Changes in processes downstream of the hypothalamus are associated with seasonal follicle development in a songbird, the dark-eyed junco (Junco hyemalis)
Introduction
Most temperate-zone animals breed seasonally to ensure that offspring are born at an optimal time for rearing and survival (Baker, 1938, Murton and Westwood, 1977). Before young arrive, parents must undergo extensive physiological and behavioral preparation for breeding. Often, preparatory events must be initiated well in advance of seasonal increases in food availability (Gibb, 1950).
In most seasonally breeding species, environmental cues are perceived and transduced at the level of the hypothalamus, where gonadotropin-releasing hormone (GnRH) neurons trigger an endocrine cascade resulting in gonadal activation (Dawson, 2008, Jacobs and Wingfield, 2000). More specifically, GnRH triggers secretion of gonadotropins, luteinizing hormone (LH) and follicle-stimulating hormone (FSH), from the anterior pituitary. LH stimulates the synthesis and release of steroids such as testosterone (T) and estradiol (E2) from the gonads (Adkins-Regan, 2008, Wingfield, 2012). These hormones are then transported to target tissues where they bind to receptors, thus shaping physiological, morphological, and behavioral traits. While the above sequence is fairly well established, particularly in males, it is less well known how changes in sensitivity of tissues downstream of the hypothalamus may influence the final transition leading to female clutch initiation in oviparous species (Caro, 2012). This investigation seeks to document whether changes in sensitivities at one or more levels downstream of the hypothalamus are observed as females transition from a non-breeding status in early spring into the onset of egg development.
Here, we asked whether female pituitary and gonadal hormonal responsiveness to stimulation with gonadotropin-releasing hormone (GnRH) changes from pre-breeding to egg-development. In addition, we also assessed whether expression of key genes in the ovary and liver are important for responding to endocrine signal changes during the transition into a reproductively mature state. The ovary is the site of follicular maturation and the liver is necessary for the production of yolk-precursors utilized in the developing follicle (Williams, 2012). Specifically, we asked whether expression for reproductive hormone receptors on the ovary (LHR, FSHR) and the liver (ERα) increase during the transition to breeding maturity, which would likely increase responsiveness to these hormones following stimulation with GnRH. Finally, we also assessed whether expression of the two main receptors for corticosterone (CORT), mineralocorticoid receptor (MR), which binds CORT with high affinity, and the low-affinity glucocorticoid receptor (GR), (De Kloet et al., 1998, Funder, J.W., 1997), display increases in expression during the transition to breeding. Reproduction is energetically expensive, and glucocorticoid hormones, which play an essential role in metabolism and energy regulation (Landys et al., 2006, Sapolsky et al., 2000) may play an integral role in the ability of the ovary and liver to be responsive to a seasonal increase in baseline circulating glucocorticoids leading up to reproduction (Romero, 2002). Alternatively, an increase in expression of these hormone receptors, particularly the low-affinity GR, may also increase the sensitivity of these tissues to stress-induced levels of CORT (Abraham et al., 2013, Bambino and Hsueh, 1981, Denari and Ceballos, 2006, Hsueh and Erickson, 1978, Kwok et al., 2007, Lattin et al., 2011), which may enable a delayed investment in and maturation of reproductive tissues when conditions are sub-optimal (Lattin et al., 2016, Wingfield et al., 1998).
Section snippets
Study species
The dark-eyed junco (Junco hyemalis) is a seasonally breeding songbird commonly found throughout North America (Nolan, 2002). Dark-eyed juncos are an excellent model organism because they have been studied extensively, are abundant, and are relatively easy to capture. Juncos are ground-nesters with clutches ranging between 3 and 5 eggs (mean and median = 4) per nest attempt (Nolan, 2002). Our field site was located in the Black Hills National Forest, South Dakota, USA, where juncos are observed
Breeding stage and LH responsiveness to GnRH
There was a significant main effect of time point (pre-injection or 15 min post injection) (F1,51 = 13.6, p < 0.001) and of breeding stage (pre-breeding or egg development) (F1,40 = 11.1, p < 0.010) on LH levels. There was also a significant interaction between time point and breeding stage (F1,51 = 4.3, p = 0.044) on LH levels. Post-hoc pairwise comparisons within each breeding stage revealed that following a GnRH challenge, females significantly elevated LH during the pre-breeding (t = −5.53,
Discussion
Despite knowledge that females play the critical role in determining onset of reproduction (Ball and Ketterson, 2008, Caro et al., 2009), research on the mechanisms regulating seasonal reproduction in songbirds has continued to focus more on males than on females (Caro, 2012, Dawson, 2015, Dawson, 2003). Here, we focused on female birds during the time period from an early reproductive stage prior to rapid yolking of follicles, to full reproductive status when follicles were yolking. While we
Acknowledgements
Thank you to Emily Bertucci for assistance with 2016 data collection. Also, thank you to the 2009 field assistants: Rachel Maranto, Matthew Boser, Connor Wood, and Elizabeth Schultz. Thank you to the Black Hills National Forest, and Jim and Connie Gorsuch for access to the 2009 field sites. Tony Williams kindly provided guidance on measuring VLDL levels. All procedures used in this study were conducted under the appropriate state and federal permits and approved by the NDSU and Bloomington
Competing Interests
The authors declare no competing or financial interests.
Funding
We gratefully acknowledge the following funding sources for support during this work: the National Science Foundation (NSF IOS-1257527, IOS-1738591 to TJG; NSF IOS-0820055 to EKD), South Dakota Ornithologists’ Union Nathaniel R. Whitney Jr. Memorial Research Grant, and the North Dakota State University Department of Biological Sciences.
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