ArticlePublisher preview available

Paternal nutrient provisioning during male pregnancy in the seahorse Hippocampus abdominalis

  • Charles Sturt University, Albury-Wodonga Campus
To read the full-text of this research, you can request a copy directly from the authors.

Abstract and Figures

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.
This content is subject to copyright. Terms and conditions apply.
1 3
Journal of Comparative Physiology B (2020) 190:547–556
Paternal nutrient provisioning duringmale pregnancy intheseahorse
Hippocampus abdominalis
ZoeM.G.Skalkos1· JamesU.VanDyke2· CamillaM.Whittington1
Received: 31 October 2019 / Revised: 22 April 2020 / Accepted: 18 June 2020 / Published online: 2 July 2020
© Springer-Verlag GmbH Germany, part of Springer Nature 2020
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 preg-
nancy 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 Hippocam-
pus 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.
Keywords Brood pouch· Dry mass· Embryo incubation· Lipid mass· Matrotrophy· Parental care· Paternal investment·
Patrotrophy· Syngnathid
Viviparity (live-bearing reproduction) has independently
evolved from oviparity (egg-laying) over 150 times in ver-
tebrates, including at least 13 independent origins in tel-
eost fishes, all of which exhibit embryo incubation inside
the female reproductive tract (Blackburn 2015). However,
the teleost family Syngnathidae, which includes seahorses,
sea dragons, and pipefishes, exhibits a unique form of male
pregnancy, in which pregnant males incubate embryos inside
a brood pouch (Stölting and Wilson 2007; Whittington and
Friesen 2020). Syngnathids are important models for evo-
lutionary research because they allow comparative analyses
of pregnancy independent of the female reproductive tract.
Such studies can determine whether the pathways regulating
female pregnancy are also co-opted in male pregnancy, or
whether novel pathways have evolved to support gestation.
Pregnant vertebrates exhibit a range of parental care
strategies for fetal nourishment during pregnancy (Black-
burn 1992). Lecithotrophy is defined as embryos relying
solely on the egg yolk for nutrients required for growth
and development, whilst matrotrophy describes species in
which embryos receive nutritional supplementation from
their mother during development, in addition to the yolk.
Lecithotrophy and matrotrophy represent two extremes of
a fetal nutritional continuum: species can be strictly lec-
ithotrophic, have incipient matrotrophy (primarily reliant
on yolk), or substantial matrotrophy (primarily reliant on
Communicated by Kathrin H. Dausmann.
Electronic supplementary material The online version of this
article (https :// 0-020-01289 -y) contains
supplementary material, which is available to authorized users.
* Camilla M. Whittington
1 School ofLife andEnvironmental Sciences, The University
ofSydney, Heydon-Laurence A08, Camperdown,
NSW2006, Australia
2 School ofMolecular Sciences, College ofScience, Health
andEngineering, La Trobe University, Wodonga, VIC,
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Fertilization and embryo development depend on interactions with multiple extracellular proteins (Saint-Dizier et al., 2020). Oviductin (OVGP1) is induced in the mammalian oviduct and endometrium, and is involved in sperm function, fertilization and embryo development (González-Brusi et al., 2020) Many genes in the reproductive transcriptome of pregnant male seahorses are homologous to those found in the uterus of female mammals (Whittington et al., 2015;Roth et al., 2020;Skalkos et al., 2020) Similar Oviductin (OVGP1) is among the top 30 most highly upregulated pregnancy-related genes in the seahorse pouch. It is involved in the regulation of adhesion and embryo protection (Whittington et al., 2015) Birth Via parturition and expulsion of the placenta (Aguilar and Mitchell, 2010) Release of free-living juveniles and expulsion of a pseudoplacenta (Ripley and Foran, 2006). ...
... The developing embryos are in close contact with the paternal goblet-like structures in seahorses and pipefishes, with there being highly vascularized pouch regions developing around the embryos (Ripley et al., 2010). These regions of the pouch have been viewed as functionally equivalent to a mammalian placenta (Whittington and Friesen, 2020), and have functions that result in providing the embryos with nutritional resources (Skalkos et al., 2020) and immunological capacities (Roth et al., 2012(Roth et al., , 2020Wu et al., 2021), as well as providing osmoregulatory functions and, importantly, a mechanism for gaseous exchange. In the following section, there is focus on the potential nutritive associations resulting from pouch functions and the embryos contained in the pouch, and on the description of two experiments that were conducted to evaluate (a) how the males' body condition before and during the gestational period not only affects embryonic development, but also (b)to determine whether there are specific periods during gestation when the quality of diet of the male is especially important for normal development. ...
... Results indicated the radiolabel was transferred to both the brood pouch and to embryos contained in the pouch. Furthermore, by using a completely different approach, Skalkos et al. (2020) reported that there was no significant loss of lipid mass between newly fertilized Hippocampus abdominalis eggs and neonates, an effect which was attributed to continued paternal provisioning of nutrients via the pouch. Fig. 3. Panel A depicts the standard lengths of newborn seahorses from four different treatment groups. ...
The Syngnathidae (seahorses and pipefishes) are a group of teleost fishes in which, uniquely, developing embryos are hosted throughout pregnancy by males, using a specialized brood pouch situated on the abdomen or tail. Seahorses have evolved the most advanced form of brood pouch, whereby zygotes and embryos are intimately connected to the host's circulatory system and also bathed in pouch fluid. The pouch is closed to the external environment and has to perform functions such as gaseous exchange, removal of waste and maintenance of appropriate osmotic conditions, much like the mammalian placenta. Fertilization of the oocytes occurs within the brood pouch, but unlike the mammalian situation the sperm transport mechanism from the ejaculatory duct towards the pouch is unclear, and the sperm: egg ratio (about 5:1) is possibly the least of any vertebrate. In this review, there is highlighting of the difficulty of elucidating the sperm transport mechanism, based on studies of Hippocampus kuda. The similarities between seahorse pouch function and the mammalian placenta have led to suggestions that the pouch provides important nutritional support for the developing embryos, supplementing the nutritional functions of the yolk sac provided by the oocytes. In this review, there is a description of the recent evidence in support of this hypothesis, and also emphasis, as in mammals, that embryonic development depends on nutritional support from the placenta-like pouch at important stages of the gestational period ("critical windows").
... Nerophinae, however, develop integument tissue, which swells in order to help hold and partially immerse the eggs (Carcupino et al., 2002) (Figure 1). Syngnathid research has highlighted genetic and morphological congruencies found between male and eutherian mammal reproductive systems Small et al., 2013;Stölting & Wilson, 2007;Whittington et al., 2015), with special interest being funnelled into immunological and nutrient transfer processes (Beemelmanns et al., 2019;Beemelmanns & Roth, 2017;Ripley & Foran, 2009;Roth et al., 2012Roth et al., , 2020Skalkos et al., 2020). Similarly, F I G U R E 1 Syngnathid brooding types: Nerophis ophidion (external egg-gluing/pregnancy), Syngnathus typhle (inverted brood pouch) and Hippocampus erectus (sealed brood pouch) several studies have characterised brood pouch tissue gene expression at multiple pregnancy stages in Hippocampus abdominalis (Lin et al., 2017;Whittington et al., 2015) and more recently two Syngnathus species (Keller & Roth, 2020;Roth et al., 2020;Small et al., 2013), showing transcriptional changes in pathway processes such as tissue remodelling, nutrient transport and immunity. ...
... As such, syngnathid species have evolved a number of brooding methods, which vary in tissue structure, morphological location and degree of investment (Carcupino et al., 2002;Stölting & Wilson, 2007;Wilson et al., 2001). Nutrient provisioning from father to offspring has been suggested in pouched syngnathid species (Kvarnemo et al., 2011;Ripley & Foran, 2009;Skalkos et al., 2020), while evidence of its presence in the more basal pregnancy forms of the Nerophinae are more tenuous (Berglund et al., 1986). Catabolic process upregulation in the concluding stages and the converse downregulation during its initiation periods suggest similar metabolic process fluctuations exist in male pregnancy as in mammals indicating that metabolic processes are a key requirement for the evolution of pregnancy. ...
... Excessive structural change in brooding tissue is not as pronounced in N. ophidion during pregnancy compared with pouched brooders, with the integument appearing consistent in form from egg deposition to egg hatching. Convincing evidence for the tissue's nutrient transfer and osmoregulation function, which characterises pouched syngnathid pregnancy (Kvarnemo et al., 2011;Ripley & Foran, 2009;Skalkos et al., 2020), is limited in nonpouched species (Berglund et al., 1986;Kronester-Frei, 1975). Considering the deductions made here regarding the lack of foeto-paternal immune connection, the scope for nutrient partitioning also appears implausible. ...
Full-text available
The unique male pregnancy in pipefishes and seahorses ranges from basic attachment (pouch-less species: Nerophinae) of maternal eggs to specialized internal gestation in pouched species (e.g. Syngnathus and Hippocampus) with many transitions in between. Due to this diversity, male pregnancy offers a unique platform for assessing physiological and molecular adaptations in pregnancy evolution. These insights will contribute to answering long-standing questions of why and how pregnancy evolved convergently in so many vertebrate systems. To understand the molecular congruencies and disparities in male pregnancy evolution, we compared transcriptome-wide differentially expressed genes in four syngnathid species, at four pregnancy stages (non-pregnant, early, late and parturition). Across all species and pregnancy forms, metabolic processes and immune dynamics defined pregnancy stages, especially pouched species shared expression features akin to female pregnancy. The observed downregulation of adaptive immune genes in early-stage pregnancy and its reversed upregulation during late/parturition in pouched species, most notably in Hippocampus, combined with directionless expression in the pouch-less species, suggests immune modulation to be restricted to pouched species that evolved placenta-like systems. We propose that increased feto-paternal intimacy in pouched syngnathids commands immune suppression processes in early gestation, and that the elevated immune response during parturition coincides with pouch opening and reduced progeny reliance. Immune response regulation in pouched species supports the recently described functional MHC II pathway loss as critical in male pregnancy evolution. The independent co-option of similar genes and pathways both in male and female pregnancy highlights immune modulation as crucial for the evolutionary establishment of pregnancy.
... A minority exhibit a complex, nutritive placenta that also transports significant quantities of nutrients to developing embryos. There are multiple origins of such placentae, including a single origin in mammals; six origins in squamate reptiles (all Scincidae); a single origin in amphibians (Hemiphractidae); one possible origin in sarcopterygians; six origins in teleosts (Anaplepinae, Embiotocidae, Goodeinae, Ophidiiformes (Bythitidae), Poeciliinae, Syngnathidae); and one (or possibly more) origin in chondrichthyans (Carcharhinidae, Hemigaleidae, Leptochariidae, Sphyrnidae and Triakidae) [1,8,[52][53][54] (figure 1). Other origins of complex, nutritive placentae are possible in relatively unstudied taxa or based on future taxonomic revisions. ...
... Whittington 2018, pers. obs.), and yet nutrients and respiratory gases are transported across a placenta in some species [52,146]. The morphological specializations at the attachment sites in the parent suggest that some physiological feto-paternal exchange occurs, but the biology of such placentae is largely unexplored. ...
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’.
... Reproductively mature male and female pot-bellied seahorses (H. abdominalis) were sourced from a captive bred population (Seahorse Australia, Tasmania, Australia) and maintained under previously described laboratory conditions [40]. All animal experimentation was undertaken with permission from the Animal Ethics Committee of the University of Sydney (2018/1302). ...
... Tissue proliferation results in the inner layer of the pouch becoming thicker and more diffuse as it surrounds and partially encloses developing embryos. Some of these changes are initiated soon after fertilisation, because H. abdominalis embryos become deeply embedded into the epithelial lining of the pouch within the first three days of pregnancy, to the point where some are completely enveloped by pouch tissue [7,40]. During pregnancy, large dark staining eosinophilic cells are present underlying the pouch epithelium. ...
Introduction Embryonic growth and development require efficient respiratory gas exchange. Internal incubation of developing young thus presents a significant physiological challenge, because respiratory gas diffusion to embryos is impeded by the additional barrier of parental tissue between the embryo and the environment. Therefore, live-bearing species exhibit a variety of adaptations facilitating respiratory gas exchange between the parent (usually the mother) and embryos. Syngnathid fishes are the only vertebrates to exhibit male pregnancy, allowing comparative studies of the biology and evolution of internal incubation of embryos, independent of the female reproductive tract. Here, we examine the fleshy, sealed, seahorse brood pouch, and provide the first quantification of structural changes to this gestational organ across pregnancy. Methods We used histological analysis and morphometrics to quantify the surface area for exchange across the brood pouch epithelium, and the structure of the vascular bed of the brood pouch. Results We show dramatic remodelling of gestational tissues as pregnancy progresses, including an increase in tortuosity of the gestational epithelium, an increase in capillary density, and a decrease in diffusion distance between capillaries and the pouch lumen. Discussion These changes produce an increased surface area and expansion of the vascular bed of the placenta that likely facilitates respiratory gas exchange. These changes mirror the remodelling of gestational tissue in viviparous amniotes and elasmobranchs, and provide further evidence of the convergence of adaptations to support pregnancy in live-bearing animals.
... A singular characteristic of seahorses is reproduction, in which females provide most nutrients to eggs whereas males take care and also supply nutrients to embryos developing from eggs transferred by females to their brood pouches (Carcupino et al., 2002;Skalkos et al., 2020;Wittington and Friesen, 2020). Mating and parturition are highly synchronized with egg maturation so that the release of eggs and newborn occur almost simultaneously and at similar time intervals, which vary depending on species, temperature, and breeder's diet (Lin et al., 2006(Lin et al., , 2007Planas et al., 2010;Otero-Ferrer et al., 2020). ...
... However, the effect of enhanced diets provided to H. kuda females on egg size was limited to the first spawning (Saavedra et al., 2014). From a nutritional and energetical point of view, the roles played by seahorse males and females in the production of eggs and neonates remain unclear, even though the contribution of males (and the effect of their diets) seems to be important in nutritional supply (Skalkos et al., 2020) and a key determinant in newborn quality (Otero-Ferrer et al., 2020). ...
Full-text available
Seahorses (Hippocampus spp.) are exceptional marine species considering their reproductive patterns and other features. Due to the iconic characteristics of these fishes, aquarium trade, and research efforts have increased in the last years. Consequently, novel rearing techniques have been developed; however, there is a need for improvements on a series of issues, namely reproduction success enhancement. The tropical species Hippocampus reidi is the most traded seahorse but many aspects of breeding and its impact on the quality of neonates are still poorly understood. In the present study, we assessed the effects of two pre-breeding diets on newborn quality and viability considering biochemical characteristics, energetic status, and ultrastructural aspects of muscular tissue. During the whole pre-breeding season (5 months), the breeders were fed on one of the following diets: M0 (adult non-enriched Artemia) and M5 (adult non-enriched Artemia + mysidaceans). From the onset of the reproduction period, all breeders were fed for 6 months on diet M5. Breeding success and energetic status (ATP, total adenylic nucleotides, AEC, and NAD) of newborns resulted considerably enhanced in treatment M5. However, initial differences in neonates quality did not affect further newborn performance (survival and growth until day 7 after male's pouch release) while gaining access to high-quality preys (copepods). Besides, morphological alterations in muscle tissue were not observed. The reproduction in the species followed a capital-income continuum pattern characterized by an initial mixed capital-income period (until 70-100 days since the onset of the breeding season) followed by an income breeding period with progressive exhaustion of body reserves, especially in M0-newborns. Interestingly, the effects of pre-breeding diets were also noticed in the second half of the breeding period. Our results seemed to indicate that the requirements in essential fatty acids in H. reidi are lower than in other seahorse species (e.g., Hippocampus guttulatus). Globally, the results achieved revealed that high-quality pre-breeding diets enhanced reproduction success and would likely result advantageous to improve newborn endurance in conditions of moderate starvation or sub-optimal feeding.
... It is hypothesized to be functionally similar to the uterus of amniotes. Indeed, a recent study provided evidence that the pouch is critical for sustaining the lipid mass of embryos (Skalkos, Van Dyke, & Whittington, 2020). Another study characterizing the transcriptomes of developing pouches of big-belly seahorse (Hippocampus abdominalis) identified many upregulated genes that are also upregulated during mammalian pregnancy (Whittington, Griffith, Qi, Thompson, & Wilson, 2015). ...
Full-text available
Seahorses belong to the teleost family Syngathidae that evolved a distinct body plan and unique male pregnancy compared to other teleosts. As a classic model for studying evolution of viviparity and sexual selection of teleosts, seahorse species still lack a publicly available high-quality reference genome. Here we generated the genome assembly of big-belly seahorse, Hippocampus abdominalis with the long-read and Hi-C technologies. We managed to place over 99% of the total length of 444.7Mb of assembled genome into 21 linkage groups with almost no gaps. We reconstructed a phylogenomic tree with the big-belly seahorse genome and other representative Syngnathidae and teleost species. We also reconstructed the historical population dynamics of four representative Syngnathidae species. We found the gene families that underwent expansion or contraction in the Syngnathidae ancestor were enriched for immune-related or ion transporter gene ontology terms. Many of these genes were also reported to show a dynamic expression pattern during the pregnancy stages of H. abdominalis. We also identified putative positively selected genes in the Syngnathidae ancestor or in H. abdominalis, whose mouse mutants are enriched for abnormal craniofacial and limb morphological phenotypes. Overall, our work provides an important genome resource for evolutionary and developmental studies of seahorse species, and candidate genes for future experimental works.
Full-text available
Background: Syngnathids are a highly derived and diverse fish clade comprising the pipefishes, pipe-horses, and seahorses. They are characterized by a plethora of iconic traits that increasingly capture the attention of biologists, including geneticists, ecologists, and developmental biologists. The current understanding of the origins of their derived body plan is, however, hampered by incomplete and limited descriptions of the early syngnathid ontogeny. Results: We provide a comprehensive description of the development of Nerophis ophidion, Syngnathus typhle, and Hippocampus erectus from early cleavage stages to release from the male brooding organ and beyond, including juvenile development. We comparatively describe skeletogenesis with a particular focus on dermal bony plates, the snout-like jaw morphology, and appendages. Conclusions: This most comprehensive and detailed account of syngnathid development to date suggests that convergent phenotypes (e.g., reduction and loss of the caudal fins), likely arose by distinct ontogenetic means in pipefishes and seahorses. Comparison of the ontogenetic trajectories of S. typhle and H. erectus provides indications that characteristic features of the seahorse body plan result from developmental truncation. Altogether, this work provides a valuable resource and framework for future research to understand the evolution of the outlandish syngnathid morphology from a developmental perspective.
Introduction Syngnathids (seahorses, pipefishes and seadragons) are among the few vertebrates that display male pregnancy. During seahorse pregnancy, males incubate developing embryos embedded in a placenta within a fleshy brood pouch, before expelling fully developed neonates at parturition. The mechanisms underpinning seahorse parturition are poorly understood. Methods We examined the morphology of the brood pouch using microcomputed tomography and histological techniques, in combination with physiological assays, to examine how male pot-bellied seahorses (Hippocampus abdominalis) control labour. In female-pregnant vertebrates, nonapeptide hormones (such as vasopressin- and oxytocin-like hormones) produce contractions of gestational smooth muscle to produce labour. Results Histological analysis of the seahorse brood pouch reveals only scattered small smooth muscle bundles in the brood pouch, and in-vitro application of isotocin (a teleost nonapeptide hormone) to the brood pouch do not produce measurable muscle contractions. Micro-computed tomography shows differences in size and orientation of the anal fin assembly between male and female pot-bellied seahorses, and histological analysis reveals large skeletal muscle bundles attached to the anal fin bones at the male brood pouch opening. Discussion We conclude that seahorse parturition may be facilitated by contraction of these muscles, which, in combination with body movements, serves to gape open the pouch and expel the neonates. Future biomechanical studies are needed to test this hypothesis.
Introduction Fishes of the Syngnathidae family are unique in having male pregnancy: males receive eggs from females and egg development occurs in the male brood pouch that diverged during evolution. The family is divided into two subfamilies: Nerophinae and Syngnathinae. Methods We compared histologically five types of the brood pouch in Syngnathinae: an open pouch without skinfolds (alligator pipefish); an open pouch with skinfolds (messmate pipefish); a closed pouch with skinfolds (seaweed pipefish); and closed pouches with a sac-like pouch on the tail (pot-bellied seahorse) or within a body cavity (Japanese pygmy seahorse). Results Histological observations revealed that all the examined species possess vascular egg compartments during the brooding period. The present immunohistochemical study revealed that the pregnant egg compartment epithelium grows thin in both open and closed pouches. The placenta of open and closed pouches is composed of dermis and reticulin fibers, respectively. The closed pouch placenta is a flexible and moist tissue, suitable for substance transport between the father and embryos through the epithelium and blood vessels and responsible for supplying nutrition and removing waste. Discussion These results suggest that the basic egg incubation structures were established at an early stage of Syngnathinae evolution. On the other hand, it is likely that the innovation of tissue structure, where dermis was replaced with reticular fibers, occurred in closed brood pouches to regulate the pregnant pouch environment. The present study presents the morphological evolutionary pathway of the brood pouch in Syngnathinae, providing a basis for further molecular-level evolutionary studies.
Full-text available
Sex role reversal is not uncommon in the animal kingdom but is taken to the extreme by the Syngnathidae, in which male pregnancy is one of the most astonishing idiosyncrasies. However, critical and time-dependent environmental effects on developing embryos, such as those extensively studied in mammalian pregnancy, have not been investigated in the male pregnancy context. Here, we tested the hypothesis that seahorse pregnancy is subject to 'critical windows' of environmental sensitivity by feeding male long-snouted seahorses (Hippocampus reidi) a diet deficient in polyunsaturated fatty acids during specific periods before and during pregnancy. Despite embryos being nourished principally by maternally supplied yolk, we found that offspring morphology, fatty acid composition, and gene expression profiles were influenced by paternal diet in a manner that depended critically on the timing of manipulation. Specifically, reception of a diet deficient in polyunsaturated fatty acids in the days preceeding pregnancy resulted in smaller newborn offspring, while the same diet administered towards the end of pregnancy resulted in substantial alterations to newborn gene expression and elongation of the snout at 10-days old. Although paternal diet did not affect 10-day survival, the observed morphological alterations in some cases could have important fitness consequences in the face of natural selective pressures such as predation and food availability. Our results demonstrate that, under male pregnancy, fine-scale temporal variation in parental diet quality and subsequent critical window effects should not be overlooked as determinants of developing offspring fitness.
Full-text available
Developmental plasticity in offspring phenotype occurs as a result of the environmental conditions embryos experience during development. The nutritional environment provided to a fetus is an important source of developmental plasticity. Reptiles are a particularly interesting system to study this plasticity because of their varied routes of maternal nutrient allocation to reproduction. Most reptiles provide their offspring with all or most of the nutrients they require in egg yolk (lecithotrophy) while viviparous reptiles also provide their offspring with nutrients via a placenta (placentotrophy). We review the ways in which both lecithotrophy and placentotrophy can lead to differences in the nutrients embryonic reptiles receive, and discuss how these differences lead to developmental plasticity in offspring phenotype. We finish by reviewing the ecological and conservation consequences of nutritional‐driven developmental plasticity in reptiles. If nutritional‐driven developmental plasticity has fitness consequences, then understanding the basis of this plasticity has exciting potential to identify how reptile recruitment is affected by environmental changes in food supply. Such knowledge is critical to our ability to protect taxa threatened by environmental change.
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.
Reproducing sharks must provide their offspring with an adequate supply of nutrients to complete embryonic development. In oviparous (egg-laying) sharks, offspring develop outside the mother, and all the nutrients required for embryonic growth are contained in the egg yolk. Conversely, in viviparous (live-bearing) sharks, embryonic development is completed inside the mother, providing offspring with the opportunity to receive supplementary embryonic nourishment, known as matrotrophy. Viviparous sharks exhibit nearly all forms of matrotrophy known in vertebrates, including a yolk-sac placenta, which involves several significant ontogenetic modifications to fetal and maternal tissues. The selective pressures that have driven the evolution of complex placentas in some shark species, but not in others, are unresolved. Herein we review the mechanisms of reproductive allocation and placental diversity in sharks, and consider the application of both adaptive and conflict hypotheses for the evolution of placental nutrient provisioning. Both have likely played roles in placental evolution in sharks, perhaps at different times in evolutionary history. Finally, we recommend sharks as an outstanding model system to investigate the evolution of placentas and mechanisms for fetal nutrition during pregnancy in vertebrates.
The family Syngnathidae is a large and diverse clade of morphologically unique bony fishes, with 57 genera and 300 described species of seahorses, pipefishes, pipehorses, and seadragons. They primarily inhabit shallow coastal waters in temperate and tropical oceans, and are characterized by a fused jaw, male brooding, and extraordinary crypsis. Phylogenetic relationships within the Syngnathidae remain poorly resolved due to lack of generic taxon sampling, few diagnostic morphological characters, and limited molecular data. The phylogenetic placement of the threatened, commercially exploited seahorses remains a topic of intense interest, with conflicting topologies based on morphology and predominantly mitochondrial genetic data. In this study, we integrate eight nuclear and mitochondrial markers and 17 morphological characters to investigate the phylogenetic structure of the family Syngnathidae at the generic level. We include 91 syngnathid species representing 48 of the 57 recognized genera, all major ocean basins, and a broad array of temperate and tropical habitats including rocky and coral reefs, sand and silt, mangroves, seagrass beds, estuaries, and rivers. Maximum likelihood and Bayesian analyses of 5160 bp from eight loci produced high congruence among alternate topologies, defining well-supported and sometimes novel clades. We present a hypothesis that confirms a deep phylogenetic split between lineages with trunk- or tail-brood pouch placement, and provides significant new insights into the morphological evolution and biogeography of this highly derived fish clade. Based on the fundamental division between lineages - the tail brooding “Urophori” and the trunk brooding “Gastrophori” - we propose a revision of Syngnathidae classification into only two subfamilies: the Nerophinae and the Syngnathinae. We find support for distinct principal clades within the trunk-brooders and tail-brooders, the latter of which include seahorses, seadragons, independent lineages of pipehorses, and clades that originated in Southern Australia and the Western Atlantic. We suggest the seahorse genus Hippocampus is of Indo-Pacific origin and its sister clade is an unexpected grouping of several morphologically disparate Indo-Pacific genera, including the Pacific pygmy pipehorses. Taxonomic revision is required for multiple genera, particularly to reflect deep evolutionary splits in nominal lineages from the Atlantic versus the Indo-Pacific.
Seahorses are teleosts that have evolved a brood pouch analogous to the mammalian uterus. Attempts to breed the fish in captivity - a prerequisite for aquaculture and conservation of this species - are hampered by many unanswered questions regarding its general reproductive biology, especially its gestation. To determine if the hormones secreted by gestating female mammals are the same hormones involved in the unique pattern of male gestation in the seahorse (Hippocampus barbouri Jordan and Richardson 1908), the site of synthesis of hormones apparently involved in male gestation was localized by immunohistochemistry, and the presence of 3 β-hydroxysteroid dehydrogenase was investigated through enzyme histochemical analysis. Ultrastructure of the brood epithelium was further analyzed using transmission electron microscope. Results showed that both progesterone and estradiol are involved in gestation in the male seahorse. Synthesis of estrogen and progesterone was observed in the testis, brood pouch and interrenal tissues of gravid seahorse. Increase in the number and size of mitochondria was noted in gravid pouch.
Recently ovulated eggs and newborn of two species of viviparous reptiles, Gerrhonotus coeruleus (Sauria: Anguidae) and Nerodia rhombifera (Serpentes: Colubridae), were analyzed for organic (nitrogen, lipid) and inorganic (total ash, sodium, potassium, calcium, magnesium) content. Eggs contain 41%-48% water, 46%-56% organic matter, and 3%-5% inorganic salts. Total protein (based on measurement of nitrogen) is higher in egg yolk than total lipid. Analysis of the composition of newborn indicates that eggs of both species gain water and lose dry mass during development. Most of the dry mass loss is a reduction in amount of lipid, presumably due to catabolism. There was no substantial change in total nitrogen in newborn compared to yolk. There was evidence of an extravitellogenic source of mineral ions in both species. Newborn G. coeruleus have a substantially higher ash content than recently ovulated eggs. Although total ash was not higher, newborn N. rhombifera contain more sodium and potassium than eggs. Transplacental transfer of inorganic material occurs in both species but to a greater degree in Gerrhonotus than Nerodia.
This chapter discusses the maternal–embryonic relationship in viviparous fishes. Viviparity is a highly successful mode of reproduction that has evolved independently many times and with many variations in widely separated taxonomic groups. It occurs in all classes of vertebrates, except birds, and among many different groups of invertebrates. Initial steps in the evolution of viviparity involved a shift from external to internal fertilization and the retention of fertilized eggs in the female reproductive system. The osmoregulation of early embryos can be accomplished more efficiently and with less expenditure of embryonic energy in a maternally controlled uterine environment, but as development progresses to term, the embryos presumably acquire an increasing degree of osmoregulatory independence. Available evidence suggests that maternal regulation of the osmotic and chemical environment of the embryo also confers a selective advantage on viviparous teleosts. The uterine wall of most viviparous elasmobranchs and the coelocanth both delimits and defines the embryonic environment. The most spectacular maternal specializations for uterine gestation involve the uterine wall and involve (1) the amplification of the surface area in the form of folds, villi, or trophonemata; (2) the production of histotrophe or uterine milk’ (3) the compartmentalization of embryos; and (4) the development of placental attachment sites.