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

Abstract

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, andPhymaturusplusDiplolaemusleopardinusandTropidurusmelanopleurusas 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 ofC. adspersa,D. leopardinus, andT. 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. adspersawas found to be more related toLiolaemusspecies instead of being basal toLiolaemusplusPhymaturus.

Neuroanatomy of the lumbosacral plexus in a highly diversified clade of South‐American lizards. Evolution and phylogenetic implications

“…To identify and name the muscles of the hind limbs, we followed to Hoyos (1990) and for the identification of the muscles of the cloacal region we followed Arnold (1984) and Quipildor, Abdala, Santa Cruz Farfán, and Lobo (2018).…”

Male genitalia's evolutionary rate is higher than those of body traits: the case of two Liolaemus lizards' group

“…In many groups of animals, such as beetles, molluscs, fishes, snakes, lizards, and some mammals, male genitalia present morphological characteristics which have been used for systematic and taxonomic studies (Sharp & Muir, 1912; Hamilton, 1946; Gordon & Roses, 1951; Jeannel, 1955; Tuxen, 1956; Arnold, 1986a; Fitzpatrick et al ., 2012; Klaczko, Ingram & Losos, 2015; D'Angiolella et al ., 2016). In some cases, given the uniformity of some genital features, these have been used to define genera or higher taxonomic categories (Böhme, 1988; Keogh, 1999; Maduwage et al ., 2008; Köhler, 2009; Quipildor et al ., 2018a). Despite the strong phylogenetic correspondence in genital morphology, it is interesting to observe that many sister or closely related species often exhibit high divergences in some aspects of their morphology, including greater than those observed among more phylogenetically distant species (Arnold, 1986a; Böhme, 1988; Lobo, 2000; Köhler, Dehling & Köhler, 2010; Köhler, Hahn & Köhler, 2012; Quipildor et al ., 2018a).…”

“…In some cases, given the uniformity of some genital features, these have been used to define genera or higher taxonomic categories (Böhme, 1988; Keogh, 1999; Maduwage et al ., 2008; Köhler, 2009; Quipildor et al ., 2018a). Despite the strong phylogenetic correspondence in genital morphology, it is interesting to observe that many sister or closely related species often exhibit high divergences in some aspects of their morphology, including greater than those observed among more phylogenetically distant species (Arnold, 1986a; Böhme, 1988; Lobo, 2000; Köhler, Dehling & Köhler, 2010; Köhler, Hahn & Köhler, 2012; Quipildor et al ., 2018a). Some authors have suggested that these divergences could be consequence of a high rate of change in genital features respect to non‐genital features (Eberhard, 2009; Rowe & Arnqvist, 2011; Klaczko, Ingram & Losos, 2015).…”

“…This genus is divided into two subgenera, Liolaemus sensu stricto or Chilean group and Eulaemus , or Argentinean group (Laurent, 1983), differing in their evolutionary history, which is in turn reflected in the diversity of species of the internal groups (e.g., Esquerré et al ., 2019). Previous work on the genus' hemipenial morphological diversity has shown a great diversity in shapes among species in each subgenus, reflecting their potential use in taxonomic and systematic studies (Lobo, 2000; Quipildor et al ., 2018a,b). Even though the phylogenetic relationships are well studied, until this moment no comparative studies have been made evaluating the evolution of different genital features with respect to other non‐genital features and their potential relationship to the diversity of species within Liolaemus .…”

Hemipenial morphology of nine South American species of Mabuya (Scincidae: Lygosominae) with comments on the morphology of the family

“…Additionally, the specific interest in investigating variations in these sexual structures can be related to supposed independence from evolutionary pressures, which probably would affect other morphological characters (Arribas, ; Myers, ) as demonstrated by Klaczko, Ingram, and Losos () in anoles. Studies about hemipenial morphology and its systematic implications are published for some groups of lizards such as agamids (Maduwage & Silva, ), amphisbaenids (Rosenberg, ), anguimorphs (e.g., Böhme, ; Böhme & Ziegler, ; Branch, ; Ziegler, Gaulke, & Böhme, ); anoles (e.g., D'Angiolella, Klaczko, Rodrigues, & Avila‐Pires, ; Klaczko et al, ; Klaczko, Gilman, & Irschick, ; Köhler, Hahn, & Köhler, ; Köhler & Sunyer, ), geckonids (e.g., Das & Purkayastha, ; Kluge, ; Rösler, ; Rösler & Böhme, ), gymnophthalmids (e.g.,Köhler & Veselý, ; Myers, Fuenmayor, & Jadin, ; Nunes et al, ; Nunes, Curcio, Roscito, & Rodrigues, ; Rodrigues et al, ), iguanids (e.g., Böhme & Ziegler, ; Brygoo & Doumergue, ; Lobo, ; Noble & Bradley, ; Quipildor et al, ,b), lacertids (e.g., Arnold, , , , ; Arribas, , ), and teiids (Uzzell, , , , , ). For scincids , the available descriptions are of a few taxa from Australia and the Old World (Cope, ; Noble & Bradley, ; Greer, ; Zug, ; Linkem, Diesmos, & Brown, ; Mecke, Doughty, & Donnellan, ; Nunes et al, ; Vergilov, Zlatkov, & Tzankov, ; Neang, Chan, & Poyarkov, ; Mecke and Doughty, 2018).…”