Publications by authors named "Paul D Heideman"

19 Publications

  • Page 1 of 1

Testosterone does not mediate variation in basal metabolic rate and activity in relation to reproductive condition and photoperiod in white-footed mice (Peromyscus leucopus).

J Exp Zool A Ecol Integr Physiol 2019 10 5;331(8):456-462. Epub 2019 Aug 5.

Department of Biology, College of William and Mary, Williamsburg, Virginia.

The photoperiodic response of many temperate zone rodents, including white-footed mice (Peromyscus leucopus), is a heritable life-history trait with underlying physiological variation. Previous studies of intact male P. leucopus utilized two wild-derived bidirectional selection lines, a short photoperiod responsive (R) line selected for reproductive suppression in short-day conditions (SD) and a nonresponsive (NR) line selected for reproductive maturity in SD. NR mice in SD had greater food intake, but also higher levels of locomotor activity, and basal metabolic rate (BMR) than R mice. We hypothesized that testosterone may be a key mediator of this metabolic difference, as it is likely to be significantly reduced in R SD mice. Male P. leucopus from either line in SD were castrated and given either an implant containing testosterone (T) or a sham control (C). They were then tested for variation in metabolic rate and activity in SD, thermoneutral conditions. T mice had significantly higher levels of food intake, testosterone, and seminal vesicle dry weight than C mice. Seminal vesicle dry weight was significantly and positively correlated with average testosterone level, indicating an effect of the T implants. There was no statistically significant difference among treatment groups in BMR and average daily metabolic rate, suggesting that differences in testosterone alone are not the cause of differences in metabolic rate between selection lines.
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http://dx.doi.org/10.1002/jez.2312DOI Listing
October 2019

Flexible clock systems: adjusting the temporal programme.

Philos Trans R Soc Lond B Biol Sci 2017 Nov;372(1734)

Chronobiology Unit, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands.

Under natural conditions, many aspects of the abiotic and biotic environment vary with time of day, season or even era, while these conditions are typically kept constant in laboratory settings. The timing information contained within the environment serves as critical timing cues for the internal biological timing system, but how this system drives daily rhythms in behaviour and physiology may also depend on the internal state of the animal. The disparity between timing of these cues in natural and laboratory conditions can result in substantial differences in the scheduling of behaviour and physiology under these conditions. In nature, temporal coordination of biological processes is critical to maximize fitness because they optimize the balance between reproduction, foraging and predation risk. Here we focus on the role of peripheral circadian clocks, and the rhythms that they drive, in enabling adaptive phenotypes. We discuss how reproduction, endocrine activity and metabolism interact with peripheral clocks, and outline the complex phenotypes arising from changes in this system. We conclude that peripheral timing is critical to adaptive plasticity of circadian organization in the field, and that we must abandon standard laboratory conditions to understand the mechanisms that underlie this plasticity which maximizes fitness under natural conditions.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.
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http://dx.doi.org/10.1098/rstb.2016.0254DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5647281PMC
November 2017

Effectiveness and Adoption of a Drawing-to-Learn Study Tool for Recall and Problem Solving: Minute Sketches with Folded Lists.

CBE Life Sci Educ 2017 ;16(2)

Department of Biology, College of William and Mary, Williamsburg, VA 23187.

Drawing by learners can be an effective way to develop memory and generate visual models for higher-order skills in biology, but students are often reluctant to adopt drawing as a study method. We designed a nonclassroom intervention that instructed introductory biology college students in a drawing method, minute sketches in folded lists (MSFL), and allowed them to self-assess their recall and problem solving, first in a simple recall task involving non-European alphabets and later using unfamiliar biology content. In two preliminary ex situ experiments, students had greater recall on the simple learning task, non-European alphabets with associated phonetic sounds, using MSFL in comparison with a preferred method, visual review (VR). In the intervention, students studying using MSFL and VR had ∼50-80% greater recall of content studied with MSFL and, in a subset of trials, better performance on problem-solving tasks on biology content. Eight months after beginning the intervention, participants had shifted self-reported use of drawing from 2% to 20% of study time. For a small subset of participants, MSFL had become a preferred study method, and 70% of participants reported continued use of MSFL. This brief, low-cost intervention resulted in enduring changes in study behavior.
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http://dx.doi.org/10.1187/cbe.16-03-0116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5459246PMC
June 2018

Genetic variation in total number and locations of GnRH neurons identified using in situ hybridization in a wild-source population.

J Exp Zool A Ecol Genet Physiol 2016 Feb 24;325(2):106-15. Epub 2015 Dec 24.

Department of Biology, College of William and Mary, Williamsburg, Virginia.

The evolution of brain function in the regulation of physiology may depend in part upon the numbers and locations of neurons. Wild populations of rodents contain natural genetic variation in the inhibition of reproduction by winter-like short photoperiod, and it has been hypothesized that this functional variation might be due in part to heritable variation in the numbers or location of gonadotropin releasing hormone (GnRH) neurons. A naturally variable wild-source population of white-footed mice was used to develop lines artificially selected for or against mature gonads in short, winter-like photoperiods. We compared a selection line that is reproductively inhibited in short photoperiod (Responsive) to a line that is weakly inhibited by short photoperiod (Nonresponsive) for differences in counts of neurons identified using in situ hybridization for GnRH mRNA. There was no effect of photoperiod, but there were 60% more GnRH neurons in total in the Nonresponsive selection line than the Responsive selection line. The lines differed specifically in numbers of GnRH neurons in more anterior regions, whereas numbers of GnRH neurons in posterior areas were not statistically different between lines. We compare these results to those of an earlier study that used immunohistochemical labeling for GnRH neurons. The results are consistent with the hypothesis that the selection lines and natural source population contain significant genetic variation in the number and location of GnRH neurons. The variation in GnRH neurons may contribute to functional variation in fertility that occurs in short photoperiods in the laboratory and in the wild source population in winter.
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http://dx.doi.org/10.1002/jez.2000DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6779586PMC
February 2016

Genetic variation in male sexual behaviour in a population of white-footed mice in relation to photoperiod.

Anim Behav 2015 Jun;104:203-212

Department of Biology, College of William and Mary, Williamsburg, VA, U.S.A.

In natural populations, genetic variation in seasonal male sexual behaviour could affect behavioural ecology and evolution. In a wild-source population of white-footed mice, , from Virginia, U.S.A., males experiencing short photoperiod show high levels of genetic variation in reproductive organ mass and neuroendocrine traits related to fertility. We tested whether males from two divergent selection lines, one that strongly suppresses fertility under short photoperiod (responder) and one that weakly suppresses fertility under short photoperiod (nonresponder), also differ in photoperiod-dependent sexual behaviour and responses to female olfactory cues. Under short, but not long, photoperiod, there were significant differences between responder and nonresponder males in sexual behaviour and likelihood of inseminating a female. Males that were severely oligospermic or azoospermic under short photoperiod failed to display sexual behaviour in response to an ovariectomized and hormonally primed receptive female. However, on the day following testing, females were positive for spermatozoa only when paired with a male having a sperm count in the normal range for males under long photoperiod. Males from the nonresponder line showed accelerated reproductive development under short photoperiod in response to urine-soiled bedding from females, but males from the responder line did not. The results indicate genetic variation in sexual behaviour that is expressed under short, but not long, photoperiod, and indicate a potential link between heritable neuroendocrine variation and male sexual behaviour. In winter in a natural population, this heritable behavioural variation could affect fitness, seasonal life history trade-offs and population growth.
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http://dx.doi.org/10.1016/j.anbehav.2015.03.026DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4428349PMC
June 2015

Insulins, leptin and feeding in a population of Peromyscus leucopus (white-footed mouse) with variable fertility.

Horm Behav 2014 Jun 26;66(1):169-79. Epub 2014 Feb 26.

Department of Biology, College of William and Mary, Williamsburg, VA, USA. Electronic address:

This article is part of a Special Issue "Energy Balance". Natural populations display a variety of reproductive responses to environmental cues, but the underlying physiology that causes these responses is largely unknown. This study tested the hypothesis that heritable variation in reproductive traits can be described by heritable variation in concentrations of hormones critical to both energy balance and reproduction. To test this hypothesis, we used mouse lines derived from a wild population and selectively bred for response to short day photoperiod. Reproductive and metabolic traits of Peromyscus leucopus display heritable variation when held in short photoperiods typical of winter. Our two lines of mice have phenotypes spanning the full range of variation observed in nature in winter. We tested male and female mice for heritable variation in fasted serum concentrations of three hormones involved in energetic regulation: leptin, insulin-like growth factor 1 (IGF-1) and insulin, as well as the effects of exogenous leptin and a high energy diet on reproductive maturation. Exogenous leptin decreased food intake, but protected males from the reduction in testis mass caused by equivalent food restriction in pair-fed, saline-infused controls. A high energy diet resulted in calorie adjustment by the mice, and failed to alter reproductive phenotype. Concentrations of the three hormones did not differ significantly between selection lines but had correlations with measures of food intake, fertility, blood glucose, and/or body mass. There was evidence of interactions between reproductive traits and hormones related to energy balance and reproduction, but this study did not find evidence that variation in these hormones caused variation in reproductive phenotype.
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http://dx.doi.org/10.1016/j.yhbeh.2014.02.006DOI Listing
June 2014

Heritable variation in reaction norms of metabolism and activity across temperatures in a wild-derived population of white-footed mice (Peromyscus leucopus).

J Comp Physiol B 2014 May 19;184(4):525-34. Epub 2014 Feb 19.

Department of Biology, Virginia State University, P.O. Box 9064, Petersburg, VA, 23806, USA,

Heritable variation in metabolic traits is likely to affect fitness. In this study, white-footed mice from wild-derived photoresponsive [R, infertile in short day length (SD)] and non-photoresponsive (NR, fertile in SD) selection lines were maintained under short-day (SD 8Light:16Dark), sub-thermoneutral conditions (22 or 12 °C). Mice had significantly higher levels of food intake and resting metabolic rates (RMR) at low temperature. RMR differed significantly between lines (greater in NR mice). In contrast to previous work under thermoneutral conditions, there was no significant difference in overall activity or average daily metabolic rates (ADMR) of mice from the two lines. Reduced activity may reflect behavioral changes under cooler conditions (e.g., nest building) reducing the overall energetic cost of fertility (for NR mice). There was no significant difference in maximal rate of oxygen consumption ([Formula: see text]) between lines. R mice had significantly greater brown adipose tissue and white abdominal fat mass due to both line and temperature. Reaction norms for intake, resting metabolism (RMR/BMR) and level of activity from current (12 and 22 °C) and previously published data (28 °C) demonstrate independent effects of genetics (line) and environment (temperature) for resting metabolism, but a clear interaction between these for activity. The results suggest that fertility under winter conditions imposes metabolic costs that are related to the level of reproductive development. Under the coldest conditions tested, however, mice that remained fertile in SD reduced activity, ADMR and food requirements, decreasing the differential between selection lines. Heritable variation in reaction norms suggests a genetic by environment effect that could be subject to selection.
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http://dx.doi.org/10.1007/s00360-014-0811-6DOI Listing
May 2014

Variation in levels of luteinizing hormone and reproductive photoresponsiveness in a population of white-footed mice (Peromyscus leucopus).

Am J Physiol Regul Integr Comp Physiol 2010 Jun 31;298(6):R1543-8. Epub 2010 Mar 31.

Department of Biology, College of William and Mary, Williamsburg, VA 23187, USA.

Natural genetic variation in reproduction and life history strategies is a manifestation of variation in underlying regulatory neuronal and endocrine systems. A test of the hypothesis that genetic variation in luteinizing hormone (LH) level could be related to a life history trait, seasonal reproduction, was conducted on artificial selection lines from a wild-source population of white-footed mice (Peromyscus leucopus). Variation exists in the degree of suppression of reproduction by winter short-day photoperiods (SD) in wild-source individuals and in the laboratory population. In this population, most individuals from a photoperiod-responsive (R) artificial selection line are strongly suppressed reproductively in SD, while most individuals from a photoperiod-nonresponsive (NR) artificial selection line are only weakly reproductively suppressed in SD. We assayed levels of LH to test for genetic variation between lines that could contribute to variation in reproductive status in SD. Females from both lines were raised in long-day photoperiods (LD) or SD, ovariectomized under isoflurane anesthesia, and given estradiol implants. Levels of LH were significantly higher in the NR line than in the R line, indicating genetic variation for levels of LH. Levels of LH were higher in LD than in SD, indicating that levels of LH were sensitive to photoperiod treatment even with a controlled level of estradiol negative feedback. The results indicate that there is genetic variation in levels of LH that could be functionally important both in the laboratory in SD and in the wild population in winter. Thus genetic variation in levels of LH is a plausible causal factor determining winter reproductive phenotype in the wild population.
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http://dx.doi.org/10.1152/ajpregu.00686.2009DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2886702PMC
June 2010

Microevolution of neuroendocrine mechanisms regulating reproductive timing in Peromyscus leucopus.

Integr Comp Biol 2009 Nov 22;49(5):550-62. Epub 2009 May 22.

Department of Biology, College of William and Mary, Williamsburg, VA 23187, USA.

A key question in the evolution of life history and in evolutionary physiology asks how reproductive and other life-history traits evolve. Genetic variation in reproductive control systems may exist in many elements of the complex inputs that can affect the hypothalamic-pituitary-gonadal (HPG) or reproductive axis. Such variation could include numbers and other traits of secretory cells, the amount and pattern of chemical message released, transport and clearance mechanisms, and the number and other traits of receptor cells. Selection lines created from a natural population of white-footed mice (Peromyscus leucopus) that contains substantial genetic variation in reproductive inhibition in response to short winter daylength (SD) have been used to examine neuroendocrine variation in reproductive timing. We hypothesized that natural genetic variation would be most likely to occur in the inputs to GnRH neurons and/or in GnRH neurons themselves, but not in elements of the photoperiodic pathway that would have pleiotropic effects on nonreproductive functions as well as on reproductive functions. Significant genetic variation has been found in the GnRH neuronal system. The number of GnRH neurons immunoreactive to an antibody to mature GnRH peptide under conditions maximizing detection of stained neurons was significantly heritable in an unselected control (C) line. Furthermore, a selection line that suppresses reproduction in SD (photoperiod responsive, R) had fewer IR-GnRH neurons than a selection line that maintains reproduction in SD (photoperiod nonresponsive, NR). This supports the hypothesis that genetic variation in characteristics of GnRH neurons themselves may be responsible for the observed phenotypic variation in reproduction in SD. The R and NR lines differ genetically in food intake and iodo-melatonin receptor binding, as well as in other characteristics. The latter findings are consistent with the hypothesis that genetic variation occurs in the nutritional and hormonal inputs to GnRH neurons. Genetic variation also exists in the phenotypic plasticity of responses to two combinations of treatments, (1) food and photoperiod, and (2) photoperiod and age, indicating genetic variation in individual norms of reaction within this population. Overall, the apparent multiple sources of genetic variation within this population suggest that there may be multiple alternative combinations of alleles for both the R and NR phenotypes. If that interpretation is correct, we suggest that this offers some support for the evolutionary "potential" hypothesis and is inconsistent with the evolutionary "constraint" and "symmorphosis" hypotheses for the evolution of complex neuroendocrine pathways.
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http://dx.doi.org/10.1093/icb/icp014DOI Listing
November 2009

Variation in nocturnality and circadian activity rhythms between photoresponsive F344 and nonphotoresponsive Sprague Dawley rats.

J Circadian Rhythms 2008 Sep 9;6. Epub 2008 Sep 9.

Department of Biology, College of William and Mary, Williamsburg, VA 23187, USA.

Background: Variation in circadian rhythms and nocturnality may, hypothetically, be related to or independent of genetic variation in photoperiodic mediation of seasonal changes in physiology and behavior. We hypothesized that strain variation in photoperiodism between photoperiodic F344 rats and nonphotoperiodic Harlan Sprague Dawley (HSD) rats might be caused by underlying variation in clock function. We predicted that HSD rats would have more activity during the day or subjective day, longer free-running rhythms, poor entrainment to short day length, and shorter duration of activity, traits that have been associated with nonphotoperiodism in other laboratory rodent species, relative to F344 rats. An alternative hypothesis, that differences are due to variation in melatonin secretion or responses to melatonin, predicts either no such differences or inconsistent combinations of differences.

Methods: We tested these predictions by examining activity rhythms of young male F344 and HSD rats given access to running wheels in constant dark (DD), short day length (L8:D16; SD), and long day length (L16:D8; LD). We compared nocturnality (the proportion of activity during night or subjective night), duration of activity (alpha), activity onset and offset, phase angle of entrainment, and free running rhythms (tau) of F344 and HSD rats.

Results: HSD rats had significantly greater activity during the day, were sometimes arrhythmic in DD, and had significantly longer tau than F344 rats, consistent with predictions. However, HSD rats had significantly longer alpha than F344 rats and both strains entrained to SD, inconsistent with predictions.

Conclusion: The ability of HSD rats to entrain to SD, combined with longer alpha than F344 rats, suggests that the circadian system of HSD rats responds correctly to SD. These data offer best support for the alternative hypothesis, that differences in photoresponsiveness between F344 and HSD rats are caused by non-circadian differences in melatonin secretion or the response to melatonin.
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http://dx.doi.org/10.1186/1740-3391-6-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2542993PMC
September 2008

Number of immunoreactive GnRH-containing neurons is heritable in a wild-derived population of white-footed mice (Peromyscus leucopus).

Physiol Biochem Zool 2007 Sep-Oct;80(5):534-41. Epub 2007 Jul 13.

Department of Biology, College of William and Mary, Williamsburg, Virginia 23187, USA.

The evolution of mammalian brain function depends in part on levels of natural, heritable variation in numbers, location, and function of neurons. However, the nature and amount of natural genetic variation in neural traits and their physiological link to variation in function or evolutionary change are unknown. We estimated the level of within-population heritable variation in the number of gonadotropin-releasing hormone (GnRH) neurons, which play a major role in reproductive regulation, in an unselected outbred population recently derived (<10 generations) from a single natural population of white-footed mice (Peromyscus leucopus, Rafinesque). Young adult male mice exhibited an approximately threefold variation in the number of neurons immunoreactive for GnRH in the brain areas surveyed, as detected using SMI-41 antibody with a single-label avidin-biotin complex method. Consistent with earlier findings of selectable variation in GnRH neurons in this population, the level of genetic variation in this neuronal trait within this single population was high, with broadsense heritability using full-sib analysis estimated at 0.72 (P<0.05). Either weak selection on this trait or environmental variation that results in inconsistent selection on this trait might allow a high level of variation in this population.
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http://dx.doi.org/10.1086/519960DOI Listing
November 2007

Phenotypic plasticity of reproductive traits in response to food availability and photoperiod in white-footed mice (Peromyscus leucopus).

Oecologia 2006 Dec 6;150(3):373-82. Epub 2006 Sep 6.

Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14853, USA.

Although most temperate-zone mammals are seasonal breeders, many populations display variation in winter reproductive phenotype. For most mammals, the primary environmental cues regulating reproductive status are food availability and photoperiod, and these two factors can interact in their effect. Low food availability is primarily thought to suppress reproduction by reducing body mass and thereby forcing energy allocations to survival alone. However, because most small mammals rely on an increase in food intake rather than stored nutrients for reproduction, we hypothesized that food availability could act as a signal for low resource availability and affect reproduction even when body condition was not affected. We tested the prediction that restricted food access, without reduced body mass, could alter reproductive responses to short photoperiod. We used genetically distinct lines of white-footed mice (Peromyscus leucopus) derived from a wild population with genetic variation in the neuroendocrine pathway that regulates reproduction in response to environmental cues. The lines were created by artificial selection on gonad size in short photoperiods. Individuals from one line strongly suppress gonadal development in response to short photoperiods, while individuals from the other line suppress gonadal development weakly or not at all. Unresponsive individuals from the selected and an unselected control line were exposed to an intermittent food access protocol that did not affect body mass and only slightly reduced total food intake. We found that restricting food access caused reproductive suppression in short photoperiods but not long photoperiods, with no decrease in body mass. These results provide evidence for an interaction between food and photoperiod that is not dependent upon body condition or energy balance. The results also demonstrate plasticity in the reproductive response to photoperiod of otherwise reproductively nonphotoperiodic white-footed mice.
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http://dx.doi.org/10.1007/s00442-006-0533-xDOI Listing
December 2006

Failure to respond to endogenous or exogenous melatonin may cause nonphotoresponsiveness in Harlan Sprague Dawley rats.

J Circadian Rhythms 2005 Sep 14;3:12. Epub 2005 Sep 14.

Department of Biology, College of William and Mary, Williamsburg, VA 23187, USA.

Background: Responsiveness to changing photoperiods from summer to winter seasons is an important but variable physiological trait in most temperate-zone mammals. Variation may be due to disorders of melatonin secretion or excretion, or to differences in physiological responses to similar patterns of melatonin secretion and excretion. One potential cause of nonphotoresponsiveness is a failure to secrete or metabolize melatonin in a pattern that reflects photoperiod length.

Methods: This study was performed to test whether a strongly photoresponsive rat strain (F344) and strongly nonphotoresponsive rat strain (HSD) have similar circadian urinary excretion profiles of the major metabolite of melatonin, 6-sulfatoxymelatonin (aMT6s), in long-day (L:D 16:8) and short-day (L:D 8:16) photoperiods. The question of whether young male HSD rats would have reproductive responses to constant dark or to supplemental melatonin injections was also tested. Urinary 24-hour aMT6s profiles were measured under L:D 8:16 and L:D 16:8 in young male laboratory rats of a strain known to be reproductively responsive to the short-day photoperiod (F344) and another known to be nonresponsive (HSD).

Results: Both strains exhibited nocturnal rises and diurnal falls in aMT6s excretion during both photoperiods, and the duration of the both strains' nocturnal rise was longer in short photoperiod treatments. In other experiments, young HSD rats failed to suppress reproduction or reduce body weight in response to either constant dark or twice-daily supplemental melatonin injections.

Conclusion: The results suggest that HSD rats may be nonphotoresponsive because their reproductive system and regulatory system for body mass are unresponsive to melatonin.
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http://dx.doi.org/10.1186/1740-3391-3-12DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1242245PMC
September 2005

Behavioral neuroendocrinology in nontraditional species of mammals: things the 'knockout' mouse CAN'T tell us.

Horm Behav 2005 Nov 28;48(4):474-83. Epub 2005 Jun 28.

Departments of Zoology, Michigan State University, East Lansing, MI 48843, USA.

The exploration of many of the fundamental features of mammalian behavioral neuroendocrinology has benefited greatly throughout the short history of the discipline from the study of highly inbred, genetically characterized rodents and several other "traditional" exemplars. More recently, the impact of genomic variation in the determination of complex neuroendocrine and behavioral systems has advanced through the use of single and multiple gene knockouts or knockins. In our essay, we argue that the study of nontraditional mammals is an essential approach that complements these methodologies by taking advantage of allelic variation produced by natural selection. Current and future research will continue to exploit these systems to great advantage and will bring new techniques developed in more traditional laboratory animals to bear on problems that can only be addressed with nontraditional species. We highlight our points by discussing advances in our understanding of neuroendocrine and behavioral systems in phenomena of widely differing time scales. These examples include neuroendocrine variation in the regulation of reproduction across seasons in Peromyscus, variation in parental care by biparental male rodents and primates within a single infant rearing attempt, and circadian variation in the regulation of the substrates underlying mating in diurnal vs. nocturnal rodents. Our essay reveals both important divergences in neuroendocrine systems in our nontraditional model species, and important commonalities in these systems.
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http://dx.doi.org/10.1016/j.yhbeh.2005.05.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2981860PMC
November 2005

Response to selection for photoperiod responsiveness on the density and location of mature GnRH-releasing neurons.

Am J Physiol Regul Integr Comp Physiol 2005 May 13;288(5):R1226-36. Epub 2005 Jan 13.

Dept. of Biology, The College of William and Mary, Williamsburg, VA 23187, USA.

Natural variation in neuroendocrine traits is poorly understood, despite the importance of variation in brain function and evolution. Most rodents in the temperate zones inhibit reproduction and other nonessential functions in short winter photoperiods, but some have little or no reproductive response. We tested whether genetic variability in reproductive seasonality is related to individual differences in the neuronal function of the gonadotropin-releasing hormone network, as assessed by the number and location of mature gonadotropin-releasing hormone-secreting neurons under inhibitory and excitatory photoperiods. The experiments used lines of Peromyscus leucopus previously developed by selection from a wild population. One line contained individuals reproductively inhibited by short photoperiod, and the other line contained individuals nonresponsive to short photoperiod. Expression of mature gonadotropin-releasing hormone (GnRH) immunoreactivity in the brain was detected using SMI-41 antibody in the single-labeled avidin-biotin-peroxidase-complex method. Nonresponsive mice had 50% more immunoreactive GnRH neurons than reproductively inhibited mice in both short- and long-day photoperiods. The greatest differences were in the anterior hypothalamus and preoptic areas. In contrast, we detected no significant within-lines differences in the number or location of immunoreactive GnRH neurons between photoperiod treatments. Our data indicate that high levels of genetic variation in a single wild population for a specific neuronal trait are related to phenotypic variation in a life history trait, i.e., winter reproduction. Variation in GnRH neuronal activity may underlie some of the natural reproductive and life history variation observed in wild populations of P. leucopus. Similar genetic variation in neuronal traits may be present in humans and other species.
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http://dx.doi.org/10.1152/ajpregu.00562.2004DOI Listing
May 2005

Short photoperiod inhibition of growth in body mass and reproduction in ACI, BUF, and PVG inbred rats.

Reproduction 2004 Dec;128(6):857-62

Department of Biology, College of William and Mary, PO Box 8795, Williamsburg, Virginia 23187-8795, USA.

Laboratory rats have been generally considered non-photoresponsive, but strains of laboratory rats have been found to be variable for this trait. Young males of both the Fischer (F344) and Brown Norway strains (BN) suppress reproductive development, food intake and body mass in short winter photoperiod (short days (SD); 8 h light:16 h darkness), and food restriction interacts with SD to enhance the effect of SD alone. Conversely, young male Harlan Sprague Dawley outbred rats, along with other outbred laboratory rats tested, have little or no response to SD except when unmasked by food restriction or other treatments, and have generally been considered nonphotoperiodic. In order to assess how widespread this trait might be among rat strains, and to test for uncoupling of reproductive and nonreproductive responses, we tested 3 additional inbred strains, including ACI, PVG and BUF rats, for photoresponsiveness and for unmasking of photoperiodic responses by food restriction. Young males of all three inbred strains exhibited photoresponsiveness in testis mass (5-20% lower in SD), seminal vesicle mass (20-50% lower in SD), and body mass (5-10% lower in SD). Food restriction also suppressed reproduction, but there was little or no interaction with the effects of photoperiod. The results are consistent with the hypothesis that laboratory rats are genetically variable for photoperiodism, and that photoresponsiveness may be widespread among inbred rat strains, as all five inbred strains tested have shown photoperiodic responses. The results are particularly important because standard research protocols may unknowingly manipulate this pathway in rats, causing unsuspected variability among or within studies.
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http://dx.doi.org/10.1530/rep.1.00390DOI Listing
December 2004

Top-down approaches to the study of natural variation in complex physiological pathways using the white-footed mouse (Peromyscus leucopus) as a model.

Authors:
Paul D Heideman

ILAR J 2004 ;45(1):4-13

College of William and Mary, Williamsburg, VA, USA.

Variation in complex physiological pathways has important effects on human function and medical treatment. Complex pathways involve cells at multiple locations, which serve different functions regulated by many genes and include complex neuroendocrine pathways that regulate physiological function. One of two competing hypotheses regarding the effects of selection on complex pathways predicts that variability should be common within complex pathways. If this hypothesis is correct, then we should expect wide variation in neuroendocrine function to be typical within natural populations. To test this hypothesis, a complex neuroendocrine pathway that regulates photoperiod-dependent changes in fertility in a natural population of white-footed mice (Peromyscus leucopus) was used to test for natural genetic variability in multiple components of the pathway. After testing only six elements in the photoperiod pathway in P. leucopus, genetic variation in the following four of these elements was evident: the circadian clock, melatonin receptor abundance or affinity, sensitivity of the reproductive axis to steroid negative feedback, and gonadotropin-releasing hormone neuronal activity. If this result can be extended to humans, the prediction would be that significant variation at multiple loci in complex neuroendocrine pathways is common among humans, and that variation would exist even in human populations from a common genetic background. This finding could only be drawn from an "exotic" animal model derived from a natural source population, confirming the continuing importance of nontraditional models alongside the standard laboratory species.
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http://dx.doi.org/10.1093/ilar.45.1.4DOI Listing
February 2004

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

BMC Ecol 2003 Nov 21;3:11. Epub 2003 Nov 21.

Department of Biology, College of William and Mary, Williamsburg, VA, 23187-8795, USA.

Background: Differences 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.

Results: In 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.

Conclusion: The 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.
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http://dx.doi.org/10.1186/1472-6785-3-11DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC305358PMC
November 2003

Reduced body mass, food intake, and testis size in response to short photoperiod in adult F344 rats.

BMC Physiol 2002 Jul 22;2:11. Epub 2002 Jul 22.

Dept. of Biology, College of William and Mary, PO Box 8795, Williamsburg, VA 23187-8795, USA.

Background: Although laboratory rats are often considered classic nonseasonal breeders, peripubertal rats of two inbred strains, F344 and BN, have both reproductive and nonreproductive responses to short photoperiods. Unmanipulated adult rats have not been reported to have robust responses to short photoperiod alone, although several treatments can induce photoperiodic responses in adults. In this study, we tested the hypotheses that unmanipulated F344 rats retain responses to short photoperiod as adults and that they have the necessary elements for an endogenous circannual rhythm of sensitivity to short photoperiod.

Results: Relative to rats kept in long photoperiods (L16:D8), adult F344 rats transferred at 4.5 months of age to short photoperiods (L8:D16) had significantly lower testis size, food intake, and body weight. In a second experiment, newly weaned F344 rats underwent an initial period of inhibition of reproductive maturation, lower food intake, and lower body weight in short photoperiod or intermediate photoperiod (L12:D12) relative to rats in long photoperiod. By 18 weeks of treatment, rats in the two inhibitory photoperiods no longer differed from long photoperiod controls. In short photoperiod, rats underwent a second period of slight reproductive inhibition between weeks 35 and 48, but there was an effect on body weight and slight inhibition of food intake only in an intermediate photoperiod.

Conclusion: Male F344 rats retain photoresponsiveness as adults, with less reproductive inhibition but equivalent nonreproductive responses. There was only weak evidence for an endogenous timer controlling a circannual cycle of sensitivity to short photoperiod.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC122066PMC
http://dx.doi.org/10.1186/1472-6793-2-11DOI Listing
July 2002