2. BIOL30001 Reproductive Physiology Seasonal breeding – a matter of time Geoff Shaw Circadian and circannual rhythms Retino-hypothalamic tract Pineal and melatonin References Johnson (7 th Ed) Ch 6, esp pp 122-127. Johnson and Everitt (6 th ed) Chapter 6 Austin and Short: Reproduction in Mammals Book 3 (2nd edition) Chapter 3 The pineal gland Lincoln et al., 2003 J Endocrinol 179,1-13

3. Patterns of breeding cycle Many patterns continuous continuous with seasonal variation extended period of breeding very brief breeding season variation within species depending on environment

4. Environmental control of breeding cycles Environmental variation affects survival Powerful selection pressure to time breeding to maximise reproductive success Ultimate factors provide the evolutionary selection pressure and include food, temperature, rainfall, humidity Because in many environments the availability of food, temperature etc vary seasonally, and many species breed on an annual cycle cued by photoperiod as a proximate factor. Not all species breed seasonally –continuous –opportunistic cued by environmental factors Male - female differences in patterns

5. Food as a proximate factor Nutritional influences on reproduction –calorie balance –hormones or other factors in feed

6. hormones and other factors in feed affect timing of breeding

7. Food and rainfall

8. Flexibility in breeding patterns depending on location alternate cues alternate use of cues rapid selection for variants that maximise success Observed breeding seasons (% females pregnant) of Peromyscus over USA. rectangles marked X are all same species P. maniculatus

9. Photoperiod correlates with seasonal changes in weather, food etc. most obvious changes in temperate environments photoperiod changes with latitude –little photoperiod change in equatorial region –extreme photoperiod change in polar regions absolute daylength vs change in daylength allows long-term synchronization - eg autumn mating for spring births

10. Seasonal breeding patterns Photoperiodic control requires 3 components 1.photoreceptor (clock) 2.neural pathway linking clock to neuroendocrine pathways 3.endocrine response of hypothalamo-pituitary- gonadal axis variation between species –short day breeders –long day breeders

11. Seasonal breeding Climate and food availability = survival ensure offspring born best time more pronounced away from tropics (greater seasonal variation) Ultimate factors: temperature, rainfall, food availability Proximal factors or predictors: daylength Regulating time of conception short gestation spp – spring eg hamster, birds long gestation spp – autumn eg sheep, deer variable gestation spp (delayed implantation/ embryonic diapause) eg kangaroos, mustelids, seals Alignment with season crucial for species survival

12. Breeding pattern in Soay sheep from Foster et al, 1986

13. 20% 50% 1 st winter mortality Cycle of breeding and birth in Soay sheep

14. Circannual rhythms in the Soay ram

15. “Thank goodness breeding season is over”

16. Circannual rhythms Seasonal sexual cycle of a Soay ram AutumnSummerSpring Other circannual rhythms moulting, antlers, food intake, weight gain, seasonal breeding Sequence of seasonal reactivation similar to puberty

17. Circadian rhythms Cyclical activities in the female rat nocturnal activity cycle – a 24 h cycle production of oocyte – a 4-5 day cycle –LH Surge (2-4 pm), 5-7 h before darkness –Ovulation (2-4 am), during active period Johnson and Everitt Fig 6.25: Serum hormone levels during the oestrous cycle of the rat Other circadian rhythms temperature, melatonin, prolactin, growth hormone, corticosterone, sleep-wake, etc

18. The pineal gland endocrine gland in roof of brain photoreceptive in lower vertebrates receives photic input via suprachiasmatic nucleus and superior cervical ganglion makes the indole hormone melatonin in dark tammar wallaby pineal. Photo: G Shaw

19. The photo-neuro-endocrine pathway seasonality is disturbed by: blinding lesions of the SCN ablation of the SCG pinealectomy photoperiod changes and continuous light or dark long-lasting melatonin implants

20. control of melatonin secretion Tryptophan Serotonin N-Acetyl-serotonin Melatonin Tryptophan-5-hydroxylase N-acetyl-transferase (NAT) hydroxyindole-o-methyl-transferase (HIOMT) c-AMP NA sympathetic nerves RR nocturnal stimulation +

21. Photoperiod and melatonin effects on LH in ewes from J&E fig 6-27 16:0024:0008:0016:00 Serum melatonin 0100 10 5 1 Serum LH (ng/ml) days intact pineal & controlled photoperiod long dayshort day 16:0024:0008:0016:00 Serum melatonin 16:0024:0008:0016:00 Serum melatonin 16:0024:0008:0016:00 Serum melatonin pinealectomy & melatonin infusion to mimic long/short photoperiod 0100 10 5 1 Serum LH (ng/ml) days

22. Melatonin profiles in Soay rams moved to continuous dark Endogenous melatonin cycle persists in continuous dark but is normally entrained by light-dark cycle

23. Retino-hypothalamic-pineal tract

24. Melatonin: the hormone of darkness melatonin secreted at night synthesized in the pineal gland and released reflects the length of the night changing melatonin profile alters GnRH secretion TRYPTOPHAN Tryptophan hydroxylase 5-HYDROXYTRYPTOPHAN 5-hydroxytryptophan decarboxylase SEROTONIN N-acetyl transferase N- ACTEYLSEROTONIN hydroxyindole-o-methyl transferase MELATONIN (5- METHOXYTRYPTAMINE)

25. MBH medial basal hypothalamus PT pars tuberalis POA preoptic area OC optic chiasma PVN paraventricular nucleus A15 dopaminergic A15 nucleus VMH ventromedial nucleus ARC arcuate nucleus ME median eminence MB mammilary bodies MT receptors in medial basal hypothalamus & pars tuberalis MT affects electrical activity GnRH neurones MT affects synthesis of neurotransmitters Ovine hypothalamus MB MBH PT PVN Pituitary gland OC POA A15 VMH ME ARC 3 RD VENTRICLE Distribution of melatonin binding areas

26. Seasonal cycle in prolactin secretion in Syrian hamster and Soay sheep SD = Low Prl LD = High Prl Photoinduction = response to change from SD to LD or vice versa Refractoriness = inhibitory or stimulatory effects of photoperiod wear off All photoperiodic species show high prolactin under long days Prolactin secretion and the pelage/moult cycle

27. The biological clock self sustaining biological clock or oscillator in SCN constant light or dark free - runs c. 24 h located in suprachiasmatic nucleus entrained by photic stimuli via retinohypothalamic tract (feeds photoperiod info to clock in SCN) lesion to tract (SCN  SCG  pineal) disrupts circadian rhythms rhythm expressed by melatonin secretion melatonin receptor found in MBH and PT circannual cycles in prolactin associated with pelage pars tuberalis has calendar cells

28. Control of seasonal breeding Pineal gland transducer of photic information from retina involved in time perception via clock genes makes melatonin in dark Hypothalamus GnRH release modulated by melatonin (via MBH?) regulation of steroid feedback pars tuberalis  prolactin Gonads CNS integrates environmental cues light, olfactory stimuli, temperature,..... neural signals melatonin GnRH Anterior Pituitary tuberalin from pars tuberalis  prolactin GnRH regulates LH and FSH secretion LH & FSH