Evolution of the cloacal and genital musculature, and the genitalia morphology in liolemid lizards (Iguania: Liolaemidae) with remarks on their phylogenetic bearing

in Amphibia-Reptilia
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

In this study, we describe the intra- and interspecific anatomical variations of cloacal and related muscles of male and female genitalia in species of five iguanian genera (three liolemid: Ctenoblepharys, Liolaemus, and Phymaturus plus Diplolaemus leopardinus and Tropidurus melanopleurus as outgroups). We found variations (seventeen characters) in topology, origin and insertion areas, tendon morphology and size of the musculature of this region. We also describe the variations of hemipeneal morphology, which is especially notable for the hemipenis of C. adspersa, D. leopardinus, and T. melanopleurus, as this is first time they are described in the literature. Among the most significant findings are the identification of three new muscles, two of them inserted on the roof of the cloacal chamber (anterior and posterior cloacal retractor) and the third inserted superficially in the floor of the cloaca, just before anterior to the precloacal glands row (superficialis cloacalis retractor). We report sexual dimorphism in seven muscle characters. Musculature related to hemiclitoris is reduced in proportion to its size in comparison to the degree of development of male genitalia and associated musculature. The evolution of characters was traced on the known phylogenetic hypotheses of relationships among families. Characters taken from the cloacal/genital myology bring similar support to the liolaemid tree even rooting the analysis using different outgroups. In addition, a phylogenetic study using only myological characters was performed. In this case, C. adspersa was found to be more related to Liolaemus species instead of being basal to Liolaemus plus Phymaturus.

Evolution of the cloacal and genital musculature, and the genitalia morphology in liolemid lizards (Iguania: Liolaemidae) with remarks on their phylogenetic bearing

in Amphibia-Reptilia

Sections

References

AbdalaC.QuinterosS. (2014): Los últimos 30 años de estudios de la familia de lagartijas más diversa de Argentina. Actualización taxonómica y sistemática de Liolaemidae. Cuad. Herpetol. 28 (2): 55-82.

AbdalaV.AbdalaC.TulliM. (2006): Muscular characters in the phylogeny of Liolaemus (Squamata: Iguania: Liolaemidae): a reappraisal. Zootaxa 68 (1205): 55-68.

AbdalaV.MoroS. (2003): A cladistic analysis of ten lizard families (Reptilia: Squamata) based on cranial musculature. Russian Journal of Herpetology 10 (1): 53-73.

ArnoldE.N. (1984): Variation in the cloacal and hemipenial muscles of lizard and its bearing on their relationships. Symp. Zool. Soc. Lond. 52: 47-85.

BarbadilloL.J.BauwensD.BarahonaF.Sanchez-HerraizM. (1995): Sexual differences in caudal morphology and its relation to tail autotomy in lacertid lizards. J. Zool. 236: 83-93.

BiewenerA. (1998): Muscle function in vivo: a comparison of muscles used for elastic energy savings versus muscles used to generate mechanical power. Am. Zool. 38: 703-717.

BiewenerA.GillisG.B. (1999): Dynamics of muscle function during locomotion: accommodating variable conditions. The Journal of experimental biology 202: 3387-3396.

BiewenerA.RobertsT. (2000): Muscle and tendon contributions to force, work, and elastic energy savings: a comparative perspective. Exercise and Sport Science Reviews. The American College of Sports Medicine 28 (3): 99-107.

BockW.ShearC. (1972): A staining method for Gross dissection of vertebrate muscles. Anat. Anz. 130: 222-227.

BöhmeW. (1988): Zur Genitalmorphologie der Sauria: Funktionelle und stammesgeschichtliche Aspekte. Bonner Zoologische Monographien 27: 1-176.

BoninoM.Moreno AzocarD.TulliM.AbdalaC.PerottiM.CruzF. (2011): Running in cold weather: morphology, thermal biology, and performance in the southernmost lizard clade in the world (Liolaemus lineomaculatus section: Liolaemini: Iguania). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 315: 495-503.

CeiJ. (1986): Reptiles del centro centro-oeste y sur de la Argentina. Herpetofauna de las zonas áridas y semiáridas. Monogr.4. Museo Regionale di Scienze Naturali di TorinoTurin.

CeiJ. (1993): Reptiles del noroeste nordeste y este de la Argentina. Herpetofauna de las selvas subtropicales puna y pampas. Monogr.14. Museo Regionale di Scienze Naturali di TorinoTurin.

CooperW.VittL. (1984): Conspecific odor detection by the male broad headed skink, Eumeces laticeps: effects of sex and site of odor source and of male reproductive condition. J. Exp. Zool. 230 (2): 199-209.

CooperW.VittL. (1986): Interspecific odour discrimination by a lizard (Eumeces laticeps). Anim. Behav. 34 (2): 367-376.

Díaz GómezJ. (2009): Historical biogeography of Phymaturus (Iguania: Liolaemidae) from Andean and Patagonian South America. Zool. Scr. 38: 1-7.

DowlingH.SavageJ. (1960): A guide to the snake hemipenis: a survey of basic structure and systematic characteristics. Zoologica 45: 17-28.

EtheridgeR. (1967): Lizard caudal vertebrae. Copeia 4: 699-721.

EtheridgeR. (1995): Redescription of Ctenoblepharys adspersa Tschudi, 1845, and the Taxonomy of Liolaeminae (Reptilia: Squamata: Tropiduridae). Am. Mus. Novit. 3142: 1-34.

FrostD.R.EtheridgeR. (1989): A phylogenetic analysis and taxonomy of iguanian lizards (Reptilia: Squamata). University of Kansas Natural History Museum Miscellaneous Publication 81: 1-65.

FukunagaT.KawakamiY.KuboK.KanehisaH. (2002): Muscle and tendon interaction during human movements. Exercise & Sport Sciences Revivews 30 (3): 106-110.

GabeM.Saint-GironsH. (1965): Contribution à la morphologie comparée du cloaque et des glandes épidermoïdes de la región cloacale chez les lépidosauriens. Mémoires Du Muséum National d’histoire Naturelle Série A: Zoologie 33: 151-292.

GadowH. (1887): Remarks on the cloaca and on the copulatory organs of the amniota. Philosophical Transactions of the Royal Society B: Biological Sciences 178: 5-37.

GauthierJ.A.KearneyM.MaisanoJ.RieppelO.BehlkeA. (2012): Assembling the squamate tree of life: perspectives from the phenotype and the fossil record. Bulletin of the Peabody Museum of Natural History 53: 3-308.

GoloboffP.A.FarrisJ.NixonK. (2003): TNT: Tree Analysis Using New Technology. Version 1.5 2008. Program and documentation available from the authors and at www.zmuc.dk/public/phylogeny.

González MarínA.HernandoA. (2016): Osteologia craneal de Liolaemus azarai Avila 2003 (Squamata: Liolaemidae): Aportes a la variación morfológica del género. Boletin Sociedad Zoologica de Uruguay 25 (1): 52-60.

GrazziotinF.ZaherH.MurphyR.ScrocchiG.BenavidesM.ZhangY.BonattohS. (2012): Molecular phylogeny of the new world Dipsadidae (Serpentes: Colubroidea): a reappraisal. Cladistics 1: 1-23.

GüntherA. (1867): Contribution to the Anatomy of Hatteria (Rhynchocephalus, Owen). Philos. Trans. R. Soc. London 157: 595-629.

HainesW. (1935): Some muscular changes in the tail and thigh of reptiles and mammals. J. Morphol. 58 (2): 355-383.

KellerC.KrauseL. (1986): The appendicular skeleton of Liolaemus occipitalis Boulenger, 1885 (Sauria, Iguanidae). Rev. Bras. Biol. 46 (4): 727-740.

LereboulletD. (1851): Recherches sur l’anatomie des organes génitaux des animaux vertébrés.

LieberR.BrownC.TrestikC. (1992): Model of muscle-tendon interaction during frog semitendinosis fixed-end contractions. Journal of Biomechanics 25 (4): 421-428.

LoboF. (2000): La ornamentación de los hemipenes en Liolaemus (Iguania: Tropiduridae). Cuad. Herpetol. 14 (2): 145-151.

LoboF.AbdalaC. (2002): La información cladística de un set de datos morfológicos en lagartos del género Liolaemus (Iguania: Liolaemidae). Cuad. Herpetol. 16 (2): 137-150.

LoboF.EspinozaR.QuinterosS. (2010): A critical review and systematic discussion of recent classification proposals for liolaemid lizards. Zootaxa 2549: 1-10.

LoboF.AbdalaC.ValdecantosV. (2012): Morphological diversity and phylogenetic relationships within a south-american clade of iguanian lizards (Liolaemidae: Phymaturus). Zootaxa 3315: 1-41.

LoboF.BarrassoD.HibbardT.BassoN. (2016): On the evolution and diversification of an Andean clade of reptiles: combining morphology and DNA sequences of the palluma group (Liolaemidae: Phymaturus). J. Linn. Soc. London Zool. 176 (3): 648-673.

MorandoM.AvilaL.PérezC.HawkinsM.SitesJ.Jr. (2013): A molecular phylogeny of the lizard genus Phymaturus (Squamata, Liolaemini): implications for species diversity and historical biogeography of southern South America. Mol. Phylogenet. Evol. 66 (3): 694-714.

PyronR.BurbrinkF.WiensJ. (2013): A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13: 1-93.

ReederT.W.TownsendT.MulcahyD.NoonanB.WoodP.SitesJ.WiensJ. (2015): Integrated analyses resolve conflicts over squamate reptile phylogeny and reveal unexpected placements for fossil taxa. PLoSONE 10 (3): 1-22.

RitzmanT.StroikL.JulikE.HutchinsE.LaskuE.DenardoD.Wilson-RawlsJ.RawlsJ.KusumiK.FisherR. (2012): The Gross anatomy of the original and regenerated tail in the green anole (Anolis carolinensis). Anat. Rec. 295: 1596-1608.

RussellA.BauerA.M. (1992): The m. caudifemoralis longus and its relationship to caudal autotomy and locomotion in lizards (Reptilia: Sauria). J. Zool. 227: 127-143.

RussellA.BergmannP.BarbadilloL. (2001): Maximal caudal autotomy in Podarcis hispanica (Lacertidae): the caudofemoralis muscle is not sundered. Copeia 1: 154-163.

Sanchez-MartinezP.Ramirez-PinillaM.Miranda-EsquivelD. (2007): Comparative histology of the vaginal-cloacal region in Squamata and its phylogenetic implications. Acta Zoologica 88 (4): 289-307.

SchulteJ.ValladaresJ.LarsonA. (2003): Phylogenetic relationships within Iguanidae inferred using molecular and morphological data and a phylogenetic taxonomy of iguanian lizards. Herpetologica 59 (3): 399-419.

ThieleK. (1993): The holy grail of the perfect character: the cladistic treatment of morphometric data. Cladistics 9: 275-304.

TulliM.CruzF.HerrelA.VanhooydonckB.AbdalaV. (2009): The interplay between claw morphology and microhabitat use in Neotropical iguanian lizards. Zoology 112 (5): 379-392.

ValdecantosS.LoboF. (2015): First report of hemiclitores in females of South American liolaemid lizards. J. Herpetol. 49 (2): 291-294.

ValdecantosS.MartinezV.LabraA. (2015): Description of a proctodeal gland present in three South American Liolaemus lizards (Iguania: Liolaemidae). Salamandra 51 (2): 182-186.

WiensJ.J.HutterC.R.MulcahyD.G.NoonanB.P.TownsendT.M.SitesJ.W.ReederT.W. (2012): Resolving the phylogeny of lizards and snakes (Squamata) with extensive sampling of genes and species. Biol. Lett. 8: 1043-1046.

ZaherH.PrudenteA. (2003): Hemipenes of Siphlophis (Serpentes, Xenodontinae) and techniques of hemipenial preparation in snakes: a response to dowling. Herpetological Review 34 (4): 302-307.

ZhengY.WiensJ. (2016): Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol. Phylogenet. Evol. 94: 537-547.

ZieglerT.BöhmeW. (1999): Genital morphology and systematics of two recently described monitor lizards of the varanus (Euprepiosaurus) indicus group. Mertensiella 11: 121-128.

Figures

  • View in gallery

    Ventral view of the cloacal region muscles in a male of Liolaemus irregularis (MCN 1885). The head of the specimen is located upwards, while the tail is located down. (A) General disposition of the superficial muscles. (B) Post cloacal superficial muscles. See the disposition of the posterior cloacal retractor, partially covering the transversus penis. (C) Pre-cloacal superficial muscles. (D) Anterior and posterior lateral retractor muscles. See the retractor lateral anterior division. (E) Compressor glandulae located dorsal to the transversus perinei (transversus perinei cut off from its position on the left side). (F) Disposition of the anterior cloacal retractor passing dorsal to the cloacal chamber and the origin of the ischiocaudalis tendon (superficial muscles dissected). Abbreviations as follows = H: hemipenis; Is: ischium; IC: ischiocaudalis; ILC: Iliocaudalis; PC: precloacal glands; PCR: posterior cloacal retractor; TP: transversus perinei; TPN: transversus penis; SCR: superficialis cloacal retractor; CG: compressor glandulae; ACR: anterior cloacal retractor; RLA: retractot lateral anterior; RLP: retractor lateral posterior; ICT: ischiocaudalis tendon. Scale = 0.5 mm.

  • View in gallery

    The head of the specimen is located upwards, while the tail is located down. (A) Internal muscles in a male of Tropidurus melanopleurus (IBIGEO 5317). See the origin of the ischiocaudalis tendon in the lateral margin of the ischium, the common insertion of anterior and posterior cloacal retractors in a fascia dorsal to the cloacal chamber. (B) Internal muscles in the male of Phymaturus palluma (MCN 2894). See the dorsal insertion of the ischiocaudalis tendon in the ischial bone. (C) See how the posterior cloacal retractor partially covers the transversus penis. (D) Posterior cloacal retractor located medially to the ischiocaudalis, not in contact or covering the transversus penis. Abbreviations as follows = Is: ischium; H: hemipenis; IC: ischiocaudalis; PC: precloacal glands; PCR: posterior cloacal retractor; TPN: transversus penis; ACR: anterior cloacal retractor; ICT: ischiocaudalis tendon; CF: caudofemoralis. Scale = 0.5 mm.

  • View in gallery

    (A) Hemipenis asulcate face of Liolaemus irregularis (MCN 1884). (B) Hemipenis sulcate face of L. irregularis. (C) Asulcate face of Liolaemus austromendocinus (MCN 3686). (D) Sulcate face of L. austromendocinus. (E) Asulcate view of hemipenis of P. patagonicus (MCN 3275). (F) Sulcate face of the hemipenis of P. patagonicus. See dark pigmentation of the sulcus spermaticus in this species. (G) Asulcate face of the hemipenis of P. palluma (MCN 2894). (H) Sulcate face of the hemipenis of P. palluma. The arrow indicates the extended ornamentation in P. patagonicus. Abbreviations = C: calices; P: plicae; SS: sulcus spermaticus; AL: apical lobes; RP: round prominence; SSP: sulcus spermaticus plicae. Scale = 0.5 mm.

  • View in gallery

    (A) Asulcate view of hemipenis of Ctenoblepharys adspersa (MUSA 4613). (B) Sulcate face of the hemipenis of C. adspersa. (C) View asulcate face of hemipenis of Diplolaemus leopardinus (IBIGEO 5493). (D) View sulcate face the hemipenis of D. leopardinus. (E) View asulcate face of hemipenis of Tropidurus melanopleurus (IBIGEO 5317). (F) Sulcate face the hemipenis of Phymaturus T. melanopleurus. Scale = 0.5 mm.

  • View in gallery

    Trees obtained from the data set of this work. (A) Consensus tree recovered performing an analysis of the present anatomical data with the Tropidurus melanopleurus as outgroup. (B) Consensus tree of the same analysis but rooting the tree with Diplolaemus leopardinus. (C) Rebuilt tree with Ctenoblepharys adspersa as the basal taxon in the Liolaemidae family following relationships recovered molecular and morphological in previous studies. Numbers on branches (apomorphies) correspond to characters described in the character list (see also table S1).

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 17 17 15
Full Text Views 11 11 10
PDF Downloads 2 2 1
EPUB Downloads 0 0 0