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The evolution of alternate modes of development may occur through genetic changes in metamorphic timing. This hypothesis was examined by crossing salamanders that express alternate developmental modes: metamorphosis vs. paedomorphosis. Three strains were used in the crossing design: Ambystoma tigrinum tigrinum (Att; metamorph), wild-caught A. mexic...
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Citations
... But several species changed the timing of their sexual maturity and became pedomorph or neotene (gaining fertility while still retaining larval characters, see also McDiarmid & Altig 1999). Some species (mainly salamander) are facultative pedomorph, that is they can, depending on population density and other environmental factors, undergo metamorphosis or not (Voss and Smith, 2005). ...
Amphibians are a diverse animal class but are often only associated with frogs and salamanders in their most classical forms. However, each order within amphibians (frogs, salamanders, and caecilians) has highly specialized characters and/or species that fascinate researchers as well as laypersons world-wide. This special issue is aimed to provide an overview of some fascinating or even spectacular adaptations in amphibians.
... region was revealed by analysis of read coverage. In A tigrinum, this region is represented by approximately four times more reads than the corresponding A mexicanum region and adjacent (presumably diploid) regions, and coverage is also increased across this interval in sequence data from 48 A mexicanum X A mexicanum/A tigrinum backcross hybrids 21 (Figure 4). This observation was initially interpreted as evidence that A tigrinum had experienced one or more large-scale duplications over this region. ...
... To test this idea, we extracted recombination frequencies from a backcross mapping family A mexicanum X A mexicanum/A tigrinum that was previously used to perform QTL analyses of metamorphosis and sex, and more recently to generate scaffolding information necessary to achieve chromosome-scale contiguity of the A mexicanum reference genome. 8,21,22 Curiously, this region appears to recombine at only slightly reduced frequencies. The albino interval recombined at a rate of 8. Figure 10). ...
... Four genomic intervals are shown for each repeat family, Mapped RNAseq reads are color coded by study: orange, 38 green, 4 and blue 13 previously published 8X coverage shotgun sequence dataset from the male axolotl that was used to generate primary contigs for the A mexicanum reference assembly ("d/d male": SRX3655578-SRX3655581, SAMN06554622, 250 bp paired-end reads). 13 Finally, set of previouslyreported reads from a collection of low coverage sequence data from 48 A mexicanum X A mexicanum/A tigrinum backcross hybrids (PRJNA477812, 124 bp paired-end reads) 8,21 was used to calculate coverage and estimate copy number for a candidate introgressed region on chr1P. ...
Background
Recent efforts to assemble and analyze the Ambystoma mexicanum genome have dramatically improved the potential to develop molecular tools and pursue genome‐wide analyses of genetic variation.
Results
To better resolve the distribution and origins of genetic variation with A mexicanum, we compared DNA sequence data for two laboratory A mexicanum and one A tigrinum to identify 702 million high confidence polymorphisms distributed across the 32 Gb genome. While the wild‐caught A tigrinum was generally more polymorphic in a genome‐wide sense, several multi‐megabase regions were identified from A mexicanum genomes that were actually more polymorphic than A tigrinum. Analysis of polymorphism and repeat content reveals that these regions likely originated from the intentional hybridization of A mexicanum and A tigrinum that was used to introduce the albino mutation into laboratory stocks.
Conclusions
Our findings show that axolotl genomes are variable with respect to introgressed DNA from a highly polymorphic species. It seems likely that other divergent regions will be discovered with additional sequencing of A mexicanum. This has practical implications for designing molecular probes and suggests a need to study A mexicanum phenotypic variation and genome evolution across the tiger salamander clade.
... Genomic analyses have implicated the met1, met2 and met3 genes in these species differences. After axolotl treatment with exogenous T4, the effects of non-paedomorphic salamander alleles for these genes are additive in reducing time to metamorphosis (Voss and Smith, 2005). ...
Development encompasses processes that occur at multiple length-scales, includ- ing gene regulatory interactions, cell movements and reorganisation, cell signalling and growth. It is essential that the timing of events in all of these different processes are coordinated to generate well patterned tissues and organs. However, how the timing of intrinsic cell state changes is coordinated with events at the multi-tissue and whole organism level is unknown. Here, we argue that an important mechanism which accounts for integration of timing across levels of organisation is provided by tissue tectonics: i.e. how morphogenetic events driving tissue shape change result in the relative displacement of signalling and responding tissues and coordinate devel- opmental timing across scales. In doing so, tissue tectonics provides a mechanism by which the cell specification events intrinsic to cells can be modulated by the temporal exposure to extracellular signals. This exposure is in turn regulated by higher-order properties of the embryo such as their physical properties, rates of growth and the combination of dynamic cell behaviours impacting tissue morphogenesis. Tissue tec- tonics creates a downward flow of information from higher to lower levels of biological organisation, providing an instance of downward causation in development.
... Paedomorphosis has also been used to describe developmental variation among siblings within genetic crosses. Taking advantage of the recent evolution of paedomorphosis among tiger salamander complex species, interspecific genetic crosses have been performed in the laboratory to segregate metamorphic and paedomorphic modes of development and map the genomic location of genetic factors (13)(14)(15)(16)(17)(18). These crosses have identified major effect quantitative trait loci (QTL) that regulate the timing of metamorphosis and expression of paedomorphosis. ...
The Mexican axolotl (Ambystoma mexicanum) is an important model organism in biomedical research. Much current attention is focused on the axolotl's amazing ability to regenerate tissues and whole organs after injury. However, not forgotten is the axolotl's equally amazing ability to thwart aspects of tissue maturation and retain juvenile morphology into the adult phase of life. Unlike close tiger salamander relatives that undergo a thyroid hormone regulated metamorphosis, the axolotl does not typically undergo a metamorphosis. Instead, the axolotl exhibits a paedomorphic mode of development that enables a completely aquatic life cycle. The evolution of paedomorphosis allowed axolotls to exploit relatively permanent habitats in Mexico, and preadapted axolotls for domestication and laboratory study. In this perspective, we first introduce the axolotl and the various meanings of paedomorphosis, and then stress the need to move beyond endocrinology-guided approaches to understand the axolotl's hypothyroid state. With the recent completion of the axolotl genome assembly and established methods to manipulate gene functions, the axolotl is poised to provide new insights about paedomorphosis and the role of thyroid hormone in development and evolution.
... This is typical of amphibian metamorphosis but suggests further questions on the causes of such variation. Previous work on ambystomatids showed that different alleles can be associated with early versus late metamorphosis (Voss and Smith 2005), whereas hormonal pathways can trigger metamorphosis in response to environmental stressors (Denver et al. 2002). Predation risk was also associated with both higher glucocorticoid levels (corticosterone) and lower activity in a plethodontid paedomorphic species (Davis and Gabor 2015). ...
Evolutionary theory predicts the evolution of metamorphosis over paedomorphosis (the retention of larval traits at the adult stage) in response to life in unfavourable habitats and to the benefits of dispersal. Although many organisms are canalised into obligatory complex or simple life cycles, some species of newts and salamanders can express both processes (facultative paedomorphosis). Previous research highlighted the detrimental effect of fish on both metamorphic and paedomorphic phenotypes, but it remains unknown whether predation risk could induce shifts from paedomorphosis to metamorphosis, whether behavioural avoidance could be an alternative strategy to metamorphosis and whether these responses could be sex-biased. Testing these hypotheses is important because metamorphosed paedomorphs are dispersal individuals which could favour the long-term persistence of the process by breeding subsequently in more favourable waters. Therefore, we quantified the spatial behaviour and timing of the metamorphosis of facultative paedomorphic palmate newts Lissotriton helveticus in response to predation risk. We found that fish induced both male and female paedomorphs to hide more often, but behavioural avoidance was not predictive of metamorphosis. Paedomorphs did not metamorphose more in the presence of fish, yet there was an interaction between sex and predation risk in metamorphosis timing. These results improve our understanding of the lower prevalence of paedomorphs in fish environments and of the female-biased sex ratios in natural populations of paedomorphic newts. Integrating sex-dependent payoffs of polyphenisms and dispersal across habitats is therefore essential to understand the evolution of these processes in response to environmental change.
... This led us to adapt established meiotic mapping methods for Ambystoma as a tool to generate dense genome-wide scaffolding information. Hybrid crosses between A. mexicanum and A. tigrinum (and other species) have been generated and used to develop meiotic maps for the species and infer the positions of quantitative trait loci (QTL), sex, and Mendelian pigment mutants Shaffer 1997, 2000;Voss et al. 2001;Voss and Smith 2005;Voss 2006, 2009;Page et al. 2013;Woodcock et al. 2017). For example, hybrid crosses have been used to dissect the genetic basis of paedomorphosis, a hallmark trait of salamanders Shaffer 1997, 2000;Voss and Smith 2005). ...
... Hybrid crosses between A. mexicanum and A. tigrinum (and other species) have been generated and used to develop meiotic maps for the species and infer the positions of quantitative trait loci (QTL), sex, and Mendelian pigment mutants Shaffer 1997, 2000;Voss et al. 2001;Voss and Smith 2005;Voss 2006, 2009;Page et al. 2013;Woodcock et al. 2017). For example, hybrid crosses have been used to dissect the genetic basis of paedomorphosis, a hallmark trait of salamanders Shaffer 1997, 2000;Voss and Smith 2005). Paedomorphosis reflects the loss of metamorphic changes in a derived species relative to its ancestor. ...
The axolotl (Ambystoma mexicanum) provides critical models for studying regeneration, evolution, and development. However, its large genome (∼32 Gb) presents a formidable barrier to genetic analyses. Recent efforts have yielded genome assemblies consisting of thousands of unordered scaffolds that resolve gene structures, but do not yet permit large-scale analyses of genome structure and function. We adapted an established mapping approach to leverage dense SNP typing information and for the first time assemble the axolotl genome into 14 chromosomes. Moreover, we used fluorescence in situ hybridization to verify the structure of these 14 scaffolds and assign each to its corresponding physical chromosome. This new assembly covers 27.3 Gb and encompasses 94% of annotated gene models on chromosomal scaffolds. We show the assembly's utility by resolving genome-wide orthologies between the axolotl and other vertebrates, identifying the footprints of historical introgression events that occurred during the development of axolotl genetic stocks, and precisely mapping several phenotypes including a large deletion underlying the cardiac mutant. This chromosome-scale assembly will greatly facilitate studies of the axolotl in biological research.
... This would explain why axolotls do not release T 4 in response to CRH treatment as other amphibians do, including the closely related tiger salamander. Moreover, this hypothesis fits with the observation that paedomorphosis in the axolotl is the result of a major-gene effect (Shaffer and Voss, 1996;Voss, 1995;Voss andShaffer, 1997, 2000;Voss and Smith, 2005). The offspring of F 1 A. mexicanum × A. tigrinum hybrids backcrossed to axolotls segregated in ∼1:1 ratios (metamorphosing:paedomorphic) compatible with a major-effect locus controlling most of the variation in life cycle mode. ...
... The offspring of F 1 A. mexicanum × A. tigrinum hybrids backcrossed to axolotls segregated in ∼1:1 ratios (metamorphosing:paedomorphic) compatible with a major-effect locus controlling most of the variation in life cycle mode. Interestingly, a molecular marker that associated with the inheritance of the unknown 'metamorphosis locus' is located on the same chromosome as the crhr2 gene in the axolotl (Voss and Smith, 2005) (see further). ...
... As mentioned earlier, A. mexicanum × A. tigrinum backcrosses have shown that axolotl paedomorphosis is based on a major-gene effect, suggesting that a mutation in a single but hitherto unidentified gene (referred to as met1) is responsible for paedomorphosis in the axolotl (Shaffer and Voss, 1996;Voss, 1995;Voss andShaffer, 1997, 2000;Voss and Smith, 2005). Individuals that inherited one or two copies of the dominant tigrinum allele would undergo spontaneous metamorphosis, whereas animals that inherited two copies of the recessive mexicanum allele exhibited paedomorphism. ...
The Mexican axolotl (Ambystoma mexicanum) is a salamander species that does not undergo metamorphosis, resulting in the retention of juvenile characteristics in the mature breeding stage (paedomorphosis). Here we review the endocrinological studies investigating the proximate cause of axolotl paedomorphosis with a focus on the hypothalamo-pituitary-thyroid (HPT) axis. It is well established that axolotl paedomorphosis is a consequence of low activity of the HPT axis. The pituitary hormone thyrotropin (TSH) is capable of inducing metamorphosis in the axolotl, which indicates that all processes and interactions in the HPT axis below the pituitary level are functional, but that TSH release is impaired. In metamorphosing species, TSH secretion is largely controlled by the hypothalamic neuropeptide corticotropin-releasing hormone (CRH), which seems to have lost its thyrotropic activity in the axolotl. However, preliminary experiments have not yet confirmed a role for faulty CRH signalling in axolotl paedomorphosis. Other hypothalamic factors and potential pituitary inhibitors need to be investigated to identify their roles in amphibian metamorphosis and axolotl paedomorphosis.
... This work is particularly exciting in that it demonstrated a relatively simple and fast process for developing linkage maps from large-genome species without the requirement for tremendous sequencing resources (only one HiSeq2000 lane was used) or >F1 generations (a single mother and her 28 offspring were used). Given that whole-genome sequence assemblies for most salamanders are likely to be unavailable in the near future, transcriptome-based linkage maps will continue to serve as our best resources for studying genome structure and the placement of ecologically and functionally relevant loci (e.g., Voss and Smith 2005). ...
Salamanders have some of the largest genomes among all extant organisms, due in large part to the proliferation of repetitive elements and the expansion of intron size. This increased complexity and size has limited the application of genomic tools to the population genetic and phylogenetic study of salamanders, even as these methods have become common for most other organisms. However, the generation of genomic data in salamanders is not out of reach for most researchers. High-quality and informative data sets can be acquired for salamander-centric research projects with careful consideration of the genomic tool(s) most appropriate for the question at hand and how best to apply these to a salamander genome. Here, we review a range of genomic tools representing the current best options for use in the study of genome-wide variation within and between salamander species. This includes the use of transcriptomics (RNAseq), restriction site-associated DNA sequencing (RADseq), sequence capture enrichment methods, and PCR-based parallel tagged amplicon sequencing. Each of these methods has a particular set of benefits, as well as limitations in the study of salamander genomics. We highlight their trade-offs and the factors that should be considered when choosing among them, and we provide descriptions of exemplar studies that illustrate their empirical applications. By making informed decisions about the choice and implementation of these subgenomic methods, we believe that they can be broadly and effectively applied as important resources for the study of salamander evolution and conservation.
... This led us to adapt established meiotic mapping methods for Ambystoma as a tool to generate dense genome-wide scaffolding information. Hybrid crosses between A. mexicanum and A. tigrinum (and other species) have been generated and used to develop meiotic maps for the species and infer the positions of quantitative trait loci (QTL), sex and Mendelian pigment mutants (Voss and Shaffer 1997;Voss and Shaffer 2000;Voss et al. 2001;Voss and Smith 2005;Smith and Voss 2006;Page et al. 2013;Woodcock et al. 2017). For example, hybrid crosses have been used to dissect the genetic basis of paedomorphosis, a hallmark trait of salamanders (Voss and Shaffer 1997;Voss and Shaffer 2000;Voss and Smith 2005). ...
... Hybrid crosses between A. mexicanum and A. tigrinum (and other species) have been generated and used to develop meiotic maps for the species and infer the positions of quantitative trait loci (QTL), sex and Mendelian pigment mutants (Voss and Shaffer 1997;Voss and Shaffer 2000;Voss et al. 2001;Voss and Smith 2005;Smith and Voss 2006;Page et al. 2013;Woodcock et al. 2017). For example, hybrid crosses have been used to dissect the genetic basis of paedomorphosis, a hallmark trait of salamanders (Voss and Shaffer 1997;Voss and Shaffer 2000;Voss and Smith 2005). Paedomorphosis reflects the loss of metamorphic changes in a derived species relative to its ancestor. ...
The axolotl (Ambystoma mexicanum) provides critical models for studying regeneration, evolution and development. However, its large genome (~32 gigabases) presents a formidable barrier to genetic analyses. Recent efforts have yielded genome assemblies consisting of thousands of unordered scaffolds that resolve gene structures, but do not yet permit large scale analyses of genome structure and function. We adapted an established mapping approach to leverage dense SNP typing information and for the first time assemble the axolotl genome into 14 chromosomes. Moreover, we used fluorescence in situ hybridization to verify the structure of these 14 scaffolds and assign each to its corresponding physical chromosome. This new assembly covers 27.3 gigabases and encompasses 94% of annotated gene models on chromosomal scaffolds. We show the assembly's utility by resolving genome-wide orthologies between the axolotl and other vertebrates, identifying the footprints of historical introgression events that occurred during the development of axolotl genetic stocks, and precisely mapping several phenotypes including a large deletion underlying the cardiac mutant. This chromosome-scale assembly will greatly facilitate studies of the axolotl in biological research.
... Salamanders from the Ambystoma genus have provided important models for biological studies focusing on development, ecology and evolution (Voss and Smith 2005;Smith and Voss 2009;Eisthen and Krause 2012). The axolotl, Ambystoma mexicanum is an amphibian from the Urodela order, pertaining to the Ambystomatidae family (Servín 2011). ...
Ambystoma mexicanum is an endemic neotenic urodele amphibian from Mexico; although it belongs to the Salamandridae family, it is characterized by retaining larval structures and hence has been widely used as an experimental model. In the present study, we describe the main events of gonadal morphogenesis in A. mexicanum and correlate these with stages in embryonic and larval development. In this way, it was established that during stage 41 (St41), the gonadal primordium is formed, consisting of primordial germ cells (PGC) and somatic cells. During St45, the undifferentiated gonad is formed from a larger number of PGC interacting with somatic cells. During St53, the germ and somatic cells arrange into the cortical and medullary region. As development proceeds between St55 and 57, morphological differentiation of the gonadal sex takes place, primarily manifested in ovarian differentiation. Our observations and the way these correlate with other urodeles suggest that gonadal morphogenesis in A. mexicanum does not depend on larval age. Besides, onset of gonadal sexual differentiation takes place from St53 onward, evidenced by ovarian structural changes, thus neotenic condition does not influence gonadal differentiation events. Finally, it has been established that gonadal development is controlled by chronological regulation that differs from that of somatic development which in the case of A. mexicanum suggests that gonadal development is completely independent of metamorphosis, thus implying a process of heterochrony.
