Changes in processes downstream of the hypothalamus are associated with seasonal follicle development in a songbird, the dark-eyed junco (Junco hyemalis)

Needham, Katie B.; Burns, Christy Bergeon; Graham, Jessica Lynn; Bauer, Carolyn M.; Kittilson, Jeffrey D.; Ketterson, Ellen D.; Hahn, Thomas P.; Greives, Timothy J.

doi:10.1016/j.ygcen.2018.10.012

Cited by 15 publications

(17 citation statements)

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“…Pre‐breeding stage females (i.e. prior to yolking when female has pre‐vitellogenic “white follicles”) of another subspecies of junco (white‐winged junco; J. h. aikeni ) exhibit higher FSHR mRNA transcript abundance than early breeding females (Needham et al, ). In our study, resident and migrant females likely did not differ in FSHR because they were both in an early stage of follicle development.…”

Section: Discussionmentioning

confidence: 99%

“…Estradiol stimulates the production of yolk precursors, vitellogenin (VTG) and VLDL in the liver (Christians & Williams, ). Female white‐winged juncos in the pre‐breeding stage exhibit higher transcript abundance of ER mRNA in the liver than reproductive females (Needham et al, ). Our results suggest that migrant and resident females did not differ in their sensitivity to stimulation of the liver and that no females were ready to lay eggs.…”

Section: Discussionmentioning

confidence: 99%

“…Females in our study did not differ in their mRNA transcript abundance of GR or MR in either the ovary or the liver based on migratory strategy, suggesting that migrants and residents are responding similarly to circulating CORT levels at the dates we studied them. In comparison, female white‐winged juncos in the pre‐breeding stage have higher GR transcript abundance in the ovary and liver and higher MR mRNA transcript abundance in the liver than reproductively developed females (Needham et al, ). Females shifting from pre‐breeding to reproductive stages might reduce their sensitivity to CORT (Krause, McGuigan, Bishop, Wingfield, & Meddle, ; Krause et al, ).…”

Section: Discussionmentioning

confidence: 99%

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Migratory strategy explains differences in timing of female reproductive development in seasonally sympatric songbirds

et al. 2019

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Divergent migratory strategies among populations can result in population‐level differences in timing of reproduction (allochrony) and local adaptation. However, the mechanisms underlying among‐population variation in timing are insufficiently understood, particularly in females. We studied differences in reproductive development and its related mechanisms along the hypothalamic–pituitary–gonadal axis (HPG) in closely related migratory and sedentary (i.e. resident) female dark‐eyed juncos (Junco hyemalis) living together in sympatry during early spring. Despite exposure to the same environmental cues in early spring, residents initiate breeding prior to the departure of migrants for their breeding grounds. We investigated whether residents would be more reproductively developed than migrants based on their behavioural differences. Alternatively, females could exhibit similar reproductive development in response to the same environmental cues despite differences in migratory behaviour. To compare their degree of reproductive development during seasonal sympatry and the underlying mechanisms of these differences, we collected ovarian and liver tissue in early spring prior to migration and compared transcript abundance of genes associated with reproduction using quantitative PCR. We also used stable hydrogen isotopes to infer relative breeding and wintering latitude of migrants. We found higher transcript abundance of luteinizing hormone receptor and aromatase in the ovary in addition to significantly heavier ovaries in residents than in migrants. Together, these results suggest greater sensitivity and response to upstream endocrine stimulation in resident females. Transcript abundance for other receptors in the ovary and liver associated with reproduction, however, did not differ between populations. When comparing ovarian development within migrants, females with lower hydrogen isotopes (indicating higher breeding latitudes) had smaller ovaries, suggesting that longer‐distance migrations may further delay reproductive development. Based on differences in ovary mass and transcript abundance, we conclude that females that differ in migratory strategy also differ in timing of reproductive development. These results support that divergent migratory behaviour drives allochrony and could enable reproductive isolation between populations; mechanistic differences at the level of gonadal stimulation can explain these differences in timing of reproductive development. A free Plain Language Summary can be found within the Supporting Information of this article.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Migratory strategy explains differences in timing of female reproductive development in seasonally sympatric songbirds

et al. 2019

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“…Although gene expression levels in the hypothalamus seem to be affected by temperature, this does not directly lead to earlier egg-laying, because we found no effect of temperature on either egg-laying date (first breeding season) or follicle size (second breeding season). Our data are in line with the hypothesis that downstream processes in the liver and ovary play a more important role in the fine-tuning of egg-laying date than hypothalamic processes (Chapter 5; Bergeon Burns et al 2014;Needham et al 2019). In this sense, the absence of an effect on egg-laying date of temperature is informative on where in the neuro-endocrine cascade fine-tuning occurs, rather than that it hampers new insights.…”

Section: Downstream Regulation Of Timing Of Breeding?supporting

confidence: 87%

The mechanisms underlying seasonal timing of breeding : a multi-level approach using bi-directional genomic selection on timing of egg-laying

Verhagen¹

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Table of contents Chapter 1 General introduction Chapter 2 Genetic and phenotypic responses to genomic selection for timing of breeding in a wild songbird Chapter 3 Temperature has a causal and plastic effect on timing of breeding in a small songbird Chapter 4 Exploration of tissue-specific gene expression patterns underlying timing of breeding in contrasting temperature environments in a songbird Chapter 5 Fine-tuning of seasonal timing of breeding is regulated downstream in the underlying neuro-endocrine system in a small songbird Chapter 6 Exploring temporal changes in DNA methylation and RNA expression in a small songbird-correlations within and between tissues Chapter 7 General discussion References Summary Samenvatting Curriculum vitae List of publications Acknowledgements WIAS Training and Education Statement CHAPTER 1 General introduction Chapter 1 10 Evolution and natural selection Evolution, the process that leads to the formation of and change in biological systems in response to their environment, has shaped life since its beginning and continues to do so. All organisms, simple and complex, evolve over different scales in both time and space. In general, evolution is described and studied as two distinct hierarchical processes; macroevolution and micro-evolution. Macro-evolution refers to the origin of new morphological forms, species and divisions of the taxonomic hierarchy above the species level, together with the origin of complex adaptations, such as the eye (Reznick & Ricklefs 2009), but on which I will not dwell further. In contrast, micro-evolution refers to the processes of adaptive modifications (i.e. through alteration in allele frequencies in gene pools) within and among populations, propelled by mutation, migration, genetic drift and natural selection. The latter, put first into words by, independently, both Charles Darwin (1859) and Alfred Russel Wallace (1858), is usually defined as the consequence of three organismal properties: (1) variation among organisms of a population, (2) differential reproduction, and (3) traits that are important for survival or reproduction show heritability (Darwin 1859; Wallace 1858).

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“…Large follicles could possess more gonadotropin (but also GnRH) receptors, and variation in gonadotropin responses to GnRH could also contribute to the observed variation in E 2 . Besides the fact that FSH antibodies are, to our knowledge, not currently available for birds, GnRHinduced LH concentrations have been shown to peak (within 5 min) and return to basal levels (within 30 min) very rapidly in different bird species [47,59,60]. As for VLDL, the optimal time point for measuring GnRH-induced LH is therefore very different than for E 2 , and further studies are warranted to elucidate how the various tiers of the HPG-axis interact in the minutes/hours following brain stimulation.…”

Section: Discussionmentioning

confidence: 98%

Personality and gonadal development as sources of individual variation in response to GnRH challenge in female great tits

et al. 2019

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Seasonal timing of reproduction is a key life-history trait, but we know little about the mechanisms underlying individual variation in female endocrine profiles associated with reproduction. In birds, 17b-oestradiol is a key reproductive hormone that links brain neuroendocrine mechanisms, involved in information processing and decision-making, to downstream mechanisms in the liver, where egg-yolk is produced. Here, we test, using a simulated induction of the reproductive system through a Gonadotropin-Releasing Hormone (GnRH) challenge, whether the ovary of pre-breeding female great tits responds to brain stimulation by increasing oestradiol. We also assess how this response is modified by individual-specific traits like age, ovarian follicle size, and personality, using females from lines artificially selected for divergent levels of exploratory behaviour. We show that a GnRH injection leads to a rapid increase in circulating concentrations of oestradiol, but responses varied among individuals. Females with more developed ovarian follicles showed stronger responses and females from lines selected for fast exploratory behaviour showed stronger increases compared to females from the slow line, indicating a heritable component. This study shows that the response of the ovary to reproductive stimulation from the brain greatly varies among individuals and that this variation can be attributed to several commonly measured individual traits, which sheds light on the mechanisms shaping heritable endocrine phenotypes.

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Changes in processes downstream of the hypothalamus are associated with seasonal follicle development in a songbird, the dark-eyed junco (Junco hyemalis)

Cited by 15 publications

References 64 publications

Migratory strategy explains differences in timing of female reproductive development in seasonally sympatric songbirds

Migratory strategy explains differences in timing of female reproductive development in seasonally sympatric songbirds

The mechanisms underlying seasonal timing of breeding : a multi-level approach using bi-directional genomic selection on timing of egg-laying

Personality and gonadal development as sources of individual variation in response to GnRH challenge in female great tits

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