Origin of Amniotes and the Amniotic Egg

by

Robert R. Reisz, Tea Maho

• LAST MODIFIED: 22 August 2023
• DOI: 10.1093/obo/9780199941728-0149

Introduction

Amniota is the name assigned to a large group of limbed vertebrates that includes not only extant reptiles, birds, and mammals because of their reproductive strategy involving the amniotic egg, but also a rich record of extinct animals whose reproductive mode cannot be determined directly. The origin of amniotes is therefore anchored by two disparate disciplines: developmental biology and vertebrate paleontology. The amniotic egg is at the center of the great evolutionary success of the crown group Amniota. The developmental strategy of amniotes is characterized by the evolutionary innovation of a series of four extraembryonic membranes—the yolk sac, allantois, chorion, and amnion—that provide a complete developmental environment for the embryonic life of a reptile, bird, or mammal. These extraembryonic membranes allowed the common ancestor of amniotes and its descendants to invest the mother’s resources into fewer but larger eggs; protect the developing embryos by placing them in a nest or retain them in the reproductive canal; and therefore also eliminate the need for a prolonged larval stage and metamorphosis. It has been suggested that this evolutionary innovation provided an unprecedented opportunity to complete the conquest of the terrestrial realm by amniotes and has led to the great success of aquatic reptiles, Mesozoic dinosaurs and their descendants, the birds, and the Cenozoic mammals, including humans. Interestingly, it also appears to have been instrumental in allowing amniotes to invade other parts of the biosphere, including the air, through flying or gliding organisms, and even to return repeatedly to the aquatic environment. The fossil record of crown amniotes is very rich and extends over at least 318 million years of earth’s history, providing a detailed accounting of the evolutionary history of Amniota. As such, they provide the primary evidence for the origin and early evolution of this important clade of animals. Unfortunately, the fossil record is quite limited in the preservation of amniotic eggs, with the oldest documented evidence of fossilized amniotic eggs being those of 195-million-year-old dinosaurs. Thus, the origin and early diversification of amniotes, the transition from anamniotes to amniotes, and the composition of crown Amniota can only be determined by studies of the fossil record and through phylogenetic analyses. Since the fossil record of amniotes and their presumed close relatives is represented mainly by the remains of their bony skeletons, analyses can only be based on the morphological information provided by the skeletons of these ancient limbed vertebrates. The results of these analyses will determine the nature not only of the anamniote-amniote transition, but also the composition of crown Amniota, even in the absence of direct evidence of their embryology.

General Overviews

There are no textbooks on amniote origins, partly because this is an interdisciplinary subject, and, generally, there is a strong tendency to publish on vertebrates either as a whole or about readily recognizable extant groups in disciplines like herpetology, mammalogy, and ornithology. Sumida and Martin 1997, a book on amniote origins, is the closest book to the topic of amniote origins and early amniote evolution. While Haeckel 1866 introduces the concept of Amniota, the volumes are not readily available. Other books on tetrapod evolution, such as Clack 2002, dwell briefly on amniote origins and early evolution as part of a discussion of the invasion of land by tetrapods. Similarly, Sues 2019 is a book on the rise of reptiles that deals briefly with the origin of amniotes as part of a treatise on 320 million years of reptile evolution. Two general books dealing with vertebrates as a whole, Benton 2014 and Carroll 1988, provide accessible treatments of amniote origins and early evolution as part of their treatment of the fossil record. The amniotic egg is the innovation that apparently allowed amniotes to complete the transition from an aquatic to a terrestrial environment and not rely on the aquatic habitat for reproduction, as Reisz 1997 describes.

• Benton, M. J. 2014. Vertebrate palaeontology. 4th ed. Chicester, UK: Wiley-Blackwell.

  The most up-to-date textbook currently available on vertebrate paleontology. As such, it emphasizes the fossil record of vertebrates, but it also discusses amniote origins and early evolution as part of the treatment of tetrapod phylogeny, osteology, and evolution. First published in 1990 (London: Chapman & Hall).

• Carroll, R. L. 1988. Vertebrate paleontology and evolution. New York: W. H. Freeman.

  Although less up-to-date than Benton 2014, this book gives more anatomical descriptions and illustrations, including fossils related to the origin and early evolution of amniotes. Notable for its emphasis on the origins of extant taxa, and deals extensively with extinct and some extant vertebrates.

• Clack, J. A. 2002. Gaining ground: The origin and evolution of tetrapods. Bloomington: Indiana Univ. Press.

  Very thorough descriptions of the origin and relationships of tetrapods. Includes a brief section on the anamniote-amniote transitions, as well as an interesting segment on the evolution of hearing.

• Haeckel, E. 1866. Generelle Morphologie der Organismem. 2 vols. Berlin: G. Reimer.

  DOI: 10.1515/9783110848281

  In this large work, Haeckel introduces the concept that the evolution of the amniotic egg was the key innovation for the large group of vertebrate tetrapods known as “Amniota,” which encompasses mammals, birds, crocodiles, squamates, and turtles.

• Reisz, R. R. 1997. The origin and early evolutionary history of amniotes. Trends in Ecology & Evolution 12:218–222.

  DOI: 10.1016/S0169-5347(97)01060-4

  A review of the hypotheses of the origin of amniotes and previous phylogenetic analyses.

• Sues, H. D. 2019. The rise of reptiles: 320 million years of evolution. Baltimore: Johns Hopkins Univ. Press.

  DOI: 10.1353/book.67468

  An excellent book detailing the evolution of the reptilian branch of amniote evolution, with a thorough examination of the fossil record. This includes some information on amniote origins and the oldest known amniotes. Wonderful visual representation of the fossil record of reptile evolutionary history.

• Sumida, S. S., and K. L. M. Martin. 1997. Amniote origins: Completing the transition to land. San Diego: Academic Press.

  A typical academic book with thirteen chapters on various aspects of amniote origins and early evolution associated with the anamniote-amniote transitions, with twenty-four contributors. A fairly successful attempt at integrating several aspects of the origin of amniotes and includes ecological, biogeographic, behavioral, and phylogenetic considerations.