Photoperiod-Independent Changes in Immunoreactive Brain Gonadotropin-Releasing Hormone (GnRH) in a Free-Living, Tropical Bird

Abstract

Timing of seasonal reproduction in high latitude vertebrates is generally regulated by photoperiodic cues. Increasing day length in the spring is associated with changes in the brain that are responsible for mediating reproductive activities. A primary example of this is the increased content of gonadotropin-releasing hormone (GnRH) in the preoptic area of the hypothalamus in birds as they enter the spring breeding season. Increased GnRH activity stimulates the release of luteinizing hormone and follicle-stimulating hormone from the anterior pituitary. These gonadotropins induce growth of the gonads and release of sex steroids which act on the brain to mediate reproductive behaviors. By contrast, seasonal breeding in the tropics can occur in the absence of significant changes in photoperiod. To our knowledge, no studies have investigated whether seasonal breeding in free-living tropical vertebrates is associated with seasonal changes in the GnRH system. We studied two populations of rufous-collared sparrows (Zonotrichia capensis) at the equator, separated by only 25 km, but with asynchronous reproductive phenologies associated with local climate and independent of photoperiodic cues. We collected brains and measured GnRH immunoreactivity (GnRH-ir) during each population’s breeding and non-breeding periods. Breeding males had larger, but not more, GnRH-ir cells than non-breeding birds. The plasticity of the GnRH system was associated with local climate, such that the two populations exhibited asynchronous changes in GnRH-ir despite experiencing identical photoperiod conditions. Our results demonstrate that tropical birds can exhibit neural changes similar to those exhibited in higher latitude birds. However, these tropical populations appear to be using supplementary cues (e.g., rainfall, temperature, food availability) in a similar way to higher latitude species using an initial predictive cue (photoperiod). These results raise questions about the evolution of reliance upon photoperiodism and the strength of reproductive responses to other environmental cues in congeners from higher latitudes. The ability to respond to a multitude of environmental cues might be part of the ancestral condition, and the subsequent obligate photoperiodism in high-latitude congeners could reflect a loss of flexibility in response to environmental signals.

Photoperiod-Independent Hypothalamic Regulation of Luteinizing Hormone Secretion in a Free-Living Sonoran Desert Bird, the Rufous-Winged Sparrow <i>(Aimophila carpalis)</i>

“…The decrease in GnIH-ir fiber immunolabeling in the POA after the beginning of the monsoon season suggests that GnIH could directly inhibit cGnRH-I cells prior to breeding, which is consistent with data on putative contact of GnIH axonal terminals with cGnRH-I and -II neurons in other passerines [Bentley et al, 2003b[Bentley et al, , 2006b and in mammals [Kriegsfeld et al, 2006]. A variety of non-photoperiodic factors may influence cGnRH-I cell activity in birds [Donoghue et al, 1989;Dunn et al, 1996;Cheng et al, 1998;Ottinger et al, 2005], however, to our knowledge this is only the second data set to demonstrate changes in cGnRH-I cell activity in a passerine that are ostensibly due to non-photoperiodic factors [Moore et al, 2006], and the first to demonstrate changes in GnIH in a free-living vertebrate.…”

Control of the annual cycle in birds: endocrine constraints and plasticity in response to ecological variability

“…The development of song nuclei and initial testicular development occurred at approximately the same time, but the subsequent rate of testicular development was faster in the early breeding population (Caro et al 2004(Caro et al , 2005b(Caro et al , 2006. Two tropical populations of Rufous-collared sparrows (Zonotrichia capensis), separated by only 25 km, have highly asynchronous breeding seasons (Moore et al 2005) and reproductive physiology (Moore et al 2006) associated with different local rainfall patterns. Clearly, non-photoperiodic cues must be important.…”

Individual variation in avian reproductive physiology does not reliably predict variation in laying date

“…In avian research, timing of reproduction often refers to the laying date of the first egg in spring [41]. However, the initiation of gonadal growth and the underlying activation of the reproductive endocrine system is also part of the timing mechanism [5,8,13,14,17,20,23,34,37]. This dual vision originates from the fact that evolutionary ecologists are more concerned with behavioral decisions and their fitness consequences, while physiologists are by definition more interested in the proximate mechanisms underlying a certain phenotype, such as gonadal growth and ovulation.…”

“…These measures can be taken at regular intervals during different reproductive stages. More recently, also processes higher upstream in the hypothalamo-pituitary-gonadal (HPG) axis have been added to the physiologist's toolbox, including the release of GnRH-I [20,36], or even gene expression [19,22].…”