Physiology of Reproductive Senescence in Florida Scrub-Jays: Results from a Long-Term Study and Gnrh Challenge ⇑ Travis E

General and Comparative Endocrinology 194 (2013) 168–174 Contents lists available at ScienceDirect General and Comparative Endocrinology journal homepage: www.elsevier.com/locate/ygcen Physiology of reproductive senescence in Florida scrub-jays: Results from a long-term study and GnRH challenge ⇑ Travis E. Wilcoxen a,e, , Eli S. Bridge b, Raoul K. Boughton c, Thomas P. Hahn d, Stephan J. Schoech a a Department of Biological Sciences, University of Memphis, 3778 Walker Avenue, Memphis, TN 38111, USA b Oklahoma Biological Survey, University of Oklahoma, 111 East Chesapeake Street, Norman, OK 73019, USA c Disease Ecology Program, Archbold Biological Station, 123 Main Drive, Venus, FL 33960, USA d Department of Neurobiology, Physiology, and Behavior, University of California – Davis, One Shields Avenue, Davis, CA 95616, USA e Biology Department, Millikin University, 1184 West Main Street, Decatur, IL 62522, USA article info abstract Article history: In most vertebrates, production of reproductive hormones wanes with age, co-occurring with a decline in Received 25 May 2013 reproductive output. Measurement of these hormones can serve as a key marker of the onset of reproduc- Revised 10 September 2013 tive senescence. Longitudinal studies of physiological parameters in populations of free-living animals Accepted 13 September 2013 are relatively uncommon; however, we have monitored baseline concentrations of hormones for nine Available online 1 October 2013 years in a population of Florida scrub-jays (Aphelocoma coerulescens). We hypothesized that concentrations of circulating reproductive hormones change with age, and predicted declines in reproductive hor- Keywords: mones in the oldest jays. We found that baseline levels of luteinizing hormone (LH) and testosterone (T) Aging were relatively low in both young and old male breeders and reach their highest levels in birds aged 4– Aphelocoma coerulescens Estradiol 7 years. Conversely, we found no age-related patterns in baseline levels of LH or estradiol in female jays. Gonadotropin-releasing hormone In males we determined which component of the hypothalamo-pituitary-gonadal (HPG) axis is respon- Reproduction sible for observed age-based differences, by challenging males of different ages with gonadotropin- Testosterone releasing hormone (GnRH); thereby allowing assessment of pituitary and gonadal responsiveness by measuring plasma concentrations of luteinizing hormone and testosterone, respectively. The magnitude of increase in levels of both LH and T in response to GnRH challenge decreased with age in male breeders. Combined with the baseline levels, the results from the GnRH challenge suggest that younger birds have the capability to produce higher levels of reproductive hormone, whereas the old birds may be con- strained by senescence in their ability to produce these hormones. Ó 2013 Elsevier Inc. All rights reserved. 1. Introduction study in practical application, particularly in populations of free- living animals (reviewed by Nisbet, 2001). A number of studies Senescence is a decline in physiological function with age that of birds have documented an increase in mortality rate in older can affect survival, reproductive performance, or both. In most ver- members of both short- and long-lived species (Holmes et al., tebrates, production of reproductive hormones wanes with age, co- 2001; Newton and Rothery, 1997). This type of senescence, termed occurring with a decline in reproductive output (Hughes et al., actuarial senescence (McDonald et al., 1996), needs to be distin- 2002). Accordingly, measurement of these hormones can serve as guished from reproductive senescence which is characterized by a key marker of the onset of reproductive senescence. Birds are rel- reductions in reproductive success or the function of reproduc- atively long-lived, when compared to size-matched mammals tively-related physiological systems with age. Actuarial senescence (Holmes and Austad, 1995), and therefore they are good models does occur in the Florida scrub-jay (Aphelocoma coerulescens; for studying mechanisms of reproductive aging (Holmes and Ottin- McDonald et al., 1996), the focal species of this study. ger, 2004). Although reproductive senescence has been considered There are a number of physiological measures that are known extensively in a theoretical framework, it has proven difficult to to change, sometimes dramatically, with age in birds. These include telomerase activity, thyroid hormone production, response to stressors, immune system response, antioxidant activity, and endocrine signaling (reviewed in Vleck et al., 2007), but few stud- ⇑ Corresponding author at: Millikin University, Biology Department, 1184 West ies have examined these phenomena in free-living species in which Main Street, Decatur, IL 62522, USA. the age of each individual is known. The existing studies of free-liv- E-mail addresses: [email protected] (T.E. Wilcoxen), [email protected] (E.S. Bridge), [email protected] (R.K. Boughton), [email protected] ing birds have provided mixed findings that largely reflect the dif- (T.P. Hahn). ferences in life spans of the species studied. For example, Nisbet 0016-6480/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ygcen.2013.09.016 T.E. Wilcoxen et al. / General and Comparative Endocrinology 194 (2013) 168–174 169 et al. (1999) found only slight changes in plasma levels of repro- and the low levels of T were due to an insufficient LH signal. Final- ductive hormones with age in long-lived (max longevity 21 years) ly, should an individual with low baseline levels of LH and T show a common terns (Sterna hirundo) and concluded that because this oc- robust LH response to GnRH injection, but an insignificant increase curred in such a small percentage of the population that it could in T levels, senescence has likely occurred at the level of the go- not have much of an impact on reproductive success. This study nads. Although, these scenarios are slightly oversimplified, this was a snapshot of different aged birds over a two year period technique provides valuable insight into the mechanisms of repro- and the authors suggested that a longitudinal study that included ductive senescence. samples from more breeding seasons would be more informative. On the opposite end of the pace-of-life spectrum, Ottinger (1992, 2007) studied neuroendocrine changes with age in short-lived 2. Material and methods (max longevity 5 years) Japanese quail (Coturnix japonica) in a lab- oratory setting and found dramatic decreases in circulating levels 2.1. Study species and location of reproductive hormones in the oldest birds. Although reproductive output and success among different aged birds have been The Florida scrub-jay is a federally threatened, non-migratory, studied for many moderately long-lived species of birds (e.g., cooperatively breeding passerine with a range restricted to xeric Møller et al., 2006; Newton and Rothery, 1997; Saino et al., oak scrub habitats of peninsular Florida. We monitored a popula- 2002), no research that we are aware of has taken a multi-year lon- tion of Florida scrub-jays at Archbold Biological Station in south gitudinal approach to investigate changes in reproductive hormone central Florida (27° 100 N, 81° 2l0 W, elevation 38–68 m; see Scho- physiology among different aged birds. ech et al., 1996a, 2007 for further details). The sex and social status Physiological processes and behaviors associated with repro- (i.e., breeder or non-breeding helper) of each bird in this popula- duction are largely regulated by the hypothalamo-pituitary-gona- tion are known, as are family group affiliation, and reproductive dal (HPG) axis. In a seasonal breeder, the hypothalamus output from 1989 to present. Each Florida scrub-jay territory has integrates information from the exogenous and endogenous envi- a breeding pair and zero to six non-breeding helpers residing with- ronment to assure the appropriate timing of up-regulation of hor- in the territory. The nonbreeders are typically offspring of the mone production and initiation of reproductive preparedness. At a breeding pair that are themselves delaying reproduction, often basic level (see Besser and Mortimer, 1974, for a review of the mul- contributing alloparental care to the nestlings and fledglings in tiple neuroendocrine functions of the hypothalamus), the hypo- the territory (Schoech et al., 1996a). For all breeding jays in our thalamus releases gonadotropin-releasing hormone (GnRH, also population, we locate all nests and determine laying, hatching, called luteinizing hormone releasing hormone, or LHRH), which fledging dates, and fledging success; further, we band each nestling stimulates the release of the gonadotropins, luteinizing hormone prior to fledging, and thus, know the age and pedigree of all birds in (LH) and follicle stimulating hormone (FSH), from the anterior the population. Many factors are known to influence fitness and pituitary. True to their names, both LH and FSH are critical for go- longevity in this population of jays (originally reviewed by Wool- nadal function in males and females. fenden and Fitzpatrick, 1984), and some of the more recent find- We first asked if there was evidence of reproductive senescence, ings include habitat quality (Mumme et al., 2000; Schoech and determined by age related fledgling success for male and female Bowman, 2001), food availability (Reynolds et al., 2003), stress re- breeders from 20 years of nest monitoring in

Load more