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.
Prolactin and the evolution of male pregnancy Wilson, Anthony B.; Whittington, Camilla M.; Meyer, Axel ...
General and comparative endocrinology,
04/2023, Letnik:
334
Journal Article
Recenzirano
•PRL is involved in the maintenance of male pregnancy in the seahorse.•PRL/PRLR structure and activity are conserved in simple/complex forms of pregnancy.•PRL expression is restricted to the ...pituitary of both seahorses and pipefish.•PRLR is specifically upregulated in the male brood pouch during pregnancy.•PRL, PRLR and Na/K ATPase colocalize in the brood pouch – osmoregulatory function.
Prolactin (PRL) is a multifunctional hormone of broad physiological importance, and is involved in many aspects of fish reproduction, including the regulation of live birth (viviparity) and both male and female parental care. Previous research suggests that PRL also plays an important reproductive role in syngnathid fishes (seahorses, pipefish and seadragons), a group with a highly derived reproductive strategy, male pregnancy - how the PRL axis has come to be co-opted for male pregnancy remains unclear. We investigated the molecular evolution and expression of the genes for prolactin and its receptor (PRLR) in an evolutionarily diverse sampling of syngnathid fishes to explore how the co-option of PRL for male pregnancy has impacted its evolution, and to clarify whether the PRL axis is also involved in regulating reproductive function in species with more rudimentary forms of male pregnancy. In contrast to the majority of teleost fishes, all syngnathid fishes tested carry single copies of PRL and PRLR that cluster genetically within the PRL1 and PRLRa lineages of teleosts, respectively. PRL1 gene expression in seahorses and pipefish is restricted to the pituitary, while PRLRa is expressed in all tissues, including the brood pouch of species with both rudimentary and complex brooding structures. Pituitary PRL1 expression remains stable throughout pregnancy, but PRLRa expression is specifically upregulated in the male brood pouch during pregnancy, consistent with the higher affinity of pouch tissues for PRL hormone during embryonic incubation. Finally, immunohistochemistry of brood pouch tissues reveals that both PRL1 protein and PRLRa and Na+/K+ ATPase-positive cells line the inner pouch epithelium, suggesting that pituitary-derived PRL1 may be involved in brood pouch osmoregulation during pregnancy. Our data provide a unique molecular perspective on the evolution and expression of prolactin and its receptor during male pregnancy, and provide the foundation for further manipulative experiments exploring the role of PRL in this unique form of reproduction.
In therian mammals (placentals and marsupials), sex is determined by an XX female: XY male system, in which a gene (SRY) on the Y affects male determination. There is no equivalent in other amniotes, ...although some taxa (notably birds and snakes) have differentiated sex chromosomes. Birds have a ZW female: ZZ male system with no homology with mammal sex chromosomes, in which dosage of a Z-borne gene (possibly DMRT1) affects male determination. As the most basal mammal group, the egg-laying monotremes are ideal for determining how the therian XY system evolved. The platypus has an extraordinary sex chromosome complex, in which five X and five Y chromosomes pair in a translocation chain of alternating X and Y chromosomes. We used physical mapping to identify genes on the pairing regions between adjacent X and Y chromosomes. Most significantly, comparative mapping shows that, contrary to earlier reports, there is no homology between the platypus and therian X chromosomes. Orthologs of genes in the conserved region of the human X (including SOX3, the gene from which SRY evolved) all map to platypus chromosome 6, which therefore represents the ancestral autosome from which the therian X and Y pair derived. Rather, the platypus X chromosomes have substantial homology with the bird Z chromosome (including DMRT1) and to segments syntenic with this region in the human genome. Thus, platypus sex chromosomes have strong homology with bird, but not to therian sex chromosomes, implying that the therian X and Y chromosomes (and the SRY gene) evolved from an autosomal pair after the divergence of monotremes only 166 million years ago. Therefore, the therian X and Y are more than 145 million years younger than previously thought.
Seahorses exhibit male pregnancy and are thus valuable comparative models for the study of the physiology and evolution of pregnancy. This study shows that protein is transported from fathers to ...developing embryos during gestation, and provides new knowledge about paternal contributions to embryonic development.
Syngnathid embryos (seahorses, pipefishes and seadragons) develop on or in the male in a specialised brooding structure (brood pouch). Seahorse brood pouches supply nutrients, including lipids, to developing embryos (patrotrophy). We tested the hypothesis that proteins, vital for gene regulation and tissue growth during embryogenesis, are also transported from father to embryos, using the Australian pot-bellied seahorse, Hippocampus abdominalis. We used dry masses and total nitrogen content to estimate the total protein content of newly fertilised egg and neonate H. abdominalis. Neonates contained significantly greater protein mass than newly fertilised eggs. This result indicates that paternal protein transport to developing embryos occurs during H. abdominalis pregnancy. This study is the first to show paternal protein transport during pregnancy in seahorses, and furthers our understanding of paternal influence on embryonic development in male pregnant vertebrates.
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, Ctenophorus pictus, 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.
Blood, brain, heart, liver, and spleen telomeres are largely correlated in juvenile painted dragon lizards, Ctenophorus pictus. Females have longer telomeres than males across all tissues and brain telomeres that are twice as long.
The source of embryonic nutrition for development varies across teleost fishes. A parentotrophy index (ratio of neonate: ovulated egg dry mass) is often used to determine provisioning strategy, but ...the methodologies used vary across studies. The variation in source and preservation of tissue, staging of embryos, and estimation approach impedes our ability to discern between methodological and biological differences in parentotrophy indices inter- and intra-specifically. The threshold value used to distinguish between lecithotrophy and parentotrophy (0.6-1) differs considerably across studies. The lack of a standardised approach in definition and application of parentotrophy indices has contributed to inconsistent classifications of provisioning strategy. Consistency in both methodology used to obtain a parentotrophy index, and in the classification of provisioning strategy using a threshold value are essential to reliably distinguish between provisioning strategies in teleosts. We discuss alternative methods for determining parentotrophy and suggest consistent standards for obtaining and interpreting parentotrophy indices.
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.
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.
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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