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 along the hypothalamic-pituitary (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 the 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 by 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
Highlights
Over the past several centuries, urban landscapes have replaced native habitat in many parts of the world (Marzluff, 2016; Alberti et al, 2017)
Seasonal fluctuations in climate and resource availability are often reduced in urban environments, which can lead to longer breeding seasons and year-round occupancy by formerly migratory lineages (Adriaensen and Dhondt, 1990; Partecke and Gwinner, 2007; Chamberlain et al, 2009; Atwell et al, 2014)
This study focused on a population of dark-eyed juncos (J. hyemalis thurberi) that became established in urban San Diego CA USA in the early 1980s, likely as a result of overwintering migratory birds remaining to breed (Rasner et al, 2004; Yeh, 2004; Atwell et al, 2012, 2014)
Summary
Over the past several centuries, urban landscapes have replaced native habitat in many parts of the world (Marzluff, 2016; Alberti et al, 2017). If advanced reproduction in urban populations is the result of selection for greater sensitivity of the HPG at shorter day lengths—either by an earlier seasonal response or responding at a faster rate— the resulting reproductive allochrony (asynchronous reproduction) may limit gene flow between urban and rural populations, leading to selection against hybrids. If advanced timing in urban populations is modulated by plastic responses, the scope for divergence may be limited, as immigrants would be capable of adopting the timing of established urban populations. These alternatives have important implications for the adaptability of both urban and rural populations to cope with future environmental change
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