skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: In vivo treatment with a non-aromatizable androgen rapidly alters the ovarian transcriptome of previtellogenic secondary growth coho salmon (Onchorhynchus kisutch)
Recent evidence suggests that androgens are a potent driver of growth during late the primary stage of ovarian follicle development in teleosts. We have previously shown that the non-aromatizable androgen, 11-ketotestosterone (11-KT), both advances ovarian follicle growth in vivo and dramatically alters the primary growth ovarian transcriptome in coho salmon. Many of the transcriptomic changes pointed towards 11-KT driving process associated with the transition to a secondary growth phenotype. In the current study, we implanted previtellogenic early secondary growth coho salmon with cholesterol pellets containing 11-KT and performed RNA-Seq on ovarian tissue after 3 days in order to identify alterations to the ovarian transcriptome in early secondary growth. We identified 8,707 contiguous sequences (contigs) that were differentially expressed (DE) between control and 11-KT implanted fish and were able to collapse those to 3,853 gene-level IDs, more than a 3-fold more DE contigs than at the primary growth stage we reported previously. These contigs included genes encoding proteins involved in steroidogenesis, vitellogenin and lipid uptake, follicle stimulating hormone signaling, growth factor signaling, and structural proteins, suggesting androgens continue to promote previtellogenic secondary growth.  more » « less
Award ID(s):
1921746 1922541
PAR ID:
10561477
Author(s) / Creator(s):
; ; ; ;
Editor(s):
Schubert, Michael
Publisher / Repository:
PLOS One
Date Published:
Journal Name:
PLOS ONE
Volume:
19
Issue:
10
ISSN:
1932-6203
Page Range / eLocation ID:
e0311628
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ABSTRACT Teleost fishes are a highly diverse, ecologically essential group of aquatic vertebrates that include coho salmon (Oncorhynchus kisutch). Coho are semelparous and all ovarian follicles develop synchronously. Owing to their ubiquitous distribution, teleosts provide critical sources of food worldwide through subsistence, commercial fisheries, and aquaculture. Enhancement of hatchery practices requires detailed knowledge of teleost reproductive physiology. Despite decades of research on teleost reproductive processes, an in‐depth proteome of teleost ovarian development has yet to be generated. We have described a coho salmon ovarian proteome of over 5700 proteins, generated with data independent acquisition, revealing the proteins that change through the transition from primary to secondary ovarian follicle development. This transition is critical during the onset of puberty and for determining egg quality and embryonic development. Primary follicle development was marked by differential abundances of proteins in carbohydrate metabolism, protein turnover, and the complement pathway, suggesting elevated metabolism as the follicles develop through stages of oogenesis. The greatest proteomic shift occurred during the transition from primary to secondary follicle growth, with increased abundance of proteins underlying cortical alveoli formation, extracellular matrix reorganization, iron binding, and cell–cell signaling. This work provides a foundation for identifying biomarkers of salmon oocyte stage and quality. 
    more » « less
  2. Predation is a major source of mortality in the early life stages of fishes and a driving force in shaping fish populations. Theoretical, modeling, and laboratory studies have generated hypotheses that larval fish size, age, growth rate, and development rate affect their susceptibility to predation. Empirical data on predator selection in the wild are challenging to obtain, and most selective mortality studies must repeatedly sample populations of survivors to indirectly examine survivorship. While valuable on a population scale, these approaches can obscure selection by particular predators. In May 2018, along the coast of Washington, USA, we simultaneously collected juvenile quillback rockfish Sebastes maliger from both the environment and the stomachs of juvenile coho salmon Oncorhynchus kisutch . We used otolith microstructure analysis to examine whether juvenile coho salmon were age-, size-, and/or growth-selective predators of juvenile quillback rockfish. Our results indicate that juvenile rockfish consumed by salmon were significantly smaller, slower growing at capture, and younger than surviving (unconsumed) juvenile rockfish, providing direct evidence that juvenile coho salmon are selective predators on juvenile quillback rockfish. These differences in early life history traits between consumed and surviving rockfish are related to timing of parturition and the environmental conditions larval rockfish experienced, suggesting that maternal effects may substantially influence survival at this stage. Our results demonstrate that variability in timing of parturition and sea surface temperature leads to tradeoffs in early life history traits between growth in the larval stage and survival when encountering predators in the pelagic juvenile stage. 
    more » « less
  3. Abstract Mitochondria play important roles in ovarian follicle development. Mitochondrial dysfunction, including mitochondrial gene deficiency, impairs ovarian development. Here, we explored the role and mechanism of mitochondrial inner membrane gene Immp2l in ovarian follicle growth and development. Our results revealed that female Immp2l-/- mice were infertile, whereas Immp2l+/- mice were normal. Body and ovarian weights were reduced in the female Immp2l-/- mice, ovarian follicle growth and development were stunted in the secondary follicle stage. Although a few ovarian follicles were ovulated, the oocytes were not fertilized because of mitochondrial dysfunction. Increased oxidative stress, decreased estrogen levels, and altered genes expression of Wnt/β-catenin and steroid hormone synthesis pathways were observed in 28-day-old Immp2l-/- mice. The Immp2l mutation accelerated ovarian aging process, as no ovarian follicles were detected by age 5 months in Immp2l-/- mice. All the aforementioned changes in the Immp2l-/- mice were reversed by administration of antioxidant melatonin to the Immp2l-/- mice. Furthermore, our in vitro study using Immp2l knockdown granulosa cells confirmed that the Immp2l downregulation induced granulosa cell aging by enhancing reactive oxygen species (ROS) levels, suppressing Wnt16, increasing β-catenin, and decreasing steroid hormone synthesis gene cyp19a1 and estrogen levels, accompanied by an increase in the aging phenotype of granulosa cells. Melatonin treatment delayed granulosa cell aging progression. Taken together, Immp2l causes ovarian aging through the ROS-Wnt/β-catenin-estrogen (cyp19a1) pathway, which can be reversed by melatonin treatment. 
    more » « less
  4. ABSTRACT Warming associated with climate change is driving poleward shifts in the marine habitat of anadromous Pacific salmon (Oncorhynchusspp.). Yet the spawning locations for salmon to establish self‐sustaining populations and the consequences for the ecosystem if they should do so are unclear. Here, we explore the role of temperature‐dependent incubation survival and developmental phenology of coho salmon (Oncorhynchus kisutch) as a potential early life history barrier to establishment in an Arctic stream. We exposed embryos to temperatures previously recorded in the substrate of an Arctic groundwater spring‐fed spawning environment. Using a common garden experimental design, coho salmon embryos were exposed to treatments that thermally mimicked four spawning dates from August 1 to October 1 (AUG1, SEPT1, SEPT15, and OCT1). Spawning temperatures were 6°C at the warmest (AUG1) and 1.25°C at the coldest (OCT1). We observed low survival rates in SEPT1 (41%) and OCT1 (34%) and near complete mortality in the other treatments. While far below what is considered normal in benign hatchery‐like conditions, these rates suggest that temperatures experienced at these spawning dates are survivable. We detected differences in developmental rates across treatments; embryos developed 1.9 times faster in the warmest treatment (AUG1, 120 days) compared to the coldest (OCT1, 231 days). Differences in accumulated thermal units (ATUs) needed for hatching ranged from 392 ATUs in AUG1 to 270 ATUs in OCT1, revealing compensation in developmental requirements. Given these findings, the most thermally suitable spawning dates within our study are between September 15 and October 1, which facilitates hatching and projected nest emergence to occur in spring warming conditions (March–September). Broadly, our findings suggest that spawning sites within thermal tolerances that can support the survival and development of coho salmon exist in the North American Arctic. Whether the habitat is otherwise suitable for transitions through other life stages remains unknown. 
    more » « less
  5. Ovarian aging in women can be described as highly unpredictable within individuals but predictable across large populations. We showed previously that modeling an individual woman’s ovarian reserve of primordial follicles using mathematical random walks replicates the natural pattern of growing follicles exiting the reserve. Compiling many simulations yields the observed population distribution of the age at natural menopause (ANM). Here, we have probed how stochastic control of primordial follicle loss might relate to the distribution of the preceding menopausal transition (MT), when women begin to experience menstrual cycle irregularity. We show that identical random walk model conditions produce both the reported MT distribution and the ANM distribution when thresholds are set for growing follicle availability. The MT and ANM are shown to correspond to gaps when primordial follicles fail to grow for 7 and 12 days, respectively. Modeling growing follicle supply is shown to precisely recapitulate epidemiological data and provides quantitative criteria for the MT and ANM in humans. 
    more » « less