ABSTRACT
The seahorses, pipefishes and seadragons (Syngnathidae) are among the few vertebrates in which pregnant males incubate developing embryos. Syngnathids are popular in studies of sexual ...selection, sex‐role reversal, and reproductive trade‐offs, and are now emerging as valuable comparative models for the study of the biology and evolution of reproductive complexity. These fish offer the opportunity to examine the physiology, behavioural implications, and evolutionary origins of embryo incubation, independent of the female reproductive tract and female hormonal milieu. Such studies allow us to examine flexibility in regulatory systems, by determining whether the pathways underpinning female pregnancy are also co‐opted in incubating males, or whether novel pathways have evolved in response to the common challenges imposed by incubating developing embryos and releasing live young. The Syngnathidae are also ideal for studies of the evolution of reproductive complexity, because they exhibit multiple parallel origins of complex reproductive phenotypes. Here we assay the taxonomic distribution of syngnathid parity mode, examine the selective pressures that may have led to the emergence of male pregnancy, describe the biology of syngnathid reproduction, and highlight pressing areas for future research. Experimental tests of a range of hypotheses, including many generated with genomic tools, are required to inform overarching theories about the fitness implications of pregnancy and the evolution of male pregnancy. Such information will be widely applicable to our understanding of fundamental reproductive and evolutionary processes in animals.
Embryonic specializations for vertebrate placentation Whittington, Camilla M.; Buddle, Alice L.; Griffith, Oliver W. ...
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
12/2022, Letnik:
377, Številka:
1865
Journal Article
Recenzirano
Odprti dostop
The vertebrate placenta, a close association of fetal and parental tissue for physiological exchange, has evolved independently in sharks, teleost fishes, coelacanths, amphibians, squamate reptiles ...and mammals. This transient organ forms during pregnancy and is an important contributor to embryonic development in both viviparous and oviparous, brooding species. Placentae may be involved in transport of respiratory gases, wastes, immune molecules, hormones and nutrients. Depending on the taxon, the embryonic portion of the placenta is comprised of either extraembryonic membranes (yolk sac or chorioallantois) or temporary embryonic tissues derived via hypertrophy of pericardium, gill epithelium, gut, tails or fins. These membranes and tissues have been recruited convergently into placentae in several lineages. Here, we highlight the diversity and common features of embryonic tissues involved in vertebrate placentation and suggest future studies that will provide new knowledge about the evolution of pregnancy.
This article is part of the theme issue ‘Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom’.
Viviparity (live birth) has evolved more than 150 times in vertebrates, and represents an excellent model system for studying the evolution of complex traits. There are at least 23 independent ...origins of viviparity in fishes, with syngnathid fishes (seahorses and pipefish) unique in exhibiting male pregnancy. Male seahorses and pipefish have evolved specialized brooding pouches that provide protection, gas exchange, osmoregulation, and limited nutrient provisioning to developing embryos. Pouch structures differ widely across the Syngnathidae, offering an ideal opportunity to study the evolution of reproductive complexity. However, the physiological and genetic changes facilitating male pregnancy are largely unknown. We used transcriptome profiling to examine pouch gene expression at successive gestational stages in a syngnathid with the most complex brood pouch morphology, the seahorse Hippocampus abdominalis. Using a unique time-calibrated RNA-seq data set including brood pouch at key stages of embryonic development, we identified transcriptional changes associated with brood pouch remodeling, nutrient and waste transport, gas exchange, osmoregulation, and immunological protection of developing embryos at conception, development and parturition. Key seahorse transcripts share homology with genes of reproductive function in pregnant mammals, reptiles, and other live-bearing fish, suggesting a common toolkit of genes regulating pregnancy in divergent evolutionary lineages.
ABSTRACT
How innovations such as vision, flight and pregnancy evolve is a central question in evolutionary biology. Examination of transitional (intermediate) forms of these traits can help address ...this question, but these intermediate phenotypes are very rare in extant species. Here we explore the biology and evolution of transitional forms of pregnancy that are midway between the ancestral state of oviparity (egg‐laying) and the derived state, viviparity (live birth). Transitional forms of pregnancy occur in only three vertebrates, all of which are lizard species that also display intraspecific variation in reproductive phenotype. In these lizards (Lerista bougainvillii, Saiphos equalis, and Zootoca vivipara), geographic variation of three reproductive forms occurs within a single species: oviparity, viviparity, and a transitional form of pregnancy. This phenomenon offers the valuable prospect of watching ‘evolution in action’. In these species, it is possible to conduct comparative research using different reproductive forms that are not confounded by speciation, and are of relatively recent origin. We identify major proximate and ultimate questions that can be addressed in these species, and the genetic and genomic tools that can help us understand how transitional forms of pregnancy are produced, despite predicted fitness costs. We argue that these taxa represent an excellent prospect for understanding the major evolutionary shift between egg‐laying and live birth, which is a fundamental innovation in the history of animals.
Highlights • Prolactin has a broad range of functions but is poorly characterised in non-mammals. • PRL plays an important role in reproduction in mammals, birds, reptiles, and fish. • Functions ...include reproductive cycling, pregnancy, brood care and feeding. • Both observational and manipulative research is necessary to clarify PRL function. • Further progress requires a solid foundation in a small number of well-studied models.
Facultative changes in parity mode (oviparity to viviparity and vice versa) are rare in vertebrates, yet offer fascinating opportunities to investigate the role of reproductive lability in parity ...mode evolution. Here, we report apparent facultative oviparity by a viviparous female of the bimodally reproductive skink Saiphos equalis-the first report of different parity modes within a vertebrate clutch. Eggs oviposited facultatively possess shell characteristics of both viviparous and oviparous S. equalis, demonstrating that egg coverings for viviparous embryos are produced by the same machinery as those for oviparous individuals. Since selection may act in either direction when viviparity has evolved recently, squamate reproductive lability may confer a selective advantage. We suggest that facultative oviparity is a viable reproductive strategy for S. equalis and that squamate reproductive lability is more evolutionarily significant than previously acknowledged.
Structural and physiological changes in the female reproductive system underlie the origins of pregnancy in multiple vertebrate lineages. In mammals, the glandular portion of the lower reproductive ...tract has transformed into a structure specialized for supporting fetal development. These specializations range from relatively simple maternal nutrient provisioning in egg-laying monotremes to an elaborate suite of traits that support intimate maternal-fetal interactions in Eutherians. Among these traits are the maternal decidua and fetal component of the placenta, but there is considerable uncertainty about how these structures evolved. Previously, we showed that changes in uterine gene expression contributes to several evolutionary innovations during the origins of pregnancy (Mika et al., 2021b). Here, we reconstruct the evolution of entire transcriptomes (‘ancestral transcriptome reconstruction’) and show that maternal gene expression profiles are correlated with degree of placental invasion. These results indicate that an epitheliochorial-like placenta evolved early in the mammalian stem-lineage and that the ancestor of Eutherians had a hemochorial placenta, and suggest maternal control of placental invasiveness. These data resolve major transitions in the evolution of pregnancy and indicate that ancestral transcriptome reconstruction can be used to study the function of ancestral cell, tissue, and organ systems.
Abstract
The repeated evolution of the same traits in distantly related groups (convergent evolution) raises a key question in evolutionary biology: do the same genes underpin convergent phenotypes? ...Here, we explore one such trait, viviparity (live birth), which, qualitative studies suggest, may indeed have evolved via genetic convergence. There are >150 independent origins of live birth in vertebrates, providing a uniquely powerful system to test the mechanisms underpinning convergence in morphology, physiology, and/or gene recruitment during pregnancy. We compared transcriptomic data from eight vertebrates (lizards, mammals, sharks) that gestate embryos within the uterus. Since many previous studies detected qualitative similarities in gene use during independent origins of pregnancy, we expected to find significant overlap in gene use in viviparous taxa. However, we found no more overlap in uterine gene expression associated with viviparity than we would expect by chance alone. Each viviparous lineage exhibits the same core set of uterine physiological functions. Yet, contrary to prevailing assumptions about this trait, we find that none of the same genes are differentially expressed in all viviparous lineages, or even in all viviparous amniote lineages. Therefore, across distantly related vertebrates, different genes have been recruited to support the morphological and physiological changes required for successful pregnancy. We conclude that redundancies in gene function have enabled the repeated evolution of viviparity through recruitment of different genes from genomic “toolboxes”, which are uniquely constrained by the ancestries of each lineage.
Vertebrates that incubate embryos on or within the body cavity exhibit diverse strategies to provide nutrients to developing embryos, ranging from lecithotrophy (solely yolk-provided nutrition) to ...substantial matrotrophy (supplemental nutrients from the mother before birth). Syngnathid fishes (seahorses, pipefishes and sea dragons) are the only vertebrates to exhibit male pregnancy. Therefore, they provide a unique opportunity for comparative evolutionary research, in examining pregnancy independent of the female reproductive tract. Here, we tested the hypothesis that the most complex form of syngnathid pregnancy involves nutrient transport from father to offspring. We compared the dry masses of newly fertilised
Hippocampus abdominalis
eggs with those of fully developed neonates to derive a patrotrophy index. The patrotrophy index of
H. abdominalis
was 1, indicating paternal nutrient supplementation to embryos during gestation. We also measured the lipid content of newly fertilised eggs and neonates and found that there was no significant decrease in lipid mass during embryonic development. Since lipids are likely to be the main source of energy during embryonic development, our results suggest that lipid yolk reserves being depleted by embryonic metabolism are replaced by the brooding father. The results of our study support the hypothesis that nutrient transport occurs in the most advanced form of male pregnancy in vertebrates.
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