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

1. Divergent migratory strategies among populations can result in population-level differences in timing of reproduction (allochrony) and local adaptation. However, the mechanisms underlying among-population variation in timing are insufficiently understood, particularly in females.

2. We studied differences in reproductive development and its related mechanisms along the hypothalamic-pituitary-gonadal axis (HPG) in closely related migratory and sedentary (i.e., resident) female dark-eyed juncos (Junco hyemalis) living together in sympatry during early spring. We predicted that residents would be more reproductively developed than migrants. Alternatively, we predicted that females might exhibit similar reproductive development in response to the same environmental cue despite differences in migratory behavior. To compare their degree of reproductive development during seasonal sympatry and the underlying mechanisms of these differences, we collected ovarian and liver tissue in early spring prior to migration, and compared abundance of gene transcripts associated with reproduction using quantitative PCR. We also used stable hydrogen isotopes to infer relative breeding and wintering latitude of migrants.

3. We found more abundant transcripts for luteinizing hormone receptor and aromatase in addition to significantly heavier ovaries in residents than in migrants. Together these results suggest greater sensitivity and response to upstream endocrine stimulation in resident females. Transcript abundance for other receptors associated with reproduction, however, did not differ between populations. When comparing ovarian development within migrants, females with lower hydrogen isotopes (indicating higher breeding latitudes) had smaller ovaries, suggesting that longer-distance migrations may further delay reproductive development.

4. Based on differences in ovary mass and transcript abundance, we conclude that females that differ in migratory strategy also differ in timing of reproductive development. Differences in timing of reproductive development between migrant and resident females could drive reproductive isolation between populations. This study also reveals mechanisms that could drive allochrony and enable us to predict how seasonal organisms will respond to a changing world.