Publications by authors named "Camilla M Whittington"

41 Publications

Exercise training has morph-specific effects on telomere, body condition and growth dynamics in a color-polymorphic lizard.

J Exp Biol 2021 05 5;224(9). Epub 2021 May 5.

School of Earth, Atmospheric and Life Sciences, University of Wollongong, Wollongong, NSW 2522, Australia.

Alternative reproductive tactics (ARTs) are correlated suites of sexually selected traits that are likely to impose differential physiological costs on different individuals. While moderate activity might be beneficial, animals living in the wild often work at the margins of their resources and performance limits. Individuals using ARTs may have divergent capacities for activity. When pushed beyond their respective capacities, they may experience condition loss, oxidative stress, and molecular damage that must be repaired with limited resources. We used the Australian painted dragon lizard that exhibits color polymorphism as a model to experimentally test the effect of exercise on body condition, growth, reactive oxygen species (ROS) and telomere dynamics - a potential marker of stress and aging and a correlate of longevity. For most males, ROS levels tended to be lower with greater exercise; however, males with yellow throat patches - or bibs - had higher ROS levels than non-bibbed males. At the highest level of exercise, bibbed males exhibited telomere loss, while non-bibbed males gained telomere length; the opposite pattern was observed in the no-exercise controls. Growth was positively related to food intake but negatively correlated with telomere length at the end of the experiment. Body condition was not related to food intake but was positively correlated with increases in telomere length. These results, along with our previous work, suggest that aggressive - territory holding - bibbed males suffer physiological costs that may reduce longevity compared with non-bibbed males with superior postcopulatory traits.
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http://dx.doi.org/10.1242/jeb.242164DOI Listing
May 2021

Structure of the paraplacenta and the yolk sac placenta of the viviparous Australian sharpnose shark, Rhizoprionodon taylori.

Placenta 2021 05 20;108:11-22. Epub 2021 Mar 20.

School of Life and Environmental Sciences, The University of Sydney, Heydon-Laurence Building (A08), Sydney, NSW, 2006, Australia. Electronic address:

Introduction: Viviparity (live-birth) has evolved from oviparity (egg-laying) multiple times in sharks. While most transitions from oviparity to viviparity have resulted in non-placental forms of viviparity, some sharks develop a yolk sac placenta during pregnancy. The Australian sharpnose shark (Rhizoprionodon taylori) is a placental species that suspends embryonic development in a diapause for most of pregnancy.

Methods: To identify structures involved in supporting rapid embryonic growth in late pregnancy, we examined uterine and placental morphology by light and electron microscopy.

Results: Paraplacental uterine regions have morphological specialisations consistent with secretion and fluid transport between uterine tissues and the lumen. Uterine secretions in the lumen may be absorbed by the outgrowths on the embryonic umbilical cord ('appendiculae'), which are densely covered by microvilli. The placenta consists of uterine villi that interdigitate with the yolk sac and enhance the surface area available for fetomaternal exchange. The yolk sac does not invade the uterine epithelium, and the egg capsule remains intact at the placental interface, separating maternal and fetal tissues. Some placental uterine epithelial cells are secretory, and endocytic vesicles in the opposing yolk sac ectodermal cells suggest that nutrient transport is by histotrophic uterine secretion followed by fetal absorption. Respiratory gases, water and possibly small nutrients likely diffuse across the placenta, where maternal and fetal blood vessels are ~2 μm apart.

Discussion: Placental structure in R. taylori is similar to most other sharks, but there are differences in cellular structures between species that may indicate species-specific placental transport mechanisms.
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http://dx.doi.org/10.1016/j.placenta.2021.03.010DOI Listing
May 2021

Scavenging by threatened turtles regulates freshwater ecosystem health during fish kills.

Sci Rep 2020 09 17;10(1):14383. Epub 2020 Sep 17.

School of Molecular Sciences, La Trobe University, Wodonga, VIC, 3689, Australia.

Humans are increasing the frequency of fish kills by degrading freshwater ecosystems. Simultaneously, scavengers like freshwater turtles are declining globally, including in the Australian Murray-Darling Basin. Reduced scavenging may cause water quality problems impacting both ecosystems and humans. We used field and mesocosm experiments to test whether scavenging by turtles regulates water quality during simulated fish kills. In the field, we found that turtles were important scavengers of fish carrion. In mesocosms, turtles rapidly consumed carrion, and water quality in mesocosms with turtles returned to pre-fish kill levels faster than in turtle-free controls. Our experiments have important ecological implications, as they suggest that turtles are critical scavengers that regulate water quality in freshwater ecosystems. Recovery of turtle populations may be necessary to avoid the worsening of ecosystem health, particularly after fish kills, which would have devastating consequences for many freshwater species.
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http://dx.doi.org/10.1038/s41598-020-71544-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7499268PMC
September 2020

Author Correction: Transcriptomic changes in the pre-implantation uterus highlight histotrophic nutrition of the developing marsupial embryo.

Sci Rep 2020 Jul 22;10(1):12453. Epub 2020 Jul 22.

The University of Sydney, School of Medical Sciences, Camperdown, NSW, 2006, Australia.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41598-020-68759-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7376021PMC
July 2020

Paternal nutrient provisioning during male pregnancy in the seahorse Hippocampus abdominalis.

J Comp Physiol B 2020 09 2;190(5):547-556. Epub 2020 Jul 2.

School of Life and Environmental Sciences, The University of Sydney, Heydon-Laurence A08, Camperdown, NSW, 2006, Australia.

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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http://dx.doi.org/10.1007/s00360-020-01289-yDOI Listing
September 2020

The evolution and physiology of male pregnancy in syngnathid fishes.

Biol Rev Camb Philos Soc 2020 10 5;95(5):1252-1272. Epub 2020 May 5.

The University of Wollongong, School of Earth, Atmospheric and Life Sciences, Faculty of Science, Medicine and Health, Wollongong, New South Wales, 2522, Australia.

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.
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http://dx.doi.org/10.1111/brv.12607DOI Listing
October 2020

Emergence of an evolutionary innovation: Gene expression differences associated with the transition between oviparity and viviparity.

Mol Ecol 2020 04 8;29(7):1315-1327. Epub 2020 Apr 8.

School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, Australia.

Our understanding of the evolution of complex biological traits is greatly advanced by examining taxa with intermediate phenotypes. The transition from oviparity (egg-laying) to viviparity (live-bearing) has occurred independently in many animal lineages, but there are few phenotypic intermediates. The lizard Saiphos equalis exhibits bimodal reproduction, with some viviparous populations, and other oviparous populations with long egg-retention, a rare trait where most of embryonic development occurs inside the mother prior to late ovipositioning. We posit that oviparous S. equalis represent an intermediate form between "true" oviparity and viviparity. We used transcriptomics to compare uterine gene expression in these two phenotypes, and provide a molecular model for the genetic control and evolution of reproductive mode. Many genes are differentially expressed throughout the reproductive cycle of both phenotypes, which have clearly different gene expression profiles overall. The differentially expressed genes within oviparous and viviparous individuals have broadly similar biological functions putatively important for sustaining embryos, including uterine remodelling, respiratory gas and water exchange, and immune regulation. These functional similarities indicate either that long egg-retention is an exaptation for viviparity, or might reflect parallel evolution of similar gravidity-related changes in gene expression in long egg-retention oviparity. In contrast, gene expression changes across the reproductive cycle of long egg-retaining oviparous S. equalis are dramatically different from those of "true" oviparous skinks (such as Lampropholis guichenoti), supporting our assertion that oviparous S. equalis exhibit an intermediate phenotype between "true" oviparity and viviparity.
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http://dx.doi.org/10.1111/mec.15409DOI Listing
April 2020

Structural changes to the uterus of the dwarf ornate wobbegong shark (Orectolobus ornatus) during pregnancy.

J Morphol 2020 04 7;281(4-5):428-437. Epub 2020 Feb 7.

School of Life and Environmental Sciences, The University of Sydney, Sydney, New South Wales, Australia.

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.
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http://dx.doi.org/10.1002/jmor.21109DOI Listing
April 2020

A comparison of uterine contractile responsiveness to arginine vasopressin in oviparous and viviparous lizards.

J Comp Physiol B 2020 01 19;190(1):49-62. Epub 2019 Dec 19.

School of Life and Environmental Sciences, University of Sydney, Heydon-Laurence Building A08, Sydney, NSW, 2006, Australia.

Nonapeptides and their receptors regulate a diverse range of physiological processes. We assessed the contractile responsiveness of uteri from the squamate viviparous-oviparous species pair, Pseudemoia entrecasteauxii and Lampropholis guichenoti, as well as the bimodally reproductive species, Saiphos equalis, to arginine vasopressin (AVP). We assessed the resulting uterine contractility as a function of pregnancy status, species and parity mode. We also measured mRNA abundance for the nonapeptide receptor, oxytocin receptor (oxtr), in uteri from P. entrecasteauxii and L. guichenoti and compared expression across pregnancy status and parity mode. We found that pregnant uteri exhibited a significantly greater contractile response to AVP than non-pregnant uteri in all three lizard species studied. Cross-species comparisons revealed that uteri from viviparous P. entrecasteauxii were significantly more responsive to AVP than uteri from oviparous L. guichenoti during both pregnant and non-pregnant states. Conversely, for non-pregnant S. equalis, uteri from viviparous individuals were significantly less responsive to AVP than uteri from oviparous individuals, while during pregnancy, there was no difference in AVP contractile responsiveness. There was no difference in expression of oxtr between L. guichenoti and P. entrecasteauxii, or between pregnant and non-pregnant individuals within each species. We found no significant correlation between oxtr expression and AVP contractile responsiveness. These findings indicate that there are differences in nonapeptide signalling across parity mode and suggest that in these lizards, labour may be triggered either by an increase in plasma nonapeptide concentration, or by an increase in expression of a different nonapeptide receptor from the vasopressin-like receptor family.
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http://dx.doi.org/10.1007/s00360-019-01254-4DOI Listing
January 2020

Sex- And tissue-specific differences in telomere length in a reptile.

Ecol Evol 2019 Jun 22;9(11):6211-6219. Epub 2019 May 22.

Department of Biological & Environmental Sciences University of Gothenburg Gothenburg Sweden.

The usage of telomere length (TL) in blood as a proxy for the TL of other tissues relies on the assumption that telomere dynamics across all tissues are similar. However, telomere attrition can be caused by reactive oxygen species (ROS) which may vary with metabolic rate, which itself varies across organs depending upon the life history strategy of an organism. Thus, we chose to measure the telomeres of various cell types in juvenile painted dragon lizards, , given their unusual life history strategy. Individuals typically only experience a single mating season. We measured the TL of male and female dragons using qPCR and observed that TL varied with tissue type and sex. Telomeres of blood cells were longer than those of liver, heart, brain, and spleen, and females had longer telomeres than males. Brain telomeres in males were approximately half the length of those in females. Telomeric attrition in the male brain may be due to the need for rapid learning of reproductive tactics (territory patrol and defense, mate-finding). Significant correlations between the TL of tissue types suggest that blood TL may be a useful proxy for the TL of other tissues. Our comparison of organ-specific telomere dynamics, the first in a reptile, suggests that the usage of blood TL as a proxy requires careful consideration of the life history strategy of the organism.
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http://dx.doi.org/10.1002/ece3.5164DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6580261PMC
June 2019

Dynamic changes to claudins in the uterine epithelial cells of the marsupial Sminthopsis crassicaudata (Dasyuridae) during pregnancy.

Mol Reprod Dev 2019 06 4;86(6):639-649. Epub 2019 Apr 4.

School of Medical Sciences and Bosch Institute, University of Sydney, Sydney, Australia.

The fluid that surrounds the embryo in the uterus contains important nourishing factors and secretions. To maintain the distinct microenvironment in the uterine lumen, the tight junctions between uterine epithelial cells are remodeled to decrease paracellular movement of molecules and solutes. Modifications to tight junctions between uterine epithelial cells is a common feature of pregnancy in eutherian mammals, regardless of placental type. Here we used immunofluorescence microscopy and western blot analysis to describe distributional changes to tight junctional proteins, claudin-1, -3, -4, and -5, in the uterine epithelial cells of a marsupial species, Sminthopsis crassicaudata. Immunofluorescence microscopy revealed claudin-1, -3, and -5 in the tight junctions of the uterine epithelium of S. crassicaudata during pregnancy. These specific claudins are associated with restricting passive movement of fluid between epithelial cells in eutherians. Hence, their function during pregnancy in S. crassicaudata may be to maintain the uterine luminal content surrounding developing embryos. Claudin-4 disappears from all uterine regions of S. crassicaudata at the time of implantation, in contrast with the distribution of this claudin in some eutherian mammals. We conclude that like eutherian mammals, distributional changes to claudins in the uterine epithelial cells of S. crassicaudata are necessary to support pregnancy. However, the combination of individual claudin isoforms in the tight junctions of the uterine epithelium of S. crassicaudata differs from that of eutherian mammals. Our findings suggest that the precise permeability of the paracellular pathway of the uterine epithelium is species-specific.
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http://dx.doi.org/10.1002/mrd.23140DOI Listing
June 2019

Facultative oviparity in a viviparous skink ( Saiphos equalis).

Biol Lett 2019 04;15(4):20180827

2 School of Life and Environmental Sciences, The University of Sydney , Sydney , Australia.

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.
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http://dx.doi.org/10.1098/rsbl.2018.0827DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6501355PMC
April 2019

IFPA meeting 2018 workshop report I: Reproduction and placentation among ocean-living species; placental imaging; epigenetics and extracellular vesicles in pregnancy.

Placenta 2019 09 10;84:4-8. Epub 2019 Feb 10.

Mother Infant Research Institute, Tufts Medical Center, USA. Electronic address:

Workshops are an important part of the IFPA annual meeting as they allow for discussion of specialized topics. At IFPA meeting 2018 there were nine themed workshops, four of which are summarized in this report. These workshops discussed new knowledge and technological innovations in the following areas of research: 1) viviparity in ocean-living species; 2) placental imaging; 3) epigenetics; and 4) extracellular vesicles in pregnancy.
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http://dx.doi.org/10.1016/j.placenta.2019.02.003DOI Listing
September 2019

Long-term effects of superoxide and DNA repair on lizard telomeres.

Mol Ecol 2018 12 10;27(24):5154-5164. Epub 2018 Dec 10.

School of Biological Sciences, The University of Wollongong, Wollongong, New South Wales, Australia.

Telomeres are the non-coding protein-nucleotide "caps" at chromosome ends that contribute to chromosomal stability by protecting the coding parts of the linear DNA from shortening at cell division, and from erosion by reactive molecules. Recently, there has been some controversy between molecular and cell biologists, on the one hand, and evolutionary ecologists on the other, regarding whether reactive molecules erode telomeres during oxidative stress. Many studies of biochemistry and medicine have verified these relationships in cell culture, but other researchers have failed to find such effects in free-living vertebrates. Here, we use a novel approach to measure free radicals (superoxide), mitochondrial "content" (a combined measure of mitochondrial number and size in cells), telomere length and DNA damage at two primary time points during the mating season of an annual lizard species (Ctenophorus pictus). Superoxide levels early in the mating season vary widely and elevated levels predict shorter telomeres both at that time as well as several months later. These effects are likely driven by mitochondrial content, which significantly impacts late season superoxide (cells with more mitochondria have more superoxide), but superoxide effects on telomeres are counteracted by DNA repair as revealed by 8-hydroxy-2'-deoxyguanosine assays. We conclude that reactive oxygen species and DNA repair are fundamental for both short- and long-term regulation of lizard telomere length with pronounced effects of early season cellular stress detectable on telomere length near lizard death.
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http://dx.doi.org/10.1111/mec.14913DOI Listing
December 2018

Adaptation and conservation insights from the koala genome.

Nat Genet 2018 08 2;50(8):1102-1111. Epub 2018 Jul 2.

Sydney School of Veterinary Science, Faculty of Science, University of Sydney, Sydney, New South Wales, Australia.

The koala, the only extant species of the marsupial family Phascolarctidae, is classified as 'vulnerable' due to habitat loss and widespread disease. We sequenced the koala genome, producing a complete and contiguous marsupial reference genome, including centromeres. We reveal that the koala's ability to detoxify eucalypt foliage may be due to expansions within a cytochrome P450 gene family, and its ability to smell, taste and moderate ingestion of plant secondary metabolites may be due to expansions in the vomeronasal and taste receptors. We characterized novel lactation proteins that protect young in the pouch and annotated immune genes important for response to chlamydial disease. Historical demography showed a substantial population crash coincident with the decline of Australian megafauna, while contemporary populations had biogeographic boundaries and increased inbreeding in populations affected by historic translocations. We identified genetically diverse populations that require habitat corridors and instituting of translocation programs to aid the koala's survival in the wild.
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http://dx.doi.org/10.1038/s41588-018-0153-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6197426PMC
August 2018

Ovarian Hyperstimulation Reduces Vascular Endothelial Growth Factor-A During Uterine Receptivity.

Reprod Sci 2019 02 5;26(2):259-268. Epub 2018 Apr 5.

1 Anatomy and Histology, School of Medical Sciences, Bosch Institute, University of Sydney, Sydney, New South Wales, Australia.

The angiogenic factor vascular endothelial growth factor-A (VEGFA) plays a critical role during early pregnancy in many species including the rat, and any alterations in VEGFA levels can severely impact blastocyst implantation rates. The rat ovarian hyperstimulation (OH) model is useful in studying how the induction of superovulation affects VEGFA levels and endometrial receptivity to blastocyst implantation. The present study shows that the major isoform in the rat uterus, Vegf, is reduced at the time of receptivity in OH compared to normal pregnancy, whereas there is no change in Vegf and Vegf messenger RNA (mRNA). The VEGFA receptor 2 (VEGFR2) protein levels are also reduced at the time of receptivity in OH. Our ovariectomy studies show that Vegf, Vegf, and Vegf are significantly decreased by estrogen, and, to a lesser extent progesterone, when compared to control animals. Although no change in the percentage of endometrial blood vessels was seen across all stages of pregnancy, at the time of receptivity in OH pregnancies, blood vessels were typically larger compared to other stages. The altered progesterone-estrogen ratio seen in OH, taken together with our ovariectomy studies, explains the changes to Vegfa mRNA in OH at the time of receptivity. Since VEGFA is important during implantation, the changes to Vegfa and VEGFR2 levels in the endometrium may help explain the observed lower endometrial receptivity following OH. This study aimed to analyse how ovarian hyperstimulation alters the levels of vascular endothleial growth factor and its major receptor, VEGFR2 in the uterus in a rat model.
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http://dx.doi.org/10.1177/1933719118768703DOI Listing
February 2019

Transcriptomic changes in the pre-implantation uterus highlight histotrophic nutrition of the developing marsupial embryo.

Sci Rep 2018 02 5;8(1):2412. Epub 2018 Feb 5.

The University of Sydney, School of Medical Sciences, Camperdown, NSW, 2006, Australia.

Early pregnancy is a critical time for successful reproduction; up to half of human pregnancies fail before the development of the definitive chorioallantoic placenta. Unlike the situation in eutherian mammals, marsupial pregnancy is characterised by a long pre-implantation period prior to the development of the short-lived placenta, making them ideal models for study of the uterine environment promoting embryonic survival pre-implantation. Here we present a transcriptomic study of pre-implantation marsupial pregnancy, and identify differentially expressed genes in the Sminthopsis crassicaudata uterus involved in metabolism and biosynthesis, transport, immunity, tissue remodelling, and uterine receptivity. Interestingly, almost one quarter of the top 50 genes that are differentially upregulated in early pregnancy are putatively involved in histotrophy, highlighting the importance of nutrient transport to the conceptus prior to the development of the placenta. This work furthers our understanding of the mechanisms underlying survival of pre-implantation embryos in the earliest live bearing ancestors of mammals.
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http://dx.doi.org/10.1038/s41598-018-20744-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5799185PMC
February 2018

Age-related sex differences in body condition and telomere dynamics of red-sided garter snakes.

Proc Biol Sci 2017 Apr;284(1852)

School of Life and Environmental Sciences, University of Sydney, Heydon-Laurence Building (A08), New South Wales 2006, Australia

Life-history strategies vary dramatically between the sexes, which may drive divergence in sex-specific senescence and mortality rates. Telomeres are tandem nucleotide repeats that protect the ends of chromosomes from erosion during cell division. Telomeres have been implicated in senescence and mortality because they tend to shorten with stress, growth and age. We investigated age-specific telomere length in female and male red-sided garter snakes, We hypothesized that age-specific telomere length would differ between males and females given their divergent reproductive strategies. Male garter snakes emerge from hibernation with high levels of corticosterone, which facilitates energy mobilization to fuel mate-searching, courtship and mating behaviours during a two to four week aphagous breeding period at the den site. Conversely, females remain at the dens for only about 4 days and seem to invest more energy in growth and cellular maintenance, as they usually reproduce biennially. As male investment in reproduction involves a yearly bout of physiologically stressful activities, while females prioritize self-maintenance, we predicted male snakes would experience more age-specific telomere loss than females. We investigated this prediction using skeletochronology to determine the ages of individuals and qPCR to determine telomere length in a cross-sectional study. For both sexes, telomere length was positively related to body condition. Telomere length decreased with age in male garter snakes, but remained stable in female snakes. There was no correlation between telomere length and growth in either sex, suggesting that our results are a consequence of divergent selection on life histories of males and females. Different selection on the sexes may be the physiological consequence of the sexual dimorphism and mating system dynamics displayed by this species.
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http://dx.doi.org/10.1098/rspb.2016.2146DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5394656PMC
April 2017

The Regulation of Uterine Proinflammatory Gene Expression during Pregnancy in the Live-Bearing Lizard, Pseudemoia entrecasteauxii.

J Exp Zool B Mol Dev Evol 2017 06 10;328(4):334-346. Epub 2017 Mar 10.

School of Life and Environmental Sciences, University of Sydney, Sydney, Australia.

The evolutionary transition from egg-laying to live-bearing in amniote vertebrates (reptiles and mammals) requires the development of a closer association between the maternal and embryonic tissue to facilitate gas and nutrient exchange with the embryo. Because the embryo is an allograft to the father and mother, it could be considered foreign by the maternal immune system and thus be immunologically rejected during pregnancy. In eutherian ("placental") mammals, the proinflammatory genes interleukin 1B (IL1B), tumor necrosis factor (TNF) and tumor necrosis factor receptor superfamily 1A (TNFRSF1A) are tightly regulated in the pregnant uterus to prevent embryonic rejection. We tested whether inflammation is similarly regulated in pregnant viviparous reptiles by comparing the expression of IL1B, TNF, and TNFRSF1A in the pregnant and nonpregnant uterus of the viviparous lizard, Pseudemoia entrecasteauxii. We found statistically significant support for the downregulation of pregnant uterine TNF mRNA expression in P. entrecasteauxii, but no statistically significant changes in mRNA expression of TNFRSF1A or IL1B between pregnant and nonpregnant uteri. Although these genes are apparently not regulated at the transcriptional level, our immunofluorescence microscopy analyses nonetheless demonstrate that the IL1B proteins are stored intracellularly during pregnancy, possibly resulting in inhibition of inflammatory response. We therefore conclude that processes of both transcriptional (TNF) and posttranslational (IL1B) gene regulation may reduce inflammation in the pregnant uterus of this viviparous reptile. Our study is important because it demonstrates that regulating the maternal immune system to prevent embryonic rejection may be important in reptilian pregnancy as it is in mammalian pregnancy.
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http://dx.doi.org/10.1002/jez.b.22733DOI Listing
June 2017

Expression of VEGF and other VEGF-A variants in the rat uterus is correlated with stage of pregnancy.

J Comp Physiol B 2017 Feb 8;187(2):353-360. Epub 2016 Oct 8.

School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, Australia.

Vascular endothelial growth factor A is a major mediator of angiogenesis, a critically important process in vertebrate growth and development as well as pregnancy. Here we report for the first time the expression of a rare and unusually potent splice variant, VEGF , in vivo in mammals. This variant has previously only been found in mammals in cultured human cells exposed to genotoxic agents. Our discovery of VEGF in the uterus of both a eutherian (rat) and a marsupial (fat-tailed dunnart) suggests that the splice variant may be common to all mammals. As VEGF is also expressed in the uterus of at least one lineage of lizards, the expression of this splice variant may be a widespread amniote phenomenon. We measured expression of VEGF and two major VEGF-A splice variants in the uterus of pregnant rats, showing that the three variants show different expression patterns across pregnancy. Our results suggest that viviparous mammals possess a precisely regulated milieu of VEGF isoforms producing the angiogenesis required for successful pregnancy. The discovery of VEGF in rat uterus paves the way for the development of in vivo models of VEGF activity in a highly tractable laboratory animal, and is particularly significant in the context of early pregnancy loss and cancer research.
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http://dx.doi.org/10.1007/s00360-016-1040-yDOI Listing
February 2017

Ageing and the cost of maintaining coloration in the Australian painted dragon.

Biol Lett 2016 Jul;12(7)

School of Life and Environmental Sciences, University of Sydney, New South Wales, Australia.

There is now good evidence in several taxa that animal coloration positively reflects an individual's antioxidant capacity. However, even though telomeres, a marker of ageing, are known to be vulnerable to reactive oxygen species (ROS) attacks, no studies have ever assessed whether colour fading reflects the rate of biological ageing in any taxa. Here, we measured colour fading, telomere erosion (a measure of biological ageing) and ROS levels in painted dragons. We show that individuals that were better at maintaining their coloration during the three months of the study suffered a higher cost in terms of telomere erosion, but overall ROS levels measured at the start of the study were not significantly related to colour maintenance and telomere shortening. We therefore suggest that colour maintenance is a costly phenomenon in terms of telomere erosion, and that overall ROS levels do not seem to be a crucial component linking ornamental coloration and telomere erosion in our study system.
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http://dx.doi.org/10.1098/rsbl.2016.0077DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4971163PMC
July 2016

Comparative genomics of hormonal signaling in the chorioallantoic membrane of oviparous and viviparous amniotes.

Gen Comp Endocrinol 2017 04 19;244:19-29. Epub 2016 Apr 19.

School of Life and Environmental Sciences, Heydon-Laurence Building, University of Sydney, Sydney, NSW 2006, Australia.

In oviparous amniotes (reptiles, birds, and mammals) the chorioallantoic membrane (CAM) lines the inside of the egg and acts as the living point of contact between the embryo and the outside world. In livebearing (viviparous) amniotes, communication during embryonic development occurs across placental tissues, which form between the uterine tissue of the mother and the CAM of the embryo. In both oviparous and viviparous taxa, the CAM is at the interface of the embryo and the external environment and can transfer signals from there to the embryo proper. To understand the evolution of placental hormone production in amniotes, we examined the expression of genes involved in hormone synthesis, metabolism, and hormone receptivity in the CAM of species across the amniote phylogeny. We collected transcriptome data for the chorioallantoic membranes of the chicken (oviparous), the lizards Lerista bougainvillii (both oviparous and viviparous populations) and Pseudemoia entrecasteauxii (viviparous), and the horse Equus caballus (viviparous). The viviparous taxa differ in their mechanisms of nutrient provisioning: L. bougainvillii is lecithotrophic (embryonic nourishment is provided via the yolk only), but P. entrecasteauxii and the horse are placentotrophic (embryos are nourished via placental transport). Of the 423 hormone-related genes that we examined, 91 genes are expressed in all studied species, suggesting that the chorioallantoic membrane ancestrally had an endocrine function. Therefore, the chorioallantoic membrane appears to be a highly hormonally active organ in all amniotes. No genes are expressed only in viviparous species, suggesting that the evolution of viviparity has not required the recruitment of any specific hormone-related genes. Our data suggest that the endocrine function of the CAM as a placental tissue evolved in part through co-option of ancestral gene expression patterns.
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http://dx.doi.org/10.1016/j.ygcen.2016.04.017DOI Listing
April 2017

Seahorse Brood Pouch Transcriptome Reveals Common Genes Associated with Vertebrate Pregnancy.

Mol Biol Evol 2015 Dec 1;32(12):3114-31. Epub 2015 Sep 1.

School of Biological Sciences, The University of Sydney, Sydney, NSW, Australia Department of Biology, Brooklyn College The Graduate Center, City University of New York

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.
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http://dx.doi.org/10.1093/molbev/msv177DOI Listing
December 2015

Unusual angiogenic factor plays a role in lizard pregnancy but is not unique to viviparity.

J Exp Zool B Mol Dev Evol 2015 Mar 2;324(2):152-8. Epub 2015 Mar 2.

School of Biological Sciences, University of Sydney, Sydney, New South Wales, Australia.

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.
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http://dx.doi.org/10.1002/jez.b.22615DOI Listing
March 2015

Ancestral state reconstructions require biological evidence to test evolutionary hypotheses: A case study examining the evolution of reproductive mode in squamate reptiles.

J Exp Zool B Mol Dev Evol 2015 Sep 2;324(6):493-503. Epub 2015 Mar 2.

School of Biological Sciences, Heydon Laurence Building (A08), University of Sydney, Camperdown, NSW, Australia.

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.
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http://dx.doi.org/10.1002/jez.b.22614DOI Listing
September 2015

High intralocus variability and interlocus recombination promote immunological diversity in a minimal major histocompatibility system.

BMC Evol Biol 2014 Dec 20;14:273. Epub 2014 Dec 20.

Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland.

Background: The genes of the major histocompatibility complex (MHC/MH) have attracted considerable scientific interest due to their exceptional levels of variability and important function as part of the adaptive immune system. Despite a large number of studies on MH class II diversity of both model and non-model organisms, most research has focused on patterns of genetic variability at individual loci, failing to capture the functional diversity of the biologically active dimeric molecule. Here, we take a systematic approach to the study of MH variation, analyzing patterns of genetic variation at MH class IIα and IIβ loci of the seahorse, which together form the immunologically active peptide binding cleft of the MH class II molecule.

Results: The seahorse carries a minimal class II system, consisting of single copies of both MH class IIα and IIβ, which are physically linked and inherited in a Mendelian fashion. Both genes are ubiquitously expressed and detectible in the brood pouch of male seahorses throughout pregnancy. Genetic variability of the two genes is high, dominated by non-synonymous variation concentrated in their peptide-binding regions. Coding variation outside these regions is negligible, a pattern thought to be driven by intra- and interlocus recombination. Despite the tight physical linkage of MH IIα and IIβ loci, recombination has produced novel composite alleles, increasing functional diversity at sites responsible for antigen recognition.

Conclusions: Antigen recognition by the adaptive immune system of the seahorse is enhanced by high variability at both MH class IIα and IIβ loci. Strong positive selection on sites involved in pathogen recognition, coupled with high levels of intra- and interlocus recombination, produce a patchwork pattern of genetic variation driven by genetic hitchhiking. Studies focusing on variation at individual MH loci may unintentionally overlook an important component of ecologically relevant variation.
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http://dx.doi.org/10.1186/s12862-014-0273-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4302578PMC
December 2014

Tracing monotreme venom evolution in the genomics era.

Toxins (Basel) 2014 Apr 2;6(4):1260-73. Epub 2014 Apr 2.

Faculty of Veterinary Science, The University of Sydney, Camperdown, NSW 2006, Australia.

The monotremes (platypuses and echidnas) represent one of only four extant venomous mammalian lineages. Until recently, monotreme venom was poorly understood. However, the availability of the platypus genome and increasingly sophisticated genomic tools has allowed us to characterize platypus toxins, and provides a means of reconstructing the evolutionary history of monotreme venom. Here we review the physiology of platypus and echidna crural (venom) systems as well as pharmacological and genomic studies of monotreme toxins. Further, we synthesize current ideas about the evolution of the venom system, which in the platypus is likely to have been retained from a venomous ancestor, whilst being lost in the echidnas. We also outline several research directions and outstanding questions that would be productive to address in future research. An improved characterization of mammalian venoms will not only yield new toxins with potential therapeutic uses, but will also aid in our understanding of the way that this unusual trait evolves.
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http://dx.doi.org/10.3390/toxins6041260DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4014732PMC
April 2014

The role of prolactin in fish reproduction.

Gen Comp Endocrinol 2013 Sep 18;191:123-36. Epub 2013 Jun 18.

Institute of Evolutionary Biology and Environmental Science, University of Zurich, Winterthurerstrasse 190, Zurich 8057, Switzerland.

Prolactin (PRL) has one of the broadest ranges of functions of any vertebrate hormone, and plays a critical role in regulating aspects of reproduction in widely divergent lineages. However, while PRL structure, mode of action and functions have been well-characterised in mammals, studies of other vertebrate lineages remain incomplete. As the most diverse group of vertebrates, fish offer a particularly valuable model system for the study of the evolution of reproductive endocrine function. Here, we review the current state of knowledge on the role of prolactin in fish reproduction, which extends to migration, reproductive development and cycling, brood care behaviour, pregnancy, and nutrient provisioning to young. We also highlight significant gaps in knowledge and advocate a specific bidirectional research methodology including both observational and manipulative experiments. Focusing research efforts towards the thorough characterisation of a restricted number of reproductively diverse fish models will help to provide the foundation necessary for a more explicitly evolutionary analysis of PRL function.
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http://dx.doi.org/10.1016/j.ygcen.2013.05.027DOI Listing
September 2013

Standardised classification of pre-release development in male-brooding pipefish, seahorses, and seadragons (Family Syngnathidae).

BMC Dev Biol 2012 Dec 29;12:39. Epub 2012 Dec 29.

Institute of Evolutionary Biology and Environmental Studies, University of Zürich, Winterthurerstrasse 190, Zürich, CH-8057, Switzerland.

Background: Members of the family Syngnathidae share a unique reproductive mode termed male pregnancy. Males carry eggs in specialised brooding structures for several weeks and release free-swimming offspring. Here we describe a systematic investigation of pre-release development in syngnathid fishes, reviewing available data for 17 species distributed across the family. This work is complemented by in-depth examinations of the straight-nosed pipefish Nerophis ophidion, the black-striped pipefish Syngnathus abaster, and the potbellied seahorse Hippocampus abdominalis.

Results: We propose a standardised classification of early syngnathid development that extends from the activation of the egg to the release of newborn. The classification consists of four developmental periods - early embryogenesis, eye development, snout formation, and juvenile - which are further divided into 11 stages. Stages are characterised by morphological traits that are easily visible in live and preserved specimens using incident-light microscopy.

Conclusions: Our classification is derived from examinations of species representing the full range of brooding-structure complexity found in the Syngnathidae, including tail-brooding as well as trunk-brooding species, which represent independent evolutionary lineages. We chose conspicuous common traits as diagnostic features of stages to allow for rapid and consistent staging of embryos and larvae across the entire family. In view of the growing interest in the biology of the Syngnathidae, we believe that the classification proposed here will prove useful for a wide range of studies on the unique reproductive biology of these male-brooding fish.
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http://dx.doi.org/10.1186/1471-213X-12-39DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3541971PMC
December 2012

Proteomics and deep sequencing comparison of seasonally active venom glands in the platypus reveals novel venom peptides and distinct expression profiles.

Mol Cell Proteomics 2012 Nov 16;11(11):1354-64. Epub 2012 Aug 16.

Faculty of Veterinary Science, The University of Sydney, Camperdown, NSW 2006, Australia.

The platypus is a venomous monotreme. Male platypuses possess a spur on their hind legs that is connected to glands in the pelvic region. They produce venom only during the breeding season, presumably to fight off conspecifics. We have taken advantage of this unique seasonal production of venom to compare the transcriptomes of in- and out-of-season venom glands, in conjunction with proteomic analysis, to identify previously undiscovered venom genes. Comparison of the venom glands revealed distinct gene expression profiles that are consistent with changes in venom gland morphology and venom volumes in and out of the breeding season. Venom proteins were identified through shot-gun sequenced venom proteomes of three animals using RNA-seq-derived transcripts for peptide-spectral matching. 5,157 genes were expressed in the venom glands, 1,821 genes were up-regulated in the in-season gland, and 10 proteins were identified in the venom. New classes of platypus-venom proteins identified included antimicrobials, amide oxidase, serpin protease inhibitor, proteins associated with the mammalian stress response pathway, cytokines, and other immune molecules. Five putative toxins have only been identified in platypus venom: growth differentiation factor 15, nucleobindin-2, CD55, a CXC-chemokine, and corticotropin-releasing factor-binding protein. These novel venom proteins have potential biomedical and therapeutic applications and provide insights into venom evolution.
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http://dx.doi.org/10.1074/mcp.M112.017491DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3494181PMC
November 2012
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