Food availability, energetic constraints and reproductive development in a wild seasonally breeding songbird

Abstract

Summary In many organisms, food availability is a proximate cue that synchronizes seasonal development of the reproductive system with optimal environmental conditions. Growth of the gonads and secondary sexual characteristics is orchestrated by the hypothalamic–pituitary–gonadal (HPG) axis. However, our understanding of the physiological mechanisms by which food availability modulates activity of the HPG axis is limited.It is thought that many factors, including energetic status, modulate seasonal reproductive activation. We tested the hypothesis that food availability modulates the activity of the HPG axis in a songbird. Specifically, we food‐restricted captive adult male Abert's Towhees Melozone aberti for 2 or 4 weeks during photoinduced reproductive development. A third group (control) received ad libitum food throughout. We measured multiple aspects of the reproductive system including endocrine activity of all three levels of the HPG axis [i.e. hypothalamic gonadotropin‐releasing hormone‐I (GnRH‐I), plasma luteinizing hormone (LH) and testosterone (T)], and gonad morphology. Furthermore, because gonadotropin‐inhibitory hormone (GnIH) and neuropeptide Y (NPY; a potent orexigenic peptide) potentially integrate information on food availability into seasonal reproductive development, we also measured the brain levels of these peptides.At the hypothalamic level, we detected no effect of food restriction on immunoreactive (ir) GnRH‐I, but the duration of food restriction was inversely related to the size of ir‐GnIH perikarya. Furthermore, the number of ir‐NPY cells was higher in food‐restricted than control birds. Food restriction did not influence photoinduced testicular growth, but decreased plasma LH and T, and width of the cloacal protuberance, an androgen‐sensitive secondary sexual characteristic. Returning birds to ad libitum food availability had no effect on plasma LH or T, but caused the cloacal protuberance to rapidly increase in size to that of ad libitum‐fed birds.Our results support the tenet that food availability modulates photoinduced reproductive activation. However, they also suggest that this modulation is complex and depends upon the level of the HPG axis considered. At the hypothalamic level, our results are consistent with a role for the GnIH and NPY systems in integrating information on energetic status. There also appears to be a role for endocrine function at the anterior pituitary gland and testicular levels in modulating reproductive development in the light of energetic status and independently of testicular growth.

Food restriction negatively affects multiple levels of the reproductive axis in male house finches, Haemorhous mexicanus

“…We sought to identify potential hypothalamic mediators of GnRH activity in the house finch. The GnIH-NPY axis is a good candidate for mediating energetic signals on the reproductive axis (Davies and Deviche, 2014), with GnIH-ir and NPY-ir affected by 4 weeks of food restriction in Abert's towhees (Davies et al, 2015a). However, we found no change in hypothalamic GnIH expression in response to food restriction, which provides no evidence that GnIH is involved in mediating energy-related signals in house finches.…”

“…Consistent with this observation, food-restricted finches were in lower body condition and had lower plasma testosterone than ad libitum-fed finches. Chronic food restriction (Davies et al, 2015a;Pérez-Rodríguez et al, 2006) and fasting (Lynn et al, 2010) also decrease plasma testosterone in other avian species, indicating the generality of the plasma testosterone response to energetic challenges. Taken together, these morphological and hormonal data reveal inhibition of both endocrine and exocrine testicular functions during energetic deficit.…”

“…To our knowledge, however, our study is among the first to show an inhibition of testicular development in a predictably breeding, photoperiodic wild songbird under energetic deficit. European starlings, Sturnus vulgaris, with reduced body mass as a result of experimentally changing the daily duration of food availability also have underdeveloped testes (Dawson, 1986;Meijer, 1991), but testis growth is unaffected by food availability in Abert's towhees (Davies et al, 2015a). Seasonal testicular growth is primarily due to proliferation of Sertoli cells, which make up the majority of the mass in developed testes (Deviche et al, 2011;Young et al, 2001).…”

Behavioral and physiological traits of migrant and resident White-crowned Sparrows: a common garden approach

“…This response allows migrants such as Z. l. gambelii to synchronize timing and progression of seasonal events on the wintering grounds with a timely arrival at the distant breeding site. For the resident, Z. l. nuttalli, residing at only one location, responsiveness to initial predictive information is relevant to initiate development of the breeding stage but with much more flexibility as to when actual nesting begins (Davies et al, 2015;Visser et al, 2009;Wingfield and Silverin, 2009). Therefore, it is possible that Z. l. nuttalli, without the complications of a migratory life history stage, would be far less constrained to initiate development of the breeding stage than Z. l. gambelii (Davies et al, 2015;Visser et al, 2009;Wingfield and Silverin, 2009).…”

Two Neural Measures Differ between Urban and Rural Song Sparrows after Conspecific Song Playback

“…We identified the lateral and medial portions of the VMH at the level of the median eminence following Goodson et al (2005a) and Maney et al (2008). We quantified FOS-ir in the PVN starting rostrally from the ventral supraoptic decussation and caudally until the anterior commissure and occipitomesencephalic tract fuse following Davies et al (2015). We made cell counts within a 0.20 mm 2 circle placed within the AM, BSTm, VTA, and PVN; a 0.15 mm 2 circle in CG and TnA; a 0.13 mm 2 circle inside VMH-m and VMH-l; a 0.05 mm 2 circle placed within the LSc.vl; and a 0.03 mm 2 circle placed in POM.…”