Mechanisms Associated with an Advance in the Timing of Seasonal Reproduction in an Urban Songbird

Abstract

The colonization of urban environments by animals is often accompanied by earlier breeding and associated changes in seasonal schedules. Accelerated timing of seasonal reproduction in derived urban populations is a potential cause of evolutionary divergence from ancestral populations if differences in physiological processes that regulate reproductive timing become fixed over time. We compared reproductive development in free-living and captive male dark-eyed juncos deriving from a population that recently colonized a city (∼35 years) and ceased migrating to that of conspecifics that live in sympatry with the urban population during winter and spring but migrate elsewhere to breed. We predicted that the earlier breeding sedentary urban birds would exhibit accelerated reproductive development in the spring along the hypothalamic-pituitary-gonadal (HPG) axis as compared to migrants. We found that free-living sedentary urban and migrant juncos differed at the level of the pituitary when measured as baseline luteinizing hormone (LH) levels, but not in increased LH when challenged with Gonadotropin-Releasing Hormone (GnRH). Among captives held in a common garden, and at the level of the gonad, we found that sedentary urban birds produced more testosterone in response to GnRH than migrants living in the same common environment, suggesting greater gonadal sensitivity in the derived urban population. Greater gonadal sensitivity could arise from greater upstream activation by LH or FSH or from reduced suppression of gonadal development by the adrenal axis. We compared abundance of gonadal transcripts for LH receptor (LHR), follicle stimulating hormone receptor (FSHR), glucocorticoid receptor (GR), and mineralocorticoid receptor (MR) in the common-garden, predicting either more abundant transcripts for LHR and FSHR or fewer transcripts for GR and MR in the earlier breeding sedentary urban breeders, as compared to the migrants. We found no difference in the expression of these genes. Together these data suggest that advanced timing of reproduction in a recently derived urban population is facilitated by earlier increase in upstream baseline activity of the HPG and earlier release from gonadal suppression Fudickar et al. Timing of Reproduction following Urbanizationby yet-to-be-discovered mechanisms. Evolutionarily, our results suggest that potential for gene flow between seasonally sympatric populations may be limited due to urban-induced advances in the timing of reproduction and resulting allochrony with ancestral forms.

Seasonally sympatric but allochronic: differential expression of hypothalamic genes in a songbird during gonadal development

“…Therefore, our results do not support the hypothesis that differences in the seasonal timing of gonadal growth and reproductive maturation are controlled by sensitivity to gonadotropins. Our findings are in line with a recent comparison of testis LHR and FSHR mRNA expression in seasonally sympatric migrant and resident dark-eyed juncos (J. h. thurberi) in California, USA, wherein Fudickar et al [13] found that early breeding urban juncos had similar gonadal LHR and FSHR mRNA expression in early spring compared to late breeding migrant juncos that are found in sympatry outside of breeding. Increased hypothalamic GnRH mRNA expression in residents during early spring, as we report in the current study, could lead to earlier testis growth due to increased LH and FSH production without the need for increased LHR and FSHR.…”

“…Increased hypothalamic GnRH mRNA expression in residents during early spring, as we report in the current study, could lead to earlier testis growth due to increased LH and FSH production without the need for increased LHR and FSHR. In previous comparisons of LH in freeliving migrant and resident juncos in Virginia and California, residents tended to have higher circulating LH than migrants in early spring [13,22].…”

Migratory strategy explains differences in timing of female reproductive development in seasonally sympatric songbirds

“…Recent evidence suggests that juncos may not fully moult on the breeding grounds (Pyle, Saracco, & DeSante, 2018); however, the most distal secondary flight feather is one of the first feathers to moult (Nolan et al, 2002). We used δ 2 H composition of feathers to infer the female's breeding latitude based on the known isotopic structure of North American precipitation (Bowen, Wassenaar, & Hobson, 2005;Fudickar et al, 2017Fudickar et al, , 2016. All feather samples were stored in paper coin envelopes at room temperature and then cleaned of oils using a 2:1 chloroform: methanol solution.…”

Dose‐response effects of light at night on the reproductive physiology of great tits (Parus major): Integrating morphological analyses with candidate gene expression

“…Open and closed bars represent birds culled at noon or midnight respectively. Sample sizes: dark: day = 6, night = 7; 0.5 lux: day = 2, night = 5; 1.5 lux: day = 2, night = 5; 5 lux: day = 2, night = 5 work in captive dark-eyed juncos (Junco hyemalis thurberi) has also questioned the direct effect of glucocorticoids on gonadal processes (Fudickar et al, 2017). While we did not measure corticosterone, the ratio of MR/GR, which is often used to test for altered stability of the stress axis (Marasco, Herzyk, Robinson, & Spencer, 2016), did not vary between the four treatments (Supporting Information Figure S2a), and individual gr and mr transcript levels were highly correlated (Supporting Information Figure S2b).…”

“…During gonadal development in birds, transcript levels of glucocorticoid ( nr3c1 , also referred to as gr ) and mineralocorticoid receptors ( nr3c2 , also referred to as mr ) also increase (Fudickar et al., ; Kirby, Geraghty, Ubuka, Bentley, & Kaufer, ; Lattin et al., ; McGuire, Koh, & Bentley, ). This provides a mechanistic basis for the widespread links between adrenal steroids and timing of reproduction and reproductive investment reported in several bird species (Crespi, Williams, Jessop, & Delehanty, ; Deviche et al., ; Goutte et al., ; Lattin, Breuner, & Michael Romero, ; McGuire et al., ; Schoech, Rensel, Bridge, Boughton, & Wilcoxen, ).…”