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Production of an Embryo by an Acrochordus javanicus Isolated for Seven Years
... In snakes, a positive association between midpiece length and the strength of sperm competition exists, though this same pattern is not observed in lizards (Friesen et al., 2020). Snakes also have a significantly longer period of sperm storage on average than is found in lizards, with the Javan file snake (Acrochordus javanicus) holding the record for longest known period of sperm storage among all animals (7 years- Magnusson, 1979;Friesen et al., 2020). Whether longer midpieces are more common in snakes with high levels of sperm competition due to conferring an advantage during extended periods of sperm storage, or because they relay another type of advantage, remains unknown. ...
Managing a species of conservation concern can be best achieved when there is information on the reproductive physiology of both sexes available; however, many species lack this critical, baseline information. One such species, the tuatara (Sphenodon punctatus), is the last surviving member of one of the four reptile orders (Rhynchocephalia) and is the only reptile known to lack a male intromittent organ. Culturally and evolutionarily significant, the conservation of this species is a global priority for the maintenance of biodiversity. In light of this, we characterized the morphology, viability and swim speed of mature tuatara sperm for the first time. We found that tuatara sperm are filiform and bear the remarkably conserved three-part sperm structure seen across the animal kingdom. Tuatara sperm are long (mean total length 166 μm), with an approximate head:midpiece:tail ratio of 15:1:17. While tuatara sperm are capable of high levels of within-mating viability (94.53%), the mean viability across all samples was 58.80%. Finally, tuatara sperm had a mean curvilinear velocity swim speed (μ × s − 1) of 82.28. At the population level, there were no differences in viability or mean swim speed between sperm collected from a male’s first mating of a season and repeat matings; however, the maximum sperm swim speed increased in observed repeated matings relative to first matings. Interestingly, faster sperm samples had shorter midpieces, but had greater viability and longer head and tail sections. This work expands our understanding of male reproductive characteristics and their variation to a new order, provides wild references for the assessment of captive individuals, lays the groundwork for potential assisted reproductive techniques and highlights variation in male reproductive potential as an important factor for consideration in future conservation programs for this unique species.
... Squamates can also reproduce via obligate parthenogenesis (Figure 1), resulting in species or populations composed entirely of females, including in certain geckos (Lepidodactylus lugubris [64] and Hemidactylus garnotii [65]), the well-known 'flowerpot snake' (Indotyphlops braminus [66]), and several hybrid species from the genera Cnemidophorus/Aspidoscelis [67] and Darevskia [68]. Numerous examples of facultative parthenogenesis have recently been documented in captive squamates, including the Komodo dragon [69] and various snakes [70][71][72][73][74][75][76], and wild populations of pit vipers [77]. As was the case with sex determination, squamate reptiles are an ideal group for investigating the genetics and evolution of reproductive mode and unappreciated examples of unique reproductive modes likely remain to be discovered. ...
Simple Summary
As a group of organisms, non-avian reptiles, most of which are the ~11,000 species of lizards and snakes, are an extraordinarily diverse group, displaying a greater diversity of genetic, genomic, and phenotypic traits than mammals or birds. Yet the number of genomes available for non-avian reptiles lags behind that for other major vertebrate groups. Here we review the diversity of genome structures and reproductive and genetic traits of non-avian reptiles and discuss how this diversity can fuel the next generation of whole-genome phylogenomic analyses. Whereas most higher-level phylogenies of non-avian reptile groups have been driven by a group of markers known as ultraconserved elements (UCEs), many other types of markers, some with likely greater information content than UCEs, exist and are easily mined bioinformatically from whole-genomes. We review methods for bioinformatically harvesting diverse marker sets from whole genomes and urge the community of herpetologists to band together to begin collaboratively constructing a large-scale, whole-genome tree of life for reptiles, a process that has already begun for birds and mammals. Such a resource would provide a much-needed high-level view of the phylogenetic relationships and patterns of genome evolution in this most diverse clade of amniotes.
Abstract
Non-avian reptiles comprise a large proportion of amniote vertebrate diversity, with squamate reptiles—lizards and snakes—recently overtaking birds as the most species-rich tetrapod radiation. Despite displaying an extraordinary diversity of phenotypic and genomic traits, genomic resources in non-avian reptiles have accumulated more slowly than they have in mammals and birds, the remaining amniotes. Here we review the remarkable natural history of non-avian reptiles, with a focus on the physical traits, genomic characteristics, and sequence compositional patterns that comprise key axes of variation across amniotes. We argue that the high evolutionary diversity of non-avian reptiles can fuel a new generation of whole-genome phylogenomic analyses. A survey of phylogenetic investigations in non-avian reptiles shows that sequence capture-based approaches are the most commonly used, with studies of markers known as ultraconserved elements (UCEs) especially well represented. However, many other types of markers exist and are increasingly being mined from genome assemblies in silico, including some with greater information potential than UCEs for certain investigations. We discuss the importance of high-quality genomic resources and methods for bioinformatically extracting a range of marker sets from genome assemblies. Finally, we encourage herpetologists working in genomics, genetics, evolutionary biology, and other fields to work collectively towards building genomic resources for non-avian reptiles, especially squamates, that rival those already in place for mammals and birds. Overall, the development of this cross-amniote phylogenomic tree of life will contribute to illuminate interesting dimensions of biodiversity across non-avian reptiles and broader amniotes.
... Relative to other animal taxa, female reptiles are known to have an ability to store sperm for very long periods; fertile eggs have been laid by female geckos isolated from males for more than one year (Yamamoto and Ota, 2006), female turtles isolated from males for four years (Ewing, 1943), and female snakes isolated from males for seven years (Magnusson, 1979). Genetic studies have also reported multiple paternity arising from mixing of sperm stored from matings in previous years and recently inseminated sperm in captive snakes (Agkistrodon contortrix; Schuett and Gillingham,1986) and ...
... In wild populations, clutch fertilization by stored sperm has a documented duration of one to two years in female Blanding"s Turtles (Emydoidea blandingii; Anthonysamy, Dreslik, Douglas, Marioni, & Phillips, 2014) and six years in a female Western Diamondback Rattlesnake (Crotalus atrox; Levine, Schuett, & Booth, 2021). The record duration for female sperm storage in vertebrates is for Javan Wart Snakes, Acrochordus javanicus, that can store sperm for up to seven years (Magnusson, 1979). As with parthenogenesis, female sperm storage may be particularly adaptive in species where encounter rates between males Downloaded from https://academic.oup.com/jhered/advance-article/doi/10.1093/jhered/esab048/6354702 by Macquarie University user on 27 September 2021 A c c e p t e d M a n u s c r i p t 6 and females are low (Gist & Congdon, 1998;Orr & Zuk, 2012;Uller & Olsson, 2008). ...
The ability to produce viable offspring without recently mating, either through sperm storage or parthenogenesis, can provide fitness advantages under a suite of challenging ecological scenarios. Using genetic analysis, we demonstrate that three wild-caught female Tree Skinks (Egernia striolata) reproduced in captivity with no access to males for over a year, and that this is best explained by sperm storage. To the best of our knowledge, this is the first time female sperm storage has been documented in any monogamous family-living reptile, including social Australian egerniine skinks (from the subfamily Egerniinae). Furthermore, by using paternal reconstruction of genotypes we show that captive-born offspring produced by the same females in the preceding year, presumably without sperm storage, were sired by different males. We qualitatively compared aspects of these females’ mates and offspring between years. The parents of each litter were unrelated, but paternal and offspring genotypes from litters resulting from stored sperm were more heterozygous than those inferred to be from recent matings. Family-living egerniine skinks generally have low rates of multiple paternity, yet our study suggests that female sperm storage, potentially from outside social partners, offers the real possibility of benefits. Possible benefits include increasing genetic compatibility of mates and avoiding inbreeding depression via cryptic female choice. Sperm storage in Tree Skinks, a family-living lizard with a monogamous mating system, suggests that females may bet-hedge through extra-pair copulation with more heterozygous males, reinforcing the idea that females could have more control on reproductive outcomes than previously thought.
... In contrast, litters genetically confirmed as LTSS in pitvipers, have been indistinguishable from those produced without sperm storage (results presented here, [15]). Given these distinct differences in litter characteristics, the longest reported case that is attributed to LTSS (84 months in the Javan File Snake, Acrochordus javanicus, [53]), cannot be conclusively confirmed as LTSS, as the litter characteristics are also strongly indicative of FP [15,17]. Furthermore, it was believed that the embryo died during development, shortly prior to the death of the mother. ...
Females of many vertebrate species have the capacity to store sperm within their reproductive tracts for prolonged periods of time. Termed long-term sperm storage, this phenomenon has many important physiological, ecological, and evolutionary implications, particularly to the study of mating systems, including male reproductive success and post-copulatory sexual selection. Reptiles appear particularly predisposed to long-term sperm storage, with records in most major lineages, with a strong emphasis on turtles and squamates (lizards, snakes, but not the amphisbaenians). Because facultative parthenogenesis is a competing hypothesis to explain the production of offspring after prolonged separation from males, the identification of paternal alleles through genetic analysis is essential. However, few studies in snakes have undertaken this. Here, we report on a wild-collected female Western Diamond-backed Rattlesnake, Crotalus atrox, maintained in isolation from the time of capture in September 1999, that produced two healthy litters approximately one and six years post capture. Genetic analysis of the 2005 litter, identified paternal contribution in all offspring, thus rejecting facultative parthenogenesis. We conclude that the duration of long-term sperm storage was approximately 6 years (71 months), making this the longest period over which a female vertebrate has been shown to store sperm that resulted in the production of healthy offspring.
... Alligator mississipiensis Birkhead & Møller (1993), Crotalus durissus terrificus Almeida-Santos & Salomão (1997), apresentam túbulos de fundo cego para essa função. A cobra asiática, Acrochordus javanicus Hornstedt (1787), possui a capacidade de armazenar seu esperma por um período de até sete anos (Magnusson, 1979). O avestruz, Struthio camelus Linnaeus (1758), consegue armazenar o esperma por até 4 semanas (Malecki et al., 2004). ...
O presente estudo conheceu em detalhes a estrutura e função da glândula oviducal do tubarão-azul, Prionace glauca, de fundamental importância na reprodução e perpetuação da espécie no Atlântico Sul. Foram aplicadas técnicas histológicas em glândulas oviducais de duas fêmeas adultas no estágio 3 e de três no estágio 5, segundo os critérios de Colonello. Cortes histológicos longitudinais de 7µm de espessura inicialmente foram corados com hematoxilina e eosina. Posteriormente, testes histoquímicos foram aplicados, utilizando as colorações Ácido Periódico-Schiff (PAS) e o Azul Alciano (AB). Quatro zonas foram identificadas: Club, Papillary, Baffle e Terminal. Na zona Baffle foi observada intensa atividade secretora de colágeno da cápsula, sinal de fase ovulatória. Na zona Terminal, foi observado armazenamento de esperma. Os testes histoquímicos indicaram reação positiva com o corante PAS nas regiões epiteliais e glandulares das quatro zonas, bem como nos agrupamentos de espermatozoides, indicativo da presença de glicosaminoglicanos neutros. A reação foi positiva com o corante AB apenas nas regiões glandulares das zonas Club e Papillary, nos espermatozoides, bem como nas secreções dentro dos cistos que os armazenam, indicativo de atividade secretora de glicosaminoglicanos ácidos. Com os resultados obtidos, observou-se que a glândula oviducal é extremamente especializada em termos fisiológicos. Além da sua capacidade de armazenamento de esperma por longos períodos, apresenta elevada atividade secretora e que, em conjunto com os movimentos ciliares na sua região luminal, propiciam a formação da gelatina e da cobertura terciária protetora do ovo, sendo este posteriormente depositado no interior do útero, para dar início à fase gestacional.
... The need for sperm to survive for extended periods in either the female or male reproductive tract could result in selection for sperm with higher energy stores. Reptiles are also the record holders for the maximum duration of sperm storage across vertebrates [69], and snakes top the charts with an impressive seven years of storage reported for the Javan file snake (Acrochordus javanicus [70]). Lizards also store sperm for extended periods, but the maximum duration often only spans a single reproductive season [69]. ...
Multiple paternity is ubiquitous within the polyphyletic group called 'reptiles', especially within the lizards and snakes. Therefore, the probability of sperm competition occurring, and being intense, is high. Squamates exhibit a diversity of tactics to ensure fertilization success in the face of sperm competition. The duration of female sperm storage, which can be many months and even years in some species, remains an enigma. Here, we emphasize some mechanisms that might affect patterns of paternity, the source and function of ejaculates and features of the female reproductive tract that may aid in long-term sperm storage. In doing so, we present a new analysis of the relationship between sperm size, the strength of sperm competition and the duration of female sperm storage. Lizards and snakes are a diverse group that has provided many excellent models for the study of an array of life-history strategies. However, when it comes to postcopulatory sexual selection, there is much left to discover. This article is part of the theme issue 'Fifty years of sperm competition'.
... The need for sperm to survive for extended periods in either the female or male reproductive tract could result in selection for sperm with higher energy stores. Reptiles are also the record holders for the maximum duration of sperm storage across vertebrates [69], and snakes top the charts with an impressive seven years of storage reported for the Javan file snake (Acrochordus javanicus [70]). Lizards also store sperm for extended periods, but the maximum duration often only spans a single reproductive season [69]. ...
Multiple paternity is ubiquitous within the polyphyletic group called ‘reptiles', especially within the lizards and snakes. Therefore, the probability of sperm competition occurring, and being intense, is high. Squamates exhibit a diversity of tactics to ensure fertilization success in the face of sperm competition. The duration of female sperm storage, which can be many months and even years in some species, remains an enigma. Here, we emphasize some mechanisms that might affect patterns of paternity, the source and function of ejaculates and features of the female reproductive tract that may aid in long-term sperm storage. In doing so, we present a new analysis of the relationship between sperm size, the strength of sperm competition and the duration of female sperm storage. Lizards and snakes are a diverse group that has provided many excellent models for the study of an array of life-history strategies. However, when it comes to postcopulatory sexual selection, there is much left to discover.
This article is part of the theme issue ‘Fifty years of sperm competition'.
... The female in this study has had no contact with any conspecific male for 13 years now. Prolonged sperm storage has been documented in various snake species, but the longest time period of suspected sperm storage reported for a snake was seven years and six months (Magnusson 1979, Birkhead & MØller 1993, Booth & Schuett 2011. In our case we described the lack of male genetic contribution to the offspring using molecular analysis, thus excluding prolonged sperm storage. ...
Parthenogenesis is a biological process of asexual reproduction. Recent studies have highlighted the significance of this fascinating phenomenon in vertebrate evolution. Although parthenogenetic reproduction appears to be widespread among reptiles, a restricted number of cases have been reported both in captivity and in the wild. Here we studied and reported an intriguing case of a 20-year old captive female Cuban boa (Chilabothrus angulifer), from the Zoo da Maia (Maia, Portugal) collection, isolated from conspecific males, that has given birth twice in four years. The neonates from both deliveries, one fresh and the other fixed in formalin, were subjected to histopathological and molecular genetics analyses. Both neonates were homozygous for the loci analysed, carrying only maternal alleles. Furthermore, morphological abnormalities (anophthalmia) were observed in the second neonate. Our data support a pattern of parthenogenetic reproduction. This is the first documented case suggesting facultative parthenogenesis in a Cuban boa, which can be of great interest for further research on ecology, evolution, captive breeding and conservation of the species.
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