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Map depicting distribution of Heloderma horridum and H. suspectum with shaded areas depicting putative subspecific ranges (following Campbell and Lamar, 2004).
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We analyzed both mitochondrial (mt-) and nuclear (n) DNAs in a conservation phylogenetic framework to examine deep and shallow histories of the Beaded Lizard (Heloderma horridum) and Gila Monster (H. suspectum) throughout their geographic ranges in North and Central America. Both mtDNA and intron markers clearly partitioned each species. One intron...
Citations
... This result could mean that low levels of diversifying selection act on indels to a greater extent than SNPs in our data set, perhaps due to effects on gene regulation. In animals, indels have not been examined extensively in studies of geographic variation of nuclear genes of birds or other groups (Brito & Edwards, 2009), although they have been important in phylogenetic reconstruction (Douglas et al., 2010;Lee et al., 2012;Houde et al., 2019). Schaeffer (2002) examined indel diversity among multiple strains of Drosophila pseudoobscura, modelled as a single population, and found that purifying selection acted on deletion variants but not insertion variants. ...
The Carpentarian barrier across north-eastern Australia is a major biogeographic barrier and a generator of biodiversity within the Australian Monsoonal Tropics. Here we present a continent-wide analysis of mitochondrial (control region) and autosomal (14 anonymous loci) sequence and indel variation and niche modelling of brown and black-tailed treecreepers (Climacteris picumnus and Climacteris melanurus), a clade with a classic distribution on either side of the Carpentarian barrier. mtDNA control region sequences exhibited reciprocal monophyly and strong differentiation (Fst = 0.91), and revealed a signature of a recent selective sweep in C. picumnus. A variety of tests support an isolation-with-migration model of divergence, albeit with low levels of gene flow across the Carpentarian barrier and a divergence time between species of ~1.7–2.8 Mya. Palaeoecological niche models show that both range size as measured by available habitat and estimated historical population sizes of both species declined in the past ~600 kyr and that the area of interspecific range overlap was never historically large, perhaps decreasing opportunities for extensive gene flow. The relatively long divergence time and low opportunity for gene flow may have facilitated speciation more so than in other co-distributed bird taxa across the Australian Monsoonal Tropics.
... Animal venoms evolved in a wide phylogenetic range of organisms for predatory and defensive purposes (Fry et al., 2009a;Calvete 2017;Schendel et al., 2019;Zancolli and Casewell, 2020). In reptiles, venom has been hypothesized to originated just once, approximately in the mid-Jurassic (170 mya), in a monophyletic clade coined Toxicofera that combines the suborders Serpentes, Anguimorpha, and Iguania of scaled reptiles (Vidal and Hedges, 2009;Fry et al., 2006Fry et al., , 2012Douglas et al., 2010;Koludarov et al., 2017). ...
... In other anguimorphan lizards, like the Varanidae species, both the existence of a "venom system" and their denomination as "venomous" animals have been called in question (Weinstein et al., , 2013Kardong 2012;Sweet, 2016). This also applies to the earless monitor lizard Lanthanotus borneensis (Mebs et al., 2021), a close relative of the Varanidae family (Ast 2001;Douglas et al., 2010;Wiens et al., 2012;Pyron et al., 2013). Proteomic analysis confirmed the presence of kallikrein as the major biologically active component of the monitor lizard's submandibular gland extract (Mebs et al., 2021), as shown also in previous studies (Koludarov et al., 2017;Fry et al., 2006Fry et al., , 2009bFry et al., , 2010aFry et al., , 2010b. ...
... Based on its many primitive anatomical features, S. crocodilurus is considered a remnant reptile from the Pleistocene (Huang et al., 2008), thus bearing a great taxonomic value for understanding the origin and evolutionary radiation of Toxicofera squamates and their venoms. The extant monophyletic Anguimorpha clade is split into two groups (Fig. 3) (Douglas et al., 2010;Reeder et al., 2015;Brennan et al., 2021). One clade includes the lineages Shinisauridae and Lanthanotidae, represented respectively by the non-venomous Chinese crocodile lizard Shinisaurius crocodilurus (this work) and the earless monitor lizard Lanthanotus borneensis (Mebs et al., 2021) as sister taxa to Varanidae (which among its roughly 80 described members includes venomous varanid species, such as the Komodo dragon, Varanus komodoensis (Brennan et al., 2021). ...
Based on its phylogenetic relationship to monitor lizards (Varanidae), Gila monsters (Heloderma spp.), and the earless monitor Lanthanotus borneesis, the Chinese crocodile lizard, Shinisaurus crocodilurus, has been assigned to the Toxicofera clade, which comprises venomous reptiles. However, no data about composition and biological activities of its oral secretion have been reported. In the present study, a proteomic analysis of the mandibular gland of S. crocodilurus and, for comparison, of the herbivorous Solomon Island skink Corucia zebrata, was performed. Scanning electron microscopy (SEM) of the teeth from S. crocodilurus revealed a sharp ridge on the anterior surface, but no grooves, whereas those of C. zebrata possess a flattened crown with a pointed cusp. Proteomic analysis of their gland extracts provided no evidence of venom-derived peptides or proteins, strongly supporting the non-venomous character of these lizards. Data are available via ProteomeXchange with identifier PXD039424.
... The topology and divergence times were gathered from the TimeTree database (accessed 1 December 2022) [4,5]. For taxa that were not already included in TimeTree, we used existing studies of Gehyra [149][150][151][152], Heloderma [153], Physignathus [154], Gopherus [155,156], Actinemys [157], Cuora [158,159], and Myanophis [160,161] to place taxa and determine the approximate divergence time. ...
... The topology and divergence times were gathered from the TimeTree database (accessed 1 December 2022) [4,5]. For taxa that were not already included in TimeTree, we used existing studies of Gehyra [149][150][151][152], Heloderma [153], Physignathus [154], Gopherus [155,156], Actinemys [157], Cuora [158,159], and Myanophis [160,161] to place taxa and determine the approximate divergence time. Horizontal bars delineate the major clades: Squamata, Rhyncocephalia ("R"), Testudines, and Crocodylia ("Croc"). ...
Non-avian reptiles comprise a large proportion of amniote vertebrate diversity, with squamate reptiles—lizards and snakes—recently overtaking birds as the most species-rich tetrapod radiation. Despite displaying an extraordinary diversity of phenotypic and genomic traits, genomic resources in non-avian reptiles have accumulated more slowly than they have in mammals and birds, the remaining amniotes. Here we review the remarkable natural history of non-avian reptiles, with a focus on the physical traits, genomic characteristics, and sequence compositional patterns that comprise key axes of variation across amniotes. We argue that the high evolutionary diversity of non-avian reptiles can fuel a new generation of whole-genome phylogenomic analyses. A survey of phylogenetic investigations in non-avian reptiles shows that sequence capture-based approaches are the most commonly used, with studies of markers known as ultraconserved elements (UCEs) especially well represented. However, many other types of markers exist and are increasingly being mined from genome assemblies in silico, including some with greater information potential than UCEs for certain investigations. We discuss the importance of high-quality genomic resources and methods for bioinformatically extracting a range of marker sets from genome assemblies. Finally, we encourage herpetologists working in genomics, genetics, evolutionary biology, and other fields to work collectively towards building genomic resources for non-avian reptiles, especially squamates, that rival those already in place for mammals and birds. Overall, the development of this cross-amniote phylogenomic tree of life will contribute to illuminate interesting dimensions of biodiversity across non-avian reptiles and broader amniotes.
... The taxonomy of Reiserer et al. (2013), adopted by Reptile Database (www.reptile-database.org), recognizes the species-level designation of H. charlesbogerti, and is followed here (See Douglas et al. 2010). The mating ecology of this species is poorly understudied due to its cryptic nature, where individuals live and likely mate in underground shelters (Ariano-Sanchez and Salazar 2015). ...
Within captive management programs for species of conservation concern, understanding the genetic mating system is of fundamental importance, given its role in generating and maintaining genetic diversity and promoting opportunities for sperm competition. If a goal of a conservation program is reintroduction, knowledge of the mating system may also inform prediction models aimed at understanding how genetic diversity may be spatially organized, thus informing decisions regarding where and which individuals should be released to maximize genetic diversity in the wild population. Within captive populations, such information may also influence how animals are maintained in order to promote natural behaviors. Here we investigate the genetic mating system of the Guatemalan beaded lizard, Heloderma charlesbogerti, a member of an entire clade lacking such information. A group of adult male and female H. charlesbogerti co-habited a large outdoor enclosure for five years during the species’ perceived breeding season. Through genomic parentage analysis, 50% of clutches comprising multiple offspring were found to result from multiple paternity, with up to three males siring offspring within single clutches. Both males and females were observed to produce offspring with multiple partners within a given year. As such, within this captive environment, where opportunities existed for mating with multiple partners, the genetic mating system was found to be highly polygamous, with multiple paternity common within clutches. These findings are novel for the family Helodermatidae, and the results have broader implications about how reproductive opportunities should be managed within captive conservation programs.
... The available results suggest that Iguania now is not the basal clade of squamates but, on the contrary, is regarded as a derived evolutionary lineage clustering with anguinomorphan lizards and/or snakes. Subsequent molecular studies have confirmed that the group Scincomorpha is not monophyletic, and they demonstrated profound differences in the interpretation of the position of Iguania as a sister group to the snakes [51], Anguimorpha [26,52,53], Gekkota [54], Anguimorpha + Scincidae [55], or Anguimorpha + Serpentes [51]. In the recovered phylogenetic tree [56], Iguania is not a monophyletic group, while Acrodonta and Serpentes form a clade positioned as a sister group relative to the remaining squamates; Iguanidae is united in one clade with Scincomorpha. ...
We present a review of the data on the intervertebral autotomy and regeneration of agamid lizards based on an analysis of information obtained over a 35-year period after the publication of thorough reviews (Arnold, 1984, 1988 and Bellairs, Bryant, 1985). It is supplemented by our own studies of 869 specimens of agamid lizards (Sauria, Agamidae) stored in the herpetological collections of the Zoological Institute of the Russian Academy of Sciences (St. Petersburg, Russia) and the Zoological Museum of the Moscow State University (Moscow, Russia), represented by 31 species of 16 genera. The manifestations of the ability for autotomy and regeneration in phylogenetic lineages within the family—Leiolepidinae, Amphibolurinae, Agaminae, Draconinae—are considered. A comparative morphological analysis of the structure of the caudal vertebrae was carried out using the Computer Microtomography Methods (micro-CT) in the following ecomorphological types of agama: (1) with developed abilities to caudal autotomy and regeneration, (2) with the ability to caudal autotomy but without regeneration and (3) without the ability to autotomy. The phenomenon of intervertebral autotomy (urotomy) in snakes is considered too. Possible ways of evolution of the ability to caudal autotomy as a defense strategy against predators are discussed in the phylogenetic context.
... Heloderma (the only extant truly venomous lizard; Beck, 2005) is widely studied throughout its present distribution from southern-most Nevada and Utah, south through the deserts of Arizona, south through Sonora, and along the Pacific coastal region of Mexico to southern Guatemala (Bogert and Martín del Campo, 1956;Lowe et al., 1986;Campbell and Vannini, 1988;Beck, 1990). In the United States there is one extant species, Heloderma suspectum (Gila Monster), which ranges south into northern Mexico, and from northern Mexico to Guatemala there are four more related species (Douglas et al., 2010;Reiserer et al., 2013): Heloderma alvarezi (Chiapan Beaded Lizard), Heloderma charlesbogerti (Guatemala Beaded Lizard), Heloderma exasperatum (Rio Fuerte Beaded Lizard), and Heloderma horridum (Mexican Beaded Lizard) (Bogert and Martín del Campo, 1956;Campbell and Vannini, 1988). The Monstersauria have a long but spotty fossil record in North America extending from the late Cretaceous (Nydam, 2000) through the Quaternary (Mead et al., 2012). ...
Paleontological occurrences of helodermatid lizards (Helodermatidae) are relatively uncommon and scattered in the North American fossil record. A recently discovered concentration of vertebrate fossils was exposed in a karstic fissure filling in an active rock quarry in southwestern Oklahoma. Underwater screening of the ancient cave fill yielded numerous isolated and fragmentary skeletal elements of a diversity of small, and a few large, vertebrates including unexpected remains of Heloderma sp. as well as extinct large mammals (horse, peccary, Dwarf Pronghorn), indicating Pleistocene age. Radiometric dating of the locality is not possible because of the leaching, but fossils of the Prairie Vole, Microtus ochrogaster, from the locality help to constrain the age of the deposit between 1.21 Ma and 0.01 Ma. The fossils are the first of Heloderma in the Pleistocene of Oklahoma and the southern Great Plains. Based on taphonomic evidence and the relative abundance of rodent teeth, we infer that the fossils accumulated at least partly as the remains of vertebrates fed upon by Ringtails (Bassariscus; Procyonidae) and other small carnivorous mammals. The Pleistocene occurrence of Heloderma in the southern Great Plains of North American has potential implications for the paleobiogeography of the genus and begs further investigation of fossil herpetofaunas in North America.
... Much later, based on anatomical characters, such as lack of grooved teeth and absence of a venom gland, McDowell and Bogert (1954) concluded that it should represent its own family, Lanthanotidae, as member of the Angiomorpha lineage. More recently, molecular genetic evidence confirmed its close relationship to monitor lizards (Varanidae) (Ast, 2001;Douglas et al., 2010;Wiens et al., 2012;Pyron et al., 2013). ...
Based on its mandibular gland secretion, the earless monitor lizard, Lanthanotus borneensis, has been considered a venomous animal like other members of the Toxicofera group, including Heloderma. In the present study, the gland structure and teeth of L. borneensis were examined by micro-tomography (μCT) and scanning electron microscopy (SEM), respectively, and proteomic analysis of the gland extract was performed. The mandibular gland consists of six compartments with separate ducts. The pleurodont teeth of the lower and upper jaw are not grooved but possess a sharp ridge on the anterior surface. Proteomic analysis of the gland extract confirmed previous studies that kallikrein enzymes are the major biologically active components. In view of the lizard's biology, its mandibular gland secretion is obviously not needed for prey capture or defence. It seems not justified the labelling of L. borneensis as a venomous animal. However, definitively answering this question requires toxinological studies on natural prey.
... Aspidoscelis t. septentrionalis (clade G, excluding mundus samples) demonstrates 238 significantly negative values for both Tajima's and Fu and Li's D statistics, with exceptionally low nucleotide diversity and haplotype diversity much less than that recorded for A. t. 240 punctilinealis and A. t. tigris (Table 1). These suggest a population expansion following a bottleneck (Douglas et al., 2010). Aspidoscelis marmoratus showed similar signatures, although 242 with a much greater differential between haplotype and nucleotide diversities, and a reduced number of segregating sites relative to sample size (Table 1) ...
... We suggest this ecological gradient represents a 'soft boundary,' similar to those 370 that mediate the transition between A. t. punctilinealis and A. marmoratus. Unique communities characterize both the Colorado Plateau and Sonoran Desert (e.g., Douglas et al., 2002Douglas et al., , 2010, and 372 this suggests a common, underlying process driving diversification therein (Riddle and Hafner, 2006;Pianka, 1967 . CC-BY-NC 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. ...
(225)Biodiversity in southwestern North America has a complex biogeographic history involving tectonism interspersed with climatic fluctuations. This yields a contemporary pattern replete with historic idiosyncrasies often difficult to interpret when viewed from through the lens of modern ecology. The Aspidoscelis tigris (Tiger Whiptail) complex (Squamata: Teiidae) is one such group in which potential taxonomic boundaries have been confounded by a series of complex biogeographic processes that have defined the evolution of the clade. To clarify this situation, we first generated multiple taxonomic hypotheses, which were subsequently tested using mitochondrial DNA sequences (ATPase 8 and 6) evaluated across 239 individuals representing five continental members of this complex. To do so, we evaluated the manner by which our models parsed phylogenetic and biogeographic patterns. We found considerable variation among species ‘hypotheses’, which we suggest in part reflects inflated levels of inter-population genetic divergence caused by historical demographic expansion and contraction cycles. Inter-specific boundaries with A. marmoratus juxtaposed topographically with the Cochise Filter Barrier that separates Sonoran and Chihuahuan deserts (interpreted herein as case of ‘soft’ allopatry). Patterns of genetic divergence were consistent across the Cochise Filter Barrier, regardless of sample proximity. Surprisingly, this also held true for intraspecific comparisons that spanned the Colorado River. These in turn suggest geomorphic processes as a driver of speciation in the tigris complex, with intraspecific units governed locally by demographic processes.
HIGHLIGHTS
Phylogeographies of vertebrates within the southwestern deserts of North America have been shaped by climatic fluctuations imbedded within broad geomorphic processes.
The resulting synergism drives evolutionary processes, such as an expansion of within-species genetic divergence over time. Taxonomic inflation often results (i.e., an increase in recognized taxa due to arbitrary delineations), such as when morphological divergences fail to juxtapose with biogeographic hypotheses.
However, isolated groups can be discriminated within-species by mapping genetic variability onto geographic distances. This approach can often diagnose ‘hard’ barriers to dispersal, or alternatively, strong selection acting against hybridization. On the other hand, elevated genetic divergences among groups less-isolated would underscore isolation-by-distance (i.e., an increase in genetic differentiation concomitant with geographic distance).
The biogeographic patterns we identified in Tiger Whiptail are largely synonymous with those found in other regional species, particularly given the geomorphic separation of Mohave and Sonoran deserts by the Colorado River, and Sonoran/ Chihuahuan deserts by the Cochise Filter Barrier.
Our results for the Tiger Whiptail complex broaden and extend the context within which polytypic species are conserved and managed, particularly those that reflect an incongruence among molecular and morphological standards.
... Aspidoscelis t. septentrionalis (clade G, excluding mundus samples) demonstrates significantly negative values for both Tajima's and Fu and Li's D statistics, with exceptionally low nucleotide diversity and haplotype diversity much less than that recorded for A. t. punctilinealis and A. t. tigris (Table 1). These suggest a population expansion following a bottleneck (Douglas et al. 2010). Aspidoscelis marmoratus showed similar signatures, although with a much greater differential between haplotype and nucleotide diversities, and a reduced number of segregating sites relative to sample size (Table 1) ...
... We suggest this ecological gradient represents a 'soft boundary,' similar to those that mediate the transition between A. t. punctilinealis and A. marmoratus. Unique communities characterize both the Colorado Plateau and Sonoran Desert (e.g., Douglas et al. 2002Douglas et al. , 2010, and this suggests a common, underlying process driving diversification therein (Pianka 1967, Riddle andHafner 2006). ...
... Scaffold 79, which was assigned to the Z chromosome, contains an orthologue of the anti-Müllerian hormone (amh) gene, which plays a crucial role in testis differentiation in vertebrates 17 . Scaffolds assigned to the Z chromosome were homologous to [19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38] . We used 1,394 orthologous proteins from the Komodo dragon genome, 14 representative non-avian reptile species (seven squamates, three turtles and four crocodilians), three avian species (chicken, wild turkey and zebra finch) and four mammalian species (platypus, mouse, dog and human) to estimate a species tree (Fig. 1). ...
Monitor lizards are unique among ectothermic reptiles in that they have high aerobic capacity and distinctive cardiovascular physiology resembling that of endothermic mammals. Here, we sequence the genome of the Komodo dragon Varanus komodoensis, the largest extant monitor lizard, and generate a high-resolution de novo chromosome-assigned genome assembly for V. komodoensis using a hybrid approach of long-range sequencing and single-molecule optical mapping. Comparing the genome of V. komodoensis with those of related species, we find evidence of positive selection in pathways related to energy metabolism, cardiovascular homoeostasis, and haemostasis. We also show species-specific expansions of a chemoreceptor gene family related to pheromone and kairomone sensing in V. komodoensis and other lizard lineages. Together, these evolutionary signatures of adaptation reveal the genetic underpinnings of the unique Komodo dragon sensory and cardiovascular systems, and suggest that selective pressure altered haemostasis genes to help Komodo dragons evade the anticoagulant effects of their own saliva. The Komodo dragon genome is an important resource for understanding the biology of monitor lizards and reptiles worldwide.
