Right-Handed Penises of the Earwig Labidura Riparia (Insecta, Dermaptera, Labiduridae): Evolutionary Relationships Between Structural and Behavioral Asymmetries
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JOURNAL OF MORPHOLOGY 267:1381–1389 (2006) Right-Handed Penises of the Earwig Labidura riparia (Insecta, Dermaptera, Labiduridae): Evolutionary Relationships Between Structural and Behavioral Asymmetries Y. Kamimura1,2* 1Department of Environmental Systems, Rissho University, Kumagaya, Saitama 360-0194, Japan 2Department of Ecology and Systematics, Graduate School of Agriculture, Hokkaido University, Kita-ku, Sapporo 060-8589, Japan ABSTRACT The number of penises vary in the insect umes of reports have detailed the development, suborder Forficulina (order Dermaptera; earwigs). Males genetics, evolution, and physiological backgrounds of the families Diplatyidae, Pigidicranidae, Anisolabididae, of behavioral asymmetries in vertebrates, especially Apachyidae, and Labiduridae have two penises (right and right-handedness in humans (e.g., Ludwig, 1970; left), while those of the Spongipohridae, Chelisochidae, Neville, 1976; Rogers and Andrew, 2002; and referen- and Forficulidae have a single penis. The proposed phylo- genetic relationships among these families suggest that ces therein), studies of invertebrates are rare. This is the single-penis families evolved from an ancestor possess- especially true for cases in which behavioral asym- ing two penises. To date, examinations of double-penis ear- metries are not associated with morphological differ- wig species have found that only a single penis is used per entiation of the left and right organs, the so-called single copulation. These diversities in structural and be- structural asymmetry (Byrne et al., 2002, 2004). havioral aspects of genitalia raises the following intriguing Palmer (1996) classified conspicuous asymmetry questions: How are the two penises used? Why did a penis in animals into two major categories: directional degenerate in several earwig families, and which one was asymmetry (DA) and antisymmetry (AS). In the for- lost? To address these questions, structural and behavioral mer case, most individuals of a population are behav- asymmetries were examined in detail for a representative iorally or structurally asymmetrical toward one side species Labidura riparia (Labiduridae). Although there was no detectable morphological differentiation between (either right-handed or left-handed). In populations the right and left penises, male L. riparia predominantly with AS, ‘‘right-handed’’ and ‘‘left-handed’’ individu- used the right one for insemination. This significant als are equally frequent. Based on phylogenetic anal- ‘‘right-handedness’’ developed without any experience of ysis of asymmetry variation among animals, Palmer mating and was also manifested in the resting postures of (1996) pointed out the evolutionary trend by which the two penises when not engaged in copulation. However, AS tends to precede DA in the asymmetrical traits surgical ablation of the right penis did not influence the in- expressed in postlarval phases. For example, phylo- semination capacity of males. In wild-caught males, only genetic patterns of flatfishes suggest that DA has about 10% were left-handed; within this group, abnormal- evolved multiple times from an AS ancestor, which ities were frequently observed in the right penis. These was characterized by polymorphism in the direction lines of evidence indicate that the left penis is merely a spare intromittent organ, which most L. riparia males are of ocular migration (Policansky, 1982; Chapleau, likely never to use. Additional observations of five species 1993). In populations exhibiting AS, the handedness of single-penis families revealed that the left penis degen- of each individual can be determined by environmen- erated in the common ancestor of this group. Considering tal factors rather than genetic factors. Peculiarly, no the proposed sister relationship between the Labiduridae significant response to a particular direction has and the single-penis families, it is possible that such be- been reported for artificial selection of traits show- havioral asymmetries in penis’ use, as observed in L. riparia, ing AS. This finding indicates the significance of are parental to the evolutionary degeneration of the in- frequently used left penis. J. Morphol. 267:1381–1389, Contract grant sponsor: Japan Ministry of Education, Culture, 2006. Ó 2006 Wiley-Liss, Inc. Sports, Science, and Technology; Contract grant number: 16770017. KEY WORDS: earwigs; evolution of genitalia; structural *Correspondence to: Yoshitaka Kamimura, Laboratory of Animal asymmetry; behavioral asymmetry; penis number; ejacu- Ecology, Department of Ecology and Systematics, Graduate School latory ducts; genital damage of Agriculture, Hokkaido University, Kita 9, Nishi 9, Kita-ku, Sap- poro 060-8589, Japan. E-mail: [email protected] Behavioral asymmetry, i.e., the biased use of later- Published online 18 October 2006 in ally paired organs, is a fascinating problem in evolu- Wiley InterScience (www.interscience.wiley.com) tionary and developmental biology. Although vol- DOI: 10.1002/jmor.10484 Ó 2006 WILEY-LISS, INC. 1382 Y. KAMIMURA epigenetic factors in controlling handedness in AS organ (Fig. 1A). Membranous penis lobes surround traits. In contrast, the expression of handedness in each virga (Fig. 1). In this article, a penis lobe and DA traits is likely to be genetically determined. the virga wrapped in it are collectively referred to as Therefore, the evolutionary transition AS ? DA a penis. In Diplatyidae and two subfamilies of Pygi- would be accompanied by a genetic assimilation pro- dicranidae (Pyragrinae and Esphalmeninae) two or cess, i.e., the replacement of an external environmen- bifurcated virgae are present in each of two penis tal trigger of handedness determination by a genetic lobes, resulting in four gonopores per males, while a trigger (Palmer, 1996). Although Palmer’s (1996) single virga with a gonopore per each penis lobe is arguments are focused on structural asymmetries, present in the remaining earwigs (e.g., Popham, behavioral traits are also likely to show the same 1965a). Sperm produced in paired testes and stored trend of AS preceding DA. In relation to the interplay in a seminal vesicle are transferred via a virga di- between behavioral and structural laterality, this rectly into a female sperm storage organ (sperma- possible trend is fascinating because an AS ? DA theca) during mating (Popham, 1965a; Kamimura, transition in behavior would promote the evolution of 2000, 2004a; Fig. 1A). To establish genital contact, DA in the morphology from the ancestral state of lat- males twist their abdomen in a clockwise (CW; eral symmetry. For example, consider laterally viewed from the head of the male) or in the counter- paired organs such as the right and left hand. When clockwise (CCW) direction (Fig. 1A). To date, only a one hand is rarely used for some reason (i.e., the de- handful of species of Diplatyidae and Anisolabididae velopment of behavioral asymmetry) that infre- have been examined in regard to the use patterns of quently used organ may degenerate and so a struc- their two penises. In the Diplatyidae and Pygidicra- tural asymmetry is established. Such a scenario of nidae (so-called ‘‘basal Dermaptera’’) both the right interplay between behavioral and structural asym- and left penises point toward the anterior of the metries is characterized by usage bias of paired body when not in copulation (Fig. 1A for the defini- organs preceding morphological differentiation. To tion of the left-right and anterior-posterior axes). my knowledge, no empirical examples of such transi- Hereafter, the term ‘‘resting state’’ is used to address tional states have been reported. such conditions of the penises when not in copula- tion. In a previous study, I found that male Diplatys flavicollis (Diplatyidae) used either the right (n ¼ 3) Earwig Genitalia as a Model Case or left (n ¼ 6) penis for insemination (Kamimura, Male genital organs and their use patterns in ear- 2004a). Although the sample size of that study was wigs (Insecta: Dermaptera) provide a rare opportu- small, this species can be characterized by its sym- nity to analyze the evolutionary relationship between metrical morphology and possible AS in penis-use behavioral and structural asymmetries. The Dermap- behavior. In the Apachyidae, Anisolabisidae, and tera is usually divided into three suborders: Hemi- Labiduridae the left and right penises point in oppo- merina, Arixeniina, and Forficulina. Members of the site directions when resting (Popham, 1965a; Fig. former two suborders live on mammals and show 1B,C). Because a penis should point straight posteri- special modifications adapted to phoretic habits orly during mating (Fig. 1A), organs pointing poste- (Nakata and Maa, 1974). According to the system of riorly while resting can be considered ready for mat- Sakai (1982), the Forficulina consist of eight families ing (R-ready, Fig. 1B or L-ready, Fig. 1C). For the of free-living typical earwigs: Pygidicranidae (in- Anisolabididae, no significant bias has been re- cluding Karschellidae (Popham, 1965b) as Karscheli- ported for the resting state of Euborellia plebeja (n nae), Diplatyidae (¼ Diplatyinae of Pygidicranidae ¼ 29; Kamimura and Matsuo, 2001), Anisolabis (Steinmann, 1989)), Anisolabididae (¼ Carcinophori- maritima (n ¼ 242; Kamimura and Matsuo, 2001), dae (Popham, 1965b; Steinmann, 1989)), Apachyidae, and A. littorea (n ¼ 32; Giles, 1961). In E. plebeja, Labiduridae, Spongiphoridae (¼ Labiidae (Popham, the actual use pattern of the penises was only 1965b; Steinmann, 1989)), Chelisochidae,