Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes.
Roth Olivia,Solbakken Monica Hongrø,Tørresen Ole Kristian,Bayer Till,Matschiner Michael,Baalsrud Helle Tessand,Hoff Siv Nam Khang,Brieuc Marine Servane Ono,Haase David,Hanel Reinhold,Reusch Thorsten B H,Jentoft Sissel
Proceedings of the National Academy of Sciences of the United States of America
A fundamental problem for the evolution of pregnancy, the most specialized form of parental investment among vertebrates, is the rejection of the nonself-embryo. Mammals achieve immunological tolerance by down-regulating both major histocompatibility complex pathways (MHC I and II). Although pregnancy has evolved multiple times independently among vertebrates, knowledge of associated immune system adjustments is restricted to mammals. All of them (except monotremata) display full internal pregnancy, making evolutionary reconstructions within the class mammalia meaningless. Here, we study the seahorse and pipefish family (syngnathids) that have evolved male pregnancy across a gradient from external oviparity to internal gestation. We assess how immunological tolerance is achieved by reconstruction of the immune gene repertoire in a comprehensive sample of 12 seahorse and pipefish genomes along the "male pregnancy" gradient together with expression patterns of key immune and pregnancy genes in reproductive tissues. We found that the evolution of pregnancy coincided with a modification of the adaptive immune system. Divergent genomic rearrangements of the MHC II pathway among fully pregnant species were identified in both genera of the syngnathids: The pipefishes () displayed loss of several genes of the MHC II pathway while seahorses () featured a highly divergent invariant chain (). Our findings suggest that a trade-off between immunological tolerance and embryo rejection accompanied the evolution of unique male pregnancy. That pipefishes survive in an ocean of microbes without one arm of the adaptive immune defense suggests a high degree of immunological flexibility among vertebrates, which may advance our understanding of immune-deficiency diseases.
10.1073/pnas.1916251117
Brain size evolution in pipefishes and seahorses: the role of feeding ecology, life history and sexual selection.
Tsuboi M,Lim A C O,Ooi B L,Yip M Y,Chong V C,Ahnesjö I,Kolm N
Journal of evolutionary biology
Brain size varies greatly at all taxonomic levels. Feeding ecology, life history and sexual selection have been proposed as key components in generating contemporary diversity in brain size across vertebrates. Analyses of brain size evolution have, however, been limited to lineages where males predominantly compete for mating and females choose mates. Here, we present the first original data set of brain sizes in pipefishes and seahorses (Syngnathidae) a group in which intense female mating competition occurs in many species. After controlling for the effect of shared ancestry and overall body size, brain size was positively correlated with relative snout length. Moreover, we found that females, on average, had 4.3% heavier brains than males and that polyandrous species demonstrated more pronounced (11.7%) female-biased brain size dimorphism. Our results suggest that adaptations for feeding on mobile prey items and sexual selection in females are important factors in brain size evolution of pipefishes and seahorses. Most importantly, our study supports the idea that sexual selection plays a major role in brain size evolution, regardless of on which sex sexual selection acts stronger.
10.1111/jeb.12995
Structural changes to the brood pouch of male pregnant seahorses (Hippocampus abdominalis) facilitate exchange between father and embryos.
Dudley J S,Hannaford P,Dowland S N,Lindsay L A,Thompson M B,Murphy C R,Van Dyke J U,Whittington C M
Placenta
INTRODUCTION:Embryonic growth and development require efficient respiratory gas exchange. Internal incubation of developing young thus presents a significant physiological challenge, because respiratory gas diffusion to embryos is impeded by the additional barrier of parental tissue between the embryo and the environment. Therefore, live-bearing species exhibit a variety of adaptations facilitating respiratory gas exchange between the parent (usually the mother) and embryos. Syngnathid fishes are the only vertebrates to exhibit male pregnancy, allowing comparative studies of the biology and evolution of internal incubation of embryos, independent of the female reproductive tract. Here, we examine the fleshy, sealed, seahorse brood pouch, and provide the first quantification of structural changes to this gestational organ across pregnancy. METHODS:We used histological analysis and morphometrics to quantify the surface area for exchange across the brood pouch epithelium, and the structure of the vascular bed of the brood pouch. RESULTS:We show dramatic remodelling of gestational tissues as pregnancy progresses, including an increase in tortuosity of the gestational epithelium, an increase in capillary density, and a decrease in diffusion distance between capillaries and the pouch lumen. DISCUSSION:These changes produce an increased surface area and expansion of the vascular bed of the placenta that likely facilitates respiratory gas exchange. These changes mirror the remodelling of gestational tissue in viviparous amniotes and elasmobranchs, and provide further evidence of the convergence of adaptations to support pregnancy in live-bearing animals.
10.1016/j.placenta.2021.09.002
The evolution of the testis transcriptome in pregnant male pipefishes and seahorses.
Evolution; international journal of organic evolution
In many animals, sperm competition and sexual conflict are thought to drive the rapid evolution of male-specific genes, especially those expressed in the testes. A potential exception occurs in the male pregnant pipefishes, where females transfer eggs to the males, eliminating testes from participating in these processes. Here, we show that testis-related genes differ dramatically in their rates of molecular evolution and expression patterns in pipefishes and seahorses (Syngnathidae) compared to other fish. Genes involved in testis or sperm function within syngnathids experience weaker selection in comparison to their orthologs in spawning and livebearing fishes. An assessment of gene turnover and expression in the testis transcriptome suggests that syngnathids have lost (or significantly reduced expression of) important classes of genes from their testis transcriptomes compared to other fish. Our results indicate that more than 50 million years of male pregnancy have removed syngnathid testes from the molecular arms race that drives the rapid evolution of male reproductive genes in other taxa.
10.1111/evo.14579
Evidence of feminization in seahorses from a tropical estuary.
Journal of fish biology
Intersex has been reported regularly in wild populations of gonochoristic fish. The authors investigated the possible feminization of seahorses in a population of Hippocampus reidi in Brazil, as well as report a case of a brood pouch reduction after reproductive stimuli. The female seahorses of this population showed two kinds of morphological anomalies. The proportion of the animals affected in the study population was consistent and was uncorrelated with the sex ratio. The study indicates the changes in the sexual profile of the individual.
10.1111/jfb.14759
When male seahorses take the female contraceptive pill ...
D'Alvise Nathalie Prévot,Richard Simone,Aublanc Philippe,Bunet Robert,Bonnefont Jean-Luc
Environmental science and pollution research international
17α-ethinylestradiol (EE2), the female contraceptive pill, has been detected in mediterranean coasts where seahorse populations, Hippocampus guttulatus, live. Low environmental concentrations have the potential to disrupt growth but also endocrine metabolism, and this imbalance is all the more critical in early life stage. To investigate the impact of EE2 in reared seahorses, we exposed aged 2 months and sexually undifferentiated seahorses to an environmental concentration of 21 ng/L of EE2 for a period of 30 days. EE2 exposure led to a 19% reduction in weight, but also a mortality rate of 27%. This exposure predicted demasculinization of male individuals with a late onset of secondary sexual characteristics. EE2 exposure led to an increase of the free androgen index, but significant reductions of estradiol and testosterone in males were observed. This low estrogen concentration seemed to impact the positive feedback on luteinizing hormone (LH) with a decrease in LH production. Added to this, synthetic estrogen had a negative impact on the production and the release of follicle-stimulating hormone. Contrary to all expectations, females demonstrated a significant decrease in vitellogenin, following exposure to EE2 at 21 ng/L, while no changes were detected in males. This first study on the European long-snouted seahorses confirmed the deleterious impact of the female contraceptive pill with a real impact on growth, sexual differentiation, and maturation in young immature seahorses.
10.1007/s11356-020-08152-1
Effects of pairing on color change and central gene expression in lined seahorses.
Genes, brain, and behavior
Social monogamy is a reproductive strategy characterized by pair living and defense of a common territory. Pair bonding, sometimes displayed by monogamous species, is an affective construct that includes preference for a specific partner, distress upon separation, and the ability of the partner to buffer against stress. Many seahorse species show a monogamous social structure in the wild, but their pair bond has not been well studied. We examined the gene expression of lined seahorses (Hippocampus erectus) during and after the process of pairing in the laboratory as well as color change (luminance), a potential form of social communication and behavioral synchrony between pair mates. When a seahorse of either sex was interacting with its pair mate, their changes in luminance ("brightness") were correlated and larger than when interacting with an opposite-sex stranger. At the conclusion of testing, subjects were euthanized, RNA was extracted from whole brains and analyzed via RNA sequencing. Changes in gene expression in paired males versus those that were unpaired included processes governing metabolic activity, hormones and cilia. Perhaps most interesting is the overlap in gene expression change induced by pairing in both male seahorses and male prairie voles, including components of hormone systems regulating reproduction. Because of our limited sample size, we consider our results and interpretations to be preliminary, and prompts for further exploration. Future studies will expand upon these findings and investigate the neuroendocrine and genetic basis of these behaviors.
10.1111/gbb.12812
Identification of neurohypophysial hormones and the role of VT in the parturition of pregnant seahorses ().
Frontiers in endocrinology
Neurohypophysial hormones regulate the reproductive behavior of teleosts; however, their role in the gestation and parturition of ovoviviparous fishes with male pregnancy (syngnathids) remains to be demonstrated. In the present study, the complementary DNA (cDNA) sequences of arginine vasotocin (VT) and isotocin (IT) from the lined seahorse () were cloned and identified. We observed that the mature core peptides of seahorse VT and IT were conserved among teleosts. In the phylogenic tree, seahorse VT and IT were clustered independently with teleost VT and IT. The tissue distribution patterns of and were similar, and both were highly expressed in the brain, gills, and gonads. Interestingly, they were also expressed to some extent in the brood pouch. hybridization revealed that and messenger RNA (mRNA) signals in the brain were mainly located in the preoptic area region of the hypothalamus. Intraperitoneal administration of the VT core peptide to pregnant seahorses induced premature parturition, stimulated gonadotropin release, increased serum estrogen levels, and decreased prolactin secretion. Moreover, VT injection upregulated the mRNA expression of the membrane estrogen receptor in the brood pouch. In summary, neurohypophysial hormones promote premature parturition by regulating estrogen synthesis through the hypothalamus-pituitary-gonad axis.
10.3389/fendo.2022.923234