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      Early spring sex differences in luteinizing hormone response to gonadotropin releasing hormone in co-occurring resident and migrant dark-eyed juncos ( Junco hyemalis)

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          Highlights

          • In early spring female juncos vary in LH following repeated stimulation with GnRH.

          • Resident and migrant males do not vary in LH.

          • Suggests the pituitary as a critical point of control for reproductive timing.

          • Sex difference suggests selection shaped responsiveness at critical time points.

          Abstract

          To optimally time reproduction, animals must coordinate changes in the hypothalamo-pituitary-gonadal (HPG) axis. The extent of intra-species variation in seasonal timing of reproductive function is considerable, both within and among populations. Dark-eyed junco ( Junco hyemalis) populations are known to differ in their reproductive timing response to cues experienced in the same habitat in late winter/early spring. Specifically in juncos cohabitating on shared wintering grounds, residents initiate breeding and reproductive activity but migrants delay reproductive development and prepare to migrate before breeding. Here, we test the hypothesis that the pituitary gland acts as a ‘control point’ to modulate differential HPG axis activity across populations. We sampled free-living resident and migrant juncos on their shared over-wintering grounds in March, thus all individuals were experiencing the same environmental cues, including photoperiod. We predicted that during this critical time of transition, residents would more readily respond to repeated gonadotropin releasing hormone (GnRH) stimulation with increases in luteinizing hormone (LH), in contrast to migrants, which should delay full reproductive activity. Our data indicate that migrant females, while still on the overwintering grounds, have a reduced LH response to repeated GnRH injections compared to resident females. Male migrant and resident birds did not differ in their responsiveness to repeated GnRH. Our results suggest a sex difference in the costs of mistimed activation of the HPG axis, with female migrants being less responsive than residents females and males to repeated stimulation. Further, our data implicate a key role for the pituitary in regulating appropriate reproductive timing responses.

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          Most cited references45

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          Reproduction and resistance to stress: when and how.

          Environmental and social stresses have deleterious effects on reproductive function in vertebrates. Global climate change, human disturbance and endocrine disruption from pollutants are increasingly likely to pose additional stresses that could have a major impact on human society. Nonetheless, some populations of vertebrates (from fish to mammals) are able to temporarily resist environmental and social stresses, and breed successfully. A classical trade-off of reproductive success for potential survival is involved. We define five examples. (i) Aged individuals with minimal future reproductive success that should attempt to breed despite potential acute stressors. (ii) Seasonal breeders when time for actual breeding is so short that acute stress should be resisted in favour of reproductive success. (iii) If both members of a breeding pair provide parental care, then loss of a mate should be compensated for by the remaining individual. (iv) Semelparous species in which there is only one breeding period followed by programmed death. (v) Species where, because of the transience of dominance status in a social group, individuals may only have a short window of opportunity for mating. We suggest four mechanisms underlying resistance of the gonadal axis to stress. (i) Blockade at the central nervous system level, i.e. an individual no longer perceives the perturbation as stressful. (ii) Blockade at the level of the hypothalamic-pituitary-adrenal axis (i.e. failure to increase secretion of glucocorticosteroids). (iii) Blockade at the level of the hypothalamic-pituitary-gonad axis (i.e. resistance of the reproductive system to the actions of glucocorticosteroids). (iv) Compensatory stimulation of the gonadal axis to counteract inhibitory glucocorticosteroid actions. Although these mechanisms are likely genetically determined, their expression may depend upon a complex interaction with environmental factors. Future research will provide valuable information on the biology of stress and how organisms cope. Such mechanisms would be particularly insightful as the spectre of global change continues to unfold.
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            The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding.

            Reproductive success usually declines in the course of the season, which may be a direct effect of breeding time, an effect of quality (individuals with high phenotypic or environmental quality breeding early), or a combination of the two. Being able to distinguish between these possibilities is crucial when trying to understand individual variation in annual routines, for instance when to breed, moult and migrate. We review experiments with free-living birds performed to distinguish between the 'timing' and 'quality' hypothesis. 'Clean' manipulation of breeding time seems impossible, and we therefore discuss strong and weak points of different manipulation techniques. We find that the qualitative results were independent of manipulation technique (inducing replacement clutches versus cross-fostering early and late clutches). Given that the two techniques differ strongly in demands made on the birds, this suggests that potential experimental biases are limited. Overall, the evidence indicated that date and quality are both important, depending on fitness component and species, although evidence for the date hypothesis was found more frequently. We expected both effects to be prevalent, since only if date per se is important, does an incentive exist for high-quality birds to breed early. We discuss mechanisms mediating the seasonal decline in reproductive success, and distinguish between effects of absolute date and relative date, for instance timing relative to seasonal environmental fluctuations or conspecifics. The latter is important at least in some cases, suggesting that the optimal breeding time may be frequency dependent, but this has been little studied. A recurring pattern among cross-fostering studies was that delay experiments provided evidence for the quality hypothesis, while advance experiments provided evidence for the date hypothesis. This indicates that late pairs are constrained from producing a clutch earlier in the season, presumably by the fitness costs this would entail. This provides us with a paradox: evidence for the date hypothesis leads us to conclude that quality is important for the ability to breed early.
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              Directional selection and the evolution of breeding date in birds.

              In many bird species, those pairs that breed earlier in the season have higher reproductive success than those that breed later. Since breeding date is known to be heritable, it is unclear why it does not evolve to an earlier time. Under assumptions outlined by Fisher, a model is developed that shows how breeding date may have considerable additive genetic variance, appear to be under directional selection, and yet not evolve. These results provide a general explanation for a persistent correlation of fitness with a variety of traits in natural populations.
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                Author and article information

                Contributors
                Journal
                Gen Comp Endocrinol
                Gen. Comp. Endocrinol
                General and Comparative Endocrinology
                Academic Press
                0016-6480
                1095-6840
                15 September 2016
                15 September 2016
                : 236
                : 17-23
                Affiliations
                [a ]Department of Biological Sciences and Environmental and Conservation Sciences Program, North Dakota State University, Fargo, ND, United States
                [b ]Department of Biology, Center for the Integrative Study of Animal Behavior, Indiana University, Bloomington, IN, United States
                [c ]The Roslin Institute, The Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Midlothian, EH25 9RG Scotland, UK
                Author notes
                [* ]Corresponding author. timothy.greives@ 123456ndsu.edu
                Article
                S0016-6480(16)30197-6
                10.1016/j.ygcen.2016.06.031
                5036536
                27374492
                7b762596-d26d-453e-9198-da2e503e20f8
                © 2016 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 9 February 2016
                : 27 June 2016
                : 28 June 2016
                Categories
                Research Paper

                Endocrinology & Diabetes
                seasonal breeding,phenology,supplemental cues,sex differences,songbird
                Endocrinology & Diabetes
                seasonal breeding, phenology, supplemental cues, sex differences, songbird

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