Article

Reproductive phenotype predicts adult bite‐force performance in sex‐reversed dragons (Pogona vitticeps)

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Abstract

Sex-related differences in morphology and behavior are well documented, but the relative contributions of genes and environment to these traits are less well understood. Species that undergo sex reversal, such as the central bearded dragon (Pogona vitticeps), offer an opportunity to better understand sexually dimorphic traits because sexual phenotypes can exist on different chromosomal backgrounds. Reproductively female dragons with a discordant sex chromosome complement (sex reversed), at least as juveniles, exhibit traits in common with males (e.g., longer tails and greater boldness). However, the impact of sex reversal on sexually dimorphic traits in adult dragons is unknown. Here, we investigate the effect of sex reversal on bite-force performance, which may be important in resource acquisition (e.g., mates and/or food). We measured body size, head size, and bite force of the three sexual phenotypes in a colony of captive animals. Among adults, we found that males (ZZm) bite more forcefully than either chromosomally concordant females (ZWf) or sex-reversed females (ZZf), and this difference is associated with having relatively larger head dimensions. Therefore, adult sex-reversed females, despite apparently exhibiting male traits as juveniles, do not develop the larger head and enhanced bite force of adult male bearded dragons. This pattern is further illustrated in the full sample by a lack of positive allometry of bite force in sex-reversed females that is observed in males. The results reveal a close association between reproductive phenotype and bite force performance, regardless of sex chromosome complement.

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... Despite all these reasons for studying the consequences of sex reversal, we have very little empirical information on the fitness of sexreversed individuals, apart from fish in aquaculture (Senior et al., 2012), where sex reversal is artificially induced and thus may not necessarily be ecologically relevant. Researchers have only just begun to investigate the relationship between ecologically relevant sex reversal and individual performance, and most of the little existing knowledge comes from a single reptilian species, where high incubation temperatures produce male-to-female sex-reversed individuals that display a complex combination of male-like, female-like, "supermale" and "superfemale" traits (Holleley et al., 2015;Li et al., 2016;Jones et al., 2020). ...
... Since sex reversal occurs relatively rarely under natural circumstances, most of our existing knowledge about ecologically relevant sex reversal comes from studies that include relatively small numbers of sex-reversed individuals in each population, year or treatment group (e.g., Li et al., 2016;Lambert et al., 2019;Jones et al., 2020;Nemesházi et al., 2020). The present study is no exception to this constraint. ...
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Sex reversal is a mismatch between genetic sex (sex chromosomes) and phenotypic sex (reproductive organs and secondary sexual traits). It can be induced in various ectothermic vertebrates by environmental perturbations, such as extreme temperatures or chemical pollution, experienced during embryonic or larval development. Theoretical studies and recent empirical evidence suggest that sex reversal may be widespread in nature and may impact individual fitness and population dynamics. So far, however, little is known about the performance of sex-reversed individuals in fitness-related traits compared to conspecifics whose phenotypic sex is concordant with their genetic sex. Using a novel molecular marker set for diagnosing genetic sex in agile frogs (Rana dalmatina), we investigated fitness-related traits in larvae and juveniles that underwent spontaneous female-to-male sex reversal in the laboratory. We found only a few differences in early life growth, development, and larval behavior between sex-reversed and sex-concordant individuals, and altogether these differences did not clearly support either higher or lower fitness prospects for sex-reversed individuals. Putting these results together with earlier findings suggesting that sex reversal triggered by heat stress may be associated with low fitness in agile frogs, we propose the hypothesis that the fitness consequences of sex reversal may depend on its etiology.
... Herrel et al., 2002), squamates (e.g. Herrel et al., 2001;Jones et al., 2020), frogs (Lappin et al., 2017) and mammals (e.g. Becerra et al., 2011;Dessem & Druzinsky, 1992;Freeman & Lemen, 2008;Sakamoto et al., 2010;Santana & Dumont, 2009). ...
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Animal closing forces such as bite and pinch forces may determine access to food and mates and are therefore important performance metrics related to fitness. Previous measurement setups to obtain in vivo closing force data were often custom‐made for each study, hampering comparisons among different studies. Additionally, most setups were limited in the size range of taxa they can measure, especially towards smaller species. We introduce ‘forceX’, a closing force measurement setup that allows the measurement of a large range of taxa with a great size variety, and ‘forceR’, an accompanying software package to analyse the data. forceX is mostly based on off‐the‐shelf components and 3D‐printed or metal‐turned parts. Gape distance can be modified during measurements, and replaceable tip elements of varying thickness allow a minimal gape distance of ~0.3 mm. Thus, forceX allows closing force measurements of smaller species, while still being able to measure medium‐sized animals as well. Animals are not harmed during the measurements, and the whole setup can be assembled within minutes, is battery‐powered, light‐weight, and transportable. The forceX system is able to accurately (linear regression of measured forces vs. control forces: p < 0.001; R2 > 0.999; n = 1609) and reproducibly (mean of absolute relative errors = 0.93%; SD = 1.42%; n = 1609) measure forces across three orders of magnitude (0.01 – 10 N). Importantly, whole force curves, instead of just maximum force values are stored, and forceR allows extracting individual peak shapes from these curves to facilitate the statistical analysis of both maximum force values and peak curve shapes. forceX and forceR facilitate rapid and minimally‐invasive in vivo measurements and analyses of closing forces in animals across a wider range of taxa than previously possible, including, for example, many small species of the megadiverse insects. The system allows studying the characteristics, predictors, and evolution of both maximum closing forces and force curve shape shapes.
... Depending on an individual's behaviour and reproductive strategies, sex-specific differences in survivorship may shape selection pressures across sex classes (Sillett and Holmes, 2002;York & Baird, 2017) and could influence the stability of ZW genotypes within a (Jones et al., 2020). In the absence of an obvious positive fitness advantage to sex-reversal, our data demonstrate that moderately-high rates of dispersal combined with low rates of sex-reversal may act as a buffer against a rapid localised transition to TSD in P. vitticeps and would therefore require significant perturbations to enable a full transition to a TSD form of sex determination. ...
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The sex of vertebrates is typically determined genetically, but reptile sex can also be determined by developmental temperature. In some reptiles, temperature interacts with genotype to reverse sex, potentially leading to transitions from a chromosomal to a temperature‐dependent sex determining system. Transitions between such systems in nature are accelerated depending on the frequency and fitness of sex‐reversed individuals. The Central Bearded Dragon, Pogona vitticeps, exhibits female heterogamety (ZZ/ZW) but can have its sex reversed from ZZ male to ZZ female by high incubation temperatures. The species exhibits sex‐reversal in the wild and it has been suggested that climate change and fitness of sex‐reversed individuals could be increasing the frequency of reversal within the species range. Transitions to temperature‐dependent sex determination require low levels of dispersal and high (> 50%) rates of sex‐reversal. Here, we combine genotype‐by‐sequencing, identification of phenotypic and chromosomal sex, exhaustive field surveys, and radio telemetry to examine levels of genetic structure, rates of sex‐reversal, movement, space use, and survival of P. vitticeps in a location previously identified as a hot spot for sex‐reversal. We find that the species exhibits low levels of population structure (FST ~ 0.001) and a modest (~17%) rate of sex‐reversal, and that sex‐reversed and non‐sex‐reversed females have similar survival and behavioural characteristics to each other. Overall, our data indicate this system is evolutionary stable, although we do not rule out the prospect of a more gradual transition in sex‐determining mechanisms in the future in a more fragmented landscape and as global temperatures increase.
... As such, this species possesses a sex determination system ideally suited to studying the influences of both sex chromosomes and the environment on sex. Sex reversed ZZf females differ from concordant ZWf females in several biological aspects, including karyotype, behavior, morphology, reproduction, and gene expression [5][6][7], though the two female sex classes do not differ in bite force [8]. ...
Article
The mechanisms by which sex is determined, and how a sexual phenotype is stably maintained during adulthood, has been the focus of vigorous scientific inquiry. Resources common to the biomedical field (automated staining and imaging platforms) were leveraged to provide the first immunofluorescent data for a reptile species with temperature induced sex reversal. Two four-plex immunofluorescent panels were explored across three sex classes (sex reversed ZZf females, normal ZWf females, and normal ZZm males). One panel was stained for chromatin remodelling genes JARID2 and KDM6B, and methylation marks H3K27me3, and H3K4me3 (Jumonji Panel). The other CaRe panel stained for environmental response genes CIRBP and RelA, and H3K27me3 and H3K4me3. Our study characterised tissue specific expression and cellular localisation patterns of these proteins and histone marks, providing new insights to the molecular characteristics of adult gonads in a dragon lizard Pogona vitticeps. The confirmation that mammalian antibodies cross react in P. vitticeps paves the way for experiments that can take advantage of this new immunohistochemical resource to gain a new understanding of the role of these proteins during embryonic development, and most importantly for P. vitticeps, the molecular underpinnings of sex reversal.
... In both P. vitticeps and B. duperreyi, sex-reversed individuals occur in the wild, albeit at a lower proportion than either of their concordant counterparts. In P. vitticeps, sex-reversed ZZ females are fertile, with greater fecundity than concordant ZW females [Holleley et al., 2015], and there are other attributes with implications for their fitness, like increased levels of activity and boldness [Li et al., 2016;Jones et al., 2020]. The offspring of sexreversed females have a greater propensity to reverse, which may influence sex ratios across populations. ...
Article
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Sex reversal is the process by which an individual develops a phenotypic sex that is discordant with its chromosomal or genotypic sex. It occurs in many lineages of ectothermic vertebrates , such as fish, amphibians, and at least one agamid and one scincid reptile species. Sex reversal is usually triggered by an environmental cue that alters the genetically determined process of sexual differentiation, but it can also be caused by exposure to exogenous chemicals, hormones, or pollutants. Despite the occurrence of both temperature-dependent sex determination (TSD) and genetic sex determination (GSD) broadly among reptiles, only 2 species of squamates have thus far been demonstrated to possess sex reversal in nature (GSD with overriding thermal influence). The lack of species with unambiguously identified sex reversal is not necessarily a reflection of a low incidence of this trait among reptiles. Indeed, sex reversal may be relatively common in reptiles, but little is known of its prevalence, the mechanisms by which it occurs, or the consequences of sex reversal for species in the wild under a changing climate. In this review, we present a roadmap to the discovery of sex reversal in reptiles, outlining the various techniques that allow new occurrences of sex reversal to be identified, the molecular mechanisms that may be involved in sex reversal and how to identify them, and approaches for assessing the impacts of sex reversal in wild populations. We discuss the evolutionary implications of sex reversal and use the central bearded dragon (Pogona vitticeps) and the eastern three-lined skink (Bassiana duperreyi) as examples of how species with opposing patterns of sex reversal may be impacted differently by our rapidly changing climate. Ultimately, this review serves to highlight the importance of understanding sex reversal both in the laboratory and in wild populations and proposes practical solutions to foster future research.
... Offspring sex ratio of these sex-reversed females depends on the incubation temperature, suggesting that one generation is sufficient for a GSD-to-ESD transition and the loss of the W chromosome [Holleley et al., 2015]. It was demonstrated that the lack of W chromosome and/or extreme incubation conditions affect morphological and behavioural traits of sex-reversed ZZ females [Holleley et al., 2015;Li et al., 2016;Jones et al., 2020]; however, the influence of sex reversal on fitness under natural conditions is not known. In the laboratory, the females are fully viable and fertile [Holleley et al., 2015]. ...
Article
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Transitions from environmental sex determination (ESD) to genotypic sex determination (GSD) require an intermediate step of sex reversal, i.e., the production of individuals with a mismatch between the ancestral genotypic and the phenotypic sex. Among amniotes, the sole well-documented transition in this direction was shown in the laboratory in the central bearded dragon, Pogona vitticeps, where very high incubation temperatures led to the production of females with the male-typical (ZZ) genotype. These sex-reversed females then produced offspring whose sex depended on the incubation temperature. Sex-reversed animals identified by molecular and cytogenetic markers were also reported in the field, and their increasing incidence was speculated as a climate warming-driven transition in sex determination. We show that the molecular and cytogenetic markers normally sex-linked in P. vitticeps are also sex-linked in P. henrylawsoni and P. minor, which points to quite ancient sex chromosomes in this lineage. Nevertheless, we demonstrate, based on a crossing experiment with a male bearded dragon who possesses a mismatch between phenotypic sex and genotype, that the used cytogenetic and molecular markers might not be reliable for the identification of sex reversal. Sex reversal should not be considered as the only mechanism causing a mismatch between genetic sex-linked markers and phenotypic sex, which can emerge also by other processes, here most likely by a rare recombination between regions of sex chromosomes which are normally sex-linked. We warn that sex-linked, even apparently for a long evolutionary time, and sex-specific molecular and cytogenetic markers are not a reliable tool for the identification of sex-reversed individuals in a population and that sex reversal has to be verified by other approaches, particularly by observation of the sex ratio of the progeny.
... Bite force performance can be estimated by encouraging test subjects to bite on custom bite force transducers (e.g., Dessem & DruZinsKy, 1992;PaPHanGKoraKit & osBorn, 1998;Herrel et al., 1999;anDerson et al., 2008;laPPin & Jones, 2014;van vu uren et al., 2020). This approach has been used successfully for a range of taxa, notably crocodylians, lizards, bats, and rodents but also sharks (Dessem & DruZinsKy, 1992;Herrel et al., 1999;HuBer et al., 2005;BeCerra et al., 2011;eriCKson et al., 2012;laPPin & Jones, 2014;laPPin et al., 2017;Jones et al., 2020). Muscle activity can be measured using electromyography (loeB et al., 1986;Dessem & DruZinsKy, 1992) although the relationships between EMG measurements and actual force remain problematic to determine with certainty. ...
Article
The chondrocranium is the cartilage component of the vertebrate braincase. Among jawed vertebrates it varies greatly in structure, mineralisation, and in the extent to which it is replaced by bone during development. In mammals, birds, and some bony fish, most of the chondrocranium is replaced by bone whereas in lizards, amphibians, and chondrichthyan fish it may remain a significant part of the braincase complex in adulthood. To what extent this variation relates to differences in skull biomechanics is poorly understood. However, there have been examinations of chondrocranium histology, in vivo strain, and impact on rostrum growth following partial removal of the chondrocranium. These studies have led to suggestions that the chondrocranium may provide structural support or serve to dampen external loads. Advances in computing-power have also facilitated an increase in the number of three-dimensional computer-based models. These models can be analysed (in silico) to test specific biomechanical hypotheses under specified loading conditions. However, representing the material properties of cartilage is still problematic because these properties differ according to the speed and direction of loading. The relationship between stress and strain is also non-linear. Nevertheless, analyses to date suggest that the chondrocranium does not provide a vertical support in lizards but it may serve to absorb some loads in humans. We anticipate that future models will include ever more detailed representations of the loading, anatomy, and material properties, in tandem with rigorous forms of model validation. However, comparison among a wider range of vertebrate subjects should also be pursued, in particular larvae, juveniles, and very small adult animals.
... Because sex reversal is challenging to study empirically, and only in recent years has it started to draw attention from field biologists and behavioural ecologists, no empirical study has yet tested the role of temperature-induced sex-reversal in mating success. However, increasing evidence shows that sexreversed and normal individuals differ in morphology, physiology, and behaviour [7,[21][22][23], all of which may affect mate choice. Furthermore, the sex-chromosome genotype of sex-reversed individuals differs from that of normal individuals of the same phenotypic sex, so they can be distinguished on the basis of phenotypic traits linked to sex chromosomes. ...
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Teeth have been a focus of research in both extinct and extant taxa alike; a significant portion of dental literature is concerned with dental patterning and replacement. Most non-mammalian vertebrates continuously replace their dentition but an anomalous group of squamates has forgone this process in only having one tooth generation; these squamates all have apically implanted teeth, a condition known as acrodonty. Acrodont dentition and various characteristics attributed to it, including a lack of replacement, have often been defined ambiguously. This study explores this type of implantation through histology in the ontogeny of the acrodont agamid Pogona vitticeps. The non-replacing teeth of this squamate provides an opportunity to study wear adaptations, maintenance of occlusion in a non-mammalian system, and most importantly post-eruption changes in the tooth bone interface. In this study the post-eruption changes combined with dental wear likely gives the appearance of acrodont implantation.
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Computations in the mammalian cortex are carried out by glutamatergic and GABAergic neurons forming specialized circuits and areas. Here we asked how these neurons and areas evolved in amniotes. We built a gene expression atlas of the pallium of two reptilian species using large-scale single-cell mRNA sequencing. The transcriptomic signature of glutamatergic neurons in reptilian cortex suggests that mammalian neocortical layers are made of new cell types generated by diversification of ancestral gene regulatory programs. By contrast, the diversity of reptilian cortical GABAergic neurons indicates that the interneuron classes known in mammals already existed in the common ancestor of all amniotes.
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Reptiles show remarkable diversity in modes of reproduction and sex determination, including high variation in the morphology of sex chromosomes, ranging from homomorphic to highly heteromorphic. Additionally, the coexistence of genotypic sex determination (GSD) and temperature-dependent sex determination (TSD) within and among sister clades makes this group an attractive model to study and understand the evolution of sex chromosomes. This is particularly so with Lizards (Order Squamata) which, among reptiles, show extraordinary morphological diversity. They also show no particular pattern of sex chromosome degeneration of the kind observed in mammals, birds and or even in snakes. We therefore speculate that sex determination sensu sex chromosome evolution is labile and rapid and largely follows independent trajectories within lizards. Here, we review the current knowledge on the evolution of sex chromosomes in lizards and discuss how sex chromosome evolution within that group differs from other amniote taxa, facilitating unique evolutionary pathways.
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Sex determination systems are exceptionally diverse and have undergone multiple and independent evolutionary transitions among species, particularly reptiles. However, the mechanisms underlying these transitions have not been established. Here, we tested for differences in sex-linked markers in the only known reptile that is polymorphic for sex determination system, the spotted snow skink, Niveoscincus ocellatus, to quantify the genomic differences that have accompanied this transition. In a highland population, sex is determined genetically, whereas in a lowland population, offspring sex ratio is influenced by temperature. We found a similar number of sex-linked loci in each population, including shared loci, with genotypes consistent with male heterogamety (XY). However, population-specific linkage disequilibrium suggests greater differentiation of sex chromosomes in the highland population. Our results suggest that transitions between sex determination systems can be facilitated by subtle genetic differences.
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The rise of the Evo-Devo field and the development of multidisciplinary research tools at various levels of biological organization have led to a growing interest in researching for new non-model organisms. Squamates (lizards and snakes) are particularly important for understanding fundamental questions about the evolution of vertebrates because of their high diversity and evolutionary innovations and adaptations that portrait a striking body plan change that reached its extreme in snakes. Yet, little is known about the intricate connection between phenotype and genotype in squamates, partly due to limited developmental knowledge and incomplete characterization of embryonic development. Surprisingly, squamate models have received limited attention in comparative developmental studies, and only a few species examined so far can be considered as representative and appropriate model organism for mechanistic Evo-Devo studies. Fortunately, the agamid lizard Pogona vitticeps (central bearded dragon) is one of the most popular, domesticated reptile species with both a well-established history in captivity and key advantages for research, thus forming an ideal laboratory model system and justifying his recent use in reptile biology research. We first report here the complete post-oviposition embryonic development for P. vitticeps based on standardized staging systems and external morphological characters previously defined for squamates. Whereas the overall morphological development follows the general trends observed in other squamates, our comparisons indicate major differences in the developmental sequence of several tissues, including early craniofacial characters. Detailed analysis of both embryonic skull development and adult skull shape, using a comparative approach integrating CT-scans and gene expression studies in P. vitticeps as well as comparative embryology and 3D geometric morphometrics in a large dataset of lizards and snakes, highlights the extreme adult skull shape of P. vitticeps and further indicates that heterochrony has played a key role in the early development and ossification of squamate skull bones. Such detailed studies of embryonic character development, craniofacial patterning, and bone formation are essential for the establishment of well-selected squamate species as Evo-Devo model organisms. We expect that P. vitticeps will continue to emerge as a new attractive model organism for understanding developmental and molecular processes underlying tissue formation, morphology, and evolution.
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Background The development of male- or female-specific phenotypes in squamates is typically controlled by either temperature-dependent sex determination (TSD) or chromosome-based genetic sex determination (GSD). However, while sex determination is a major switch in individual phenotypic development, it is unknownhow evolutionary transitions between GSD and TSD might impact on the evolution of squamate phenotypes, particularly the fast-evolving and diverse genitalia. Here, we take the unique opportunity of studying the impact of both sex determination mechanisms on the embryological development of the central bearded dragon (Pogona vitticeps). This is possible because of the transitional sex determination system of this species, in which genetically male individuals reverse sex at high incubation temperatures. This can trigger the evolutionary transition of GSD to TSD in a single generation, making P. vitticeps an ideal model organism for comparing the effects of both sex determination processes in the same species. Results We conducted four incubation experiments on 265 P. vitticeps eggs, covering two temperature regimes (“normal” at 28 °C and “sex reversing” at 36 °C) and the two maternal sexual genotypes (concordant ZW females or sex-reversed ZZ females). From this, we provide the first detailed staging system for the species, with a focus on genital and limb development. This was augmented by a new sex chromosome identification methodology for P. vitticeps that is non-destructive to the embryo. We found a strong correlation between embryo age and embryo stage. Aside from faster growth in 36 °C treatments, body and external genital development was entirely unperturbed by temperature, sex reversal or maternal sexual genotype. Unexpectedly, all females developed hemipenes (the genital phenotype of adult male P. vitticeps), which regress close to hatching. Conclusions The tight correlation between embryo age and embryo stage allows the precise targeting of specific developmental periods in the emerging field of molecular research on P. vitticeps. The stability of genital development in all treatments suggests that the two sex-determining mechanisms have little impact on genital evolution, despite their known role in triggering genital development. Hemipenis retention in developing female P. vitticeps, together with frequent occurrences of hemipenis-like structures during development in other squamate species, raises the possibility of a bias towards hemipenis formation in the ancestral developmental programme for squamate genitalia. Electronic supplementary material The online version of this article (10.1186/s13227-017-0087-5) contains supplementary material, which is available to authorized users.
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The jaws of lizards commonly occur in Quaternary fossil deposits and have the potential to inform our understanding of recent changes in climate and environment. Frequently, however, interpretation of their taxonomic affinity is difficult because of either a lack of morphological characters and identifications or ones which are sometimes no more than subjective visual comparisons. Here, we evaluate the taxonomic affinity of a maxilla from the Holocene of Kelly Hill Caves (Kangaroo Island, South Australia) by comparing it to a sample of modern agamid lizards using computer models generated from X-ray computed tomography data and three-dimensional geometric morphometrics. To represent the shape of the maxilla, we used 22 fixed landmarks and 30 semi-landmarks placed at equivalent points on the three-dimensional surface files of the maxillae. Procrustes distances show that, with respect to overall shape difference, the fossil does not closely resemble Ctenophorus decresii, which is the only agamid currently present on Kangaroo Island. Preliminary comparisons to other candidate agamid taxa from southeastern Australia suggest instead that the fossil is most similar to Amphibolurus muricatus and Amphibolurus norrisi and least similar to Tympanocryptis lineata. Geometric morphometrics show promise as a more objective means of quantifying and characterizing shape differences. Reliable identifications, however, require sufficient specimen collections to adequately represent within-species variation (including ontogenetic variation).
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In many vertebrates, sex of offspring is determined by external environmental cues rather than by sex chromosomes. In reptiles, for instance, temperature-dependent sex determination (TSD) is common. Despite decades of work, the mechanism by which temperature is converted into a sex-determining signal remains mysterious. This is partly because it is difficult to distinguish the primary molecular events of TSD from the confounding downstream signatures of sexual differentiation. We use the Australian central bearded dragon, in which chro-mosomal sex determination is overridden at high temperatures to produce sex-reversed female offspring, as a unique model to identify TSD-specific features of the transcriptome. We show that an intron is retained in mature transcripts from each of two Jumonji family genes, JARID2 and JMJD3, in female dragons that have been sex-reversed by temperature but not in normal chromosomal females or males. JARID2 is a component of the master chromatin modifier Polycomb Repressive Complex 2, and the mammalian sex-determining factor SRY is directly regulated by an independent but closely related Jumonji family member. We propose that the perturbation of JARID2/JMJD3 function by intron retention alters the epigenetic landscape to override chromosomal sex-determining cues, triggering sex reversal at extreme temperatures. Sex reversal may then facilitate a transition from genetic sex determination to TSD, with JARID2/JMJD3 intron retention preserved as the decisive regulatory signal. Significantly, we also observe sex-associated differential retention of the equivalent introns in JARID2/JMJD3 transcripts expressed in embryonic gonads from TSD alligators and turtles, indicative of a reptile-wide mechanism controlling TSD.
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Differences in biological performance, at both intra- and inter-specific levels, have often been linked to morphology but seldom to behavioural or genotypic effects. We tested performance at the intraspecific level by measuring bite force in the African pygmy mouse, Mus minutoides. This species displays an unusual sex determination system, with sex-reversed, X*Y females carrying a feminizing X* chromosome. X*Y females cannot be differentiated from XX females based on external or gonadal morphology; however, they are known to be more aggressive. We found that bite force was higher in X*Y females than in other females and males. We then performed geometric morphometric analyses on their skulls and mandibles and found that the higher performance of X*Y females was mainly explained by a greater overall skull size. The effects of the X*chromosome thus go beyond feminization, and extend to whole-organism performance and morphology. Our results also suggest limited effects of behaviour on bite force.
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Three-dimensional computational modeling offers tools with which to investigate forces experienced by the skull encountered during feeding and other behaviors. American alligators (Alligator mississippiensis) generate some of the highest measured bite forces among extant tetrapods. A concomitant increase in bite force accompanies ontogenetic increases in body mass, which has been linked with dietary changes as animals increase in size. Because the flattened skull of crocodylians has substantial mediolaterally-oriented muscles, they are an excellent model taxon in which to explore the role of mediolateral force components experienced by the feeding apparatus. Many previous modeling studies of archosaur cranial function focused on planar analysis, ignoring the mediolateral aspects of cranial forces. Here we use three-dimensionally accurate anatomical data to resolve 3D muscle forces. Using dissection, imaging, and computational techniques, we developed lever and finite element models of an ontogenetic series of alligators to test the effects of size and shape on cranial loading and compared estimated bite forces to those previously measured in vivo in Alligator mississippiensis We found that modeled forces matched in vivo data well for intermediately sized individuals, and somewhat overestimated force in smaller specimens and underestimated force in larger specimens, suggesting that ontogenetically static muscular parameters and bony attachment sites alone cannot account for all the variation in bite force. Adding aponeurotic muscle attachments would likely improve force predictions, but such data are challenging to model and integrate into analyses of extant taxa and are generally unpreserved in fossils. We conclude that anatomically accurate modeling of muscles can be coupled with finite element and lever analyses to produce reliable, reasonably accurate estimate bite forces and thus both skeletal and joint loading, with known sources of error, which can be applied to extinct taxa.
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With over 9000 species, squamates, which include lizards and snakes, are the largest group of reptiles and second-largest order of vertebrates, spanning a vast array of appendicular skeletal morphology. As such, they provide a promising system for examining developmental and molecular processes underlying limb morphology. Using the central bearded dragon (Pogona vitticeps) as the primary study model, we examined limb morphometry throughout embryonic development and characterized the expression of three known developmental genes (GHR, Pitx1 and Shh) from early embryonic stage through to hatchling stage via reverse transcription quantitative polymerase chain reaction (RT-qPCR) and immunohistochemistry (IHC). In this study, all genes were found to be transcribed in both the forelimbs and hindlimbs of P. vitticeps. While the highest level of GHR expression occurred at the hatchling stage, Pitx1 and Shh expression was greatest earlier during embryogenesis, which coincides with the onset of the differentiation between forelimb and hindlimb length. We compared our finding of Pitx1 expression—a hindlimb-determining gene—in the forelimbs of P. vitticeps to that in a closely related Australian agamid lizard, Ctenophorus pictus, where we found Pitx1 expression to be more highly expressed in the hindlimb compared with the forelimb during early and late morphogenesis—a result consistent with that found across other tetrapods. Expression of Pitx1 in forelimbs has only rarely been documented, including via in situ hybridization in a chicken and a frog. Our findings from both RT-qPCR and IHC indicate that further research across a wider range of tetrapods is needed to more fully understand evolutionary variation in molecular processes underlying limb morphology.
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Is sex a product of genes, the environment, or both? In this review, we describe the diversity of sex-determining mechanisms in reptiles, with a focus on systems that display gene-environment interactions. We summarise the field and laboratory-based evidence for the occurrence of environmental sex reversal in reptiles and ask whether this is a widespread evolutionary mechanism affecting the evolution of sex chromosomes and speciation in vertebrates. Sex determination systems exist across a continuum of genetic and environmental influences, blurring the lines between what was once considered a strict dichotomy between genetic sex determination and temperature-dependent sex determination. Across this spectrum, we identify the potential for sex reversal in species with clearly differentiated heteromorphic sex chromosomes (Pogona vitticeps, Bassiana duperreyi, Eremias multiocellata, Gekko japonicus), weakly differentiated homomorphic sex chromosomes (Niveoscincus ocellatus), and species with only a weak heritable predisposition for sex (Emys orbicularis, Trachemys scripta). We argue that sex reversal is widespread in reptiles (Testudines, Lacertidae, Agamidae, Scincidae, Gekkonidae) and has the potential to have an impact on individual fitness, resulting in reproductively, morphologically, and behaviourally unique phenotypes. Sex reversal is likely to be a powerful evolutionary force responsible for generating and maintaining lability and diversity in reptile sex-determining modes.
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Animal coloration has multiple functions including thermoregulation, camouflage, and social signaling, and the requirements of each function may sometimes conflict. Many terrestrial ectotherms accommodate the multiple functions of color through color change. However, the relative importance of these functions and how color-changing species accommodate them when they do conflict are poorly understood because we lack data on color change in the wild. Here, we show that the color of individual radio-tracked bearded dragon lizards, Pogona vitticeps, correlates strongly with background color and less strongly, but significantly, with temperature. We found no evidence that individuals simultaneously optimize camouflage and thermoregulation by choosing light backgrounds when hot or dark backgrounds when cold. In laboratory experiments, lizards showed both UV-visible (300?700 nm) and near-infrared (700?2,100 nm) reflectance changes in response to different background and temperature treatments, consistent with camouflage and thermoregulatory functions, respectively, but with no interaction between the two. Overall, our results suggest that wild bearded dragons change color to improve both thermoregulation and camouflage but predominantly adjust for camouflage, suggesting that compromising camouflage may entail a greater potential immediate survival cost.
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Background: Squamates (lizards and snakes) are a speciose lineage of reptiles displaying considerable karyotypic diversity, particularly among lizards. Understanding the evolution of this diversity requires comparison of genome organisation between species. Although the genomes of several squamate species have now been sequenced, only the green anole lizard has any sequence anchored to chromosomes. There is only limited gene mapping data available for five other squamates. This makes it difficult to reconstruct the events that have led to extant squamate karyotypic diversity. The purpose of this study was to anchor the recently sequenced central bearded dragon (Pogona vitticeps) genome to chromosomes to trace the evolution of squamate chromosomes. Assigning sequence to sex chromosomes was of particular interest for identifying candidate sex determining genes. Results: By using two different approaches to map conserved blocks of genes, we were able to anchor approximately 42 % of the dragon genome sequence to chromosomes. We constructed detailed comparative maps between dragon, anole and chicken genomes, and where possible, made broader comparisons across Squamata using cytogenetic mapping information for five other species. We show that squamate macrochromosomes are relatively well conserved between species, supporting findings from previous molecular cytogenetic studies. Macrochromosome diversity between members of the Toxicofera clade has been generated by intrachromosomal, and a small number of interchromosomal, rearrangements. We reconstructed the ancestral squamate macrochromosomes by drawing upon comparative cytogenetic mapping data from seven squamate species and propose the events leading to the arrangements observed in representative species. In addition, we assigned over 8 Mbp of sequence containing 219 genes to the Z chromosome, providing a list of genes to begin testing as candidate sex determining genes. Conclusions: Anchoring of the dragon genome has provided substantial insight into the evolution of squamate genomes, enabling us to reconstruct ancestral macrochromosome arrangements at key positions in the squamate phylogeny, demonstrating that fusions between macrochromosomes or fusions of macrochromosomes and microchromosomes, have played an important role during the evolution of squamate genomes. Assigning sequence to the sex chromosomes has identified NR5A1 as a promising candidate sex determining gene in the dragon.
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Sex differences in morphology, physiology, and behaviour are caused by sex-linked genes, as well as by circulating sex-steroid levels. Thus, a shift from genotypic to environmental sex determination may create an organism that exhibits a mixture of male-like and female-like traits. We studied a lizard species (Central Bearded Dragon, Pogona vitticeps), in which the hightemperature incubation of eggs transforms genetically male individuals into functional females. Although they are reproductively female, sex-reversed dragons (individuals with ZZ genotype reversed to female phenotype) resemble genetic males rather than females in morphology (relative tail length), general behaviour (boldness and activity level), and thermoregulatory tactics. Indeed, sex-reversed ‘females’ are more male-like in some behavioural traits than are genetic males. This novel phenotype may impose strong selection on the frequency of sex reversal within natural populations, facilitating rapid shifts in sex-determining systems. A single period of high incubation temperatures (generating thermally induced sex reversal) can produce functionally female individuals with male-like (or novel) traits that enhance individual fitness, allowing the new temperature-dependent sex-determining system to rapidly replace the previous genetically based one.
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We revise the taxonomy of the agamid genus Sitana Cuvier, 1829, a widely distributed terrestrial lizard from the Indian subcontinent based on detailed comparative analyses of external morphology, osteology and molecular data. We sampled 81 locations spread over 160,000 km2 in Peninsular India including type localities, which represented two known and five previously undescribed species. Based on general similarity in body shape and dewlap all species were hitherto identified as members of the genus Sitana. However, Sitana deccanensis and two other morphotypes, which are endemic to north Karnataka and Maharashtra in Peninsular India, are very distinct from the rest of the known members of the genus Sitana based on their external morphology and osteology. Moreover, members of this distinct morphological group were monophyletic in the molecular tree, and this clade (clade 1) was sister to two well-supported clades (2 and 3) constituting the rest of the Sitana. The interclade genetic divergence in mtDNA between clade 1 and clades 2 and 3 was 21-23%, whereas clade 2 and clade 3 exhibited 14-16% genetic divergence. Thus, we designate a new genus name “Sarada” gen. nov. for species represented in Clade 1, which also includes the recently resurrected Sitana deccanensis. We describe two new species in Sarada gen. nov. and three new species in Sitana. Similarity in the dewlap of Sitana and Sarada gen. nov. is attributed to similar function (sexual signaling) and similarity in body shape is attributed to a similar terrestrial life style and/or common ancestry.
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Background: The lizards of the family Agamidae are one of the most prominent elements of the Australian reptile fauna. Here, we present a genomic resource built on the basis of a wild-caught male ZZ central bearded dragon Pogona vitticeps. Findings: The genomic sequence for P. vitticeps, generated on the Illumina HiSeq 2000 platform, comprised 317 Gbp (179X raw read depth) from 13 insert libraries ranging from 250 bp to 40 kbp. After filtering for low-quality and duplicated reads, 146 Gbp of data (83X) was available for assembly. Exceptionally high levels of heterozygosity (0.85 % of single nucleotide polymorphisms plus sequence insertions or deletions) complicated assembly; nevertheless, 96.4 % of reads mapped back to the assembled scaffolds, indicating that the assembly included most of the sequenced genome. Length of the assembly was 1.8 Gbp in 545,310 scaffolds (69,852 longer than 300 bp), the longest being 14.68 Mbp. N50 was 2.29 Mbp. Genes were annotated on the basis of de novo prediction, similarity to the green anole Anolis carolinensis, Gallus gallus and Homo sapiens proteins, and P. vitticeps transcriptome sequence assemblies, to yield 19,406 protein-coding genes in the assembly, 63 % of which had intact open reading frames. Our assembly captured 99 % (246 of 248) of core CEGMA genes, with 93 % (231) being complete. Conclusions: The quality of the P. vitticeps assembly is comparable or superior to that of other published squamate genomes, and the annotated P. vitticeps genome can be accessed through a genome browser available at https://genomics.canberra.edu.au.
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Sex determination in animals is amazingly plastic. Vertebrates display contrasting strategies ranging from complete genetic control of sex (genotypic sex determination) to environmentally determined sex (for example, temperature-dependent sex determination). Phylogenetic analyses suggest frequent evolutionary transitions between genotypic and temperature-dependent sex determination in environmentally sensitive lineages, including reptiles. These transitions are thought to involve a genotypic system becoming sensitive to temperature, with sex determined by gene-environment interactions. Most mechanistic models of transitions invoke a role for sex reversal. Sex reversal has not yet been demonstrated in nature for any amniote, although it occurs in fish and rarely in amphibians. Here we make the first report of reptile sex reversal in the wild, in the Australian bearded dragon (Pogona vitticeps), and use sex-reversed animals to experimentally induce a rapid transition from genotypic to temperature-dependent sex determination. Controlled mating of normal males to sex-reversed females produces viable and fertile offspring whose phenotypic sex is determined solely by temperature (temperature-dependent sex determination). The W sex chromosome is eliminated from this lineage in the first generation. The instantaneous creation of a lineage of ZZ temperature-sensitive animals reveals a novel, climate-induced pathway for the rapid transition between genetic and temperature-dependent sex determination, and adds to concern about adaptation to rapid global climate change.
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American alligators Alligator mississippiensis undergo major transformations in morphology and ecology during development. These include several thousand-fold changes in body mass, modified snout and dental proportions, and shifts in diet from small, delicate foodstuffs to the inclusion of increasingly larger, more robust prey. How these changes in anatomical form contribute to actual physical performance and niche use is largely unknown. In the present study, bite-force measurements for 41 specimens of A. mississipiensis, were made throughout ontogeny (hatchling–older adults) using a series of precision force transducers. How this performance indicator scaled with respect to cranial and whole-body measurements was determined. Bite-force production throughout development was contrasted with ontogenetic changes in trophic ecology. The influences of this performance measure on these changes were then analysed. The results showed a 800-fold range (12–9452 N) of bite forces with values positively correlating with increases in body size. Scaling of biting forces through ontogeny showed positive allometry with respect to body mass, head length, jaw length, snout–vent length and total length. These patterns may be attributable to allometric growth of individual skeletal elements (and associated musculature), and/or progressive fusion and ossification of skull and jawbones during development. The overall pattern of force increase throughout ontogeny did not vary in association with major shifts in diet. Notably, the bite-force values for adult A. mississippiensis are the highest measured for any living animal and represent the first measures for a large crocodilian. Additionally, these data provide the first documentation of how bite force changes during ontogeny in a reptile. By bridging the rich morphological and ecological databases for these animals, this study opens the door to a comprehensive understanding of feeding in A. mississippiensis. Furthermore, it provides groundwork for standardized comparative studies of feeding among crocodilian, reptilian, or other gnathostome vertebrates.
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Sex chromosomes have evolved many times in animals and studying these replicate evolutionary "experiments" can help broaden our understanding of the general forces driving the origin and evolution of sex chromosomes. However this plan of study has been hindered by the inability to identify the sex chromosome systems in the large number of species with cryptic, homomorphic sex chromosomes. Restriction site-associated DNA sequencing (RAD-seq) is a critical enabling technology that can identify the sex chromosome systems in many species where traditional cytogenetic methods have failed. Using newly generated RAD-seq data from twelve gecko species, along with data from the literature, we reinterpret the evolution of sex-determining systems in lizards and snakes and test the hypothesis that sex chromosomes can routinely act as evolutionary traps. We uncovered between 17 and 25 transitions among gecko sex-determining systems. This is approximately ½ to ⅔ of the total number of transitions observed among all lizards and snakes. We find support for the hypothesis that sex chromosome systems can readily become trap-like and show that adding even a small number of species from understudied clades can greatly enhance hypothesis testing in a model-based phylogenetic framework. RAD-seq will undoubtedly prove useful in evaluating other species for male or female heterogamety, particularly the majority of fish, amphibian, and reptile species that lack visibly heteromorphic sex chromosomes, and will significantly accelerate the pace of biological discovery. © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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Hox genes regulate regionalization of the axial skeleton in vertebrates, and changes in their expression have been proposed to be a fundamental mechanism driving the evolution of new body forms. The origin of the snake-like body form, with its deregionalized pre-cloacal axial skeleton, has been explained as either homogenization of Hox gene expression domains, or retention of standard vertebrate Hox domains with alteration of downstream expression that suppresses development of distinct regions. Both models assume a highly regionalized ancestor, but the extent of deregionalization of the primaxial domain (vertebrae, dorsal ribs) of the skeleton in snake-like body forms has never been analysed. Here we combine geometric morphometrics and maximum-likelihood analysis to show that the pre-cloacal primaxial domain of elongate, limb-reduced lizards and snakes is not deregionalized compared with limbed taxa, and that the phylogenetic structure of primaxial morphology in reptiles does not support a loss of regionalization in the evolution of snakes. We demonstrate that morphometric regional boundaries correspond to mapped gene expression domains in snakes, suggesting that their primaxial domain is patterned by a normally functional Hox code. Comparison of primaxial osteology in fossil and modern amniotes with Hox gene distributions within Amniota indicates that a functional, sequentially expressed Hox code patterned a subtle morphological gradient along the anterior-posterior axis in stem members of amniote clades and extant lizards, including snakes. The highly regionalized skeletons of extant archosaurs and mammals result from independent evolution in the Hox code and do not represent ancestral conditions for clades with snake-like body forms. The developmental origin of snakes is best explained by decoupling of the primaxial and abaxial domains and by increases in somite number, not by changes in the function of primaxial Hox genes.
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Bite-force performance is an ecologically important measure of whole-organism performance that shapes dietary breadth and feeding strategies and, in some taxa, determines reproductive success. It also is a metric critical to testing and evaluating biomechanical models. We reviewed nearly one-hundred published studies of a range of taxa that incorporate direct in vivo measurements of bite force. Problematically, methods of data collection and processing vary considerably among studies. In particular, there is little consensus on the appropriate substrate to use on the biting surface of force transducers. In addition, the bite out-lever, defined as the distance from the fulcrum (i.e. jaw joint) to the position along the jawline at which the jaws engage the transducer, is rarely taken into account. We examined the effect of bite substrate and bite out-lever on bite-force estimates in a diverse sample of lizards. Results indicate that both variables have a significant impact on the accuracy of measurements. Maximum bite force is significantly greater using leather as the biting substrate, as compared to a metal substrate. Less forceful bites on metal are likely due to inhibitory feedback from mechanoreceptors that prevent damage to the feeding apparatus. Standardization of bite out-lever affected which trial produced maximum performance for a given individual. Indeed, maximum bite force usually is underestimated without standardization because it is expected to be greatest at the minimum out-lever (i.e. back of jaws), which in studies is rarely targeted with success. We assert that future studies should use a pliable substrate, such as leather, and employ appropriate standardization for bite out-lever.
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Amniote vertebrates, the group consisting of mammals and reptiles including birds, possess various mechanisms of sex determination. Under environmental sex determination (ESD), the sex of individuals depends on the environmental conditions occurring during their development and therefore there are no sexual differences present in their genotypes. Alternatively, through the mode of genotypic sex determination (GSD), sex is determined by a sex-specific genotype, i.e. by the combination of sex chromosomes at various stages of differentiation at conception. As well as influencing sex determination, sex-specific parts of genomes may, and often do, develop specific reproductive or ecological roles in their bearers. Accordingly, an individual with a mismatch between phenotypic (gonadal) and genotypic sex, for example an individual sex-reversed by environmental effects, should have a lower fitness due to the lack of specialized, sex-specific parts of their genome. In this case, evolutionary transitions from GSD to ESD should be less likely than transitions in the opposite direction. This prediction contrasts with the view that GSD was the ancestral sex-determining mechanism for amniote vertebrates. Ancestral GSD would require several transitions from GSD to ESD associated with an independent dedifferentiation of sex chromosomes, at least in the ancestors of crocodiles, turtles, and lepidosaurs (tuataras and squamate reptiles). In this review, we argue that the alternative theory postulating ESD as ancestral in amniotes is more parsimonious and is largely concordant with the theoretical expectations and current knowledge of the phylogenetic distribution and homology of sex-determining mechanisms.
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In vivo bone strain data are the most direct evidence of deformation and strain regimes in the vertebrate cranium during feeding and can provide important insights into skull morphology. Strain data have been collected during feeding across a wide range of mammals; in contrast, in vivo cranial bone strain data have been collected from few sauropsid taxa. Here we present bone strain data recorded from the jugal of the herbivorous agamid lizard Uromastyx geyri along with simultaneously recorded bite force. Principal and shear strain magnitudes in Uromastyx were lower than cranial bone strains recorded in Alligator but higher than those reported from herbivorous mammals. Our results suggest that variations in principal strain orientations in the facial skeleton are largely due to differences in feeding behavior and bite location, whereas food type has little impact on strain orientations. Furthermore, mean principal strain orientations differ between male and female Uromastyx during feeding, potentially due to sexual dimorphism in skull morphology.
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Sex reversal at high temperatures during embryonic development (e.g. ZZ females) provides the opportunity for new genotypic crosses (e.g. ZZ male x ZZ female). This raises the alarming possibility that climatic warming could lead to the loss of an entire chromosome – one member of the sex chromosome pair (the Y or W) – and the transition of populations to environmental sex determination (ESD). Here we examine the evolutionary dynamics of sex‐determining systems exposed to climatic warming using theoretical models. We found that the loss of sex chromosomes is not an inevitable consequence of sex reversal. A large frequency of ZZ sex reversal (50% reversal from male to female) typically divides the outcome between loss of the ZW genotype and the stable persistence of ZZ males, ZW females, and ZZ females. The amount of warming associated with sex chromosome loss depended on several features of wild populations – environmental fluctuation, immigration, heritable variation in temperature sensitivity, and differential fecundity of sex‐reversed individuals. Chromosome loss was partially or completely buffered when sex‐reversed individuals suffered a reproductive fitness cost, when immigration occurred, or when heritable variation for temperature sensitivity existed. Thus, under certain circumstances, sex chromosomes may persist cryptically in systems where the environment is the predominant influence on sex.
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Trade‐offs in performance expression occur because animals must perform multiple whole‐organism performance tasks that place conflicting demands on shared underlying morphology. Although not always detectable within populations, such trade‐offs may be apparent when analyzed at the level of the individual, particularly when all of the available data are taken into account as opposed to only maximum values. Detection of performance trade‐offs is further complicated in species where sexual dimorphism drives performance differences between males and females, leading potentially to differing patterns of trade‐offs within each sex. We tested for within‐ and between‐individual trade‐offs among three whole‐organism performance traits (sprint speed, endurance, and bite force) in adult male and female Anolis carolinensis lizards using all of the measured performance data. Sprinting and endurance did not trade‐off among individuals in either sex, but we found a significant negative among‐individual relationship between sprint speed and bite force in females only, likely driven by the mechanical burden of larger than optimal heads imposed on females through intralocus sexual conflict. We also found evidence for marked within‐individual plasticity in male bite force, but no within‐individual trade‐offs between any traits in either sex. These data offer new insight into the sex‐specific nature of performance trade‐offs and plasticity and, ultimately, into the constraints on multivariate performance evolution.
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1.Sexual size dimorphism (SSD) is pervasive across taxa and reflects differences in the effects of sexual and natural selection on body size between the sexes. However, disentangling the complex eco‐evolutionary interactions between these two mechanisms remains a major challenge for biologists. 2.Here, we combine macro‐evolutionary (between‐species), local evolutionary (between‐population) and fine‐scale evolutionary (within‐population) patterns of SSD to explore how sexual and natural selection interact and shape the evolution of SSD in Australian agamid lizards. Australian agamid lizards show substantial variation in SSD, ecological traits and species density making them an ideal study system to address this question. 3.At the between‐species level, population density, ecological generalism and mean species size significantly predict SSD variation, however, only ecological generalism was found to significantly explain variation in larger than average male‐biased SSD. At the population level, density positively correlated with SSD in native habitats, but not city park habitats. Last, agonistic behaviour acted as the primary driver of SSD at the within‐population level. 4.Our results indicate how sexual and natural selection can interact at different evolutionary scales, and show the importance of considering both selective mechanisms when investigating patterns of SSD. This article is protected by copyright. All rights reserved.
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Animals may improve camouflage by both dynamic colour change and local evolutionary adaptation of colour but we have little understanding of their relative importance in colour-changing species. We tested for differences in colour change in response to background colour and light intensity in two populations of central bearded dragon lizards (Pogona vitticeps) representing the extremes in body coloration and geographical range. We found that bearded dragons change colour in response to various backgrounds and that colour change is affected by illumination intensity. Within-individual colour change was similar in magnitude in the two populations but varied between backgrounds. However, at the endpoints of colour change, each population showed greater similarity to backgrounds that were representative of the local habitat compared with the other population, indicating local adaptation to visual backgrounds. Our results suggest that even in species that change colour, both phenotypic plasticity and geographic divergence of coloration may contribute to improved camouflage.
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Two successive mechanisms have been described in perichondral ossification: (1) in static osteo-genesis, mesenchymal cells differentiate into stationary osteoblasts oriented randomly, which differentiate into osteocytes in the same site; (2) in dynamic osteogenesis, mesenchymal cells differentiate into osteoblasts that are all oriented in the same direction and move back as they secrete collagen fibers. This study is aimed at testing the hypothesis that the ontogenetic sequence static then dynamic osteogenesis observed in the chicken and in the rabbit is homolo-gous and was acquired by the last common ancestor of amniotes or at a more inclusive node. For this we analyze the developmental patterns of Pleurodeles (Caudata, Amphibia) and those of the lizard Pogona (Squamata, Lepidosauria). We processed Pleurodeles larvae and Pogona embryos, prepared thin and ultrathin sections of appendicular bones, and analyzed them using light and transmission electron microscopy. We show that static osteogenesis does not precede dynamic osteogenesis in periosteal ossification of Pleurodeles and Pogona. Therefore, the null hypothesis is rejected and according to the parsimony method the ontogenetic sequence observed in the chicken and in the rabbit are convergent. In Pleurodeles and Pogona dynamic osteogenesis occur without a previous rigid mineralized framework, whereas in the chicken and in the rabbit dynamic osteogenesis seems to take place over a mineralized support whether bone (in perichondral ossifi-cation) or calcified cartilage (in endochondral ossification). Interestingly, in typical dynamic osteogenesis, osteoblasts show an axis (basal nucleus—distal endoplasmic reticulum) perpendicular to the front of secreted unmineralized bone matrix, whereas in Pleurodeles and Pogona this axis is parallel to the bone matrix. K E Y W O R D S bone histology, osteoblast, osteocyte, parallel fibered bone, perichondral ossification
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Objectives - To validate a thermal threshold (TT) nociceptive model in bearded dragons (Pogona vitticeps) and to document TT changes after administration of morphine. Study design - Two part randomized, blinded, controlled, experimental study. Animals - Five adult bearded dragons (242–396 g). Methods - A TT device delivered a ramped nociceptive stimulus (0.6°C second-1) to the medial thigh until a response (leg kick/escape behavior) was observed, or maximum (cut-off) temperature of 62°C was reached. In Phase I Period 1, six TT readings were determined at 20 minute intervals for evaluation of repeatability. Two of these readings were randomly assigned to be sham to assess specificity of the behavioral response. The same experiment was repeated 2 weeks later (Period 2) to test reproducibility. In Phase II, animals were administered either intramuscular morphine (10 mg kg-1) or saline 0.9%. Thermal thresholds (maximum 68°C) were determined before and 2, 4, 8, 12 and 24 hours after treatment administration. Data were analyzed using one-way ANOVA (temporal changes and repeatability) and paired t-tests (reproducibility and treatment comparisons) using Bonferroni correction (p < 0.05). Results - Mean TT was 57.4 ± 3.8°C and 57.3 ± 4.3°C for Periods 1 and 2, respectively. Data were repeatable within each period (p = 0.83 and p = 0.07, respectively). Reproducibility between periods was remarkable (p = 0.86). False-positive responses during sham-testing were 10%. TTs were significantly increased after morphine administration at 2, 4 and 8 hours when compared with baseline, and at 2 and 4 hours when compared with saline 0.9%. Highest TT was 67.7 ± 0.7°C at 4 hours after morphine administration. Conclusions and clinical relevance - Testing was repeatable, reproducible, and well tolerated in bearded dragons. TT nociceptive testing detected morphine administration and may be suitable for studying opioid regimens in bearded dragons.
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Fish sex reversal is a means to understand sex determination and differentiation, but it is also used to control sex in aquaculture. This review discusses sex reversal in gonochoristic fish, with the coexistence of genetic and environmental influences. The different periods of fish sensitivity to sex reversal treatments are presented with the mechanisms implicated. The old players of sex differentiation are revisited with transcriptome data and loss of function studies following hormone- or temperature-induced sex reversal. We also discuss whether cortisol is the universal mediator of sex reversal in fish due to its implication in ovarian meiosis and 11KT increase. The large plasticity in fish for sex reversal is also evident in the brain, with a reversibility existing even in adulthood. Studies on epigenetics are presented, since it links the environment, gene expression, and sex reversal, notably the association of DNA methylation in sex reversal. Manipulations with exogenous factors reverse the primary sex in many fish species under controlled conditions, but several questions arise on whether this can occur under wild conditions and what is the ecological significance. Cases of sex reversal in wild fish populations are shown and their fitness and future perspectives are discussed.
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Phenotypic traits such as ornaments and armaments are generally shaped by sexual selection, which often favors larger and more elaborate males compared to females. But can sexual selection also influence the brain? Previous studies in vertebrates report contradictory results with no consistent pattern between variation in brain structure and the strength of sexual selection. We hypothesize that sexual selection will act in a consistent way on two vertebrate brain regions that directly regulate sexual behavior: the medial preoptic nucleus and the ventromedial hypothalamic nucleus. The medial preoptic nucleus regulates male reproductive behavior while the ventromedial hypothalamic nucleus regulates female reproductive behavior and is also involved in male aggression. To test our hypothesis, we used high-resolution magnetic resonance imaging combined with traditional histology of brains in 14 dragon lizard species of the genus Ctenophorus that vary in the strength of precopulatory sexual selection. Males belonging to species that experience greater sexual selection had a larger medial preoptic nucleus and a smaller ventromedial hypothalamic nucleus. Conversely, females did not show any patterns of variation in these brain regions. Since the volumes of both these regions also correlated with brain volume in our models, we tested whether they show the same pattern of evolution in response to changes in brain volume and found that the do. Therefore, we show that the primary brain nuclei underlying reproductive behavior in vertebrates can evolve in a mosaic fashion, differently between males and females, likely in response to sexual selection, and that these same regions are simultaneously evolving in concert in relation to overall brain size. This article is protected by copyright. All rights reserved.
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Fighting ability is generally assumed to predict male reproductive success; yet the mechanisms responsible for this relationship are seldom known. Competitively superior males may monopolize access to females, be preferred by females, invest more into courtship, or employ more coercive mating tactics. Differentiating these alternatives is essential to understand the interaction between male–male competition and female mate choice, and their influence on the evolution of male traits such as aggression. We tested whether male fighting ability, body size, courtship, or coercive behavior in intersexual interactions predict copulation success in the Australian Lake Eyre dragon lizard, Ctenophorus maculosus. Males with superior fighting ability had higher mating success; however, male harassment (biting and chasing) was a much stronger predictor of copulation, likely because aggressive males are able to overcome female resistance. Better fighters also copulated for longer, which may increase sperm transfer and/or fertilization success. Conversely, courtship effort (head-bobs) decreased copulation success, but only for small males. Females were no less likely to reject males with higher fighting ability, suggesting that females do not prefer these males. Furthermore, males with superior fighting ability were no more or less likely to court or harass females. Instead, both fighting ability and aggression towards females independently increased mating success, potentially generating mutually reinforcing selection on male aggression.
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The bearded dragon (Pogona vitticeps) is (perhaps) the most common pet lizard in the United States. The purpose of this review article is to provide a practical overview of the natural history, husbandry, nutrition, reproduction, physical examination method, diagnostic techniques, currently recognized diseases, and therapeutics found useful for the bearded dragon. Nutritional secondary hyperparathyroidism and trauma attributable to cage-mate aggression are common problems encountered in juvenile dragons. Intestinal impaction and renal and cardiac diseases are more commonly seen in adult dragons. Newly described malignancies such as periocular squamous cell carcinoma and gastric carcinoma have also been reported in juvenile and adult bearded dragons.
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Allometry in size and shape between sexes was investigated in preserved Bearded Dragon Pogona barbata museum specimens. Measurements for snout-vent, head, leg and tail lenghts were obtained from 236 individuals ranging from hatchlings to large adults. Juveniles and adults were sexed, and size at onset of maturity was determined. Geographic variation in P. barbata was also studied by comparing lizards from three regions in New South Wales (NSW), which differ in annual rainfall. Relative to snout-vent length, head and leg lengths were in negative allometry in all specimens, and tail length was in positive allometry in juveniles, but negative in adults. Sexual dimorphism was evident in body size and shape. Males grew larger and reached maturity at larger sizes than females. While juvenile shape did not differ between the sexes, mature males had proportionately longer heads, legs and tails than adult females. This generalisation in sexual shape dimorphism did not hold true for animals from different NSW regions. Western males had proportionately longer legs and heads than western females, but relative tail lengths were not significantly different. Sexual dimorphism in body shape was not seen in the central animal group. In the east, heads and tails were longer in males than in females. Both sexes showed lower relative head and leg lenghts in more arid regions. We suggest that a combination of genetic drift and phenotypic responses are likely causes of these variations.
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Although the outcome of contests is often critical to fitness, we still have much to learn regarding the reliability of different predictors of fighting ability (e.g. morphological traits versus performance measures) and the strategies individuals use to decide when to withdraw. We examined predictors of contest success and assessment strategies in staged contests between male Lake Eyre dragon lizards, Ctenophorus maculosus, in which males engage in escalated contests. Bite force was the only significant predictor of contest success. Although head width and depth predicted the number and duration of bites during contests, neither of these traits predicted contest outcome, nor did body size or experience in the prior two contests. These results support the view that measures of physical performance may be more reliable indicators of male fighting ability in escalated contests than morphological traits, because performance is more directly linked to the quality being signalled (i.e. fighting ability). Contest intensity was positively associated with the resource holding potential (RHP) of the loser, but not that of the winner or RHP asymmetry, indicating that individuals base their decision to withdraw on assessment of their own cost threshold (self-assessment) rather than assessment of their opponent’s ability (mutual assessment). Lastly, the number of displays (head bobs and push-ups) was also correlated with the RHP of losers (but not winners or RHP asymmetry), consistent with the recently proposed ‘information conflict hypothesis’, which predicts that weaker individuals should limit information transfer about their ability by performing fewer displays.
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The evolution of large body size has often been considered a key trait allowing the evolution of herbivory in lizards. Although many omnivorous lizards appear unspecialized, they typically show high bite forces, allowing them to reduce tough and fibrous plant matter. In contrast, true herbivores often show a suite of morphological and physiological specializations, allowing them to efficiently process and assimilate plant material. Moreover, many specialized herbivores have a large body size, thus likely relaxing constraints on bite-force generation given that bite force increases with increasing body mass. In this study, we test whether large herbivorous lizards of the genus Uromastyx have relatively lower bite forces for their body size compared with a medium-sized congener. No differences in bite force or head dimensions were observed between the two species or between both sexes in our sample. Moreover, bite force scaled with positive allometry relative to jaw length, suggesting that larger animals have disproportionately large bite forces. This suggests that even in the largest species, constraints on bite-force generation are still strong, possibly due to the demands imposed on the jaw system by the mechanical properties of the diet.
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Interspecific adult bite forces for all extant crocodylian species are now known. However, how bite forces scale during ontogeny across the clade has yet to be studied. Here we test the hypotheses that extant crocodylians share positively allometric and statistically comparable developmental scaling coefficients for maximal bite-force capacity relative to body size. To do this, we measured bite forces in the Australian freshwater crocodile Crocodylus johnsoni and the Saltwater crocodile C. porosus, and determined how performance changed during ontogeny. We statistically compared these results with those for the American alligator Alligator mississippiensis using 95% prediction intervals and interpreted our findings in a phylogenetic context. We found no observable taxon-specific shifts in the intraspecific scaling of biomechanical performance. Instead, all bite-force values in our crocodylid dataset fell within the bounds of the A. mississippiensis 95% prediction intervals, suggesting similar bite-force capacity when same-sized individuals are compared. This holds true regardless of differences in developmental stage, potential adult body size, rostro-dental form, bone mineralization, cranial suturing, dietary differences or phylogenetic relatedness. These findings suggest that intraspecific bite-force scaling for crocodylians with feeding ecologies comparable with those of extant forms has likely remained evolutionarily static during their diversification.
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Limb, tail and head measurements of 36 species in 11 genera of Australian agamid lizards were analysed to study relative growth, Strong allometric growth was recorded for many species. Allometric change tends to be less rapid in larger species. Juvenile proportions are usually similar in closely related species and may be useful as phylogenetic indicators. Morphometric data appear to be useful taxonomically at the generic level, and data from this paper could be used to support the erection of some new genera.
Article
The subspecies A. barbatus barbatus as currently recognized comprises two distinct marginally sympatric morphs. Differences in external and skeletal morphology and the apparent absence of hybrids in the narrow zone of overlap imply that each morph is genetically distinct and not a particular phenotypic expression of one genotype. The low density of one morph in the region of overlap, and hybrid inferiority as suggested by laboratory cross-mating, may each be partly responsible for the apparent lack of hybridization. On this basis each morph is given full species status, one being the typical form A. barbatus (Cuvier) while the other is referred to A. vitticeps Ahl. With the morphological differences between these two species as the criteria for species status, the other described subspecies of A. barbatus are examined and likewise elevated to species rank as follows: A. minor Sternfeld, A. minimus Loveridge and A. microlepidotus Glauert. Two additional new species A. mitchelli, sp. nov., and A. nullarbor, sp. nov., are described within the species-group.