Functional morphology, diversity, and evolution of yolk processing specializations in embryonic reptiles and birds

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Evolution of the terrestrial egg of amniotes (reptiles, birds, and mammals) is often considered to be one of the most significant events in vertebrate history. Presence of an eggshell, fetal membranes, and a sizeable yolk allowed this egg to develop on land and hatch out well-developed, terrestrial offspring. For centuries, morphologicallybased studies have provided valuable information about the eggs of amniotes and the embryos that develop from them. This review explores the history of such investigations, as a contribution to this special issue of Journal of Morphology, titled Developmental Morphology and Evolution of Amniote Eggs and Embryos. Anatomically-based investigations are surveyed from the ancient Greeks through the Scientific Revolution, followed by the 19th and early 20th centuries, with a focus on major findings of historical figures who have contributed significantly to our knowledge. Recent research on various aspects of amniote eggs is summarized, including gastrulation, egg shape and eggshell morphology, eggs of Mesozoic dinosaurs, sauropsid yolk sacs, squamate placentation, embryogenesis, and the phylotypic phase of embryonic development. As documented in this review, studies on amniote eggs and embryos have relied heavily on morphological approaches in order to answer functional and evolutionary questions.

“…A different pattern has recently been documented in reptiles (Blackburn, 2020). Endodermal cells proliferate and invade the yolk sac cavity and take up yolk spheres.…”

Section: Yolk Sacs Of Sauropsidsmentioning

confidence: 94%

Section: General Features Of Amniotic Eggsmentioning

confidence: 99%

Morphological research on amniote eggs and embryos: An introduction and historical retrospective

Blackburn

Stewart

2021

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“…An outstanding diversity of reproductive modes exists among squamates (e.g., Blackburn, 2015aBlackburn, , 2020Stewart & Thompson, 2017). This diversity of reproductive modes evolved from an oviparous ancestor through multiple evolutionary origins of various forms of egg retention and viviparity (e.g., Blackburn, 1982Blackburn, , 1985Blackburn et al, 2003;Blackburn & Flemming, 2009;Hughes & Blackburn, 2020;Stewart, 2013;Stewart, 2020).…”

Section: Squamatamentioning

confidence: 99%

“…s Freyer et al (2003); Freyer and Renfree (2009). t Blackburn, Lestz, Barnes, and Powers (2019), Blackburn, Lestz, Barnes, Appiah, and Bonneau (2019); Blackburn (2020).…”

Section: Avesmentioning

confidence: 99%

Phylogeny and evolutionary history of the amniote egg

Starck

Stewart

Blackburn

2021

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We review morphological features of the amniote egg and embryos in a comparative phylogenetic framework, including all major clades of extant vertebrates. We discuss 40 characters that are relevant for an analysis of the evolutionary history of the vertebrate egg. Special attention is given to the morphology of the cellular yolk sac, the eggshell, and extraembryonic membranes. Many features that are typically assigned to amniotes, such as a large yolk sac, delayed egg deposition, and terrestrial reproduction have evolved independently and convergently in numerous clades of vertebrates. We use phylogenetic character mapping and ancestral character state reconstruction as tools to recognize sequence, order, and patterns of morphological evolution and deduce a hypothesis of the evolutionary history of the amniote egg.Besides amnion and chorioallantois, amniotes ancestrally possess copulatory organs (secondarily reduced in most birds), internal fertilization, and delayed deposition of eggs that contain an embryo in the primitive streak or early somite stage. Except for the amnion, chorioallantois, and amniote type of eggshell, these features evolved convergently in almost all major clades of aquatic vertebrates possibly in response to selective factors such as egg predation, hostile environmental conditions for egg development, or to adjust hatching of young to favorable season. A functionally important feature of the amnion membrane is its myogenic contractility that moves the (early) embryo and prevents adhering of the growing embryo to extraembryonic materials. This function of the amnion membrane and the liquid-filled amnion cavity may have evolved under the requirements of delayed deposition of eggs that contain developing embryos. The chorioallantois is a temporary embryonic exchange organ that supports embryonic development. A possible evolutionary scenario is that the amniote egg presents an exaptation that paved the evolutionary pathway for reproduction on land. As shown by numerous examples from anamniotes, reproduction on land has occurred multiple times among vertebrates-the amniote egg presenting one "solution" that enabled the conquest of land for reproduction.

“…Recently it was argued that monotremes are so highly specialized that features of their common ancestor with sauropsids are difficult to infer (Blackburn, 2020). However, the presence of a latebra in monotremes, lizards and birds seems to be just such a feature.…”

Section: The Latebra and Yolk Bedmentioning

confidence: 99%

T. Thomson Flynn and the monotreme egg from oocyte maturation to germ layer formation

Carter

2021

Knowledge of oocyte development and the early differentiation of the germ layers in monotremes stems largely from two articles by J. P. Hill and T. Thomson Flynn. The completeness of their account was due to the large series of echidna ovaries and eggs collected on Tasmania by Flynn, an Australian biologist of whom a brief account is given. A striking finding in the oocyte and early embryo of monotremes was the presence of a latebra connected to the yolk bed beneath the germinal disc as described in birds and several reptiles. A further resemblance was the presence early in vitellogenesis of a striate zone beneath the zona pellucida. Cleavage resulted first in a lens-shaped blastodisc encircled by cells called vitellocytes that later fused to form a germ-ring. The blastodisc gave rise to a blastoderm that eventually became unilaminar but comprised two cell types identified as ectoderm and primitive endoderm. Eventually these segregated into two layers and formed a blastula. This sequence resembled that in marsupials except there was no obvious distinction between future embryonic and extra-embryonic regions. As the blastoderm extended over the surface of the yolk, it was preceded by the germ-ring that eventually played a role in forming the yolk navel. This was a unique feature of monotreme development. It is shown that Flynn played an important role in analysis of the material as well as in its collection.