Evolution of placentotrophy: Using viviparous sharks as a model to understand vertebrate placental evolution

ArticleinMarine and Freshwater Research · January 2018with 330 Reads 
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Abstract
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.

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    ... The dwarf ornate wobbegong (Orectolobus ornatus) is a species of carpet shark (Orectolobiformes; Compagno, Dando, & Fowler, 2005). Within the order Orectolobiformes, there are both, oviparous and viviparous species (Buddle et al., 2018). Therefore, species of Orectolobiformes provide an important model system for testing hypotheses about the transition from oviparity to viviparity in sharks (Blackburn, 2015;Buddle et al., 2018). ...
    ... Within the order Orectolobiformes, there are both, oviparous and viviparous species (Buddle et al., 2018). Therefore, species of Orectolobiformes provide an important model system for testing hypotheses about the transition from oviparity to viviparity in sharks (Blackburn, 2015;Buddle et al., 2018). ...
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    Embryos of the viviparous dwarf ornate wobbegong shark (Orectolobus ornatus) develop without a placenta, unattached to the uterine wall of their mother. Here, we present the first light microscopy study of the uterus of O. ornatus throughout pregnancy. At the beginning of pregnancy, the uterine luminal epithelium and underlying connective tissue become folded to form uterine ridges. By mid to late pregnancy, the luminal surface is extensively folded and long luminal uterine villi are abundant. Compared to the nonpregnant uterus, uterine vasculature is increased during pregnancy. Additionally, as pregnancy progresses the uterine epithelium is attenuated so that there is minimal uterine tissue separating large maternal blood vessels from the fluid that surrounds developing embryos. We conclude that the uterus of O. ornatus undergoes an extensive morphological transformation during pregnancy. These uterine modifications likely support developing embryos via embryonic respiratory gas exchange, waste removal, water balance, and mineral transfer. The uterus of the viviparous dwarf ornate wobbegong (Orectolobus ornatus) undergoes a morphological transformation during pregnancy. This image shows the uterine wall of a late pregnant female that contains embryos just prior to birth. The extensive vascularization by the increase in blood vessels in the long uterine villi (v), uterine connective tissue and muscle layers, likely support embryonic gas exchange, waste removal, water balance, and mineral transfer.
  • ... The evolution of this type of reproductive complexity is currently of broad interest to evolutionary biologists (e.g. Griffith et al., 2015;Pyron, 2015;Blackburn, 2015b;Buddle et al., 2018;Cornetti et al., 2018;Gao et al., 2019;Foster et al., 2020). ...
    ... guppies, mollies, platies and swordtails) and is based on the mass lost during development in oviparous (solely lecithotrophic) species. However, MI thresholds are widely debated, as the amount of nutrients transferred may be small, and the metabolic cost of embryonic development (and thus mass lost as metabolic wastes and heat) may differ among species (Frazer, Ellis & Huveneers, 2012;Buddle et al., 2018). The egg size and the degree of patrotrophy have been quantified for very few syngnathids (Ripley & Foran, 2009). ...
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  • ... Here, we test the hypothesis that male seahorses transport nutrients to developing embryos. Deriving a Matrotrophy Index (MI) is an important technique used to investigate maternal transfer of nutrients in viviparous fish and reptiles (Buddle et al. 2018;e.g. Reznick et al. 2002;Stewart 2013;Thompson et al. 2000;Turcotte et al. 2008). ...
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  • ... Elasmobranchs exhibit diverse reproductive modes, including nutrient provisioning through yolk (lecithotrophy), placenta (placentotrophy), ova (oophagy), embryonic ingestion of siblings (adelphophagy), embryotrophe (embryotrophy) and secretion of lipid-rich uterine fluid (histotrophy), or a combination of the above strategies (Wourms 1981, Hamlett et al. 2005. While numerous studies have anatomically described these reproductive strategies through morphological examination (references in Conrath & Musick 2012, Buddle et al. 2018, several important questions remain unanswered over how these reproductive strategies and the degree of maternal investment associated with them affect offspring fitness. ...
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  • ... In viviparous taxa, conflict and competition can arise between sibling embryos in the womb, mother and embryos, and maternal and paternal genomes within individual embryos (Zeh & Zeh 2000). Cannibalism among shark species in the phase of embryo is widely known (Buddle et al 2019). Such kind of intra-and inter-genomic conflicts result in continual and long-term antagonistic coevolution, thereby accelerating interpopulation post-zygotic isolation (Zeh & Zeh 2000). ...
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  • ... El intervalo de tallas observadas en neonatos fue muy similar al registrado en el Golfo de . El neonato más pequeño registrado en este estudio, está dentro de la talla media descrita para embriones completamente desarrollados (40 -50 cm) White et al., 2008 Buddle et al., 2018). ...
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    The reproductive biology of the shortfin mako shark, Isurus oxyrinchus Rafinesque, 1810 is described based on 750 females and 498 males (including 24 pregnant females) collected from Oct. 2001 to Mar. 2004 at Nanfangao fish market, northeastern Taiwan. The size at maturity was 210 and 278 cm total length (TL) for males and females, respectively. Size at birth was approximately 74 cm TL, and litter size ranged from 4 to 15, with a mean of 11.1; there was no increase in litter size with maternal size. The mating period is from Jan. to June, and pupping occurs between Dec. and July. We estimated the gestation period to be 23-25 mo and the corresponding reproductive cycle to be 3 yr. Embryos are nourished by oophagy, and develop a grossly distended abdomen as their "yolk stomach" fills with ova. Small embryos, 15-22 cm in TL, are able to swallow egg capsules, but do not yet have teeth. Teeth form in embryos at about 26 cm TL, and they begin shedding at 42 cm TL. A subsequent set of teeth are formed at 61 cm TL. Uterine cannibalism (adelphophagy) occurs occasionally, most likely due to unequal embryonic growth.
  • Article
    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.
  • Article
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    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. © The Author 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
  • Article
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    Multiple paternity appears to be a common trait of elasmobranch mating systems, with its occurrence likely driven by convenience, due to females seeking to minimize the stress of male harassment. Here we use molecular markers to analyse the frequency of multiple paternity in two related viviparous sharks, Mustelus mustelus and Mustelus punctulatus. We first applied molecular methods to assign pregnant females, embryos and additional reference adults (N = 792) to one of the two species. Paternity analysis was performed using a total of 9 polymorphic microsatellites on 19 females and 204 embryos of M. mustelus, and on 13 females and 303 embryos of M. punctulatus. Multiple paternity occurs in both species, with 47% of M. mustelus and 54% of M. punctulatus litters sired by at least two fathers. Female fecundity is not influenced by multiple mating and in 56% of polyandrous litters paternity is skewed, with one male siring most of the pups. Genetic analyses also revealed hybridization between the two species, with a M. punctulatus female bearing pups sired by a M. mustelus male. The frequency of polyandrous litters in these species is consistent with aspects of their reproductive biology, such as synchronous ovulation and possible occurrence of breeding aggregations.
  • Article
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    In many viviparous vertebrates, pregnant females sustain their developing embryos and provide them with nutrients by means of placentas and a diversity of other types of specializations. With this article, we introduce a virtual (online) issue of the Journal of Morphology that presents 12 recent papers on fetal maintenance in viviparous vertebrates. We also outline the history of research in this area and document the central role of morphology in helping to explain the function and evolution of specializations for fetal nutrition. This virtual issue of the Journal of Morphology is an outgrowth of a symposium held under auspices of the International Congress of Vertebrate Morphology. The included papers reflect a diversity of taxa, research methods, and biological issues. To celebrate the publication of this virtual issue of the Journal of Morphology, the publisher is making freely available to readers a number of other relevant papers published in the journal over the past 128 years. J. Morphol., 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
  • Article
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    In placentotrophic viviparous reptiles, pregnant females deliver nutrients to their developing fetuses by diverse morphological specializations that reflect independent evolutionary origins. A survey of these specializations reveals a major emphasis on histotrophy (uterine secretion and fetal absorption) rather than hemotrophy (transfer between maternal and fetal blood streams). Of available hypotheses for the prevalence of histotrophic transfer, the most promising derives insights from the theoretical parent-offspring conflict over nutrient investment. I suggest that histotrophy gives pregnant females greater control over nutrient synthesis, storage, and delivery than hemotrophic transfer, reflecting maternal preeminence in any potential parent-offspring competition over nutrient investment. One lizard species shows invasive ovo-implantation and direct contact between fetal tissues and maternal blood vessels, potentially conferring control over nutrient transfer to the embryo. Future research on squamates will benefit from application of parent-offspring conflict theory to the transition from incipient to substantial matrotrophy, as well as by testing theory-derived predictions on both facultatively and highly placentotrophic forms. J. Exp. Zool. (Mol. Dev. Evol.) 9999B: 1-17, 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
  • Article
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    To understand evolutionary transformations it is necessary to identify the character states of extinct ancestors. Ancestral character state reconstruction is inherently difficult because it requires an accurate phylogeny, character state data, and a statistical model of transition rates and is fundamentally constrained by missing data such as extinct taxa. We argue that model based ancestral character state reconstruction should be used to generate hypotheses but should not be considered an analytical endpoint. Using the evolution of viviparity and reversals to oviparity in squamates as a case study, we show how anatomical, physiological, and ecological data can be used to evaluate hypotheses about evolutionary transitions. The evolution of squamate viviparity requires changes to the timing of reproductive events and the successive loss of features responsible for building an eggshell. A reversal to oviparity requires that those lost traits re-evolve. We argue that the re-evolution of oviparity is inherently more difficult than the reverse. We outline how the inviability of intermediate phenotypes might present physiological barriers to reversals from viviparity to oviparity. Finally, we show that ecological data supports an oviparous ancestral state for squamates and multiple transitions to viviparity. In summary, we conclude that the first squamates were oviparous, that frequent transitions to viviparity have occurred, and that reversals to oviparity in viviparous lineages either have not occurred or are exceedingly rare. As this evidence supports conclusions that differ from previous ancestral state reconstructions, our paper highlights the importance of incorporating biological evidence to evaluate model-generated hypotheses. J. Exp. Zool. (Mol. Dev. Evol.) 00B: 1-11, 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
  • Angiogenesis (blood vessel growth), a key process of mammalian pregnancy, facilitates gas exchange and nutrient transport between the mother and the embryo and is regulated by a suite of growth factors. Vascular endothelial growth factor (VEGF) is crucial to this process in pregnant mammals and potentially pregnant squamates (lizards and snakes), as we investigate here. VEGF111 , an unusual and potent angiogenic splice variant of VEGF, increases its expression during pregnancy in the uterus of a viviparous lizard, in parallel with similar increases in uterine angiogenesis during gestation. However, we also find that VEGF111 is expressed in oviparous skinks, and is not ubiquitous among viviparous skinks. Thus, different mechanisms of uterine angiogenesis during pregnancy may evolve concurrent with viviparity in different lizard lineages. J. Exp. Zool. (Mol. Dev. Evol.) 00B: 1-7, 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
  • Article
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    Reproduction, embryonic development, and general biology are described from more than 100 chain dogfish, Scyliorhinus retifer, a common catshark found on the continental slopes of the western North Atlantic. Females and males reached sexual maturity at about 520 mm TL and 500 mm TL, respectively. Follicles are ovulated in pairs when they reach 18 mm diameter. In the laboratory, females lay one egg pair at approx. 15.3 d intervals, attaching the eggs to bottom structures. Development at 11.7-12.8 C in artificial seawater averaged 256 d (±SD 8 d, n = 62) to hatching. Embryos averaged 106 mm (±SD 5 mm, n = 63) at hatching. In the wild, juveniles are often found in large numbers over smooth bottoms. Adults congregate in areas with upright structures which females use for egg attachment. Chain dogfish feed on squid, small bony fishes, polychaete worms, and crustaceans.
  • Article
    Modes of reproduction and embryonic development vary greatly among the elasmobranchs, and prior studies have suggested that the energetic toll of embryogenesis in lecithotrophic species depletes embryonic organic matter by 20% or more. Matrotrophic species experience a lesser reduction or an increase in organic matter during embryogenesis. To investigate the maternal-embryonic nutritional relationship, we measured changes in organic matter from fertilization to near-parturition in embryos of Centrophorus granulosus and Etmopterus princeps. Embryos of C. granulosus experienced a reduction of 19.5% in organic matter, while E. princeps embryos experienced a reduction of 7.7% in organic matter over the course of embryonic development, suggesting some level of matrotrophy occurs, particularly for the latter species. Uterine villi were present in both species and developed concurrently with the embryos, increasing in length and thickness while becoming progressively vascularized. Embryos of C. granulosus were dissected to track the partitioning of water, organic matter, and inorganic matter to the liver, external yolk sac, internal yolk sac, digestive tract, and evicerated body throughout development. Mating was aseasonal for both species and spatially mediated segregation by sex and maturity stage was observed. Ovarian cycles were concurrent for C. granulosus and consecutive for E. princeps. Size at maturity for C. granulosus was determined to be 111 cm TL for males and 143 cm TL for females, with an average fecundity of 5.3 embryos (range=4–7). Size at maturity for E. princeps was determined to be 56.5 cm TL for males and 61 cm TL for females north of the Azores and 54 cm TL for males and 69 cm TL for females near the Charlie Gibbs Fracture Zone. Average fecundity was 11.2 embryos (range=7–18) for this species. This is the first reporting of reproductive parameters for these two species, and the information provided will be valuable for informing stock assessment models in areas where these species are fished.
  • Article
    A description of the bramble shark Echinorhinus brucus (Bonnaterre 1788) is given here based on specimens collected during exploratory surveys from the continental slope frcm 200 to 400 metres along the west coast of India and the Gulf of Mannar. The description of a 300 mm embryo of this species is also included. A biochemical analysis of the meat and liver of this species showed that the moisture content of the meat is high (78.66 %), and the percentage of oil in the liver is as high as 78.07 %, The vitamin A content of the oil is negligible, being only 360 USP/gm of oil.
  • Article
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    Abstract Mechanisms of reproductive allocation are major determinants of fitness because embryos cannot complete development without receiving sufficient nutrition from their parents. The nourishment of offspring via placentas (placentotrophy) has evolved repeatedly in vertebrates, including multiple times in squamate reptiles (lizards and snakes). Placentotrophy has been suggested to evolve only if food is sufficiently abundant throughout gestation to allow successful embryogenesis. If scarcity of food prevents successful embryogenesis, females should recoup nutrients allocated to embryos via abortion, reabsorption, and/or cannibalism. We tested these hypotheses in the placentotrophic southern grass skink Pseudemoia entrecasteauxii. We fed females one of four diets (high constant, high variable, low constant, and low variable) during gestation and tested the effects of both food amount and schedule of feeding on developmental success, cannibalism rate, placental nutrient transport, offspring size, and maternal growth and body condition. Low food availability reduced developmental success, placental nutrient transport, offspring size, and maternal growth and body condition. Cannibalism of offspring also increased when food was scarce. Schedule of feeding did not affect offspring or mothers. We suggest that high food abundance and ability to abort and cannibalize poor-quality offspring are permissive factors necessary for placentotrophy to be a viable strategy of reproductive allocation.
  • Article
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    The evolution of the placenta from a non-placental ancestor causes a shift of maternal investment from pre- to post-fertilization, creating a venue for parent-offspring conflicts during pregnancy. Theory predicts that the rise of these conflicts should drive a shift from a reliance on pre-copulatory female mate choice to polyandry in conjunction with post-zygotic mechanisms of sexual selection. This hypothesis has not yet been empirically tested. Here we apply comparative methods to test a key prediction of this hypothesis, which is that the evolution of placentation is associated with reduced pre-copulatory female mate choice. We exploit a unique quality of the livebearing fish family Poeciliidae: placentas have repeatedly evolved or been lost, creating diversity among closely related lineages in the presence or absence of placentation. We show that post-zygotic maternal provisioning by means of a placenta is associated with the absence of bright coloration, courtship behaviour and exaggerated ornamental display traits in males. Furthermore, we found that males of placental species have smaller bodies and longer genitalia, which facilitate sneak or coercive mating and, hence, circumvents female choice. Moreover, we demonstrate that post-zygotic maternal provisioning correlates with superfetation, a female reproductive adaptation that may result in polyandry through the formation of temporally overlapping, mixed-paternity litters. Our results suggest that the emergence of prenatal conflict during the evolution of the placenta correlates with a suite of phenotypic and behavioural male traits that is associated with a reduced reliance on pre-copulatory female mate choice.
  • Article
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    Phylogenetic analyses indicate that viviparity (live-bearing reproduction) has originated independently in more than 150 vertebrate lineages, including a minimum of 115 clades of extant squamate reptiles. Other evolutionary origins of viviparity include 13 origins among bony fishes, nine among chondrichthyans, eight in amphibians, one in Paleozoic placoderms, six among extinct reptiles, and one in mammals. The origins of viviparity range geologically from the mid-Paleozoic through the Mesozoic to the Pleistocene. Substantial matrotrophy (maternal provision of nutrients to embryos during pregnancy) has arisen at least 33 times in these viviparous clades, with most (26) of these origins having occurred among fishes and amphibians. Convergent evolution in patterns of matrotrophy is widespread, as reflected by multiple independent origins of placentotrophy, histotrophy, oophagy, and embryophagy. Specializations for nutrient transfer to embryos are discontinuously distributed, reflecting the roles of phylogenetic inertia, exaptation (preadaptation), and constraint. Ancestral features that function in gas exchange and nutrition repeatedly and convergently have been co-opted for nutrient transfer, often through minor modification of their components and changes in the timing of their expression (heterochrony). Studies on functional and evolutionary morphology continue to play a central role in our attempts to understand viviparity and mechanisms of fetal nutrition. J. Morphol., 2014. © 2014 Wiley Periodicals, Inc.
  • Article
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    The spiny dogfish Squalus acanthias is widely distributed in Atlanto-Mediterranean regions, being captured off the Languedocian coast (southern France, northern Mediterranean), despite a decline of landings. The male and female sexually matured between 635–700 mm and 860–880 mm total length (TL), respectively. The largest male and female were 800 mm and 1110 mm TL, respectively and weighed 2220 g and 8900 g, respectively. There was a significant relationship for total mass versus TL, and liver mass versus TL between males and females. The diameter of the largest yolky oocytes ranged between 43 and 47 mm (mean 45.08 ± 0.98), while the mass ranged between 29.5 and 37.4 g (mean 31.79 ± 2.20). Near- term embryos ranged from 245 to 271 mm TL (mean: 258.85 ± 7.28) and weighed from 47.5 to 55.9 g (mean 53.35 ± 2.26). Ovarian fecundity ranged from 6 to 15 (mean = 10.38 ± 2.66). Uterine fecundity or litter size ranged from 4 to 12 (mean = 8.15 ± 2.07). Both fecundities showed a positive relationship with TL of females. A chemical balance of development based on mean dry masses of yolky oocytes and near-term embryos was 0.87 and suggested that S. acanthias is a pure lecithotrophic species. Hepatosomatic index (HSI) and gonadosomatic index (GSI) significantly increased with size in both males and females. HSI reached the highest values in both sub-adult and adult specimens, reflecting the role of the liver in the gonadal production as well as in buoyancy, while in the GSI the highest values were observed in pregnant females. Vitellogenesis proceeds in parallel with embryonic development. Near-term females were captured in different months of the year while a short period of resting could not be excluded between parturition and the beginning of a new pregnancy, so it appears difficult to delineate the length of gestation. However, a reproductive cycle with a wide range from 18 to 24 months remains a suitable hypothesis.
  • Article
    Genomic imprinting refers to a pattern of gene expression in which a specific parent's allele is either under-expressed or completely silenced. Imprinting is an evolutionary conundrum because it appears to incur the costs of diploidy (e.g. presenting a larger target than haploidy to mutations) while foregoing its benefits (protection from harmful recessive mutations). Here, we critically evaluate previously proposed evolutionary benefits of imprinting and suggest some additional ones. We discuss whether each benefit is capable of explaining both the origin and maintenance of imprinting, and examine how the different benefits interact. We then outline the many costs of imprinting. Simple models show that circulating deleterious recessives can prevent the initial spread of imprinting, even if imprinting would be evolutionarily stable if it could persist long enough to purge these. We also show that imprinting can raise or lower the mutation load, depending on the selective regime and the degree of dominance. We finish by discussing the population-level consequences of imprinting, which can be both positive and negative. Imprinting offers many insights into evolutionary conflict, the interaction between individual- and population-level fitness effects, and the 'gene's-eye view' of evolution.
  • Article
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    Squamate reptiles (lizards and snakes) are an excellent model system for testing hypotheses regarding the evolution of viviparity (live birth) in amniote vertebrates. Viviparity has evolved over 100 times in squamates, resulting in major changes in reproductive physiology. At a minimum, all viviparous squamates exhibit placentae formed by appositions of maternal and embryonic tissues, which are homologous in origin with the tissues that form the placenta in therian mammals. These placentae facilitate adhesion of the conceptus to the uterus as well as exchange of oxygen, carbon dioxide, water, sodium, and calcium. However, most viviparous squamates continue to rely on yolk for nearly all of their organic nutrition. In contrast, some species, which rely on the placenta for at least a portion of organic nutrition, exhibit complex placental specializations associated with the transport of amino acids and fatty acids. Some viviparous squamates also exhibit reduced immunocompetence during pregnancy, which could be the result of immunosuppression to protect developing embryos. Recent molecular studies using both candidate-gene and next-generation sequencing approaches suggest that at least some of the genes and gene families underlying these phenomena play similar roles in the uterus and placenta of viviparous mammals and squamates. Therefore, studies of the evolution of viviparity in squamates should inform hypotheses of the evolution of viviparity in all amniotes, including mammals.
  • Article
    Common misconceptions of the 'parental conflict' theory of genomic imprinting are addressed. Contrary to widespread belief, the theory defines conditions for cooperation as well as conflict in mother-offspring relations. Moreover, conflict between genes of maternal and paternal origin is not the same as conflict between mothers and fathers. In theory, imprinting can evolve either because genes of maternal and paternal origin have divergent interests or because offspring benefit from a phenotypic match, or mismatch, to one or other parent. The latter class of models usually require maintenance of polymorphism at imprinted loci for the maintenance of imprinted expression. The conflict hypothesis does not require maintenance of polymorphism and is therefore a more plausible explanation of evolutionarily conserved imprinting.Heredity advance online publication, 16 October 2013; doi:10.1038/hdy.2013.97.
  • Article
    I report evidence of plasticity in the mode of embryo nourishment by female poeciliid fish raised under contrasting environmental conditions. In two experiments, female sail fin mollies (Poecilia latipinna), raised on high and low levels of food, produced neonates of similar mass and percentage of fat by varying egg size and the amount of supplemental nourishment provided to embryos as they developed. In one experiment, females displayed plasticity in ovum size, but not neonate size; females raised in a low-food and low-salinity treatment produced larger eggs than those raised on higher food levels and at higher salinity. In a second experiment, the amount of nourishment provided to embryos, in addition to that in the egg yolk, was dependent on brood size and maternal food level. Females with small broods were less matrotrophic than those with large broods; female body size and brood size were highly correlated. The brood size at which egg mass equaled neonate mass was smaller for females raised on low levels of food than for females raised on a higher food level treatment. In the second experiment, females from two populations, different from the source of fish for the first experiment, were studied and found to differ in the amount of fat stores remaining after reproduction. Females from a population with low postparturition fat stores displayed greater brood reduction during gestation (via resorption or abortion) and fewer offspring per unit mass than females from the population with more fat. In sailfin mollies, matrotrophy appears to be an adaptation that diminishes the offspring size-offspring number trade-off by permitting a reduction in ovum size and increase in fecundity without compromising neonate size. However, matrotrophic supplementation of yolk nourishment was greatest in relatively large females raised on a restricted food level. Thus, matrotrophy may incur some energetic cost that renders it inefficient for small females and for females with substantial or dependable energy reserves available for reproduction.
  • Article
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    Many species undertake long-distance annual migrations between foraging and reproductive areas. Such migrants depend on the efficient packaging, storage and utilization of energy to succeed. A diverse assemblage of organisms accomplishes this through the use of lipid reserves; yet, it remains unclear whether the migrations of elasmobranchs, which include the largest gill breathers on Earth, depend on such a mechanism. We examine depth records from pop-up satellite archival tags to discern changes in buoyancy as a proxy for energy storage in Eastern Pacific white sharks, and assess whether lipid depletion fuels long-distance (approx. 4000 km) migrations. We develop new algorithms to assess body condition, buoyancy and drift rate during drift dives and validate the techniques using a captive white shark. In the wild, we document a consistent increase in drift rate over the course of all migrations, indicating a decrease in buoyancy caused by the depletion of lipid reserves. These results comprise, to our knowledge, the first assessment of energy storage and budgeting in migrating sharks. The methods provide a basis for further insights into using electronic tags to reveal the energetic strategies of a wide range of elasmobranchs.
  • Article
    Patterns of chondrichthyan reproduction and development are diverse. Species either are reproductively active throughout the year, or have a poorly defined annual cycle with one or two peaks of activity, or have a well defined annual or biennial cycle. Based on embryological origin and adult morphology, their reproductive system is more similar to tetrapods than to teleosts. Primordial germ cells are of endodermal origin. The Wolffian ducts in males and Mullerian ducts in females become the functional urogenital ducts. Differentiation is under hormonal control. Unusual features of the reproductive system include an epigonal organ in males and females. It contains lymphoid and hemopoietic tissue. Leydig's gland, a modified region of the kidney, produces seminal fluid. In some species, sperm passing through the vas deferens, is enclosed in spermatophores. Rotating about their long axis, helical spermatozoa can move forward or reverse direction. Spermatogenesis often occurs in bicellular units, spermatocysts. These consist of a spermatogonium enclosed in a Sertoh cell. Fertilization is internal. Claspers, modified portions of the pelvic fins act as intromittent organs. In many viviparous sharks and rays, the female reproductive system is asymmetrical. Eggs of some sharks are the largest known cells. Yolk platelets contain lipovitellin. Oocytes have lampbrush chromosomes. Eggs released from the ovary into the body cavity are transported by ciliary action to the ostium of the oviduct. There they are fertilized. Physiological polyspermy is normal. The shell gland, a specialized region of the anterior oviduct, functions both in long term sperm storage and in egg case production. Egg cases of sharks and skates consist of unique collagenous protein with a 400 Å period, organized as a cholesteric liquid crystal. Chimaeroid egg cases contain 550 Å pseudotubules in orthogonal lattices. In small sharks, males copulate by coiling around the female. A parallel position is assumed by large sharks. Skates and rays copulate with ventral surfaces apposed or by a dorsal approach. Biting is a pre-copulatory release mechanism. Parental care, except for selective oviposition, is lacking. Heavily yolked eggs undergo meroblastic, discoidal cleavage. Development is lengthy, shortest (2-4 months) in rays, longer in skates (3-8 months) and longest (9-22 months) in sharks and chimaeras. Most sharks and all rays are viviparous. Chimaeras, skates, and some sharks are oviparous. Viviparity either involves a yolk sac placenta or is aplacental. If aplacental, the embryo derives nutrients either from yolk reserves, or by intra-uterine embryonic cannibalism, or from placental analogues which secrete "uterine milk." Phylogenetic position, geographical distribution, benthic vs. pelagic habitat, adult size, egg-embryo size, feeding ecology, and embryonic osmoregulation are factors in the retention of oviparity or the evolution of viviparity.
  • Article
    A set of hypotheses are developed for the origin of living sharks and rays and the interrelationships of their major groups, using some methods of cladistic analysis to relate groups with shared derived characters. Comparative studies on living sharks and rays combined with new data on fossil sharks suggests that the living groups ultimately stem from a common ancestral group of “neoselachian” sharks with many modern characters. Reinterpretations of “amphistyly” in modern sharks is presented on new data.
  • Article
    Newborn size in the viviparous snake Virginia striatula is determined by female size, egg size, and placental nourishment and is correlated inversely with current fecundity. Of the 2 modes of embryonic nutrition used, lecithotrophy and placentotrophy, an increase in vitellogenic nourishment results in a reduction in current fecundity, whereas placental nourishment does not affect current fecundity. Newborn composition is determined by 2 mechanisms: one is correlated with female size, the other regulated by the developing embryo. -from Author