Extended embryo retention and viviparity in the first amniotes

Jiang, Baoyu; He, Yuan; Elsler, Armin; Wang, Shengyu; Keating, Joseph N.; Song, Jiuzhou; Kearns, Stuart L.; Benton, Michael J.

doi:10.1038/s41559-023-02074-0

Cited by 8 publications

(2 citation statements)

References 73 publications

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“…The early amniotes fertilized internally and retained the embryo in the female's body (extended embryo retention [EER]), and may have even been viviparous like some salamanders and 20% of squamates. Viviparity protects the embryo and neonates from environmental hazards and was sustained throughout amphibian evolution once it emerged 184 . Viviparous amphibians rarely care for their offspring after birth 177 ; thus, the emergence of EER/viviparity as a maternal investment strategy may have reduced the need for behavioral care, leading to a low (10%) prevalence of parental behaviors among reptiles.…”

Section: Parental Care Evolution In Vertebrates: Comparative Behavior...mentioning

confidence: 99%

“…Early synapsids’ eggs lacked fully calcified shells and were still vulnerable to desiccation like the eggs of monotremes and most squamates 176,184 . Thus, early synapsids such as Dimetrodon may have buried their eggs in moisture‐laden soil, hydrated them with contact from moist skin, or carried them in a moist pouch—as living monotremes do 193,194 .…”

Section: Parental Care Evolution In Vertebrates: Comparative Behavior...mentioning

confidence: 99%

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Parental brain through time: The origin and development of the neural circuit of mammalian parenting

Kuroda,

Fukumitsu,

Kurachi

et al. 2024

Annals of the New York Academy of Sciences

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This review consolidates current knowledge on mammalian parental care, focusing on its neural mechanisms, evolutionary origins, and derivatives. Neurobiological studies have identified specific neurons in the medial preoptic area as crucial for parental care. Unexpectedly, these neurons are characterized by the expression of molecules signaling satiety, such as calcitonin receptor and BRS3, and overlap with neurons involved in the reproductive behaviors of males but not females. A synthesis of comparative ecology and paleontology suggests an evolutionary scenario for mammalian parental care, possibly stemming from male‐biased guarding of offspring in basal vertebrates. The terrestrial transition of tetrapods led to prolonged egg retention in females and the emergence of amniotes, skewing care toward females. The nocturnal adaptation of Mesozoic mammalian ancestors reinforced maternal care for lactation and thermal regulation via endothermy, potentially introducing metabolic gate control in parenting neurons. The established maternal care may have served as the precursor for paternal and cooperative care in mammals and also fostered the development of group living, which may have further contributed to the emergence of empathy and altruism. These evolution‐informed working hypotheses require empirical validation, yet they offer promising avenues to investigate the neural underpinnings of mammalian social behaviors.

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Section: Parental Care Evolution In Vertebrates: Comparative Behavior...mentioning

confidence: 99%

Section: Parental Care Evolution In Vertebrates: Comparative Behavior...mentioning

confidence: 99%

Parental brain through time: The origin and development of the neural circuit of mammalian parenting

Kuroda,

Fukumitsu,

Kurachi

et al. 2024

Annals of the New York Academy of Sciences

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Palaeohistology of Macrospondylus bollensis (Crocodylomorpha: Thalattosuchia: Teleosauroidea) from the Posidonienschiefer Formation (Toarcian) of Germany, with insights into life history and ecology

Johnson,

Scheyer,

Canoville

et al. 2024

The Anatomical Record

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The Posidonienschiefer Formation of southern Germany has yielded an array of incredible fossil vertebrates. One of the best represented clades therein is Teleosauroidea, a successful thalattosuchian crocodylomorph group that dominated the coastlines. The most abundant teleosauroid, Macrospondylus bollensis, is known from a wide range of body sizes, making it an ideal taxon for histological and ontogenetic investigations. Previous studies examining thalattosuchian histology provide a basic understanding of bone microstructure in teleosauroids, but lack the taxonomic, stratigraphic, and ontogenetic control required to understand growth and palaeobiology within a species. Here, we examine the bone microstructure of three femora and one tibia from three different‐sized M. bollensis individuals. We also perform bone compactness analyses to evaluate for ontogenetic and ecological variation. Our results suggests that (1) the smallest specimen was a young, skeletally immature individual with well‐vascularized‐parallel‐fibered bone and limited remodeling in the midshaft periosteal cortex; (2) the intermediate specimen was skeletally immature at death, with vascularized parallel‐fibered bone tissue interrupted by at least 10 LAGs, but no clear external fundamental system (EFS), and rather extensive inner cortical bone remodeling; and (3) the largest specimen was skeletally mature, with parallel‐fibered bone tissue interrupted by numerous LAGs, a well‐developed EFS, and extensive remodeling in the deep cortex. Macrospondylus bollensis grew relatively regularly until reaching adult size, and global bone compactness values fall within the range reported for modern crocodylians. The lifestyle inference models used suggest that M. bollensis was well adapted for an aquatic environment but also retained some ability to move on land. Finally, both larger specimens display a peculiar, localized area of disorganized bone tissue interpreted as pathological.

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Extraembryonic Membranes and Placentation in the Mexican Snake Conopsis lineata

de Dios‐Arcos,

Villagrán‐SantaCruz

2024

Journal of Morphology

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Extraembryonic membranes provide protection, oxygen, water, and nutrients to developing embryos, and their study generates information on the origin of the terrestrial egg and the evolution of viviparity. In this research, the morphology of the extraembryonic membranes and the types of placentation in the viviparous snake Conopsis lineata are described through optical microscopy during early and late gestation. When embryos develop inside the uterus, they become surrounded by a thin eggshell membrane. In early gestation, during stages 16 and 18, the embryo is already surrounded by the amnion and the chorion, and in a small region by the chorioallantois, which is product of the contact between the chorion and the growing allantois. A trilaminar omphalopleure covers the yolk sac from the embryonic hemisphere to the level of the equator where the sinus terminalis is located, and from there a bilaminar omphalopleure extends into the abembryonic hemisphere. Thus, according to the relationship of these membranes with the uterine wall, the chorioplacenta, the choriovitelline placenta, and the chorioallantoic placenta are structured at the embryonic pole, while the omphaloplacenta is formed at the abembryonic pole. During late gestation (stages 35, 36, and 37), the uterus and allantois are highly vascularized. The allantois occupies most of the extraembryonic coelom and at the abembryonic pole, it contacts the omphaloplacenta and form the omphalallantoic placenta. This is the first description of all known placenta types in Squamata for a snake species member of the subfamily Colubrinae; where an eggshell membrane with 2.9 μm in width present throughout development is also evident. The structure of extraembryonic membranes in C. lineata is similar to that of other oviparous and viviparous squamate species. The above indicates not only homology, but also that the functional characteristics have been maintained throughout the evolution of the reproductive type.

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Extended embryo retention and viviparity in the first amniotes

Cited by 8 publications

References 73 publications

Parental brain through time: The origin and development of the neural circuit of mammalian parenting

Parental brain through time: The origin and development of the neural circuit of mammalian parenting

Palaeohistology of Macrospondylus bollensis (Crocodylomorpha: Thalattosuchia: Teleosauroidea) from the Posidonienschiefer Formation (Toarcian) of Germany, with insights into life history and ecology

Extraembryonic Membranes and Placentation in the Mexican Snake Conopsis lineata

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