Colonization of a novel environment by a few individuals can lead to rapid evolutionary change, yet evidence of the relative contributions of neutral and selective factors in promoting divergence during the early stages of colonization remain scarce. We explore the role of neutral and selective forces in the divergence of a unique urban population of the dark-eyed junco (Junco hyemalis), which became established on the campus of the University of California at San Diego (UCSD) in the early 1980s. Previous studies based on microsatellite loci documented significant genetic differentiation of the urban population as well as divergence in phenotypic traits relative to nearby montane populations, yet the geographic origin of the colonization and the factors involved remained uncertain. Our genome-wide SNP dataset confirmed the marked genetic differentiation of the UCSD population, and we identified the coastal subspecies pinosus from central California as its sister group instead of the neighboring mountain population. Demographic inference recovered a separation from pinosus as recent as 20 to 32 generations ago after a strong bottleneck, suggesting a role for drift in genetic differentiation. However, we also found significant associations between habitat variables and genome-wide variants linked to functional genes, some of which have been reported as potentially adaptive in birds inhabiting modified environments. These results suggest that the interplay between founder events and selection may result in rapid shifts in neutral and adaptive loci across the genome, and reveal the UCSD junco population as a case of contemporary evolutionary divergence in an anthropogenic environment.

Individuals and populations time annual events such as migration and reproduction to match favorable times in their environment. Physiological preparations for reproduction rely on predictive cues such as day length to accurately time reproduction. In birds, preparation typically begins with light reception by the hypothalamus, which initiates multiple central and peripheral responses. We studied two closely related populations of a songbird, the dark-eyed junco, that live in a common winter environment but diverge in their timing of reproduction as spring approaches. One population is resident and initiates reproduction earlier than the other, which migrates northward prior to reproducing. We caught resident and migrant juncos from the field during early spring and collected hypothalamic and pituitary tissues. We used isobaric tandem mass tag (TMT) labeling to identify differentially expressed proteins (DEPs) as possible regulators of the seasonal divergence in reproductive timing. We found 3038 unique proteins expressed in the hypothalamus and pituitary proteome, among which we identified 75 DEPs. These were associated with hormones, neurotransmitter secretion, transport, neuropeptide synthesis, prohormone synthesis, neurogenesis, GnRH synthesis, release and stability, food intake, locomotion, and social behavior. Some of these proteins were associated with early breeding in resident juncos, and others were associated with increased food intake, fat metabolism, locomotor activity and phenology in migratory juncos. Our results provide new insight into the neuroendocrine regulation of the timing of reproduction and migration. This study provides the first evidence of a relationship between functional protein variation in the neuroendocrine tissues and seasonal divergence in reproductive timing.

Many organisms time reproduction to photoperiod, a constant from year to year.  Predicting how anthropogenic change will influence future timing demands greater knowledge of the current role of photoperiod.  We held two closely related bird populations in a common environment. One population is resident; the other winters in sympatry with the resident population but migrates north prior to reproducing. We increased photoperiod gradually and measured preparation for migration and reproduction, using feather stable isotopes to estimate breeding latitude. We predicted population differences in the minimum stimulatory day length to elicit a response (CPP, critical photoperiod) and co-variation between CPP and distance migrated. We found clear population differences in CPP and greater CPP in longer distance migrants. We conclude that current geographic variation in reproductive timing has a genetic or early developmental basis and recommends that future research focus on how anthropogenic changes will interact with CPP to adjust the timing of reproduction and migration.