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Natural nests of egg-laying birds and reptiles exhibit substantial thermal variation, at a range of spatial and temporal scales. Rates and trajectories of embryonic development are highly sensitive to temperature, favouring an ability of embryos to respond adaptively (i.e. match their developmental biology to local thermal regimes). Spatially, thermal variation can be significant within a single nest (top to bottom), among adjacent nests (as a function of shading, nest depth etc.), across populations that inhabit areas with different weather conditions, and across species that differ in climates occupied and/or nest characteristics. Thermal regimes also vary temporally, in ways that generate differences among nests within a single population (e.g. due to seasonal timing of laying), among populations and across species. Anthropogenic activities (e.g. habitat clearing, climate change) add to this spatial and temporal diversity in thermal regimes. We review published literature on embryonic adaptations to spatio-temporal heterogeneity in nest temperatures. Although relatively few taxa have been studied in detail, and proximate mechanisms remain unclear, our review identifies many cases in which natural selection appears to have fine-tuned embryogenesis to match local thermal regimes. Developmental rates have been reported to differ between uppermost versus lower eggs within a single nest, between eggs laid early versus late in the season, and between populations from cooler versus warmer climates. We identify gaps in our understanding of thermal adaptations of early (embryonic) phases of the life history, and suggest fruitful opportunities for future research.

Early embryonic cells are capable of acquiring numerous developmental fates until they become irreversibly committed to specific lineages depending on intrinsic determinants and/or regional interactions. From fertilization to gastrulation, such pluripotent cells first increase in number and then turn to undergoing differentiation. Mechanisms regulating pluripotency in each species attract great interest in developmental biology. Also, outlining the evolutionary background of pluripotency can enhance our understanding of mammalian pluripotency and provide a broader view of early development of vertebrates. Here, we introduce integrative models of pluripotent states in amniotes (mammals, birds and reptiles) to offer a comprehensive overview of widely accepted knowledge about mammalian pluripotency and our recent findings in non-mammalian amniotes, such as chicken and gecko. In particular, we describe 1) the IL6/Stat3 signaling pathway as a positive regulator of naive pluripotency, 2) Fgf/Erk signaling as a process that prepares cells for differentiation, 3) the role of the interactions between these two signaling pathways during the transition from pluripotency to differentiation, and 4) functional diversification of two transcription factors, Class V POUs and Nanog. In the last section, we also briefly discuss possible relationships of unique cell cycle properties of early embryonic cells with signaling pathways and developmental potentials in the pluripotent cell states., (Copyright © 2019 Elsevier Inc. All rights reserved.)

Reconciling the origins of morphological diversity with the deep homology of underlying mechanisms is a question fundamental to the goals of evolutionary developmental biology ("evo-devo" or EDB). In this paper I argue that differing research agendas in evolutionary and developmental biology have hindered how we address this question, but that the limb provides ideal "common ground" for their fuller integration. To support this idea, I review two previous analyses of limb variation in mammal, bird, and reptile taxa that offer complementary approaches to explaining diversity. Specifically, I present evidence suggesting that: (1) a shared genetic architecture affects the pattern of between limb developmental integration, while their functional dissociation is linked to both increased phenotypic evolvability and diversity of interlimb proportions, and (2) within limb proportional diversity is biased such that proximal and distal segments function as tradeoffs while the middle segment is more conservative, a signal that is both evident from early in morphogenesis and suggestive of an "inhibitory cascade" model of limb proximo-distal axis development. In the first case, shared genetic mechanisms predict both observed developmental integration between limbs and patterns of clade-specific diversity. In the second case, underappreciated patterns of phenotypic diversity suggest novel insights into the underlying developmental mechanisms by which variation is generated. These studies show how insights from both evolutionary and developmental biology of the limb may be used to generate novel testable hypotheses into the origins of diversity that are broadly applicable to the integration of EDB., (© The Author 2017. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.)

The cerebral cortex covers the rostral part of the brain and, in higher mammals and particularly humans, plays a key role in cognition and consciousness. It is populated with neuronal cell bodies distributed in radially organized layers. Understanding the common and lineage-specific molecular mechanisms that orchestrate cortical development and evolution are key issues in neurobiology. During evolution, the cortex appeared in stem amniotes and evolved divergently in two main branches of the phylogenetic tree: the synapsids (which led to present day mammals) and the diapsids (reptiles and birds). Comparative studies in organisms that belong to those two branches have identified some common principles of cortical development and organization that are possibly inherited from stem amniotes and regulated by similar molecular mechanisms. These comparisons have also highlighted certain essential features of mammalian cortices that are absent or different in diapsids and that probably evolved after the synapsid-diapsid divergence. Chief among these is the size and multi-laminar organization of the mammalian cortex, and the propensity to increase its area by folding. Here, I review recent data on cortical neurogenesis, neuronal migration and cortical layer formation and folding in this evolutionary perspective, and highlight important unanswered questions for future investigation., Competing Interests: Competing interestsThe author declares no competing or financial interests., (© 2017. Published by The Company of Biologists Ltd.)

One of the most amazing transitions and innovations during the evolution of mammals was the formation of a novel jaw joint and the incorporation of the original jaw joint into the middle ear to create the unique mammalian three bone/ossicle ear. In this review, we look at the key steps that led to this change and other unusual features of the middle ear and how developmental biology has been providing an understanding of the mechanisms involved. This starts with an overview of the tympanic (air-filled) middle ear, and how the ear drum (tympanic membrane) and the cavity itself form during development in amniotes. This is followed by an investigation of how the ear is connected to the pharynx and the relationship of the ear to the bony bulla in which it sits. Finally, the novel mammalian jaw joint and versatile dentary bone will be discussed with respect to evolution of the mammalian middle ear.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'., (© 2016 The Authors.)

Reptiles and birds have been highlighted as excellent experimental models for the study of developmental biology; however, due to technical limitations in cellular analysis, dynamics of neural stem/progenitor cells of these animals remain unclear. In this chapter, we introduce the protocols for neurosphere culture and ex ovo embryonic culture of developing reptilian and avian embryos, which are modified from the method originally established for rodent embryos. Applications of these techniques provide powerful strategies for the study of comparative neural development of amniotes.

In the field of germline development in amniote vertebrates, primordial germ cell (PGC) specification in birds and reptiles remains controversial. Avians are believed to adopt a predetermination or maternal specification mode of PGC formation, contrary to an inductive mode employed by mammals and, supposedly, reptiles. Here, we revisit and review some key aspects of PGC development that channelled the current subdivision, and challenge the position of birds and reptiles as well as the 'binary' evolutionary model of PGC development in vertebrates. We propose an alternative view on PGC specification where germ plasm plays a role in laying the foundation for the formation of PGC precursors (pPGC), but not necessarily of PGCs. Moreover, inductive mechanisms may be necessary for the transition from pPGCs to PGCs. Within this framework, the implementation of data from birds and reptiles could provide new insights on the evolution of PGC specification in amniotes., (© 2016 The Authors BioEssays Published by WILEY Periodicals, Inc.)

Temperature profoundly affects the rate and trajectory of embryonic development, and thermal extremes can be fatal. In viviparous species, maternal behaviour and physiology can buffer the embryo from thermal fluctuations; but in oviparous animals (like most reptiles and all birds), an embryo is likely to encounter unpredictable periods when incubation temperatures are unfavourable. Thus, we might expect natural selection to have favoured traits that enable embryos to maintain development despite those fluctuations. Our review of recent research identifies three main routes that embryos use in this way. Extreme temperatures (i) can be avoided (e.g. by accelerating hatching, by moving within the egg, by cooling the egg by enhanced rates of evaporation, or by hysteresis in rates of heating versus cooling); (ii) can be tolerated (e.g. by entering diapause, by producing heat-shock proteins, or by changing oxygen use); or (iii) the embryo can adjust its physiology and/or developmental trajectory in ways that reduce the fitness penalties of unfavourable thermal conditions (e.g. by acclimating, by exploiting brief windows of favourable conditions, or by producing the hatchling phenotype best suited to those incubation conditions). Embryos are not simply passive victims of ambient conditions. Like free-living stages of the life cycle, embryos exhibit behavioural and physiological plasticity that enables them to deal with unpredictable abiotic challenges., (© 2014 The Authors. Biological Reviews © 2014 Cambridge Philosophical Society.)

Recent studies have demonstrated that thermoregulatory behavior occurs not only in posthatching turtles but also in turtles prior to hatching. Does thermoregulatory behavior also occur in the embryos of other reptile and bird species? Our experiments show that such behavior is widespread but not universal in reptile and bird embryos. We recorded repositioning within the egg, in response to thermal gradients, in the embryos of three species of snakes (Xenochrophis piscator, Elaphe bimaculata, and Zaocys dhumnades), two turtles (Chelydra serpentina and Ocadia sinensis), one crocodile (Alligator sinensis), and four birds (Coturnix coturnix, Gallus gallus domesticus, Columba livia domestica, and Anas platyrhynchos domestica). However, we detected no significant thermoregulation by the embryos of two lizard species (Takydromus septentrionalis and Phrynocephalus frontalis). Overall, embryonic thermoregulatory behavior is widespread in reptile as well as bird species but may be unimportant in the small eggs laid by most lizards.

Environmental conditions considerably influence embryogenesis and subsequent postnatal development; however, the roles of individual embryonic physiological systems in these effects remain largely unclear. Data on the effects of some environmental factors (temperature variation and hypoxia) on the development of embryos and extra-embryonic organs in reptiles and birds are summarized, with special emphasis on acute changes in these factors. The involvement of several physiological characteristics related to the functions of the extra-embryonic membranes, cardiovascular system, and embryonic behavior (amnion rhythmic contractions, cardiac activity, and embryonic motility) in the integrated response to temperature fluctuations and acute hypoxia is considered. The changes in this response with embryonic age in reptiles and birds are analyzed. Particular attention is paid to the maturation of the regulatory mechanisms, interactions among the above parameters, and their possible contributions to the changes in oxygen consumption (or its stability) during short-term changes in temperature and oxygenation at different stages of embryonic development., (Copyright © 2011 Elsevier B.V. All rights reserved.)

Adult galliform birds (e.g. chickens) exhibit a relatively small telencephalon and a proportionately large optic tectum compared with parrots and songbirds. We previously examined the embryonic origins of these adult species differences and found that the optic tectum is larger in quail than in parakeets and songbirds at early stages of development, prior to tectal neurogenesis onset. The aim of this study was to determine whether a proportionately large presumptive tectum is a primitive condition within birds or a derived feature of quail and other galliform birds. To this end, we examined embryonic brains of several avian species (emus, parrots, songbirds, waterfowl, galliform birds), reptiles (3 lizard species, alligators, turtles) and a monotreme (platypuses). Brain region volumes were estimated from serial Nissl-stained sections. We found that the embryos of galliform birds and lizards exhibit a proportionally larger presumptive tectum than all the other examined species. The presumptive tectum of the platypus is unusually small. The most parsimonious interpretation of these data is that the expanded embryonic tectum of lizards and galliform birds is a derived feature in both of these taxonomic groups., (Copyright 2010 S. Karger AG, Basel.)

Rhythmical contractile activity of amnion accompanies development reptiles and birds in the course of the large part of embryogenesis. These rhythmical contractions are myogenic and spontaneous. The strength, frequency, and character of the amnion contractions change in embryogenesis in a regular way. This type of rhythmical activity is sensitive to many neurotransmitters and external factors. Features of similarity and difference of the amnion rhythmical contractile activity in the reptile and bird embryogenesis are considered. There are discussed a possible functional significance of this rhythmical activity and its participation in response of embryo to external actions, such as temperature fluctuations and acute hypoxia.

Pulmonary surfactant is a mixture of lipids and proteins that is secreted by alveolar Type II cells. It reduces alveolar surface tension and hence the work of breathing. Despite the tremendous diversity of lung structures amongst the vertebrates, the composition of surfactant is highly conserved. Conserved elements of the surfactant system amongst distantly related species are likely to be crucial factors for successful lung development. Understanding the mechanisms by which the surfactant system becomes operational in animals with dramatically different birthing strategies and in distantly related species will provide important information about the role of the surfactant system in the commencement of air breathing and the processes regulating surfactant maturation and secretion. In mammals, the embryonic maturation of the surfactant system is controlled by a host of factors, including glucocorticoids, thyroid hormones, and autonomic neurotransmitters. Here we review the mechanisms controlling the maturation of surfactant production, including birthing strategy, phylogeny, lung structure, and posthatching environment. Using four species of egg-laying amniote (chicken, dragon lizard, sea turtle, and crocodile) previously described in detail and the large amount of information available for mammals, we examine the hypothesis that the control of surfactant production is dependent on glucocorticoids (dexamethasone [Dex]), thyroid hormones (T3), and autonomic neurotransmitters (epinephrine and carbachol). We also examine whether the overall intrinsic pattern of the control of surfactant maturation is conserved throughout the vertebrate radiation and then how the environment (extrinsic factors) may account for the observed differences in the patterns of development. We also discuss the utility of a coculture system of embryonic Type II cells and fibroblasts to determine the evolutionary pattern behind the control of surfactant and to demonstrate that the surfactant system matures under multihormonal control. We demonstrate that Dex and T3 are stimulators of surfactant production during embryonic development, but they lose their efficacy closer to hatching or birth. Epinephrine stimulates surfactant secretion beyond 75% of development and also after hatching or birth. Carbachol stimulates surfactant secretion in the bearded dragon and saltwater crocodile but not in the sea turtle, chicken, or mammals. It is likely that the differences in control of surfactant development are likely to be primarily related to metabolic activity and the duration of incubation (i.e., the "speed" of development). Moreover, the hormones examined appear important in promoting development and therefore appear conserved within the amniotes. However, the autonomic neurotransmitters induced different responses in different species. Hence, some factors are crucial for the proper maturation of the surfactant system, whereas others vary throughout evolution without being detrimental to the overall function of the system.

The mechanisms controlling the formation of the embryonic axis, and specifically those that give rise to the mesoderm, have received renewed attention recently. In the frog, some of these mechanisms have begun to be elucidated, and several factors have been found to cause uncommitted ectoderm cells to differentiate into mesoderm. All of the factors identified to date are related either to fibroblast growth factor (FGF) or to transforming growth factor beta (TGF-beta). Do the mechanisms that generate the embryonic axis of amphibians also operate in chick and mouse embryos? Here I address how amphibian and amniote embryos might provide complementary pieces of a puzzle.

American alligators exhibit a number of morphological features which are more characteristic of mammals than reptiles. This unique combination makes an extremely useful animal for experimental investigations of craniofacial development. Thus, it is possible to make a longitudinal study of the development of the alligator's secondary palate by utilizing shell-less culture techniques. Incubation of eggs at 28 degrees C, as opposed to 3 degrees C, slows development sufficiently to enable both the recovery of critical intermediate stages, and also great precision in the timing of teratogen administration. Injection of either 0.01 mg of 5-fluoro-2-desoxyuridine or 0.05 mg of hydrocortisone into the yolks of Days 12, 14, and 17 embryos produces cleft lip, cleft lip and palate, and cleft palate, respectively. Application of the teratogen at critical developmental stages on Day 12 reliably induces unilateral cleft lip on either the right or left sides, while injection on Day 10 yields embryos with normal lips and palates but virtually no lower jaw. The spontaneous malformation rate is very low, but highest in eggs laid by young and old animals. Changes in eggshell banding provide a noninvasive method for monitoring embryonic development. Detailed comparisons of palatal development in birds and alligators permit an accurate phylogenetic study of physiological clefting in the aves. The alligator dentition is readily amenable to experimental studies.