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

Abstract

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. 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. Despite exposure to the same environmental cues in early spring, residents initiate breeding prior to the departure of migrants for their breeding grounds. We investigated whether residents would be more reproductively developed than migrants based on their behavioural differences. Alternatively, females could exhibit similar reproductive development in response to the same environmental cues despite differences in migratory behaviour. 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 transcript abundance of genes associated with reproduction using quantitative PCR. We also used stable hydrogen isotopes to infer relative breeding and wintering latitude of migrants. We found higher transcript abundance of luteinizing hormone receptor and aromatase in the ovary 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 in the ovary and liver 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. 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. These results support that divergent migratory behaviour drives allochrony and could enable reproductive isolation between populations; mechanistic differences at the level of gonadal stimulation can explain these differences in timing of reproductive development. A free Plain Language Summary can be found within the Supporting Information of this article.

Local adaptation from afar: migratory bird populations diverge in the initiation of reproductive timing while wintering in sympatry

“…We compared early spring indices of reproductive initiation between two migratory populations of the junco complex and found population-level differences in reproductive timing despite exposure to the same environmental cues at their overwintering location. The δ 2 H f values reflect nonoverlapping geographic origins of PSJU and SCJU as expected based on plumage differences [19,24]. Significantly higher δ 2 H f values in PSJU indicate a lower breeding latitude, and thus a shorter migratory distance than SCJU [13].…”

“…150 µl) for baseline T (T 0 ) immediately after capture by puncturing the brachial wing vein. Birds then received an intrapectoral GnRH injection [16][17][18][19], and a second blood sample (approx. 150 µl) was collected after 30 min to measure elevated T (T 30 ) levels.…”

“…We captured seasonally sympatric pink-sided (PSJU) and slate-coloured juncos (SCJU) prior to spring migration and injected them with GnRH to measure naturally occurring testosterone (T) variation. Exogenous GnRH is commonly used to measure maximum gonadal T production [16][17][18][19]. We used stable isotope analyses of hydrogen in feathers (δ 2 H f ) to estimate breeding latitude and claws (δ 2 H c ) to confirm that both groups overwintered at the capture site rather than being sampled at a stopover site during vernal migration.…”

Comparative proteomics reveals molecular correlates of population-level variation in reproductive timing in a North American songbird

“…The discrete nonoverlapping feather δ 2 H f values provide strong evidence that the populations do not have overlapping breeding ranges. The hydrogen isotope values measured in claw tissue that were grown on their wintering location did not differ between two populations, suggesting that both groups overwintered at the capture site (Lymburner, Kelly, Hobson, & MacDougall-Shackleton, 2016;Kimmitt, Hardman, Stricker, & Ketterson, 2019). Together, feather and claw δ 2 H data indicate that migrant and resident juncos in the current study were sympatric during winter and originated from different breeding latitudes.…”

Plasticity in female timing may explain current shifts in breeding phenology of a North American songbird

“…Accurate predictions of future responses to climate change will require further consideration of mechanisms of female reproductive timing (Williams 2012;Chmura, Wingfield & Hahn 2020;Kimmitt 2020). Past and ongoing work in the junco is elucidating the physiological mechanisms driving reproductive timing in females based on life history, including endocrine systems and costs of early breeding (Greives et al 2016;Graham et al 2019;Kimmitt et al 2019;Kimmitt, Sinkiewicz & Ketterson 2020). However, more research is necessary to understand how females integrate supplementary cues, such as temperature, to regulate the final stages of their reproductive development and ovulation (Wingfield et al 2016;Chmura, Wingfield & Hahn 2020).…”