REPTILIAN VIVIPARITY AND DOLLO'S LAW

It has been suggested repeatedly that the evolutionary transition from oviparity (egg-laying) to viviparity (live-bearing) in reptiles is irreversible. However, these adaptive arguments have yet to be tested by detailed examination of the phylogenetic distribution of oviparity and viviparity across a broad range of taxa. Using available data on reproductive modes and phylogenetic relationships within reptiles, we here quantify the numbers and directions of evolutionary transitions between oviparity and viviparity. Phylogenetic relationships among three diverse squamate groups (scincid lizards, colubrid snakes, elapid snakes) are currently inadequately known for inclusion in this study Among the remaining reptiles, oviparity has given rise to viviparity at least 35 times. Five possible instances of reversals (from viviparity to oviparity) are identified, but closer examination indicates that all have weak empirical support (i.e., they could be “unreversed” with little loss in parsimony, and/or are based on poorly substantiated phylogenetic hypotheses). Viviparity is clearly more frequently (and presumably easily) gained than lost in several disparate groups so far examined (reptiles, fishes, polychaete worms); this evolutionary bias should be considered when reproductive mode is optimized on a phylogeny or employed in phylogenetic reconstruction.     

三叠纪胎生主龙型海洋爬行动物

现代爬行动物的生殖方式包括卵生、卵胎生和“胎生”三种类型.总体而言,卵生即母体在陆地上产出羊膜卵,并依靠外界环境加以孵化;卵胎生系指羊膜卵在母体内孵化,随即产出幼子,其间胚胎的营养来源和代谢废物均限于羊膜卵内;所谓“胎生”,是指某些类群的卵在母体内孵化后没有立刻产出,胚胎与母体建立了某种程度的营养乃至气体交换关系,此后再以幼体的形式娩出.卵胎生和“胎生”见于有鳞类.在化石中,由于无法识别胚胎与母体的营养联系等信息,通常只以“生产方式”加以定义,即除卵生以外,所有“含胚胎的化石”都统称为“胎生”,目前“胎生”已有的准确记录包括鱼龙类、鳍龙类、沧龙类和离龙类.近期报道的“怀孕恐头龙”显示原龙类可能也有此种生殖方式,但标本的保存状态显示不能排除其“同类相食”之可能.本文记述了产自云南罗平地区中三叠系内一独立保存的、完整的圆胚状化石,标本的大小、形态、姿态和埋藏环境显示这是一个处于孵化后期、因某种原因而流产的胚胎.头后骨骼显示该标本代表了一种全新类型的海生原龙类,但是由于在个体发育中很多性状特征会有较大变化,因此胚胎乃至幼体标本不宜作为正型标本而建立新属种.这也是又一个主龙型爬行动物胎生的确切证据;同时这也进一步反映了盘县—罗平动物群中原龙类的高度多样性.     

Absence of Suction Feeding Ichthyosaurs and Its Implications for Triassic Mesopelagic Paleoecology

Mesozoic marine reptiles and modern marine mammals are often considered ecological analogs, but the extent of their similarity is largely unknown. Particularly important is the presence/absence of deep-diving suction feeders among Mesozoic marine reptiles because this would indicate the establishment of mesopelagic cephalopod and fish communities in the Mesozoic. A recent study suggested that diverse suction feeders, resembling the extant beaked whales, evolved among ichthyosaurs in the Triassic. However, this hypothesis has not been tested quantitatively. We examined four osteological features of jawed vertebrates that are closely linked to the mechanism of suction feeding, namely hyoid corpus ossification/calcification, hyobranchial apparatus robustness, mandibular bluntness, and mandibular pressure concentration index. Measurements were taken from 18 species of Triassic and Early Jurassic ichthyosaurs, including the presumed suction feeders. Statistical comparisons with extant sharks and marine mammals of known diets suggest that ichthyosaurian hyobranchial bones are significantly more slender than in suction-feeding sharks or cetaceans but similar to those of ram-feeding sharks. Most importantly, an ossified hyoid corpus to which hyoid retractor muscles attach is unknown in all but one ichthyosaur, whereas a strong integration of the ossified corpus and cornua of the hyobranchial apparatus has been identified in the literature as an important feature of suction feeders. Also, ichthyosaurian mandibles do not narrow rapidly to allow high suction pressure concentration within the oral cavity, unlike in beaked whales or sperm whales. In conclusion, it is most likely that Triassic and Early Jurassic ichthyosaurs were ‘ram-feeders’, without any beaked-whale-like suction feeder among them. When combined with the inferred inability for dim-light vision in relevant Triassic ichthyosaurs, the fossil record of ichthyosaurs does not suggest the establishment of modern-style mesopelagic animal communities in the Triassic. This new interpretation matches the fossil record of coleoids, which indicates the absence of soft-bodied deepwater species in the Triassic.     

Is increased maternal basking an adaptation or a pre-adaptation to viviparity in lizards?

Pregnant females modify their thermoregulatory behaviour in many species of viviparous (live-bearing) reptiles, typically maintaining higher and more stable body temperatures at this time. Such modifications often have been interpreted as adaptations to viviparity, functioning to accelerate embryonic development and/or modify phenotypic traits of hatchlings. An alternative possibility is that similar maternal thermophily may be widespread also in oviparous species and if so, would be a pre-adaptation (rather than an adaptation) to viviparity. Because eggs are retained in utero for a significant proportion of development even in oviparous reptiles, maternal thermophily might confer similar advantages in oviparous as in viviparous taxa. Experimental trials on montane oviparous scincid lizards (Bassiana duperreyi) support the pre-adaptation hypothesis. First, captive females (both reproductive and non-reproductive) selected higher temperatures than males. Second, experimentally imposing thermal regimes on pregnant females significantly affected their oviposition dates and the phenotypic traits (body shape, running speed) of their hatchlings. Thus, as for many other behavioural correlates of pregnancy in viviparous reptiles, maternal thermophily likely may have already been present in the ancestral oviparous taxa that gave rise to present-day viviparous forms.     

Viviparity Advantages in the Lizard <Emphasis Type="Italic">Liolaemus sarmientoi</Emphasis> from the End of the World

Two hypotheses have prevailed to explain the evolution of viviparity in reptiles: the first proposed that viviparity evolved in response to cold-climates because the possibility of pregnant females to thermoregulate at higher temperatures than embryos could experience in a nest in nature. The second hypothesis posits that the advantage of viviparity is based on the possibility of females to maintain stable body temperatures during development, enhancing offspring fitness. With the aim to contribute to understanding the origins of viviparity in reptiles, we experimentally subjected pregnant females of the austral lizard Liolaemus sarmientoi to two temperature treatments until parturition: one that simulated environmental temperatures for a potential nest (17–25?°C) and another that allowed females to thermoregulate at their preferred body temperature (17–45?°C). Then, we analysed newborn body conditions and their locomotor performance to estimate their fitness. In addition, we measured the body temperature in the field and the preferred temperature in the laboratory of pregnant and non-pregnant females. Pregnant females thermoregulated to achieve higher temperatures than the environmental temperatures, and also thermoregulated within a narrower range than non-pregnant females. This could have allowed embryos to develop in higher and more stable temperatures than they would experience in a nest in nature. Thus, offspring developed at the female preferred temperature showed greater fitness and were born earlier in the season than those developed at lower environmental temperatures. Herein, we show that results are in agreement with the two hypotheses of the origin of viviparity for one of the southernmost lizards of the world.     

Life‐history strategies indicate live‐bearing in Nothosaurus (Sauropterygia)

In Sauropterygia, a diverse group of Mesozoic marine reptiles, fossil evidence of viviparity (live‐bearing) only exists for Pachypleurosauria and Plesiosauria, and was assumed to also be the case for nothosaurs. Previous studies have successfully applied an extant squamate model to sauropterygian life‐history traits. In extant squamates, oviparity and viviparity are associated with differences in life‐history trait combinations. We establish growth curves for Nothosaurus specimens based on their humeral histology. We then analyse life‐history traits derived from these curves and compare inferred traits to those of modern squamates and pachypleurosaurs to assess their reproduction mode. We show that birth to adult size ratios (i.e. birth size divided by the mother's size) provide good estimates of clutch sizes in extant squamates and in viviparous extinct marine reptiles, but these ratios cannot discriminate viviparous and oviparous squamates. Thus, large ratios do not indicate viviparity in fossil taxa to which the extant squamate model is applicable. Applying differences in birth size, age at maturation, and maximum longevity that are observed between extant viviparous and oviparous squamates to our Nothosaurus sample, we identified 7 out of 24 specimens as being potentially viviparous. Conversely, they suggested oviparity for many nothosaurs but also for many pachypleurosaur samples. Under the assumption that the entire clade Pachypleurosauria was viviparous, the majority of nothosaurs would also have been viviparous as they comprised trait combinations similar to those seen in pachypleurosaurs. Overall, this suggests that within nothosaurs and pachypleurosaurs both reproduction modes existed in different taxa.     

Ein Weg ohne Rückkehr?

Giving birth (viviparity) evolved several times independently among vertebrates, particularly often among lizards and snakes. Consequently, different physiological and anatomical changes developed such as the placenta in pure vivipar species. Fossil marine reptiles show that a marine environment can trigger the evolution of viviparity. A prerequisite is that a genomic sex determination develops, too. A reversal from viviparity to laying eggs (oviparity) is very difficult both physiologically and anatomically. It is not yet clear, whether this can happen at all.     

Influence of the evolution of viviparity on eggshell morphology in the lizard Lerista bougainvillii

In reptiles, the evolutionary transition from egg-laying to live-bearing is thought to involve a gradual increase in the duration of egg retention, with progressively more development occurring prior to oviposition, and culminating in the birth of fully developed offspring. However, prolonging the retention of fully-shelled eggs within the oviducts may pose serious gas-exchange problems for the embryos. Thus, evolutionary increases in the period of intrauterine retention may require correlated decreases in the thickness of eggshells and/or their degree of calcification to allow for adequate embryonic gas exchange. To test this evolutionary model, eggs of three distinct reproductive forms of the scincid lizard Lerista bougainvillii were examined to determine the evolutionary relationships between the thickness of the shell membrane, degree of eggshell calcification, and the duration of uterine egg retention. These comparisons revealed the predicted pattern of correlated shifts in eggshell morphology and embryonic stage at oviposition. Evolutionary increases in the duration of egg retention were accompanied by decreases in the thickness of the eggshell membrane and degree of eggshell calcification. This evolutionary model suggests that there may be a tradeoff between the advantages of extended egg retention and the disadvantages of a thinner eggshell. On the basis of this tradeoff, I propose that oviparous taxa with relatively thin eggshells may be preadapted to evolve viviparity. Comparative examination of the limited data available on eggshell thickness in lizards supports this possibility. © 1996 Wiley-Liss, Inc.     

The oldest known amniotic embryos suggest viviparity in mesosaurs

The earliest undisputed crown-group amniotes date back to the Late Carboniferous, but the fossil record of amniotic eggs and embryos is very sparse, with the oldest described examples being from the Triassic. Here, we report exceptional, well-preserved amniotic mesosaur embryos from the Early Permian of Uruguay and Brazil. These embryos provide the earliest direct evidence of reproductive biology in Paleozoic amniotes. The absence of a recognisable eggshell and the occurrence of a partially articulated, but well-preserved embryo within an adult individual suggest that mesosaurs were viviparous or that they laid eggs in advanced stages of development. Our finds represent the only known documentation of amniotic embryos in the Paleozoic and the earliest known case of viviparity, thus extending the record of these reproductive strategies by 90 and 60 Ma, respectively.     

Ichthyosauria: their diversity, distribution, and phylogeny

The Ichthyosauria is the group of Mesozoic marine reptiles that was most highly adapted to the aquatic environment. The first ichthyosaurs from the upper Lower Triassic (Spathian) already show a suite of unique characters (very large eyes, elongate snout, deeply amphicoelous vertebrae, limb modified to fins) correlated with a fully aquatic existence and probably were unable to leave the water. The key evolutionary innovation was vivipary, giving birth to live young, which is documented by the fossil record since the end of the Anisian. Major evolutionary trends in the locomotor apparatus are the increasing modification of the fin skeleton to a mosaic of bones and the change from anguiliform swimming in the earliest forms to thunniform swimming in the Jurassic and later forms, as evidenced by the shortening of the body and the evolution of a semilunate tail fin. Almost from the beginning, ichthyosaurs had a cosmopolitan distribution which was retained until their extinction in the Cenomanian. Ichthyosaurian diversity is greatest in the Middle Triassic with piscivorous, heterodont, and durophagous forms. Jurassic diversity is greatest in the Liassic, declining to one genus (Platypterygius) in the Cretaceous. Although skull characters indicate that ichthyosaurs were diapsids, their exact position within Diapsida is unclear. A cladistic analysis of the well known genera clarifies relationships within the Ichthyosauria. Most basal areGrippia andUtatsusaurus, followed by the Mixosauridae (Mixosaurus andPhalarodon). The Shastasauridae (Cymbospondylus, Shonisaurus, Besanosaurus) are the most advanced Triassic forms and represent the sistergroup of all post-Triassic ichthyosaurs. These are clearly monophyletic and are termed here the Neoichthyosauria.     

Maternal body-volume as a constraint on reproductive output in lizards: evidence from the evolution of viviparity

A few species of squamate reptiles contain both oviparous (egg-laying) and viviparous (live-bearing) populations, and thus offer exceptional opportunities to test adaptationist hypotheses on the determinants of reproductive output. We focus on the hypothesis that maternal body-volume constrains reproductive output in squamate reptiles. If females are “full” of eggs, what happens when viviparity evolves within a lineage? Eggs increase in volume and mass during development, primarily due to the uptake of water, so how can they be accommodated within the mother's abdomen? We predict that the resultant increase in relative clutch mass (RCM) will be lessened by (1) a decrease in reproductive output (by reducing the number or size of offspring), and/or (2) an increase in maternal body-volume (via modifications of size or shape of adult females). Our comparisons of conspecific oviparous and viviparous lizards (Lerista bougainvillii) confirm that live-bearers carry heavier clutches (in both absolute and relative terms) and show the predicted shifts in body size and shape of reproductive females. However, offspring size and number were unaffected by the evolution of viviparity, and the shifts in maternal morphology were too small to fully offset the increase in clutch mass. Thus, RCMs increased by 50%, indicating that viviparous females produced clutches which more completely filled the space available in the abdominal cavity. We conclude that maternal body-volume does play a role in determining reproductive output, but that the observed clutch masses may be optimized, rather than maximized, with respect to the abdominal space available.     

A survey of the rock record of reptilian ontogeny

Given the large diversity and long stratigraphical range of fossil reptiles, their development is a fundamental aspect of the evolution of ontogeny in vertebrates. Eggs, juveniles, embryos and growth series document different aspects of fossilized ontogenies. About three-fifths of the more than 850 available publications on these topics concern dinosaurs. Non-invasive imaging techniques have facilitated the study of embryos in ovo. Examination of ontogenetic trajectories is used to establish criteria to identify fossil growth series and solve taxonomic issues. Many morphological innovations in reptilian skeletal structures are associated with growth heterochronic changes, whereas sequence heterochronic changes remain largely unstudied but are a potential avenue of research. Relative age assessments via not only palaeohistology but also comparative anatomy have been used to reconstruct life history patterns in fossil archosaurs. Several fossil marine reptiles evolved viviparity convergently. Extinct adult phenotypes can reveal information on development, as in the discovery of polydactyly in diapsids, the examination of vertebral number evolution, and its relation to somitgenesis and Hox-gene boundaries, and signs of tissue regeneration provided by anatomical peculiarities following caudal autotomy.     

Late Quaternary reptile extinctions: size matters,insularity dominates

Aim A major Late Quaternary vertebrate extinction event affected mostly large‐bodied ‘megafauna’. This is well documented in both mammals and birds, but evidence of a similar trend in reptiles is scant. We assess the relationship between body size and Late Quaternary extinction in reptiles at the global level. Location Global. Methods We compile a body size database for all 82 reptile species that are known to have gone extinct during the last 50,000 years and compare them with the sizes of 10,090 extant reptile species (97% of known extant diversity). We assess the body size distributions in the major reptile groups: crocodiles, lizards, snakes and turtles, while testing and correcting for a size bias in the fossil record. We examine geographical biases in extinction by contrasting mainland and insular reptile assemblages, and testing for biases within regions and then globally by using geographically weighted models. Results Extinct reptiles were larger than extant ones, but there was considerable variation in extinction size biases among groups. Extinct lizards and turtles were large, extinct crocodiles were small and there was no trend in snakes. Lizard lineages vary in the way their extinction is related to size. Extinctions were particularly prevalent on islands, with 73 of the 82 extinct species being island endemics. Four others occurred in Australia. The fossil record is biased towards large‐bodied reptiles, but extinct lizards were larger than extant ones even after we account for this. Main conclusions Body size played a complex role in the extinction of Late Quaternary reptiles. Larger lizard and turtle species were clearly more affected by extinction mechanisms such as over exploitation and invasive species, resulting in a prevalence of large‐bodied species among extinct taxa. Insularity was by far the strongest correlate of recent reptile extinctions, suggesting that size‐biased extinction mechanisms are amplified in insular environments.     

中国三叠纪海生爬行动物化石研究的回顾与进展

中国三叠纪海生爬行动物化石研究始于20世纪50年代,近10年来取得了重要的进展。此类化石在华南分布广泛,已见于多个省区的十余处地点,涉及自下三叠统奥伦尼克阶至上三叠统诺利阶的至少7个层位,并显示出由东向西产出层位逐渐升高的趋势。我国的三叠纪海生爬行动物化石门类齐全,属种丰富,已知类群包括鱼龙类、海龙类、檐齿龙类、始鳍龙类、原龙类、初龙类和湖北鳄类,显示出典型的西特提斯动物群特征,同时也体现了与东太平洋动物群的某些联系,以及一定的地方色彩。这些化石为研究三叠纪海生爬行动物各个类群的起源、演化和绝灭以及海洋环境的变迁提供了新的材料。     

Does reduction of the eggshell occur concurrently with or subsequent to the evolution of viviparity in phrynosomatid lizards?

Viviparity and placentation have evolved many times within squamate reptiles, but the sequence in which the attendant morphological modifications occur remains unclear. In particular, it is unknown whether a reduction of the egg shell occurs concurrently with longer periods of egg retention (i.e. increasingly advanced stages of embryogenesis at oviposition) or whether such thinning occurs after viviparity has evolved. To investigate this question, we evaluated the prediction that shell morphology and permeability vary systematically with the capacity to support embryonic development in utero (as judged by the maximum embryonic stage attainable in utero) in five species of oviparous sccloporine lizards and one lizard species in the sister genus Urosuarus. Despite major differences among species in the capacity to support embryogenesis, shell morphology (structure, thickness) and physiology (permeability to water vapour) did not vary as predicted. These results raise the intriguing possibility that other features associated with simple placentation (e.g. increased oviductal and chorioallantoic vascular density) evolve concurrently with longer periods of egg retention and viviparity and that shell thinning may occur subsequent to the evolution of viviparity, at least in sceloporine lizards.     

Thermoregulation during gravidity in the children's python (Antaresia childreni): a test of the preadaptation hypothesis for maternal thermophily in snakes

Pregnant squamate reptiles (i.e. lizards and snakes) often maintain higher and more stable body temperatures than their nonpregnant conspecifics, and this maternal thermophily enhances developmental rate and can lead to increased offspring quality. However, it is unclear when this behaviour evolved relative to the evolution of viviparity. A preadaptation hypothesis suggests that maternal thermophily was a preadaptation to viviparity. Oviparous squamates are unique among oviparous reptiles for generally retaining their eggs until the embryos achieve one fourth of their development. As a result, maternal thermophily by gravid squamates may provide the same thermoregulatory benefits, at least during early development, that have been associated with viviparity. Thus, the evolution of viviparity in squamates may reflect an expanded duration of a pre-existing maternal thermoregulatory behaviour. Despite its evolutionary relevance, thermoregulation during gravidity in oviparous squamates has not yet been explored in depth. In the present study, we examined whether gravidity was associated with thermoregulatory changes in the oviparous children's python, Antaresia childreni . First, we discovered that, compared to most snakes, A. childreni is at an advanced stage of embryonic development at oviposition. Second, using surgically implanted temperature loggers, we detected a significant influence of reproductive status on thermoregulation. Reproductive females maintained higher and less variable body temperatures than nonreproductive females and this difference was most pronounced during the last 3 weeks of gravidity. Overall, these results highlight the continuum between oviparity and viviparity in squamate reptiles and emphasize the importance of thermal control of early embryonic development independent of reproductive mode.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 499–508.     

Reptilian viviparity: past research, future directions, and appropriate models

Squamate reptiles represent an ideal group for studies of viviparity, because they have evolved this reproductive pattern frequently, relatively recently, and at low taxonomic levels. A phylogenetic approach shows particular promise in helping us interpret anatomical, physiological, and ecological diversity. This review summarizes four major categories of active investigation: (1) reproductive anatomy and physiology; (2) placental structure and function; (3) reproductive endocrinology; and (4) reproductive and physiological ecology. Evolutionary reconstructions suggest that on many occasions viviparity has evolved concomitantly with functional placentation, through reduction of the shell membrane and hormonal modifications that prolong gestation. Studies of placentotrophic clades as well as reproductively bimodal species offer great potential for explaining the evolution of viviparity and placentation. However, live-bearing squamates are reproductively diverse, and appear to have solved physiological problems associated with viviparity by a variety of mechanisms. Consequently, studies on one or a few squamate species appear increasingly unlikely to yield all-inclusive explanations. Future studies and analyses should abandon assumptions of universal physiological mechanisms and a single historical sequence, in favor of the documentation of diversity in phylogenetic and quantitative terms.     

Potential targets for selection during the evolution of viviparity in cold-climate reptiles

Viviparity (live-bearing) has evolved from oviparity (egg-laying) in more than 100 lineages of squamate reptiles (lizards and snakes). This transition generally has occurred in cool climates, where thermal differentials between eggs in the (cool) nest versus the (warm) maternal oviduct influence embryonic development, in ways that may enhance offspring fitness. To identify specific traits potentially under selection, we incubated eggs of a montane scincid lizard at conditions simulating natural nests, maternal body temperatures, and an intermediate stage (2-week uterine retention of eggs prior to laying). Incubation at maternal temperatures throughout incubation affected the hatchling lizard’s activity level and boldness, as well as its developmental rate, morphology, and locomotor ability. A treatment that mimicked the initial stages of the transition toward viviparity had a major effect on some hatchling traits (locomotor speeds), a minor effect on others (tail length, total incubation period) and no effect on yet others (offspring behaviors). More generally, different aspects of the phenotype are sensitive to incubation conditions at different stages of development; thus, the evolution of reptilian viviparity may have been driven by a succession of advantages that accrued at different stages of embryogenesis.     

The Liassic ichthyosaur<Emphasis Type="Italic">Stenopterygius</Emphasis> cf.<Emphasis Type="Italic">quadriscissus</Emphasis> from the lower Toarcian of Dobbertin (northeastern Germany) and some considerations on lower Toarcian marine reptile palaeobiogeography

An incomplete skull of the lower Toarcian ichthyosaurStenopterygius cf.quadriscissus is described from the lower Toarcian of Dobbertin (Mecklenburg, northeastern Germany). It represents both the northeasternmost occurrence of this ichthyosaur genus and the first diagnostic specimen from East Germany. It therefore extends the palaeobiogeographic range ofStenopterygius considerably and demonstrates that this ichthyosaur also inhabited the Germanic Basin east of the Rhenish Massif by Early Jurassic times. A palaeobiogeographical pattern is evident within the genusStenopterygius, with the ubiquitous speciesS. longifrons andS. hauffianus on one hand, andS. megalorhinus andS. quadriscissus on the other hand, which appear not to have ranged northwest of the London-Brabant Massif. It is suggested that, whereas the Rhenish Massif was not an effective barrier for dispersal of ichthyosaurs in Western Europe during early Toarcian times, the London-Brabant Massif played a rather significant role, as is also shown by the fossil record of other marine reptile groups. A provincialism of early Toarcian marine reptiles is suggested for Western Europe, with a northwestern province which contains the British occurrences, an intermediate, Subgermanic province in France and the Benelux countries, and a southeastern province in the Germanic Basin. The British and Germanic provinces are each characterized by a typical assemblage of ichthyosaurs, plesiosaurs, and marine crocodiles, wheres the intermediate Subgermanic region shows an intermingling of faunal elements.