Histotrophy

Abstract: 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.

Abstract: Quantitative analyses based upon the superimposition of phylogenetic and reproductive data have revealed that viviparity has originated on at least 132 independent occasions among vertebrates, with 98 of these origins having occurred among reptiles. The viviparous lineages have given rise to at least 24 matrotrophic clades, all but four of which are anamniotes. Traditional scenarios assume progressive, gradualistic evolution from oviparity to lecithotrophic viviparity to matrotrophic viviparity. However, mammalian evidence indicates that matrotrophy can precede the evolution of viviparity. Moreover, data on reptiles seem to be consistent with a punctuated equilibrium model for viviparity and a saltatory model for incipient matrotrophy and placentation. Among the specializations for fetal nutrition, strong convergence is evident at organismal, organological, and cytological levels. Examples include yolk sac placentation, trophotaeniae, and adaptations for embryonic cannibalism. Certain lizards of the genera Mabuya and Chalcides have converged strongly on eutherian mammals with respect to morphology of the chorioallantoic placenta. Placental specializations that have evolved independently in some eutherians and matrotrophic lizards include placentomes, giant binucleate cells, deciduate maternal tissue, and chorionic areolae.

Abstract: Summary. 1 This is a reveiw of reptilian placentation and other phenomena in the reptilian reproductive cycle concerned with viviparity. 2 There are three distinct types of placentation so far decribed for reptiles:- Type (i). A simple where the partial degneration of maternal and embryonic epithelium allows for a close apposition of maternal and embryonic blood streams. The lizards with this type of placents have no apparent reduction in the yolk-content of thier eggs at the time of ovulation. These Lizards are Lygosoma (Hinulia) quoyi, L. (Hemiergis) quadridigitatum, Tiliqua scincoides, t. nigrolutea, and from Giacomini's decription Chalcides ocellatus, as well as the snakes Denisonia superba and D.suta. Type (ii.). A simple type where the maternal capillaries are raised into small folds. Ther grooves between the folds are lined with glandular epithelium, but the cdapillaries themselves are exporsed at the surface of the folods. The underlying chorionic ectoderm may be thickened and glandular. No early stages were available for and examination of the yolk-content of the eggs. The lizards with this type of placenta are Lygosoma (Liolepisma) pretiosum, L. (L.) ocellatum, and L. (L.) metallicum. Type (iii.). The most specialized placenta so far described for reptiles, where the uterine wall, over a distinct elliptical area beneth the main longitudinal utering blood-vessels, is raised into a series of folds filled with capillaries and lined with thickened glandular epithelium and is underlain by an elliptical embryonic area of much thickened chorionie ectoderm. The Lizards with this type of placements have a reduced yolk-content at the time of ovualion. Thes lizards are Chalcides tridactylus, Lygosoma (Liolepisma) entrecasteauxi, and L. (L.) weekesae. 3 It is suggested that (α) in reptiles with and obvious reduction in the yolk-content of their eggs at the time of ovulation, and its invaribale accompaniment by a speciallized folded glandular area of allanto-placentation, the function of this specialized placenta, is nutrition; that (b) the funciton of the yolk-sao placenta is possibly to supply water to the developing egg: and that (c) the function of the simple placenta, so consistently present in lizards with eggs with an apparently yolk-content, is respiration. 4 The condition of the large yolk-laden egg held tighly in a stretched utersu is obviously the most primitive expression of viviparity among repitles. The condition of a samll egge with a reduced yolk-content is more advanced, and is obviously but a step behind the yolkless egg, such as occures among the eutherian mammals. Hence it is suggested that the function of fixation, although one of the first concerns of the trophoblast of the small mammalian egg to-day, has probably originated secondariyly to some other funciton, presumably respiration. 5 It is suggested that with a decrease in the yolk-content of the egg the yolk-sac placenta would gradually lose significance as a water absorbing organ, but the virture of its extra-embryonic circulation, a placenta to funciton for respirtion or nutrition, or both, could be evolved, and it is conceivable that the mammalian yolk-sac placenta could have been evolved along lines similar to theses. 6 The specialized placenta. type (iii.) is considered to have evolved from the simple conditon described as type (ii.), and it is thought that the placenta in ungulates (the mammalian non-deciducte plancenta) may have had origin form some such simple type as type (i.), through a stage in placentation similar to type (iii.), which Giacomini likened to a cow's cotyledon in early stages of development. 7 The facts are condsidered to justify the conclusion that among reptiles placentation has arisen independently development of similar types of placentas is common. 8 It ws found that the proportion of viviparous to oviparous reptiles on the Great Dividing Range and the inland plain of south-easten Australia was extradinarily high, and that the number of oviparous species only approached the number of viviparsous speices on the lower slopes of the Dividing Range, and on the coastal plain. 9 In the Pyrenees and the French Alps by far the majority of lizards found at high altitudes were viviparous. the oviparous species were practically confined to the mountaind slopes up to about 3000-4000 feet above sea-level. 10 It is suggested that the failure of oviparous species to establish themselves at 4000 feet and over above sea-level amy be caused by cold interfering with development of the eggs in the nest. 12 All viviparous speices found on, or recorded from, the inland plain, the mountain slopes, ro the coastal plain of south-eastern Australia also occur at least 4000 feet above sea-level on the Great Dividing Range. 13 Two viviparous speices with teh most highly specialized allanto-placeta and reproductive cycle yet recorded for reptiles in Australia, and only equlled by the lizard C. tridactylus in Italy, are restricted to 4000-7000 feet above sea-level. 14 Therefore, it is suggested that in south-eastern Australia, at least, the factros determining the adoption of viviparity may be either (α) definitely associated with the altitudes to which these lizards are restricted or (b) may work most efficently under the conditons existing at such altitudes. 15 Cold is suggested as the most likely external factor associated with high altitudes that may influence either directly or indircectly the adoption of viviparity.

Abstract: 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.