Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis

Phylogenetic analyses indicate that viviparity (live‐bearing reproduction) has originated independently in more than 150 vertebrate lineages, including a minimum of 115 clades of extant squamate reptiles. Other evolutionary origins of viviparity include 13 origins among bony fishes, nine among chondrichthyans, eight in amphibians, one in Paleozoic placoderms, six among extinct reptiles, and one in mammals. The origins of viviparity range geologically from the mid‐Paleozoic through the Mesozoic to the Pleistocene. Substantial matrotrophy (maternal provision of nutrients to embryos during pregnancy) has arisen at least 33 times in these viviparous clades, with most (26) of these origins having occurred among fishes and amphibians. Convergent evolution in patterns of matrotrophy is widespread, as reflected by multiple independent origins of placentotrophy, histotrophy, oophagy, and embryophagy. Specializations for nutrient transfer to embryos are discontinuously distributed, reflecting the roles of phylogenetic inertia, exaptation (preadaptation), and constraint. Ancestral features that function in gas exchange and nutrition repeatedly and convergently have been co‐opted for nutrient transfer, often through minor modification of their components and changes in the timing of their expression (heterochrony). Studies on functional and evolutionary morphology continue to play a central role in our attempts to understand viviparity and mechanisms of fetal nutrition. J. Morphol. 276:961–990, 2015. © 2014 Wiley Periodicals, Inc.     

Sexual reproduction of the placental brooder Celleporella hyalina (Bryozoa,Cheilostomata) in the White Sea

The evolution of parental care is a central field in many ecological and evolutionary studies, but integral approaches encompassing various life-history traits are not common. Else, the structure, development and functioning of the placental analogues in invertebrates are poorly understood. Here, we describe the life-history, sexual colony dynamics, oogenesis, fertilization and brooding in the boreal-Arctic cheilostome bryozoan Celleporella hyalina. This placental brooder incubates its progeny in calcified protective chambers (ovicells) formed by polymorphic sexual zooids. We conducted a detailed ultrastructural study of the ovary and oogenesis, and provide evidence of both auto- and heterosynthetic mechanisms of vitellogenesis. We detected sperm inside the early oocyte and within funicular strands, and discuss possible variants of fertilization. We also detail the development and functioning of the placental analogue (embryophore) in the various stages of embryonic incubation as well as embryonic histotrophic nourishment. In contrast to all known cheilostome placentas, the main part of embryophore of C. hyalina is not a single cell layer. Rather, it is a massive “nutritive tissue” whose basal part is associated with funicular strands presumably providing transport function. C. hyalina shows a mixture of reproductive traits with macrolecithal oogenesis and well-developed placenta. These features give it an intermediate position in the continuum of variation of matrotrophic provisioning between lecithotrophic and placentotrophic cheilostome brooders. The structural and developmental differences revealed in the placental analogue of C. hyalina, together with its position on the bryozoan molecular tree, point to the independent origin of placentation in the family Hippothoidae.     

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.     

Matrotrophy and placentation in invertebrates: a new paradigm

Matrotrophy, the continuous extra‐vitelline supply of nutrients from the parent to the progeny during gestation, is one of the masterpieces of nature, contributing to offspring fitness and often correlated with evolutionary diversification. The most elaborate form of matrotrophy—placentotrophy—is well known for its broad occurrence among vertebrates, but the comparative distribution and structural diversity of matrotrophic expression among invertebrates is wanting. In the first comprehensive analysis of matrotrophy across the animal kingdom, we report that regardless of the degree of expression, it is established or inferred in at least 21 of 34 animal phyla, significantly exceeding previous accounts and changing the old paradigm that these phenomena are infrequent among invertebrates. In 10 phyla, matrotrophy is represented by only one or a few species, whereas in 11 it is either not uncommon or widespread and even pervasive. Among invertebrate phyla, Platyhelminthes, Arthropoda and Bryozoa dominate, with 162, 83 and 53 partly or wholly matrotrophic families, respectively. In comparison, Chordata has more than 220 families that include or consist entirely of matrotrophic species. We analysed the distribution of reproductive patterns among and within invertebrate phyla using recently published molecular phylogenies: matrotrophy has seemingly evolved at least 140 times in all major superclades: Parazoa and Eumetazoa, Radiata and Bilateria, Protostomia and Deuterostomia, Lophotrochozoa and Ecdysozoa. In Cycliophora and some Digenea, it may have evolved twice in the same life cycle. The provisioning of developing young is associated with almost all known types of incubation chambers, with matrotrophic viviparity more widespread (20 phyla) than brooding (10 phyla). In nine phyla, both matrotrophic incubation types are present. Matrotrophy is expressed in five nutritive modes, of which histotrophy and placentotrophy are most prevalent. Oophagy, embryophagy and histophagy are rarer, plausibly evolving through heterochronous development of the embryonic mouthparts and digestive system. During gestation, matrotrophic modes can shift, intergrade, and be performed simultaneously. Invertebrate matrotrophic adaptations are less complex structurally than in chordates, but they are more diverse, being formed either by a parent, embryo, or both. In a broad and still preliminary sense, there are indications of trends or grades of evolutionarily increasing complexity of nutritive structures: formation of (i) local zones of enhanced nutritional transport (placental analogues), including specialized parent–offspring cell complexes and various appendages increasing the entire secreting and absorbing surfaces as well as the contact surface between embryo and parent, (ii) compartmentalization of the common incubatory space into more compact and ‘isolated’ chambers with presumably more effective nutritional relationships, and (iii) internal secretory (‘milk’) glands. Some placental analogues in onychophorans and arthropods mimic the simplest placental variants in vertebrates, comprising striking examples of convergent evolution acting at all levels—positional, structural and physiological.     

Fetal adaptations for viviparity in amphibians

Live‐bearing has evolved in all three orders of amphibians—frogs, salamanders, and caecilians. Developing young may be either yolk dependent, or maternal nutrients may be supplied after yolk is resorbed, depending on the species. Among frogs, embryos in two distantly related lineages develop in the skin of the maternal parents' backs; they are born either as advanced larvae or fully metamorphosed froglets, depending on the species. In other frogs, and in salamanders and caecilians, viviparity is intraoviductal; one lineage of salamanders includes species that are yolk dependent and born either as larvae or metamorphs, or that practice cannibalism and are born as metamorphs. Live‐bearing caecilians all, so far as is known, exhaust yolk before hatching and mothers provide nutrients during the rest of the relatively long gestation period. The developing young that have maternal nutrition have a number of heterochronic changes, such as precocious development of the feeding apparatus and the gut. Furthermore, several of the fetal adaptations, such as a specialized dentition and a prolonged metamorphosis, are homoplasious and present in members of two or all three of the amphibian orders. At the same time, we know little about the developmental and functional bases for fetal adaptations, and less about the factors that drive their evolution and facilitate their maintenance. J. Morphol. 276:941–960, 2015. © 2014 Wiley Periodicals, Inc.     

Evolutionary origins of viviparity in Chamaeleonidae

Historically, an understanding of viviparity and its evolution in Old World chameleons (Chamaeleonidae) has lagged behind that of other squamate families. Not only is reproductive information scarce or entirely absent for most chameleon species, but the literature reveals no consensus as to the frequency and ecological circumstances under which chameleon viviparity evolved. We integrated information on reproductive modes for nearly all chameleon species with recently published family-scale phylogenetic and ecological analyses to clarify aspects of reproductive evolution in chameleons. Ancestral-trait reconstructions, after accounting for phylogenetic uncertainty, indicated that viviparity has arisen a minimum of three times in Chamaeleonidae, with each origin of live birth in closed-canopy forests. Our maximum-likelihood optimization therefore did not support the previous hypotheses of one, two or four origins of viviparity in the family. Past claims that arboreality would not allow for evolution of viviparity were also not supported, nor was a recent suggestion that viviparity has reverted to oviparity. However, cold climates of high latitudes and elevations may have selected for viviparity in arboreal chameleons. While peritoneal pigmentation may facilitate viviparity, its role as an exaptation rather than an adaptation remains equivocal without data from a wider range of chameleon species. Based on a comprehensive review of reproductive modes throughout the family, our study has resolved the number of origins of viviparity in Chamaeleonidae and provided evidence that live birth evolved under arboreal conditions on three separate occasions in this enigmatic squamate group. This study also reveals the value of using phylogenetic analysis in a manner that is robust to uncertainty (rather than simple correlational approaches) when the goal is to reconstruct evolutionary sequences and selective pressures.     

Fossilized ontogenies: the contribution of placoderm ontogeny to our understanding of the evolution of early gnathostomes

Placoderms, representing phylogenetically more inclusive jawed vertebrates and successive sister taxa to crown‐group gnathostomes, are critical to our understanding of character evolution within the crown‐group (chondrichthyans + osteichthyans), including developmental characters. Early ontogenetic stages of placoderms are generally poorly known, although some exceptional faunas preserve both embryonic (e.g. from the Gogo Formation, Western Australia) and post‐embryonic individuals (the Miguasha Formation, Canada; Lode Formation, Latvia; Merriganowry Formation, Gogo Formation, Australia). Information provided by these ontogenies is relevant to questions of placoderm taxonomy and phylogeny, but also to broader questions pertinent to vertebrate evolution as a whole, for example, evolution of bone development, evolution of the axial skeleton and evolution of reproduction.     

Best squirrels trade a long life for an early reproduction

Age at primiparity plays a crucial role in population dynamics and life-history evolution. Long-term data on female North American red squirrels were analysed to study the fitness consequences of delaying first reproduction. Early breeders were born earlier, had a higher breeding success and achieved a higher lifetime reproductive success than females who delayed their first reproduction, which suggests a higher quality of early breeders. However, early breeders had similar mass when tagged, and similar number of food caches available at one year of age as late breeders. Nevertheless, we found evidence of survival costs of early primiparity. Early breeders had a lower survival between one and two years of age than late breeders and a lower lifespan. Our study points out that two reproductive tactics co-occurred in this population: a tactic based on early maturity at the cost of a lower survival versus a tactic based on delayed maturity and long lifespan. High quality individuals express the most profitable tactic by breeding early whereas low quality individuals do the best of a bad job by delaying their first reproduction.     

Discovery of a normal hermaphroditic chondrichthyan species: Apristurus longicephalus

Examination of the internal genital apparatus of Apristurus longicephalus , a small, deep‐water bottom‐dwelling catshark (Scyliorhinidae) from the western Pacific and Indian Oceans has revealed that it is a hermaphroditic species. It possesses both the developed genital apparatus of one sex and the undeveloped genital apparatus of the opposite sex in the same individual. Apristurus longicephalus is the first case of normal hermaphroditism to be recorded in cartilaginous fishes and this has been further classified as rudimentary hermaphroditism.     

Rapidly advancing laying date in a seabird and the changing advantage of early reproduction

1. Bird ringing schemes have collected immense amounts of data on timing of breeding for over 100 years. These data provide an unexploited source of information on temporal change in breeding date. 2. We investigated changes in breeding date of the Arctic tern Sterna paradisaea Pont. in Denmark during 1929-98, using information on ringing date of young. 3. Mean ringing date advanced by over 18 days during 70 years, while there was no temporal change in variance in date. 4. Advanced mean ringing date was explained by an increase in mean temperature during April and May and an increase in North Atlantic Oscillation (NAO) index for May. 5. Variance in ringing date increased in years with high temperatures in April and high NAO index values in April. 6. There was changing temporal patterns of selection for early breeding as reflected by analyses of the difference in mean ringing date for Arctic tern young that were subsequently recorded as survivors and mean ringing date for all young. The intensity of selection on breeding date changed from favouring late breeding in the 1930s to favouring early breeding during the 1990s. 7. Analyses of bird ringing information for millions of offspring of hundreds of bird species deposited in national ringing schemes may provide unlimited access to long-term time series of reproductive variables.     

Cyclical parthenogenesis and viviparity in aphids as evolutionary novelties

Evolutionary novelties represent challenges to biologists, particularly those who would like to understand the developmental and genetic changes responsible for their appearance. Most modern aphids possess two apparent evolutionary novelties: cyclical parthenogenesis (a life cycle with both sexual and asexual phases) and viviparity (internal development and live birth of progeny) in their asexual phase. Here I discuss the evolution of these apparent novelties from a developmental standpoint. Although a full understanding of the evolution of cyclical parthenogenesis and viviparity in aphids can seem a daunting task, these complex transitions can at least be broken down into a handful of steps. I argue that these should include the following: a differentiation of two developmentally distinct oocytes; de novo synthesis of centrosomes and modification of meiosis during asexual oogenesis; a loss or bypass of any cell cycle arrest and changes in key developmental events during viviparous oogenesis; and a change in how mothers specify the sexual vs. asexual fates of their progeny. Grappling with the nature of such steps and the order in which they occurred ought to increase our understanding and reduce the apparent novelty of complex evolutionary transitions. J. Exp. Zool. (Mol. Dev. Evol.) 318B:448-459, 2012. ? 2012 Wiley Periodicals, Inc.     

Morphogenesis of extraembryonic membranes and placentation in Mabuya mabouya (Squamata, Scincidae)

Topological and histological analyses of Mabuya mabouya embryos at different developmental stages showed an extraembryonic membrane sequence as follows: a bilaminar omphalopleure and progressive mesodermal expansion around the whole yolk sac at gastrula stages; mesodermal split and formation of an exocoelom in the entire embryonic chamber at neurula stages; beginning of the expansion of the allantois into the exocoelom to form a chorioallantoic membrane at pharyngula stages; complete extension of the allantois into the exocoelom between limb-bud to preparturition stages. Thus, a placental sequence could be enumerated: bilaminar yolk sac placenta; chorioplacenta; allantoplacenta. All placentas are highly specialized for nutrient absorption from early developmental stages. The bistratified extraembryonic ectoderm possesses an external layer with cuboidal cells and a microvillar surface around the whole yolk sac, which absorbs uterine secretions during development of the bilaminar yolk sac placenta and chorioplacenta. During gastrulation, with mesodermal expansion a dorsal absorptive plaque forms above the embryo and several smaller absorptive plaques develop antimesometrially. Both structures are similar histologically and are active in histotrophic transfer from gastrula stages until the end of development. The dorsal absorptive plaque will constitute the placentome and paraplacentome during allantoplacental development. At late gastrula-early neurula stages some absorptive plaques form chorionic concavities or chorionic bags that are penetrated by a long uterine fold and seem to have a specialized histotrophic and/or metabolic role. The extraembryonic mesoderm does not ingress into the yolk sac and neither an isolated yolk mass nor a yolk cleft are formed. This derived pattern of development may be related to the drastic reduction of the egg size and obligatory placentotrophy from early developmental stages. Our results show new specialized placentotrophic structures and a novel arrangement of extraembryonic membrane morphogenesis for Squamata.     

Evolution of axis specification mechanisms in jawed vertebrates: insights from a chondrichthyan

The genetic mechanisms that control the establishment of early polarities and their link with embryonic axis specification and patterning seem to substantially diverge across vertebrates. In amphibians and teleosts, the establishment of an early dorso-ventral polarity determines both the site of axis formation and its rostro-caudal orientation. In contrast, amniotes retain a considerable plasticity for their site of axis formation until blastula stages and rely on signals secreted by extraembryonic tissues, which have no clear equivalents in the former, for the establishment of their rostro-caudal pattern. The rationale for these differences remains unknown. Through detailed expression analyses of key development genes in a chondrichthyan, the dogfish Scyliorhinus canicula, we have reconstructed the ancestral pattern of axis specification in jawed vertebrates. We show that the dogfish displays compelling similarities with amniotes at blastula and early gastrula stages, including the presence of clear homologs of the hypoblast and extraembryonic ectoderm. In the ancestral state, these territories are specified at opposite poles of an early axis of bilateral symmetry, homologous to the dorso-ventral axis of amphibians or teleosts, and aligned with the later forming embryonic axis, from head to tail. Comparisons with amniotes suggest that a dorsal expansion of extraembryonic ectoderm, resulting in an apparently radial symmetry at late blastula stages, has taken place in their lineage. The synthesis of these results with those of functional analyses in model organisms supports an evolutionary link between the dorso-ventral polarity of amphibians and teleosts and the embryonic-extraembryonic organisation of amniotes. It leads to a general model of axis specification in gnathostomes, which provides a comparative framework for a reassessment of conservations both among vertebrates and with more distant metazoans.     

Placental structures and their association with matrotrophy and superfetation in poeciliid fishes

Both matrotrophy, the maternal provisioning of nutrients to developing embryos after fertilization, and superfetation, the simultaneous presence of two or more groups of embryos at different stages of development, occur at varying degrees among species of the fish family Poeciliidae. However, it is still unclear if these two reproductive modes depend on the presence of relatively complex placentas. We describe the ultrastructure of the maternal follicular placenta of 11 poeciliid fishes using electron microscopy. In addition, we quantified six ultrastructure characteristics that reflect the degree of complexity (number of vesicles, area of vesicles, number of microvilli, microvilli length, thickness of the maternal follicle and follicular area). Using phylogenetic comparative methods, we evaluated the relationship between degree of matrotrophy and placental characteristics. We also analysed the potential effect of the presence of superfetation on placental complexity. We found a positive relationship between the degree of matrotrophy and follicular area, number of microvilli and number and area of vesicles. Similarly, follicular area and number of microvilli were larger in species with superfetation than in those without superfetation. We conclude that high degrees of matrotrophy and superfetation are associated with placental characteristics that increase the efficiency of nutrient transfer between mother and embryos.     

Mammalian viviparity: a complex niche in the evolution of genomic imprinting

Evolution of mammalian reproductive success has witnessed a strong dependence on maternal resources through placental in utero development. Genomic imprinting, which has an active role in mammalian viviparity, also reveals a biased role for matrilineal DNA in its regulation. The co-existence of three matrilineal generations as one (mother, foetus and post-meiotic oocytes) has provided a maternal niche for transgenerational co-adaptive selection pressures to operate. In utero foetal growth has required increased maternal feeding in advance of foetal energetic demands; the mammary glands are primed for milk production in advance of birth, while the maternal hypothalamus is hormonally primed by the foetal placenta for nest building and post-natal care. Such biological forward planning resulted from maternal–foetal co-adaptation facilitated by co-expression of the same imprinted allele in the developing hypothalamus and placenta. This co-expression is concurrent with the placenta interacting with the adult maternal hypothalamus thereby providing a transgenerational template on which selection pressures may operate ensuring optimal maternalism in this and the next generation. Invasive placentation has further required the maternal immune system to adapt and positively respond to the foetal allotype. Pivotal to these mammalian evolutionary developments, genomic imprinting emerged as a monoallelic gene dosage regulatory mechanism of tightly interconnected gene networks providing developmental genetic stability for in utero development.     

Pattern formation in development of chondrichthyan dentitions: a review of an evolutionary model

The mode of tooth development displayed in Chondrichthyans (sharks, rays and holocephalans), one of frequent tooth replacement, was possible once a dental lamina had evolved, and since 1982 this has been known as the odontode regulation theory after Reif. Today, Reif's concepts need to be transformed into those of modern biology, the crosstalk between epithelium and mesenchyme, for the regulation of timing, spacing and shape of vertebrate teeth. Although Reif's proposed ‘primordial tissue’ may be the only site of progenitor cells, to restrict odontogenic potential to time-specific sites (protogerms), as has been suggested in the sequential addition tooth (SAT) model, very little data are available. Here, his model of alternate tooth replacement files has been interpreted as an integrated tooth addition unit of two adjacent files (SAT) unit for alternate replacement of teeth, regulated by putative, precisely timed gene expression for activation and inhibition. We have provided new data on patterns of tooth succession in dentitions of extant sharks and rays to compare with those of Reif. Using a phylogeny combined from molecular and morphological data, it is suggested that the alternate tooth addition and replacement model is derived within Chondrichthyes, and diversified from single file tooth addition of the stem chondrichthyans.     

Morphological specializations for fetal maintenance in viviparous vertebrates: An introduction and historical retrospective

In many viviparous vertebrates, pregnant females sustain their developing embryos and provide them with nutrients by means of placentas and a diversity of other types of specializations. With this article, we introduce a virtual (online) issue of the Journal of Morphology that presents 12 recent papers on fetal maintenance in viviparous vertebrates. We also outline the history of research in this area and document the central role of morphology in helping to explain the function and evolution of specializations for fetal nutrition. This virtual issue of the Journal of Morphology is an outgrowth of a symposium held under auspices of the International Congress of Vertebrate Morphology. The included papers reflect a diversity of taxa, research methods, and biological issues. To celebrate the publication of this virtual issue of the Journal of Morphology, the publisher is making freely available to readers a number of other relevant papers published in the journal over the past 128 years. J. Morphol. 276:1–16, 2015. © 2015 Wiley Periodicals, Inc.     

The origin and evolution of genomic imprinting and viviparity in mammals

Genomic imprinting is widespread in eutherian mammals. Marsupial mammals also have genomic imprinting, but in fewer loci. It has long been thought that genomic imprinting is somehow related to placentation and/or viviparity in mammals, although neither is restricted to mammals. Most imprinted genes are expressed in the placenta. There is no evidence for genomic imprinting in the egg-laying monotreme mammals, despite their short-lived placenta that transfers nutrients from mother to embryo. Post natal genomic imprinting also occurs, especially in the brain. However, little attention has been paid to the primary source of nutrition in the neonate in all mammals, the mammary gland. Differentially methylated regions (DMRs) play an important role as imprinting control centres in each imprinted region which usually comprises both paternally and maternally expressed genes (PEGs and MEGs). The DMR is established in the male or female germline (the gDMR). Comprehensive comparative genome studies demonstrated that two imprinted regions, PEG10 and IGF2-H19, are conserved in both marsupials and eutherians and that PEG10 and H19 DMRs emerged in the therian ancestor at least 160 Ma, indicating the ancestral origin of genomic imprinting during therian mammal evolution. Importantly, these regions are known to be deeply involved in placental and embryonic growth. It appears that most maternal gDMRs are always associated with imprinting in eutherian mammals, but emerged at differing times during mammalian evolution. Thus, genomic imprinting could evolve from a defence mechanism against transposable elements that depended on DNA methylation established in germ cells.