The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent

McGuire, Nicolette L.; Koh, Annie; Bentley, G.

doi:10.7717/peerj.139

Cited by 65 publications

(73 citation statements)

References 66 publications

(75 reference statements)

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“…LHR and FSHR are important for seasonal gonadal growth in birds, and GR and MR can suppress gonadal growth and activation in birds (McGuire et al, 2013;Blas, 2015;Vizcarra et al, 2015). Therefore, we predicted higher LHR and FSHR transcript abundance in sedentary urban juncos in early spring and higher GR and/or MR transcript abundance in migrant juncos in early spring.…”

Section: Introductionmentioning

confidence: 84%

“…The absence of differences in gonadal LHR and FSHR transcripts, combined with elevated baseline LH observed from urban sedentary birds and elevated baseline testosterone during the final 2 weeks of our captive study, suggests that the earlier gonadal growth and responsiveness was not the result of a change in gonadal LH sensitivity to LH or FSH. Recent work has identified an inhibitory role of Gonadotropin Inhibitory Hormone (GnIH) in the gonads of male songbirds (McGuire et al, 2013;Ernst et al, 2016). Future work is needed to identify whether decreased gonadal GnIH production and/or gonadal GnIH receptor abundance in sedentary urban juncos in early spring could be acting as a mechanism for earlier onset of reproduction.…”

Section: Discussionmentioning

confidence: 99%

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Mechanisms Associated with an Advance in the Timing of Seasonal Reproduction in an Urban Songbird

et al. 2017

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The colonization of urban environments by animals is often accompanied by earlier breeding and associated changes in seasonal schedules. Accelerated timing of seasonal reproduction in derived urban populations is a potential cause of evolutionary divergence from ancestral populations if differences in physiological processes that regulate reproductive timing become fixed over time. We compared reproductive development in free-living and captive male dark-eyed juncos deriving from a population that recently colonized a city (∼35 years) and ceased migrating to that of conspecifics that live in sympatry with the urban population during winter and spring but migrate elsewhere to breed. We predicted that the earlier breeding sedentary urban birds would exhibit accelerated reproductive development in the spring along the hypothalamic-pituitary-gonadal (HPG) axis as compared to migrants. We found that free-living sedentary urban and migrant juncos differed at the level of the pituitary when measured as baseline luteinizing hormone (LH) levels, but not in increased LH when challenged with Gonadotropin-Releasing Hormone (GnRH). Among captives held in a common garden, and at the level of the gonad, we found that sedentary urban birds produced more testosterone in response to GnRH than migrants living in the same common environment, suggesting greater gonadal sensitivity in the derived urban population. Greater gonadal sensitivity could arise from greater upstream activation by LH or FSH or from reduced suppression of gonadal development by the adrenal axis. We compared abundance of gonadal transcripts for LH receptor (LHR), follicle stimulating hormone receptor (FSHR), glucocorticoid receptor (GR), and mineralocorticoid receptor (MR) in the common-garden, predicting either more abundant transcripts for LHR and FSHR or fewer transcripts for GR and MR in the earlier breeding sedentary urban breeders, as compared to the migrants. We found no difference in the expression of these genes. Together these data suggest that advanced timing of reproduction in a recently derived urban population is facilitated by earlier increase in upstream baseline activity of the HPG and earlier release from gonadal suppression Fudickar et al. Timing of Reproduction following Urbanizationby yet-to-be-discovered mechanisms. Evolutionarily, our results suggest that potential for gene flow between seasonally sympatric populations may be limited due to urban-induced advances in the timing of reproduction and resulting allochrony with ancestral forms.

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Section: Introductionmentioning

confidence: 84%

Section: Discussionmentioning

confidence: 99%

Mechanisms Associated with an Advance in the Timing of Seasonal Reproduction in an Urban Songbird

et al. 2017

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“…In the House Sparrow (Passer domesticus), GnIH inhibits T secretion of in vitro testis tissue (McGuire and Bentley 2010). Furthermore, in the Zebra Finch (Taeniopygia guttata), in vitro CORT treatment stimulated the expression of testicular GnIH (McGuire et al 2013), and higher plasma CORT during stress also was positively correlated with testicular GnIH expression (Lynn et al 2015). The studies described above examined the change in T secretion 2-10 h after treatment.…”

Section: Associations Between Initial and Stress-induced Changes In Pmentioning

confidence: 94%

Innate immunity and testosterone rapidly respond to acute stress, but is corticosterone at the helm?

et al. 2016

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When faced with a stressor, vertebrates can rapidly increase the secretion of glucocorticoids, which is thought to improve the chances of survival. Concurrent changes in other physiological systems, such as the reproductive endocrine or innate immune systems, have received less attention, particularly in wild vertebrates. It is often thought that glucocorticoids directly modulate immune performance during a stress response, but, in many species, androgens also rapidly respond to stress. However, to our knowledge, no study has simultaneously examined the interactions between the glucocorticoid, androgen, and innate immune responses to stress in a wild vertebrate. To address this issue, we tested the hypothesis that the change in plasma corticosterone (CORT) in response to the acute stress of capture and restraint is correlated with the concurrent changes in plasma testosterone (T) and innate immune performance (estimated by the capacity of plasma to agglutinate and lyse foreign cells) in the Abert's Towhee (Melozone aberti). Furthermore, to broaden the generality of the findings, we compared male and female towhees, as well as males from urban and non-urban populations. Acute stress increased plasma CORT, decreased plasma T in males, and decreased innate immune performance, but the increase in CORT during stress was not correlated with the corresponding decreases in either plasma T or innate immunity. By contrast, the plasma T stress response was positively correlated with the innate immune stress response. Collectively, our results challenge the proposition that the glucocorticoid stress response is correlated with the concurrent changes in plasma T, a key reproductive hormone, and innate immunity, as estimated by agglutination and lysis.

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“…Avian testes in vitro respond directly to metabolic stress (McGuire et al, 2013), and in mammals, the administration of glucose (Ohkura et al, 2000) and fatty acids (Garrel et al, 2011) can alter LH secretion. Generally consistent with these observations, in the European starling, decreased access to food affected gonadal maturation only when birds also lost body mass (Meijer, 1991;Dawson, 1986), implicating the importance of a metabolic pathway in influencing the HPG axis.…”

Section: Metabolic Versus Perceptual Pathwaymentioning

confidence: 99%

Food restriction negatively affects multiple levels of the reproductive axis in male house finches, Haemorhous mexicanus

Valle

Carpentier

et al. 2015

Journal of Experimental Biology

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Nutrition influences reproductive functions across vertebrates, but the effects of food availability on the functioning of the hypothalamicpituitary-gonadal (HPG) axis in wild birds and the mechanisms mediating these effects remain unclear. We investigated the influence of chronic food restriction on the HPG axis of photostimulated house finches, Haemorhous mexicanus. Food-restricted birds had underdeveloped testes with smaller seminiferous tubules than ad libitum-fed birds. Baseline plasma testosterone increased in response to photostimulation in ad libitum-fed but not in food-restricted birds. Food availability did not, however, affect the plasma testosterone increase resulting from a gonadotropin-releasing hormone-I (GnRH) or a luteinizing hormone (LH) challenge. The number of hypothalamic GnRH immunoreactive (ir) but not proGnRH-ir perikarya was higher in food-restricted than in ad libitum-fed finches, suggesting inhibited secretion of GnRH. Hypothalamic gonadotropin-inhibitory hormone (GnIH)-ir and neuropeptide Y (NPY)-ir were not affected by food availability. Plasma corticosterone (CORT) was also not affected by food availability, indicating that the observed HPG axis inhibition did not result from increased activity of the hypothalamic-pituitaryadrenal (HPA) axis. This study is among the first to examine multilevel functional changes in the HPG axis in response to food restriction in a wild bird. The results indicate that food availability affects both hypothalamic and gonadal function, but further investigations are needed to clarify the mechanisms by which nutritional signals mediate these effects.

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The direct response of the gonads to cues of stress in a temperate songbird species is season-dependent

Cited by 65 publications

References 66 publications

Mechanisms Associated with an Advance in the Timing of Seasonal Reproduction in an Urban Songbird

Mechanisms Associated with an Advance in the Timing of Seasonal Reproduction in an Urban Songbird

Innate immunity and testosterone rapidly respond to acute stress, but is corticosterone at the helm?

Food restriction negatively affects multiple levels of the reproductive axis in male house finches, Haemorhous mexicanus

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