Reproduction and larval morphology of broadcasting and viviparous species in the Cryptasterina species complex

The Cryptasterina group of asterinid sea stars in Australasia comprises cryptic species with derived life histories. C. pentagona and C. hystera have planktonic and intragonadal larvae, respectively. C. pentagona has the gonochoric, free-spawning mode of reproduction with a planktonic lecithotrophic brachiolaria larva. C. hystera is hermaphroditic with an intragonadal lecithotrophic brachiolaria, and the juveniles emerge through the gonopore. Both species have large lipid-rich buoyant eggs and well-developed brachiolariae. Early juveniles are sustained by maternal nutrients for several weeks while the digestive tract develops. C. hystera was reared in vitro through metamorphosis. Its brachiolariae exhibited the benthic exploration and settlement behavior typical of planktonic larvae, and they attached to the substratum with their brachiolar complex. These behaviors are unlikely to be used in the intragonadal environment. The presence of a buoyant egg and functional brachiolaria larva would not be expected in an intragonadal brooder and indicate the potential for life-history reversal to a planktonic existence. Life-history traits of species in the Cryptasterina group are compared with those of other asterinids in the genus Patiriella with viviparous development. Modifications of life-history traits and pathways associated with evolution of viviparity in the Asterinidae are assessed, and the presence of convergent adaptations and clade-specific features associated with this unusual mode of parental care are examined.     

Ovoviviparity and viviparity in the Diptera

The taxonomic distribution and evolution of viviparity in Diptera is critically reviewed. The phenomenon ranges from ovoviviparity (eggs deposited at an advanced stage of embryonic development; larva emerges immediately after deposition), through viviparity (larva hatches inside female before deposition) to pupiparity (offspring deposited as pupa). Some Diptera are known to be facultatively viviparous, which is hypothesized to be a step towards the evolution of obligate viviparity. Obligate viviparity is found to comprise unilarviparity (single large larva in maternal uterus) which evolved many times independently, the rare oligolarviparity (more than one but not more than 12 larvae) and multilarviparity (large numbers of developing eggs or larvae in uterus) which is typical for the two largest clades of viviparous Diptera. Unilarviparity is either lecithotrophic (developing larva nourished by yolk of egg) or pseudo-placental (larva nourished by glandular secretions of mother). Viviparity has clearly evolved on many separate occasions in Diptera. It is recorded in 22 families, and this review identifies at least 61 independent origins of viviparity. Six families appear to have viviparity in their ground-plan. Some families have a single evolution of viviparity, others multiple evolutions. Guimaraes' model for the evolution of viviparity in Diptera is tested against phylogenetic information and the adaptive significance of viviparity is reviewed in detail. Possible correlations with life-history parameters (coprophily, parasitism, breeding in ephemeral plant parts, malacophagy and adult feeding habits – especially haematophagy) are analysed critically, as are potential advantages (shorter larval life, less investment in yolk by mother, protection of vulnerable stages, better access to breeding substrates, predation on competitors). Morphological constraints, adaptations and exaptations are reviewed, including the provision of an incubation space for the egg(s), the positioning of the egg(s) in the uterus, and maternal glands. The main morphological adaptations include greater egg size, reduction of egg respiratory filaments, thinning of chorion, modified larval respiratory system and mouthparts, and instar skipping. Female morphology and behaviour is particularly strongly modified for viviparity. The terminalia are shortened, the vagina is more muscular and tracheated, and the ovaries of unilarviparous species have a reduced number of ovarioles with alternate ovulation. Many of the final conclusions are tentative, and a plea is made for more detailed morphological and experimental study of many of the viviparous species. Viviparity in Diptera provides a fascinating example of multiple parallel evolution, and a fertile field for future research.     

THE EVOLUTION OF OVIPARITY WITH EGG GUARDING AND VIVIPARITY IN LIZARDS AND SNAKES: A PHYLOGENETIC ANALYSIS

This paper investigates the evolution of viviparity and of egg guarding in lizards and snakes in which three modes of reproduction can be described: oviparity without egg guarding, oviparity with egg guarding, and viviparity. All possible transitions of reproductive modes were detected in each taxon using Maddison's method. We then tested two specific hypotheses. First, egg guarding can be regarded as an alternative to viviparity. A relatively frequent association of egg guarding and viviparous species in the same taxon may be due to similar environmental conditions or species characteristics leading to two different solutions. Second, egg guarding may facilitate the evolution of viviparity. This hypothesis is supported by the high frequency of viviparous species in taxa containing egg guarding species and by a tendency for prolonged uterine retention of eggs in brooding squamates. Our analyses demonstrate that the first hypothesis is the best supported. Egg guarding and viviparity most often evolved independently. If a major benefit of egg guarding is the repulsion of potential predators, size is one of the most obvious morphological characters that should be correlated with the evolution of reproductive modes. The two reproductive traits were correlated to a reduction in body size for viviparous species and an increase in body size for egg guarding species. This could partly explain why the evolution of these reproductive modes seems almost antagonist.     

Reproduction and sexual development in a freshwater gastrotrich

Summary Post-embryonic development of parthenogenic eggs of Lepidodermella squammata was studied by light and electron microscopy in animals of known age and reproductive history. Each bilateral gonad initially contains eight cells. No mitotic proliferation occurs during parthenogenic egg development. Germ cells are tightly clustered, have smooth plasma membranes with no interconnections, and are uninucleate. There is no surrounding ovary or oviduct. At hatching, two cells in each gonad are identifiable as parthenogenic eggs. The enlarged nucleolus of the most mature egg has already attained the morphology that persists throughout vitellogenesis, with intertwined granular and fibrillar threads. Less mature eggs have earlier stages of nucleolar development, and lack indications of meiotic events. Parthenogenic eggs enter vitellogenesis singly, with formation of RER and active Golgi complexes, and the accumulation of lipid, yolk, and various granules. The shell is formed in situ, whereas the spines elongate after egg deposition. Most animals produce four parthenogenic eggs, which undergo immediate development (tachyblastic eggs). Resting (opsiblastic) eggs are rare in isolation culture. Both types of eggs are produced only prior to the formation of sperm and primary oocytes. The absence of synaptonemal complexes, which would indicate synapsis of homologous chromosomes in prophase of meiosis I, implies that parthenogenesis is by apomixis in L. squammata.     

Lipid dynamics in the embryos of Patiriella species (Asteroidea) with divergent modes of development

Evolution of lecithotrophic development in sea stars involved a modification in maternal provisioning from the production of yolk-dominated to lipid-dominated eggs. The dynamics of lipid reserves in the embryos of four Patiriella species differing in their lipid provisions were examined. Patiriella regularis had small yolk protein-dominated eggs (150 microm in diameter) and an ancestral mode of development through planktotrophic larvae. Patiriella calcar, Patiriella exigua and Patiriella pseudoexigua had large eggs (390-440 microm in diameter) and lecithotrophic planktonic, benthic and intragonadal larvae, respectively. Patiriella exigua deposited negatively buoyant eggs containing substantial yolk protein and lipid reserves onto the substratum. In contrast, the planktonic eggs of P. calcar and the intragonadal eggs of P. pseudoexigua were dominated by lipid and were neutrally and positively buoyant, respectively. By the blastula stage there was little trace of lipid in P. regularis embryos. Blastulae of the lecithotrophic developers, by contrast, had conspicuous lipid droplets distributed through their cells. In parallel with the change from cuboidal to columnar epithelium during the blastula to gastrula transition, lipid reserves became redistributed into the basal cytoplasm. The extent of lipid transport reflected the amount of lipid reserves. In P. pseudoexigua embryos with the greatest lipid load, basal shunting was followed by secretion of lipid into the blastocoele where it was stored for the perimetamorphic period. Evolution of lecithotrophy in Patiriella appears to reflect selection to provide metamorphic stages with nutrients normally accrued by feeding larvae with the consequence that early development is burdened by voluminous, potentially inert nutritive stores. Lipid redistribution coincident with a major developmental stage transition may be required to facilitate unimpeded morphogenesis. This phenomenon may be characteristic of lecithotrophic development in echinoderms and appears pre-adaptive for extrusion of lipid in species like P. pseudoexigua with particularly extensive lipid reserves.     

Placental calcium provision in a lizard with prolonged oviductal egg retention

A prominent scenario for the evolution of viviparity and placentation in reptiles predicts a step-wise pattern with an initial phase of prolonged oviductal egg retention accompanied by progressive reduction in eggshell thickness culminating in viviparity; calcium placentotrophy evolves secondarily to viviparity. Saiphos equalis is an Australian scincid lizard with a reproductive mode that is uncommon for squamates because eggs are retained in the oviduct until late developmental stages, and the embryonic stage at oviposition varies geographically. We studied calcium mobilization by embryos in two populations with different oviductal egg retention patterns to test the hypothesis that the pattern of nutritional provision of calcium is independent of the embryonic stage at oviposition. Females from one population are viviparous and oviposit eggs containing fully formed embryos, whereas embryos in oviposited eggs of the second population are morphologically less mature, and these eggs hatch several days later. The reproductive mode of this population is denoted as prolonged oviductal egg retention. Yolk provided the highest proportion of calcium to hatchlings in both populations. Eggs of both populations were enclosed in calcified eggshells, but shells of the population with prolonged egg retention had twice the calcium content of the viviparous population and embryos recovered calcium from these eggshells. Placental transfer accounted for a substantial amount of calcium in hatchlings in both populations. Hatchling calcium concentration was higher in the population with prolonged egg retention because these embryos mobilized calcium from yolk, the eggshell and the placenta. This pattern of embryonic calcium provision in which both a calcified eggshell and placentotrophy contribute to embryonic nutrition is novel. The reproductive pattern of S. equalis illustrates that calcified eggshells are compatible with prolonged oviductal egg retention and that viviparity is not requisite to calcium placentotrophy.     

A review of the evolution of viviparity in lizards: structure,function and physiology of the placenta

The aim of this review is to collate data relevant to understanding the evolution of viviparity in general, and complex placentae in particular. The wide range of reproductive modes exhibited by lizards provides a solid model system for investigating the evolution of viviparity. Within the lizards are oviparous species, viviparous species that have a very simple placenta and little nutrient uptake from the mother during pregnancy (lecithotrophic viviparity), through a range of species that have intermediate placental complexities and placental nutrient provision, to species that lay microlecithal eggs and most nutrients are provided across the placenta during development (obligate placentotrophy). In its commonest form, lecithotrophic viviparity, some uptake of water, inorganic ions and oxygen occurs from the mother to the embryo during pregnancy. In contrast, the evolution of complex placentae is rare, but has evolved at least five times. Where there is still predominantly a reliance on egg yolk, the omphaloplacenta seems to be paramount in the provision of nutrition to the embryo via histotrophy, whereas the chorioallantoic placenta is more likely involved in gas exchange. Reliance on provision of substantial organic nutrient is correlated with the regional specialisation of the chorioallantoic placenta to form a placentome for nutrient uptake, particularly lipids, and the further development of the gas exchange capabilities of the other parts of the chorioallantois.     

Evolution of viviparity: variation between two sceloporine lizards in the ability to extend egg retention

The evolutionary transition between oviparity and viviparity in squamate reptiles presumably occurs via a gradual increase in the duration of egg retention, the production of thinner eggshells, and increases in the vascularity of maternal and embryonic tissues. The 'ease' of this transition may differ among taxa. For example, in the genus Sceloporus , the scalaris species group contains both oviparous and viviparous species, and female Sceloporus scalaris can extend egg retention facultatively in response to the absence of a suitable site for oviposition without impairing embryonic development. In contrast, the undulatus species group contains only oviparous species, and, while female Sceloporus virgatus can extend egg retention, doing so retards embryonic development. I tested several hypotheses that would explain the greater ability of 5. scalaris than S. virgatus to extend egg retention. In this study, female S. scalaris retained eggs for 19 d without affecting the mortality of embryos, total developmental time, or dry mass of hatchlings. In contrast, when female S. virgatus retained eggs for 18 d, embryos had very high mortality and eggs took significantly longer to hatch than control (non-retained) eggs, although the dry mass of hatchlings was not affected. The ability of S. scalaris females to retain eggs with little negative effect on embryonic development was associated with relatively large chorioallantois, relatively thin eggshells, and relatively small clutch masses. These observations suggest that phylogenetic differences in the ability to extend egg retention may facilitate or constrain the evolution of viviparity in some lineages.     

Lipids of the eggs and neonates of oviparous and viviparous lizards

The purpose of this article is to collate the compositional data for the lipids of the eggs and neonates of ten species of lizards displaying a range of parity modes, to highlight emergent trends and to identify some of the physiological changes central to the evolution of viviparity. The eggs of oviparous species and of viviparous species with a simple (type I) placenta are characterised by very high proportions of triacylglycerol which forms over 80% (wt. /wt.) of the total yolk lipid. The eggs of viviparous species with complex (types II and III) placentae contain lower proportions of triacylglycerol (about 70% of total yolk lipid) and commensurately greater proportions of phospholipid, cholesteryl ester and free cholesterol. The fatty acid compositions of the yolk lipids are very similar for all the lizard species, irrespective of parity mode; in particular, the proportions of docosahexaenoic acid are consistently low. For all the species, the proportions of both docosahexaenoic and arachidonic acids are higher in the phospholipid of the neonate compared with the egg. The difference between the lipid contents of the eggs and the neonates indicates that, in species of Pseudemoia which have a complex (type III) placenta, more than 50% of the total lipid supplied to the embryo is derived from placental transport.     

Thermal and reproductive biology of high and low elevation populations of the lizard Sceloporus scalaris: implications for the evolution of viviparity

Viviparity in squamate reptiles is presumed to evolve in cold climates by selection for increasingly longer periods of egg retention. Longer periods of egg retention may require modifications to other reproductive features associated with the evolution of viviparity, including a reduction in eggshell thickness and clutch size. Field studies on the thermal and reproductive biology of high (HE) and low (LE) elevation populations of the oviparous lizard, Sceloporus scalaris, support these expectations. Both day and night-time temperatures at the HE site were considerably cooler than at the LE site, and the activity period was 2 h shorter at the HE than at the LE site. The median body temperature of active HE females was 2°C lower than that of LE females. HE females initiated reproduction earlier in the spring than LE females, apparently in order to compensate for relatively low temperatures during gestation. HE females retained eggs for about 20 days longer than LE females, which was reflected by differences in the degree of embryonic development at the time of oviposition (stages 35.5–37.0 versus stages 31.0–33.5, respectively). These results support the hypotheses that evolution of viviparity is a gradual process, and is favored in cold climates. Females in the HE population exhibited other traits consistent with presumed intermediate stages in the evolution of viviparity; mean eggshell thickness of HE eggs (19.3 m) was significantly thinner than that of LE eggs (26.6 m) and the size-adjusted clutch sizes of HE females (9.4) were smaller than those of LE females (11.2).     

Gold climates and the evolution of viviparity in reptiles: cold incubation temperatures produce poor-quality offspring in the lizard, Sceloporus virgatus

Evolutionary origins of viviparity among the squamate reptiles are strongly associated with cold climates, and cold environmental temperatures are thought to be an important selective force behind the transition from egg-laying to live-bearing. In particular, the low nest temperatures associated with cold climate habitats are thought to be detrimental to the developing embryos or hatchlings of oviparous squamates, providing a selective advantage for the retention of developing eggs in utero, where the mother can provide warmer incubation temperatures for her eggs (by actively thermoregulating) than they would experience in a nest. However, it is not entirely clear what detrimental effects cold incubation temperatures may have on eggs and hatchlings, and what role these effects may play in favouring the evolution of viviparity. Previous workers have suggested that viviparity may be favoured in cold climates because cold incubation temperatures slow cmbryogenesis and delay hatching of the eggs, or because cold nest temperatures are lethal to developing eggs and reduce hatching success. However, incubation temperature has also been shown to have other, potentially long-term, effects on hatchling phcnotypcs, suggesting that cold climates may favour viviparity because cold incubation temperatures produce offspring of poor quality or low fitness. We experimentally incubated eggs of the oviparous phrynosomatid lizard, Sceloporus virgatus, at temperatures simulating nests in a warm (low elevation) habitat, as is typical for this species, and nests in a colder (high elevation) habitat, to determine the effects of cold incubation temperatures on embryonic development and hatchling phenotypes. Incubation at cold nest temperatures slowed embryonic development and reduced hatching success, but also affected many aspects of the hatchlings' phenotypes. Overall, the directions of these plastic responses indicated that cold-incubated hatchlings did indeed exhibit poorer quality phenotypes; they were smaller at hatching (in body length) and at 20 days of age (in length and mass), grew more slowly (in length and mass), had lower survival rates, and showed greater fluctuating asymmetry than their conspecifics that were incubated at warmer temperatures. Our findings suggest that cold nest temperatures are detrimental to S. virgatus, by delaying hatching of their eggs, reducing their hatching success, and by producing poorer quality offspring. These negative effects would likely provide a selective advantage for any mechanism through which these lizards could maintain warmer incubation temperatures in cold climates, including the evolution of prolonged egg retention and viviparity.     

Altitudinal variation in egg retention and rates of embryonic development in oviparous Zootoca vivipara fits predictions from the cold-climate model on the evolution of viviparity

The evolution of reptilian viviparity is favoured, according to the cold‐climate hypothesis, at high latitudes or altitudes, where egg retention would entail thermal benefits for embryogenesis because of maternal thermoregulation. According to this hypothesis, and considering that viviparity would have evolved through a gradual increase in the extent of intrauterine egg retention, highland oviparous populations are expected to exhibit more advanced embryo development at oviposition than lowland populations. We tested for possible differences in the level of egg retention, embryo development time and thermal biology of oviparous Zootoca vivipara near the extreme altitudinal limits of the species distribution in the north of Spain (mean altitude for lowland populations, 235 m asl.; for highland populations, 1895 m asl.). Altitude influenced neither temperature of active lizards in the field nor temperature selected by lizards in a laboratory thermal gradient, and pregnant females selected lower temperatures in the thermal gradient than did males and nonpregnant females across altitudinal levels. Eggs from highland populations contained embryos more developed at the time of oviposition (Dufaure and Hubert's stages 33–35) than eggs of highland populations (stages 30–34) and partly because of this difference incubation time was shorter for highland embryos. When analysed for clutches from both altitudinal extremes at the same embryonic stage at oviposition (stage 33), again incubation time was shorter for highland populations, indicating genuine countergradient variation in developmental rate. Our results indicate that temperature is an environmental factor affecting the geographical distribution of different levels of egg retention in Z. vivipara, as predicted by the cold‐climate hypothesis on the evolution of viviparity.     

Multiple origin of viviparity in Southeast Asian gastropods (Cerithioidea: Pachychilidae) and its evolutionary implications

This study aims at a better understanding of the evolutionary significance of viviparity in some freshwater gastropods. We use a phylogeny based on partial sequences of the mitochondrial 16S gene of representatives of the limnetic and pantropical Pachychilidae to infer the relationships within this particular group of cerithioideans and the evolution of reproductive strategies. The phylogeny presented herein implies a new systematization and suggests that viviparity has appeared three times among the Pachychilidae. This is supported by the finding of very distinct reproductive morphologies in different lineages of viviparous taxa that are exclusively found in Southeast Asia. Based on the observation that oviparity is the ancestral character state in this freshwater family, we conclude that viviparity has evolved subsequent to the exploration of freshwater. We present data showing that all Pachychilidae produce considerably larger but fewer egg capsules compared to most marine snails. In other studies on freshwater gastropods, this has been discussed as an adaptation to freshwater environments. In this context we hypothesize that the increased parental investment involved in the enlargement of eggs in concert with the reduction of clutch sizes was the driving factor that ultimately lead to the evolution of viviparity in the Asian taxa. Consequently, although not directly correlated with the colonization of the new adaptive zone, viviparity is strongly favored by other consequences of this step. Hence, we hypothesize that the production of large eggs, which is necessitated by the exploration of freshwater, represents a preadaptation existing in those ancestors from which viviparous pachychilid lineages eventually evolved in Southeast Asia.     

Maternal provisioning in Ophionereis fasciata and O. schayeri: brittle stars with contrasting modes of development

Evolutionary change from planktotrophic to lecithotrophic development in echinoderms is closely tied to an increase in maternal provisioning. We provide the first data on the major energetic constituents in the eggs of two ophiuroids, the planktotroph Ophionereis fasciata (egg diameter 103 microm) and the lecithotroph O. schayeri (egg diameter 248 microm), to document changes in maternal investment associated with the switch to lecithotrophy in O. schayeri. Lipid classes in the eggs of the two species did not differ except for the presence of small amounts of wax esters in the eggs of O. schayeri. Production of a large egg in O. schayeri is mostly due to enhanced deposition of one energy-storage lipid, triglyceride. The eggs of O. schayeri are not simply scaled-up versions of the ancestral-type eggs of O. fasciata. The relationship between lipid and protein content and egg volume conformed to the relationship previously established for echinoderm eggs. Surprisingly, total lipid and protein data for the eggs of O. schayeri grouped with data for the eggs of planktotrophic echinoderms. The eggs of O. schayeri are small compared with those of other echinoderms with lecithotrophic development, and their energetic contents may approach the minimum provisions necessary to permit development without feeding.     

Copulation and egg retention in an oviparous Caecilian (Amphibia: Gymnophiona)

Viviparity (i.e., the bearing of live young) has evolved from oviparity (egg laying) independently in various major vertebrate lineages, and several transitional stages have been described. The transition from oviparity to viviparity requires the retention of fertilised eggs in the female reproductive tract. Caecilian amphibians (Gymnophiona) display a considerable diversity of reproductive modes, including oviparity and viviparity. Among amphibians, caecilians have also modified the process of internal fertilisation through a special intromittent organ, or phallus, in males. Here we report the oviposition of “embryonated” eggs ranging from various gastrula-to-neurula stages by female Ichthyophis cf. kohtaoensis (Ichthyophiidae) from North-eastern Thailand. In addition, we describe a copulation resulting in an oviposition of embryonated eggs. Our findings will have implications for the further understanding of the evolutionary reproductive biology of amphibians.     

Embryonic gonadal and sexual organ development in a small viviparous skink, Niveoscincus ocellatus

The majority of research into the timing of gonad differentiation (and sex determination) in reptiles has focused on oviparous species. This is largely because: (1) most reptiles are oviparous; (2) it is easier to manipulate embryonic developmental conditions (e.g., temperature) of eggs than oviductal embryos and (3) modes of sex determination in oviparous taxa were thought to be more diverse since viviparity and environmental sex determination (ESD)/temperature-dependent sex determination (TSD) were considered incompatible. However, recent evidence suggests the two may well be compatible biological attributes, opening potential new lines of enquiry into the evolution and maintenance of sex determination. Unfortunately, the baseline information on embryonic development in viviparous species is lacking and information on gonad differentiation and sexual organ development is almost non-existent. Here we present an embryonic morphological development table (10 stages), the sequence of gonad differentiation and sexual organ development for the viviparous spotted snow skink (Niveoscincus ocellatus). Gonad differentiation in this species is similar to other reptilian species. Initially, the gonads are indifferent and both male and female accessory ducts are present. During stage 2, in the middle third of development, differentiation begins as the inner medulla regresses and the cortex thickens signaling ovary development, while the opposite occurs in testis formation. At this point, the Müllerian (female reproductive) duct regresses in males until it is lost (stage 6), while females retain both ducts until after birth. In the later stages of testis development, interstitial tissue forms in the medulla corresponding to maximum development of the hemipenes in males and the corresponding regression in the females.     

Fetal nutrition in lecithotrophic squamate reptiles: Toward a comprehensive model for evolution of viviparity and placentation

The primary pattern of embryonic nutrition for squamate reptiles is lecithotrophy; with few exceptions, all squamate embryos mobilize nutrients from yolk. The evolution of viviparity presents an opportunity for an additional source of embryonic nutrition through delivery of uterine secretions, or placentotrophy. This pattern of embryonic nutrition is thought to evolve through placental supplementation of lecithotrophy, followed by increasing dependence on placentotrophy. This review analyzes the relationship between reproductive mode and pattern of embryonic nutrition in three lecithotrophic viviparous species, and oviparous counterparts, for concordance with a current model for the evolution of viviparity and placentation. The assumptions of the model, that nutrients for oviparous embryos are mobilized from yolk, and that this source is not disrupted in the transition to viviparity, are supported for most nutrients. In contrast, calcium, an essential nutrient for embryonic development, is mobilized from both yolk and eggshell by oviparous embryos and reduction of eggshell calcium is correlated with viviparity. If embryonic fitness is compromised by disruption of a primary source of calcium, selection may not favor evolution of viviparity, yet viviparity has arisen independently in numerous squamate lineages. Studies of fetal nutrition in reproductively bimodal species suggest a resolution to this paradox. If uterine calcium secretion occurs during prolonged intrauterine egg retention, calcium placentotrophy evolves prior to viviparity as a replacement for eggshell calcium and embryonic nutrition will not be compromised. This hypothesis is integrated into the current model for evolution of viviparity and placentation to address the unique attributes of calcium nutrition. The sequence of events requires a shift in timing of uterine calcium secretion and the embryonic mechanism of calcium retrieval to be responsive to calcium availability. Regulation of uterine calcium secretion and the mechanism of embryonic uptake of calcium are important elements to understanding evolution of viviparity and placentation. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

Oogenesis in the viviparous matrotrophic lizard Mabuya brachypoda

Oogenesis in the lizard Mabuya brachypoda is seasonal, with oogenesis initiated during May-June and ovulation occurring during July-August. This species ovulates an egg that is microlecithal, having very small yolk stores. The preovulatory oocyte attains a maximum diameter of 0.9-1.3 mm. Two elongated germinal beds, formed by germinal epithelia containing oogonia, early oocytes, and somatic cells, are found on the dorsal surface of each ovary. Although microlecithal eggs are ovulated in this species, oogenesis is characterized by both previtellogenic and vitellogenic stages. During early previtellogenesis, the nucleus of the oocyte contains lampbrush chromosomes, whereas the ooplasm stains lightly with a perinuclear yolk nucleus. During late previtellogenesis the ooplasm displays basophilic staining with fine granular material composed of irregularly distributed bundles of thin fibers. A well-defined zona pellucida is also observed. The granulosa, initially composed of a single layer of squamous cells during early previtellogenesis, becomes multilayered and polymorphic. As with other squamate reptiles, the granulosa at this stage is formed by three cell types: small, intermediate, and large or pyriform cells. As vitellogenesis progresses the oocyte displays abundant vacuoles and small, but scarce, yolk platelets at the periphery of the oocyte. The zona pellucida attains its maximum thickness during late oogenesis, a period when the granulosa is again reduced to a single layer of squamous cells. The vitellogenic process observed in M. brachypoda corresponds with the earliest vitellogenic stages seen in other viviparous lizard species with larger oocytes. The various species of the genus Mabuya provided us with important models to understand a major transition in the evolution of viviparity, the development of a microlecithal egg.     

Reproduction and development ofSebastes in the context of the evolution of piscine viviparity

Synopsis Selected aspects of the reproduction and development ofSebastes and other rockfishes are reviewed in the context of piscine viviparity. Among the eight subfamilies of the Scorpaenidae, viviparity is confined to the subfamily Sebastinae; gestation is lumenal and the embryos usually develop to term within the egg envelope. Transitional states from oviparity to viviparity are evident in different species within the family. A scenario for the evolutionary origin of viviparity in rockfishes is derived from an analysis of scorpaeniform reproductive biology. Although viviparity is best developed in the genusSebastes, it is still in a primitive, unspecialized state. Rockfish viviparity is essentially lecithotrophic, i.e. embryonic nutrition is dependent on the energy reserves laid down during oogenesis. In other groups of viviparous fishes, lecithotrophy has been shown to be better suited energetically to seasonally unpredictable habitats, whereas matrotrophy requires a predictable food supply. During the evolution of an essentially primitive form of lecithotrophic viviparity in rockfishes, the advantages of high fecundity associated with oviparity were retained while an enormous increase in the survival rate of the developing embryos was acquired. The basic lecithotrophic pattern of oviparous development was not changed since it offered selective advantages both in terms of energetics and as a basis for retaining a large brood size.