce damage to the female's structure, which lacks any sclerotized genital counterparts. Instead, scanning electron microscopy and histological sections show the female subgenital plate to be covered with two different types of sensory receptors at the contact zone between the male's titillator and the female genital chamber. We interpret the non-harmful function of the titillator processes, the lack of a genital counter-structure and the presence of sensory cells on the female's subgenital plate as indicators of a copulatory courtship function of titillators, subject to sexual selection by female choice.
  • References (61)
  • Citations (11)
Cite
References61
Newest
Published on Feb 1, 2016in Biological Journal of The Linnean Society 2.20
Nadja C. Wulff3
Estimated H-index: 3
(Humboldt University of Berlin),
Gerlind U. C. Lehmann14
Estimated H-index: 14
(Humboldt University of Berlin)
Males of certain bushcrickets (Orthoptera: Ensifera: Tettigoniidae) possess sclerotized internal genital devices termed titillators. These titillators are paired chitinized structures for which the function remains to be completely determined. We studied the role of the titillators during copulation in the bushcricket Metrioptera roeselii (Hagenbach, 1822), in the context of four a priori hypotheses for their function during mating and insemination: (1) bushcricket titillators act as anchors to ...
Published on Jan 1, 2015in Journal of Insect Behavior 0.93
Alex Córdoba-Aguilar25
Estimated H-index: 25
(UNAM: National Autonomous University of Mexico),
David E. Vrech5
Estimated H-index: 5
(National University of Cordoba)
+ 3 AuthorsEnrique González-Soriano6
Estimated H-index: 6
(UNAM: National Autonomous University of Mexico)
Male abdominal grasping apparatus that are used to secure a female prior, during and after mating, are widespread in arthropods. The scarce evidence regarding its selective regime suggests that they are male adaptations to circumvent female mating decisions, as predicted by the sexual conflict hypothesis. A recent discussion regarding this way of selection suggests that, similar to weapons and traits that have to do with physical endurance, grasping apparatus should show hyperallometry (proporti...
Published on Jul 25, 2014
Yoko Matsumura9
Estimated H-index: 9
,
Izumi Yao10
Estimated H-index: 10
+ 1 AuthorsKazunori Yoshizawa19
Estimated H-index: 19
Phylogenetic relationships among major groups of Criocerinae were reconstructed using molecular data (mitochondrial cytochrome oxidase I and 12S rDNA, and nuclear histone 3). The monophyly of Criocerinae was consistently and robustly supported. The Lema group including Lema, Oulema and Neolema was recovered as a clade, with the latter two genera imbedded within Lema. The Lilioceris group was placed as the sister taxon of the Lema group, and the genus Crioceris was identified as the sister taxon ...
Published on May 6, 2014in PLOS Biology
Malin Ah-King9
Estimated H-index: 9
(Uppsala University),
Andrew B. Barron32
Estimated H-index: 32
(Macquarie University),
Marie E. Herberstein27
Estimated H-index: 27
(Macquarie University)
The diversity, variability, and apparent rapid evolution of animal genitalia are a vivid focus of research in evolutionary biology, and studies exploring genitalia have dramatically increased over the past decade. These studies, however, exhibit a strong male bias, which has worsened since 2000, despite the fact that this bias has been explicitly pointed out in the past. Early critics argued that previous investigators too often considered only males and their genitalia, while overlooking female...
Published on Feb 1, 2014in Australian Journal of Entomology
Leigh W. Simmons75
Estimated H-index: 75
(UWA: University of Western Australia)
Male genitalia show patterns of divergent evolution, and sexual selection is recognised as being responsible for this taxonomically widespread phenomenon. Much of the empirical support for the sexual selection hypothesis comes from studies of insects. Here, I synthesise the literature on insect genital evolution, and use this synthesis to address the debate over the mechanisms of selection most likely to explain observed patterns of macroevolutionary divergence in genital morphology. Studies of ...
Published on Feb 25, 2013in PLOS ONE 2.78
Amir Yassin11
Estimated H-index: 11
(CNRS: Centre national de la recherche scientifique),
Virginie Orgogozo9
Estimated H-index: 9
(CNRS: Centre national de la recherche scientifique)
In contrast to male genitalia that typically exhibit patterns of rapid and divergent evolution among internally fertilizing animals, female genitalia have been less well studied and are generally thought to evolve slowly among closely-related species. As a result, few cases of male-female genital coevolution have been documented. In Drosophila, female copulatory structures have been claimed to be mostly invariant compared to male structures. Here, we re-examined male and female genitalia in the ...
Published on Feb 1, 2013in Ecology and Evolution 2.42
Janine M. Wojcieszek6
Estimated H-index: 6
(UWA: University of Western Australia),
Leigh W. Simmons75
Estimated H-index: 75
(UWA: University of Western Australia)
Genitalia appear to evolve rapidly and divergently in taxa with internal fertilization. The current consensus is that intense directional sexual selection drives the rapid evolution of genitalia. Recent research on the millipede Antichiropus variabilis suggests that the male genitalia are currently experiencing stabilizing selection – a pattern of selection expected for lock-and-key structures that enforce mate recognition and reproductive isolation. Here, we investigate how divergence in genita...
Published on Dec 1, 2012in Current Biology 9.19
Cosima Hotzy7
Estimated H-index: 7
(Uppsala University),
Michal Polak22
Estimated H-index: 22
(UC: University of Cincinnati)
+ 1 AuthorsGöran Arnqvist49
Estimated H-index: 49
(Uppsala University)
The rapidly evolving and often extraordinarily complex appearance of male genital morphology of internally fertilizing animals has been recognized for centuries [1]. Postcopulatory sexual selection is regarded as the likely evolutionary engine of this diversity [2], but direct support for this hypothesis is limited. We used two complementary approaches, evolution through artificial selection and microscale laser surgery, to experimentally manipulate genital morphology in an insect model system. ...
Published on Aug 1, 2012in Evolution 3.57
Karl Grieshop2
Estimated H-index: 2
(UC: University of Cincinnati),
Michal Polak22
Estimated H-index: 22
(UC: University of Cincinnati)
That male genital morphology evolves via postcopulatory sexual selection is a widely held view. In contrast, the precopulatory sexual selection hypothesis for genital evolution has received less attention. Here, we test the hypothesis that male genital spines of Drosophila ananassae promote competitive male copulation success. Using laser surgery to manipulate trait size, we demonstrate that incremental reductions of spine length progressively reduce male copulation success: males without spines...
Published on May 4, 2012in Science 41.04
Abderrahman Khila12
Estimated H-index: 12
(McGill University),
Ehab Abouheif28
Estimated H-index: 28
(McGill University),
Locke Rowe48
Estimated H-index: 48
(U of T: University of Toronto)
Sexual conflict is thought to be a potent force driving the evolution of sexually dimorphic traits. In the water strider Rheumatobates rileyi , we show that elaborated traits on male antennae function to grasp resistant females during premating struggles. Using RNA interference, we uncovered novel roles of the gene distal-less ( dll ) in generating these male-specific traits. Furthermore, graded reduction of the grasping traits resulted in a graded reduction of mating success in males, thus demo...
Cited By11
Newest
Published on Jul 3, 2019in Journal of Evolutionary Biology 2.54
Nadia S. Sloan2
Estimated H-index: 2
(UWA: University of Western Australia),
Leigh W. Simmons75
Estimated H-index: 75
(UWA: University of Western Australia)
Published on May 1, 2019in Arthropod Structure & Development 1.84
Xin Tong (NWAFU: Northwest A&F University), Baozhen Hua11
Estimated H-index: 11
(NWAFU: Northwest A&F University)
Abstract Males of Panorpodidae possess a special sperm pump, through which they directly transfer seminal fluid to the female spermatheca. However, the sperm pump has not been studied in Panorpodes to date. Here, the structure of the sperm pump and the internal coupling of genitalia were investigated in the short-faced scorpionfly Panorpodes kuandianensis Zhong, Zhang, and Hua, 2011 using light and scanning electron microscopy. The sperm pump mainly consists of a piston, a pumping chamber, the a...
Published on Feb 1, 2019in Journal of Morphology 1.56
Thomas L. Semple (ANU: Australian National University), Rod Peakall31
Estimated H-index: 31
(ANU: Australian National University),
Nikolai J. Tatarnic10
Estimated H-index: 10
(UWA: University of Western Australia)
Published on Oct 1, 2018in Journal of Morphology 1.56
Xin Tong1
Estimated H-index: 1
,
Wen Zhong1
Estimated H-index: 1
(XJU: Xinjiang University),
Baozhen Hua11
Estimated H-index: 11
Published on Aug 15, 2018
Nadja C. Wulff3
Estimated H-index: 3
(Humboldt University of Berlin),
Stefan Schöneich7
Estimated H-index: 7
(Leipzig University),
Gerlind U. C. Lehmann14
Estimated H-index: 14
(Humboldt University of Berlin)
Males of the bushcricket Metrioptera roeselii bear paired titillators that are spiny genital structures supposedly functioning as copulatory courtship devices. During copulation, the male inserts its titillators into the female's genital chamber, where they rhythmically tap on the sensilla-covered dorsal surface of the genital fold. Here, we investigated the stimulatory function of male titillators during mating in M. roeselii. Tracer backfills of presumptive mechanosensory sensilla at the femal...
Published on Sep 1, 2017in Behavioral Ecology 2.69
Gerlind U. C. Lehmann14
Estimated H-index: 14
(Humboldt University of Berlin),
James D. J. Gilbert2
Estimated H-index: 2
(University of Hull)
+ 1 AuthorsArne W. Lehmann13
Estimated H-index: 13
Lay SummaryWe examined the relationships between the complexity of male genital structures (titillators) and both the mating rate of males and females, and the number of times females mate, across a range of bushcricket species. We did not find any relationship between genital complexity and the number of times females mate. Among species with titillators, however, the complexity of these structures was associated with faster re-mating rates in females. The results therefore only partly support ...
Published on Mar 1, 2017in Journal of Morphology 1.56
Derek A. Woller3
Estimated H-index: 3
(A&M: Texas A&M University),
Hojun Song5
Estimated H-index: 5
(A&M: Texas A&M University)
We investigated probable functions of the interacting genitalic components of a male and a female of the flightless grasshopper species Melanoplus rotundipennis (Scudder, 1878) (frozen rapidly during copulation) via correlative microscopy; in this case, by synergizing micro-computed tomography (micro-CT) with digital single lens reflex camera photography with focal stacking, and scanning electron microscopy. To assign probable functions, we combined imaging results with observations of live and ...
Published on Mar 1, 2017in Scientific Reports 4.01
Nadja C. Wulff3
Estimated H-index: 3
,
Thomas van de Kamp9
Estimated H-index: 9
+ 2 AuthorsGerlind U. C. Lehmann14
Estimated H-index: 14
Published on Feb 1, 2017in Zoology 1.78
Yoko Matsumura9
Estimated H-index: 9
(CAU: University of Kiel),
Jan Michels14
Estimated H-index: 14
(CAU: University of Kiel)
+ 1 AuthorsStanislav N. Gorb61
Estimated H-index: 61
(CAU: University of Kiel)
The peculiar phenomenon of hyper-elongation of intromittent organs is well known in a number of insect groups. However, the unresolved questions of how and why such a phenomenon originated independently many times continue to attract biologists’ attention. To be able to detect the evolutionary driving mechanisms that enabled insects to repeatedly acquire such a peculiarity, first of all the structural key features and the mechanics of these organs have to be determined. In the present study, the...
Published on Dec 1, 2016in Journal of Orthoptera Research
Paul A. De7
Estimated H-index: 7
(College of The Bahamas),
Glenn K. Morris18
Estimated H-index: 18
(U of T: University of Toronto)
Abstract Two new species of Caribbean conocephaline katydids (Agraeciini) are described for the previously monotypic genus Erechthis: one from the island of Eleuthera in the Bahamas, one from Hispaniola. The first-named species Erechthis gundlachi occurs on both Cuba and Hispaniola. A median projection (prong) of the subgenital plate is taken as a major generic diagnostic trait. This structure's morphology suggests a device for removal of rival sperm. The mate attraction song of males of the Ele...