Paul D. Heideman

Disrupted seasonal biology impacts health, food security and ecosystems

The rhythm of life on earth is shaped by seasonal changes in the environment. Plants and animals show profound annual cycles in physiology, health, morphology, behaviour and demography in response to environmental cues. Seasonal biology impacts ecosystems and agriculture, with consequences for humans and biodiversity. Human populations show robust annual rhythms in health and well-being, and the birth month can have lasting effects that persist throughout life. This review emphasizes the need for a better understanding of seasonal biology against the backdrop of its rapidly progressing disruption through climate change, human lifestyles and other anthropogenic impact. Climate change is modifying annual rhythms to which numerous organisms have adapted, with potential consequences for industries relating to health, ecosystems and food security. Disconcertingly, human lifestyles under artificial conditions of eternal summer provide the most extreme example for disconnect from natural seasons, making humans vulnerable to increased morbidity and mortality. In this review, we introduce scenarios of seasonal disruption, highlight key aspects of seasonal biology and summarize from biomedical, anthropological, veterinary, agricultural and environmental perspectives the recent evidence for seasonal desynchronization between environmental factors and internal rhythms. Because annual rhythms are pervasive across biological systems, they provide a common framework for trans-disciplinary research.

Divergent Regulation of Hypothalamic Neuropeptide Y and Agouti‐Related Protein by Photoperiod in F344 rats With Differential Food Intake and Growth

Hypothalamic genes involved in food intake and growth regulation were studied in F344 rats in response to photoperiod. Two sub‐strains were identified: F344/NHsd (F344/N) and F344/NCrHsd (F344/NCr); sensitive and relatively insensitive to photoperiod respectively. In F344/N rats, marked, but opposite, changes in the genes for neuropeptide Y (NPY) (+97.5%) and agouti‐related protein (AgRP) (−39.3%) expression in the arcuate nucleus were observed in response to short (8 : 16 h light/dark cycle, SD) relative to long (16 : 8 h light/dark cycle, LD) day photoperiods. Changes were associated with both reduced food intake and growth. Expression of the genes for cocaine and amphetamine‐regulated transcript (CART) and pro‐opiomelanocortin (POMC) in the arcuate nucleus was unchanged by photoperiod. POMC in the ependymal layer around the third ventricle was markedly inhibited by SD. Parallel decreases in the genes for growth hormone‐releasing hormone (GHRH) and somatostatin (Somatostatin) mRNA in the arcuate nucleus and Somatostatin in the periventricular nucleus were observed in SD. Serum levels of insulin‐like growth factor (IGF)‐1 and insulin were lower in F344/N rats in SD, whereas neither leptin nor corticosterone levels were affected. By contrast, F344/NCr rats that show only minor food intake and growth rate changes showed minimal responses in these genes and hormones. Thus, NPY/AgRP neurones may be pivotal to the photoperiodic regulation of food intake and growth. Potentially, the SD increase in NPY expression may inhibit growth by decreasing GHRH and Somatostatin expression, whereas the decrease in AgRP expression probably leads to reduced food intake. The present study reveals an atypical and divergent regulation of NPY and AgRP, which may relate to their separate roles with respect to growth and food intake, respectively.

Sensitivity of Syrian hamsters (Mesocricetus auratus) to amplitudes and rates of photoperiodic change typical of the tropics.

Empirical data suggest that reproductive photoresponsiveness occurs in some populations of mammals above 13° of latitude, but may be absent in populations from 0° to 10° of latitude. The present experiments examined the degree to which the low amplitude of change in photoperiod in the tropics constrains mammals from using daylength as a seasonal cue. The Syrian hamster, a temperate-zone species, was studied because of its well-documented ability to respond to small changes in photoperiod, and because of the absence of an alternative robustly responding species from the tropics. We subjected adult male hamsters to photoperiods that mimicked the amplitude and rate of photoperiod change of 30°, 20°, 10°, and 5° of latitude, but centered around an estimate of their critical daylength. For comparison, a fifth group was subjected to an abrupt change in daylength of a magnitude equal to the total annual variation occurring at 30°. The two groups experiencing the gradually changing daylengths of 30° and 20° showed less within-group synchrony during testicular regression; in other dimensions of the annual testis cycle, including the degree of synchrony exhibited during recrudescence, they reacted similarly to the hamsters given the abrupt change in daylength. Some of the hamsters exposed to the gradually changing daylengths of 10° responded to this challenge, as did a few in the 5° treatment-in both cases, with poor within-group synchrony and a submaximal decrease in testis size. In an abbreviated second experiment, hamsters given abrupt decreases in daylength of magnitudes equal to those of the 10° and 5° groups responded slightly more frequently, and with maximal decreases in testis size. This suggests that mammals may not be constrained absolutely by an inability to respond to changes in photoperiod at 5° to 10° latitude. Seasonally breeding populations of mammals in the deep tropics that do not use photoperiod to regulate reproduction may use nonphotoperiodic cues because they offer a higher signal-to-noise ratio than do tropical changes in photoperiod.

Environmental Regulation of Reproduction

Publisher Summary Reproductive and life-history strategies vary tremendously among bats, even within species. Understanding the nature of this variation and the evolution of these strategies requires an understanding of the mechanisms responsible. This chapter reviews what is known about environmental factors that affect reproduction in bats in the context of both ultimate causes and underlying neuroendocrine mechanisms. It focuses on the results of experimental laboratory studies; however, some field studies that offer insights into mechanisms are also discussed. In general, it addresses four vital questions. The first question examines the ultimate factors that favor or disfavor the environmental regulation of reproduction in bats. The second question explores how signals from the environment become translated into physiological signals that alter reproductive events. The third question pertains to the the additional insight that is offered by field studies. Finally, the fourth question reveals what else is needed to be known, and why it is important to know it. The chapter concludes by stating that the environment also affects reproduction in bats. Low body temperatures act directly on reproduction by slowing down the metabolic rate and slowing or delaying reproductive events. Other environmental factors, such as photoperiod, act indirectly on the reproductive axis through regulatory neuroendocrine circuits that process sensory input and modify reproductive status.

Seasonality and synchrony of reproduction in three species of nectarivorous Philippines bats.

BackgroundDifferences among species and among years in reproductive seasonality (the tendency for clusters of events to fall at approximately the same point in each year) and synchrony (amount of clustering of events within a year) have been intensively studied in bats, but are difficult to assess. Here, we use randomization methods with circular statistics to test for synchrony and seasonality of reproduction in three species of nectarivorous megachiropteran bats on Negros Island in the central Philippines.ResultsIn Rousettus amplexicaudatus, estimated dates of birth were both highly synchronous and highly seasonal. In Macroglossus minimus, estimated births were seasonal and significantly clustered within years, but within each year births occurred over a broad period, indicating a low level of synchrony. In Eonycteris spelaea, estimated births were also seasonal and had statistically significant synchrony, with birth periods within years intermediate in synchrony between R. amplexicaudatus and M. minimus. All three species had a similar seasonal pattern, with two birth periods in each year, centered on March or April and August or September. In one species, R. amplexicaudatus, primigravid females (in their first pregnancy) produced their young in June and July, a birth period significantly different in timing from the two birth periods of older adult females. This more conservative pattern of young females may allow higher survival of parents and offspring at cost of a lost reproductive opportunity. There was weak evidence that in some years primigravid females of M. minimus might differ in timing from older adults. There were few significant differences in reproductive timing among different years, and those differences were generally less than two weeks, even during a severe drought in the severe el Niño of 1983.ConclusionThe results suggest that these species follow an obligately seasonal pattern of reproductive timing with very little phenotypic plasticity. The resampling methods were sensitive to differences in timing of under two weeks, in some cases, suggesting that these are useful methods for analyses of seasonality in wild populations of bats.

Tau differences between short-day responsive and short-day nonresponsive white-footed mice (Peromyscus leucopus) do not affect reproductive photoresponsiveness.

In laboratory-bred rodent populations, intraspecific variation in circadian system organization is a known cause of individual variation in reproductive photoresponsiveness. The authors sought to determine whether circadian system variation accounted for individual variation in reproductive photoresponsiveness in a single, highly genetically variable population of Peromyscus leucopusrecently derived from the wild. Running-wheel activity patterns of male and female mice, aged 70 to 90 days, from artificially selected lines of reproductively photoresponsive (R) and nonresponsive (NR) lines were monitored under short-day photoperiod (8 h light, 16 h dark), long-day photoperiod (16 h light, 8 h dark), and constant darkness (DD). NR mice displayed a significantly longer mean free-running period (24.08 h) in DD compared with R mice (23.75 h), due in large part to a difference between NR and R females (24.25 h vs. 23.74 h, respectively). All other entrainment characteristics (alpha, phase angle of activity) under short days, long days, and DD were similar between R and NR mice. Variation in free- running period and entrainment characteristics has been shown to affect photoresponsiveness in other rodent species by altering the manner in which the circadian system interprets short days. To determine whether variation in photoresponsiveness in P. leucopus is due to differences in free-running period instead of variation downstream from the central circadian clock in the pathway controlling photoresponsiveness, the authors exposed young R and NR mice to DD and measured the effect on reproductive organ development. If variation in free-running period affected how the circadian system of mice interpreted short days, then both R and NR mice exposed to DD should have exhibited a delay in gonadal development. Only R mice exhibited pubertal delay in DD. NR mice exhibited large paired testes, paired seminal vesicles, paired ovaries, and uterine weight typical of mice nonresponsive to short days, whereas R mice exhibited reproductive organ weight typical of mice responsive to short days. These data suggest that despite significant differences in free-running period between R and NR mice, individual variation in photoresponsiveness is not due to differences in how the circadian systems of R and NR mice interpret the LD cycle.

Differences in hypothalamic 2-[125I]iodomelatonin binding in photoresponsive and non-photoresponsive white-footed mice, Peromyscus leucopus

Photoperiod is an environmental cue used by many temperate-zone species to regulate their reproductive timing. Within species, the degree of reproductive photoresponsiveness can vary widely both among and within populations. The neuroendocrine mechanisms causing this individual variation in photoresponsiveness are unknown. Using selected lines from a population of white-footed mice known to vary genetically in reproductive photoresponsiveness, we tested the hypothesis that variation in the number and/or location of melatonin receptors is the basis for individual differences in reproductive photoresponsiveness. The brains and pars tuberalis of the pituitary from sixteen mice, (eight mice from each of two lines selected for two generations to respond strongly or weakly to photoperiod), were processed for autoradiography using the radioligand 2-[125I]-iodomelatonin (IMEL). We found significantly higher specific IMEL binding in the medial preoptic area and the bed nucleus of the stria terminalis of non-responsive mice than responsive mice. There were no differences between groups in specific IMEL binding in the suprachiasmatic and dorsomedial nuclei of the hypothalamus, pars tuberalis, or paraventricular nucleus of the thalamus. These results provide support for the hypothesis that individual variation in photoresponsiveness is due in part to differences in the density or affinity of melatonin receptors.

Photoresponsive Fischer 344 Rats are Reproductively Inhibited by Melatonin and Differ in 2‐[125I] Iodomelatonin Binding from Nonphotoresponsive Sprague‐Dawley Rats

Many temperate‐zone species use photoperiod as an environmental cue to regulate reproductive timing. Strains of laboratory rats differ in their responsiveness to photoperiod, with the Fischer 344 (F344) strain being the most responsive known. F344 rats and closely related strains that differ in photoresponsiveness may be useful models to study the mechanisms and genetic basis for photoresponsiveness. We tested two hypotheses: (i) that melatonin mediates photoresponsiveness in F344 rats, as is the case in all other mammals tested, and (ii) that the location, abundance, or affinity of melatonin receptors, as estimated by the amount and location of binding of the radioligand 2‐[125I]‐iodomelatonin (IMEL) in the brain, might cause variation in photoresponsiveness among rat strains. Melatonin injections 1 h before lights off in a stimulatory photoperiod (L14 : D10) induced reproductive inhibition and reduced weight gain in a manner similar to short days of L8 : D16, while injections of ethanolic saline vehicle did not. Interestingly, melatonin injections administered during an inhibitory photoperiod (L10 : D14) caused greater inhibition of both reproduction and weight gain than short photoperiod alone. Pinealectomized F344 rats implanted subcutaneously with melatonin in a silastic capsule did not differ in testis size or body weight from controls with blank implants. The brains and pars tuberalis of the pituitary from photoresponsive F344 rats and nonphotoresponsive Harlan Sprague‐Dawley (HSD) rats were processed for autoradiography using IMEL. We found significantly higher specific IMEL binding in the anterior and posterior regions of the paraventricular nucleus of the thalamus (PVNt) and reuniens nucleus of the thalamus of F344 rats than in the same areas in HSD rats. There were no differences between strains in specific IMEL binding in the medial PVNt, anteroventral and anterodorsal nucleus of the thalamus, suprachiasmatic nucleus, or the pars tuberalis. These results indicate that melatonin mediates photoresponsiveness in F344 rats. In addition, they provide support for the hypothesis that F344 rats may be photoresponsive due to differences from other strains in the location, density, or affinity of melatonin receptors.

LABILITY OF FAT STORES IN PERIPUBERTAL WILD HOUSE MICE

SummaryTraditionally, the adaptive value of mammalian white fat stores is considered in relation to longterm needs such as providing protection against the vagaries of winter or signalling the reproductive system when energy reserves are sufficient to risk pregnancy. As shown here, the fat stores of young house mice could not serve such needs. Despite prolonged acclimation and excess nesting material, food deprivation at 10°C significantly lowered the fat stores of peripubertal female house mice in only 12 h, and would exhaust them in 30 h. Even close to thermoneutrality (24°C) the calculated time to exhaustion was only 70 h. The fat stores of a young house mouse are obviously too meager to offer any meaningful protection over a winter of several months duration, or even over a 5–6-week cycle of pregnancy and lactation. Furthermore, in a wild habitat where food availability and ambient temperature can vary rapidly and greatly, such fat stores would be too labile to effectively coordinate puberty with somatic development.

Inhibition of Reproductive Maturation and Somatic Growth of Fischer 344 Rats by Photoperiods Shorter than L14:D10 and by Gradually Decreasing Photoperiod

Abstract Photoperiod is the major regulator of reproduction in temperate-zone mammals. Laboratory rats are generally considered to be nonphotoresponsive, but young male Fischer 344 (F344) rats have a uniquely robust response to short photoperiods of 8 h of light. Rats transferred at weaning from a photoperiod of 16 h to photoperiods of < 14 h of light slowed in both reproductive development and somatic growth rate. Those in photoperiods < 13 h of light underwent the strongest responses. The critical photoperiod of F344 rats can be defined as 13.5 h of light, but photoperiods of ≤ 12.5 h are required to fully suppress reproduction and somatic growth. This demonstrates that the 12-h photoperiod that is standard in some laboratory colonies would have significant effects on reproductive maturation and growth rate of this common rat strain. Young F344 rats in decreasing photoperiods that mimic natural change experienced delayed reproductive development and decreased growth rate to a greater extent and for a longer duration than those transferred at birth to a short photoperiod. The effects of gradual changes in photoperiod persisted for at least 12 wk after weaning. This indicates that young male F344 rats possess responses to photoperiod that would result in functional photoperiodism in a wild mammal.