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Are Hemipenial Spines Related to Limb Reduction? a Spiny Discussion Focused on Gymnophthalmid Lizards (Squamata: Gymnophthalmidae)

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Are Hemipenial Spines Related to Limb Reduction? a Spiny Discussion Focused on Gymnophthalmid Lizards (Squamata: Gymnophthalmidae) THE ANATOMICAL RECORD 297:482–495 (2014) Are Hemipenial Spines Related to Limb Reduction? A Spiny Discussion Focused on Gymnophthalmid Lizards (Squamata: Gymnophthalmidae) PEDRO M. SALES NUNES,* FELIPE F. CURCIO, JULIANA G. ROSCITO, AND MIGUEL T. RODRIGUES Departamento de Zoologia, Instituto de Biociencias,^ Universidade de Sao~ Paulo, Caixa Postal 11.461, CEP 05422-970, Sao~ Paulo, SP, Brazil ABSTRACT Calcified spines in the hemipenial surface occur convergently in sev- eral gymnophthalmid lizard species and in advanced snakes. Based on the pronounced degrees of limb reduction in these distantly related line- ages, such hemipenial structures were suggested to play a functional role in couple-anchoring during copulation, partly assuming the function of the limbs during mating. Herein, we assessed the hemipenial morphology of virtually all the valid genera of the family Gymnophthalmidae to test for a phylogenetic correlation between limb reduction and the presence of calcified hemipenial spines. The occurrence of calcified structures was mapped on the two most comprehensive phylogenies of the family. We concluded that spiny hemipenes are by no means necessarily associated with reduction of limbs. Conversely, the presence of well-developed hemi- penial spines in specific limb-reduced taxa does not allow one to disregard the possibility that in some instances such structures might indeed be functionally associated with couple-anchoring, improving the success of mating. Anat Rec, 297:482–495, 2014. VC 2014 Wiley Periodicals, Inc. Key words: lepidosaurs; hemipenis; ornamentation; limb reduction; copulation INTRODUCTION Limb reduction, defined as the partial or complete phylogenetic loss of skeletal elements of the limbs rela- tive to a typical four-limbed, pentadactyl condition (Greer, 1991; Shapiro, 2002), is widespread in the evolu- Additional Supporting Information may be found in the online version of this article. tion of Tetrapoda. Different degrees of limb reduction ~ are particularly common in the order Squamata, with Grant sponsor: Fundac¸ao de Amparo a Pesquisa do Estado de Sao~ Paulo (FAPESP); Grant numbers: 2011/50146-6, 2012/ several independent events among its lineages (Greer, 00492-8, 2012/00547-7, 2012/01319-8; Grant sponsor: Conselho 1991; Wiens et al., 2006; Skinner, 2008). Nacional de Desenvolvimento Cientıfico e Tecnologico (CNPq). The most pronounced instances of fore and/or hind *Correspondence to: P. M. S. Nunes; Departamento de Zoo- limb reduction in squamates (complete limblessness or logia, Instituto de Biociencias,^ Universidade de Sao~ Paulo, partial reduction affecting functionality) occur in the Caixa Postal 11.461, CEP 05422-970, Sao~ Paulo, SP, Brazil. major clades Serpentes and Amphisbaenia, as well as in Fax: 155 11 3091 75 13. [email protected] the lizard families Anguidae, Annielidae, Cordylidae, Received 25 February 2013; Accepted 23 May 2013. Dibamidae, Gymnophthalmidae, Pygopodidae, and Scin- DOI 10.1002/ar.22876 cidae. Among lizards, the vast majority of reduction Published online 31 January 2014 in Wiley Online Library events occur in the Scincidae [16 to 20 events (Miralles (wileyonlinelibrary.com). VC 2014 WILEY PERIODICALS, INC. ARE HEMIPENIAL SPINES AND LIMB SIZE RELATED? 483 et al., 2012) or 27 events only among Lerista (Skinner of Anguis fragilis, an assumption likely based on the et al., 2008)]. Another group showing multiple events of descriptions of Cope (1896) and on an illustration by limb reduction is the Gymnophthalmidae. According to Bohme€ (1988), since they provide no evidences that such Pellegrino et al. (2001), at least five independent events structures are in fact calcified. The absence of any traces of limb reduction have occurred within the Gymnoph- of calcified structures in the hemipenis of other Angui- thalmidae: one in the subfamily Rachisaurinae (Rachi- dae (Thomas and Hedges, 1998; personal observation), saurus brachylepis); two in the subfamily even after staining tests with Alizarin Red solution casts Gymnophthalminae (tribes Gymnophthalmini and Het- further doubts upon their work and leaves the question erodactylini); and two in the subfamily Cercosaurinae open for further investigation. [genera Anotosaura (subfamily Epleopodinae, sensu The remarkable degrees of limb-reduction seen in Castoe et al., 2004) and Bachia (tribe Bachiini, sensu snakes and in some gymnophthalmids, combined with Castoe et al., 2004)] (see Pellegrino et al., 2001; Castoe the presence of calcified hemipenial spines in both et al., 2004; Rodrigues and Dos Santos, 2008; Rodrigues groups, may have led Presch (1978) to associate the com- et al., 2009 for systematic accounts). plexity in hemipenial ornamentation with dramatic Limb reduction is usually associated with body elon- instances of limb reduction and/or total limblessness. gation, resulting in a snake-like body form that is often This assumption is based on the premise that, in the related to fossorial, sand-dwelling, or grass-dwelling absence of well-developed limbs, other anatomical struc- habits (Caputo et al., 1995; Lee, 1998; Wiens and Sling- tures (i.e., hemipenial spines) could take on the role of luff, 2001). In addition, such snake-like morphology keeping male and female tightly attached while mating. implies in biomechanical and physiological adaptations However, with respect to gymnophthalmids, Presch’s of most body systems (Underwood, 1976; Caputo et al., (1978) observations were not supportive of such a 1995). However, there is only a handful of revisions straightforward rationale, since he reported virtually about modifications of the genital system and/or repro- nude hemipenes both in taxa with well-developed limbs ductive behavior of squamates and its correlation with (e.g., species of the genera Anadia, Euspondylus, Gym- limb reduction (e.g., Presch, 1978; Olsson and Madsen, nophthalmus, Proctoporus, and Riama), as well as in 1998; Sanchez-Mart ınez et al., 2007). two greatly limb-reduced species of the genus Bachia (B. The use of genital morphology as an indication of kin- intermedia and B. trisanale). Posterior studies (Myers ship (Dowling, 1957; Arnold, 1986b; Nunes et al., 2012) and Donnelly, 2001; Nunes, 2011) revealed the presence is mostly supported by evidence from sexual selection of calcified spicules embedded in the hemipenial flounces (Eberhard, 1985, 2010). In contrast, most functional of the fully limbed species Anadia ocellata, which were interpretations of hemipenial ornaments [e.g., mechani- unnoticed by Presch (1978), most likely due to prepara- cal stimulation (King et al., 2009), increase of copula tion artifacts. Thus, Presch’s (1978) observations sug- duration (King et al., 2009; Olsson and Madsen, 1998), gested an opposite pattern to the one predicted in his gaping of female cloaca (Pisani, 1976) and lifting of the first assumption, with limb-reduced taxa showing poorly anal plate (Pisani, 1976)] are widely speculative. Even ornamented organs, whereas conspicuous ornaments though, there seems to be a widespread assumption that were common among taxa with well-developed limbs. such structures must be directly involved in couple- Despite the inconclusiveness of Presch’s (1978) results, anchoring during the sexual act to ensure efficient the putative relationship of limblessness with complex sperm transfer (Pope, 1941; Edgren, 1953; Pisani, 1976; hemipenial ornamentation deserves further attention for Murphy and Baker, 1980). the following reasons: (i) Presch’s (1978) sampling was far Calcified hemipenial spines and spicules are appa- from comprehensive, including only one of the limb- rently restricted to some gymnophthalmid lizards (e.g., reduced gymnophthalmid lineages (i.e., the tribe Bachiini, Uzzel, 1965; Estes et al., 1988; Nunes, 2011; Nunes sensu Castoe et al., 2004); and (ii) the family Gymnoph- et al., 2012) and several representatives of a major line- thalmidae is especially informative for studies concerning age of snakes [Colubroides sensu Zaher et al. (2009)]. the “by-products” of limblessness because the several Calcified hemipenial structures have also been reported reduction events can be traced in the two recent phyloge- for other squamate groups, but the homology and gen- nies (Pellegrino et al., 2001; Castoe et al., 2004). There- eral structure of such elements are debatable. For exam- fore, if the patterns of hemipenial ornamentation are ple, Arnold (1973, 1986a) mentions a possible seasonal confronted with well-supported phylogenetic trees, one presence of minute spines in the Lacertidae, but this can directly assess the possible hierarchic relationship observation has received no further attention. In addi- between limb morphology and hemipenial ornamentation. tion, distinct calcified hemipenial structures have been In this study, we dedicate special attention to hemipe- reported in some Varanidae (McDowell and Bogert, nial spines. A recent study on the hemipenial morphol- 1954; Ziegler et al., 2007; Koch et al., 2009; Welton ogy of the Gymnophthalmidae allowed the unequivocal et al., 2010), Gekkonidae and Sphaerodactylidae (Kluge, detection of distinct patterns of calcified spines and spi- 1982; Rosler€ and Bohme,€ 2006) representing internal cules in the hemipenes of several genera of the family skeletal structures referred to as a hemibaculum,as (Nunes, 2011). Based on the considerable variation in well as apical horns acting as extensions of the retractor size and organization of such structures among the gym- muscles (Branch, 1982). Observations of hemipenial
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