Food availability, energetic constraints and reproductive development in a wild seasonally breeding songbird

Scott Davies, Thomas Cros, Damien Richard, Simone L. Meddle, Kazuyoshi Tsutsui, Pierre Deviche

    Research output: Contribution to journalArticle

    14 Citations (Scopus)

    Abstract

    In many organisms, food availability is a proximate cue that synchronizes seasonal development of the reproductive system with optimal environmental conditions. Growth of the gonads and secondary sexual characteristics is orchestrated by the hypothalamic-pituitary-gonadal (HPG) axis. However, our understanding of the physiological mechanisms by which food availability modulates activity of the HPG axis is limited. It is thought that many factors, including energetic status, modulate seasonal reproductive activation. We tested the hypothesis that food availability modulates the activity of the HPG axis in a songbird. Specifically, we food-restricted captive adult male Abert's Towhees Melozone aberti for 2 or 4 weeks during photoinduced reproductive development. A third group (control) received ad libitum food throughout. We measured multiple aspects of the reproductive system including endocrine activity of all three levels of the HPG axis [i.e. hypothalamic gonadotropin-releasing hormone-I (GnRH-I), plasma luteinizing hormone (LH) and testosterone (T)], and gonad morphology. Furthermore, because gonadotropin-inhibitory hormone (GnIH) and neuropeptide Y (NPY; a potent orexigenic peptide) potentially integrate information on food availability into seasonal reproductive development, we also measured the brain levels of these peptides. At the hypothalamic level, we detected no effect of food restriction on immunoreactive (ir) GnRH-I, but the duration of food restriction was inversely related to the size of ir-GnIH perikarya. Furthermore, the number of ir-NPY cells was higher in food-restricted than control birds. Food restriction did not influence photoinduced testicular growth, but decreased plasma LH and T, and width of the cloacal protuberance, an androgen-sensitive secondary sexual characteristic. Returning birds to ad libitum food availability had no effect on plasma LH or T, but caused the cloacal protuberance to rapidly increase in size to that of ad libitum-fed birds. Our results support the tenet that food availability modulates photoinduced reproductive activation. However, they also suggest that this modulation is complex and depends upon the level of the HPG axis considered. At the hypothalamic level, our results are consistent with a role for the GnIH and NPY systems in integrating information on energetic status. There also appears to be a role for endocrine function at the anterior pituitary gland and testicular levels in modulating reproductive development in the light of energetic status and independently of testicular growth.

    Original languageEnglish
    Pages (from-to)1421-1434
    Number of pages14
    JournalFunctional Ecology
    Volume29
    Issue number11
    DOIs
    Publication statusPublished - 2015 Nov 1

    Fingerprint

    songbird
    songbirds
    food availability
    hormone
    energetics
    breeding
    gonadotropins
    luteinizing hormone
    food
    secondary sexual characteristics
    reproductive system
    hormones
    gonadotropin-releasing hormone
    gonads
    bird
    hypothalamic hormones
    plasma
    peptides
    peptide
    seasonal development

    Keywords

    • Gonad development
    • Gonadotropin-inhibitory hormone
    • Gonadotropin-releasing hormone
    • Hypothalamic-pituitary-gonadal axis
    • Luteinizing hormone
    • Neuropeptide Y
    • Reproductive physiology
    • Seasonal reproduction
    • Testosterone

    ASJC Scopus subject areas

    • Ecology, Evolution, Behavior and Systematics

    Cite this

    Food availability, energetic constraints and reproductive development in a wild seasonally breeding songbird. / Davies, Scott; Cros, Thomas; Richard, Damien; Meddle, Simone L.; Tsutsui, Kazuyoshi; Deviche, Pierre.

    In: Functional Ecology, Vol. 29, No. 11, 01.11.2015, p. 1421-1434.

    Research output: Contribution to journalArticle

    Davies, Scott ; Cros, Thomas ; Richard, Damien ; Meddle, Simone L. ; Tsutsui, Kazuyoshi ; Deviche, Pierre. / Food availability, energetic constraints and reproductive development in a wild seasonally breeding songbird. In: Functional Ecology. 2015 ; Vol. 29, No. 11. pp. 1421-1434.
    @article{cb5fea48298e4352a63ca0b553207ffc,
    title = "Food availability, energetic constraints and reproductive development in a wild seasonally breeding songbird",
    abstract = "In many organisms, food availability is a proximate cue that synchronizes seasonal development of the reproductive system with optimal environmental conditions. Growth of the gonads and secondary sexual characteristics is orchestrated by the hypothalamic-pituitary-gonadal (HPG) axis. However, our understanding of the physiological mechanisms by which food availability modulates activity of the HPG axis is limited. It is thought that many factors, including energetic status, modulate seasonal reproductive activation. We tested the hypothesis that food availability modulates the activity of the HPG axis in a songbird. Specifically, we food-restricted captive adult male Abert's Towhees Melozone aberti for 2 or 4 weeks during photoinduced reproductive development. A third group (control) received ad libitum food throughout. We measured multiple aspects of the reproductive system including endocrine activity of all three levels of the HPG axis [i.e. hypothalamic gonadotropin-releasing hormone-I (GnRH-I), plasma luteinizing hormone (LH) and testosterone (T)], and gonad morphology. Furthermore, because gonadotropin-inhibitory hormone (GnIH) and neuropeptide Y (NPY; a potent orexigenic peptide) potentially integrate information on food availability into seasonal reproductive development, we also measured the brain levels of these peptides. At the hypothalamic level, we detected no effect of food restriction on immunoreactive (ir) GnRH-I, but the duration of food restriction was inversely related to the size of ir-GnIH perikarya. Furthermore, the number of ir-NPY cells was higher in food-restricted than control birds. Food restriction did not influence photoinduced testicular growth, but decreased plasma LH and T, and width of the cloacal protuberance, an androgen-sensitive secondary sexual characteristic. Returning birds to ad libitum food availability had no effect on plasma LH or T, but caused the cloacal protuberance to rapidly increase in size to that of ad libitum-fed birds. Our results support the tenet that food availability modulates photoinduced reproductive activation. However, they also suggest that this modulation is complex and depends upon the level of the HPG axis considered. At the hypothalamic level, our results are consistent with a role for the GnIH and NPY systems in integrating information on energetic status. There also appears to be a role for endocrine function at the anterior pituitary gland and testicular levels in modulating reproductive development in the light of energetic status and independently of testicular growth.",
    keywords = "Gonad development, Gonadotropin-inhibitory hormone, Gonadotropin-releasing hormone, Hypothalamic-pituitary-gonadal axis, Luteinizing hormone, Neuropeptide Y, Reproductive physiology, Seasonal reproduction, Testosterone",
    author = "Scott Davies and Thomas Cros and Damien Richard and Meddle, {Simone L.} and Kazuyoshi Tsutsui and Pierre Deviche",
    year = "2015",
    month = "11",
    day = "1",
    doi = "10.1111/1365-2435.12448",
    language = "English",
    volume = "29",
    pages = "1421--1434",
    journal = "Functional Ecology",
    issn = "0269-8463",
    publisher = "Wiley-Blackwell",
    number = "11",

    }

    TY - JOUR

    T1 - Food availability, energetic constraints and reproductive development in a wild seasonally breeding songbird

    AU - Davies, Scott

    AU - Cros, Thomas

    AU - Richard, Damien

    AU - Meddle, Simone L.

    AU - Tsutsui, Kazuyoshi

    AU - Deviche, Pierre

    PY - 2015/11/1

    Y1 - 2015/11/1

    N2 - In many organisms, food availability is a proximate cue that synchronizes seasonal development of the reproductive system with optimal environmental conditions. Growth of the gonads and secondary sexual characteristics is orchestrated by the hypothalamic-pituitary-gonadal (HPG) axis. However, our understanding of the physiological mechanisms by which food availability modulates activity of the HPG axis is limited. It is thought that many factors, including energetic status, modulate seasonal reproductive activation. We tested the hypothesis that food availability modulates the activity of the HPG axis in a songbird. Specifically, we food-restricted captive adult male Abert's Towhees Melozone aberti for 2 or 4 weeks during photoinduced reproductive development. A third group (control) received ad libitum food throughout. We measured multiple aspects of the reproductive system including endocrine activity of all three levels of the HPG axis [i.e. hypothalamic gonadotropin-releasing hormone-I (GnRH-I), plasma luteinizing hormone (LH) and testosterone (T)], and gonad morphology. Furthermore, because gonadotropin-inhibitory hormone (GnIH) and neuropeptide Y (NPY; a potent orexigenic peptide) potentially integrate information on food availability into seasonal reproductive development, we also measured the brain levels of these peptides. At the hypothalamic level, we detected no effect of food restriction on immunoreactive (ir) GnRH-I, but the duration of food restriction was inversely related to the size of ir-GnIH perikarya. Furthermore, the number of ir-NPY cells was higher in food-restricted than control birds. Food restriction did not influence photoinduced testicular growth, but decreased plasma LH and T, and width of the cloacal protuberance, an androgen-sensitive secondary sexual characteristic. Returning birds to ad libitum food availability had no effect on plasma LH or T, but caused the cloacal protuberance to rapidly increase in size to that of ad libitum-fed birds. Our results support the tenet that food availability modulates photoinduced reproductive activation. However, they also suggest that this modulation is complex and depends upon the level of the HPG axis considered. At the hypothalamic level, our results are consistent with a role for the GnIH and NPY systems in integrating information on energetic status. There also appears to be a role for endocrine function at the anterior pituitary gland and testicular levels in modulating reproductive development in the light of energetic status and independently of testicular growth.

    AB - In many organisms, food availability is a proximate cue that synchronizes seasonal development of the reproductive system with optimal environmental conditions. Growth of the gonads and secondary sexual characteristics is orchestrated by the hypothalamic-pituitary-gonadal (HPG) axis. However, our understanding of the physiological mechanisms by which food availability modulates activity of the HPG axis is limited. It is thought that many factors, including energetic status, modulate seasonal reproductive activation. We tested the hypothesis that food availability modulates the activity of the HPG axis in a songbird. Specifically, we food-restricted captive adult male Abert's Towhees Melozone aberti for 2 or 4 weeks during photoinduced reproductive development. A third group (control) received ad libitum food throughout. We measured multiple aspects of the reproductive system including endocrine activity of all three levels of the HPG axis [i.e. hypothalamic gonadotropin-releasing hormone-I (GnRH-I), plasma luteinizing hormone (LH) and testosterone (T)], and gonad morphology. Furthermore, because gonadotropin-inhibitory hormone (GnIH) and neuropeptide Y (NPY; a potent orexigenic peptide) potentially integrate information on food availability into seasonal reproductive development, we also measured the brain levels of these peptides. At the hypothalamic level, we detected no effect of food restriction on immunoreactive (ir) GnRH-I, but the duration of food restriction was inversely related to the size of ir-GnIH perikarya. Furthermore, the number of ir-NPY cells was higher in food-restricted than control birds. Food restriction did not influence photoinduced testicular growth, but decreased plasma LH and T, and width of the cloacal protuberance, an androgen-sensitive secondary sexual characteristic. Returning birds to ad libitum food availability had no effect on plasma LH or T, but caused the cloacal protuberance to rapidly increase in size to that of ad libitum-fed birds. Our results support the tenet that food availability modulates photoinduced reproductive activation. However, they also suggest that this modulation is complex and depends upon the level of the HPG axis considered. At the hypothalamic level, our results are consistent with a role for the GnIH and NPY systems in integrating information on energetic status. There also appears to be a role for endocrine function at the anterior pituitary gland and testicular levels in modulating reproductive development in the light of energetic status and independently of testicular growth.

    KW - Gonad development

    KW - Gonadotropin-inhibitory hormone

    KW - Gonadotropin-releasing hormone

    KW - Hypothalamic-pituitary-gonadal axis

    KW - Luteinizing hormone

    KW - Neuropeptide Y

    KW - Reproductive physiology

    KW - Seasonal reproduction

    KW - Testosterone

    UR - http://www.scopus.com/inward/record.url?scp=84945268627&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=84945268627&partnerID=8YFLogxK

    U2 - 10.1111/1365-2435.12448

    DO - 10.1111/1365-2435.12448

    M3 - Article

    AN - SCOPUS:84945268627

    VL - 29

    SP - 1421

    EP - 1434

    JO - Functional Ecology

    JF - Functional Ecology

    SN - 0269-8463

    IS - 11

    ER -