Random effects and selection promote rapid evolutionary change
Rapid divergence of phenotypic traits is often attributed to strong selective pressures imposed by novel biotic and abiotic environments (e.g. Chen et al. 2018; Jensen et al. 2017; Mathys & Lockwood 2011; Sendell-Price et al. 2020), or to a combination of selective and neutral factors (Grant et al. 2001; Kliber & Eckert 2005; Kolbe et al. 2012). The juncos from UCSD represent an extreme case of rapid evolutionary divergence, apparently caused by the colonization of an urban environment. Such degree of differentiation taking place over comparably short periods is only met by a few other documented examples in nature (e.g. Chen et al. 2018; Hendry & Kinnison 1999; Koskinen et al. 2002; Lescak et al. 2015; Sendell-Price et al. 2020). The small number of colonizers estimated suggests the role of severe founder effects and genetic drift in the process of differentiation of the UCSD juncos (Kolbe et al. 2012), a scenario also congruent with the lower values of genetic diversity at UCSD based on neutral markers.
However, we also found evidence of local adaptation in promoting evolutionary divergence between UCSD juncos and closely related Oregon junco forms. A redundancy analysis based on the most dissimilar set of our geo-referenced ecological variables between the UCSD and natural habitats, revealed a distinctive pattern of associations for the urban population, positively correlating with mean temperature during the breeding season and negatively with vegetation greenness, temperature seasonality and elevation. Although these ecological parameters were particularly distinct for the UCSD campus with respect to native ranges, they may not encompass key aspects of the urban environment (e.g., unsuitable habitat due to human structures, contamination, human-processed foods, mechanical noise or distressing stimuli) with which they may, in turn, present spatial correlation (Szulkin et al. 2020a). Much of the recovered correlation signal is likely to also be due to population history-related effects (Forester et al.2016; Frichot et al. 2015; Wang & Bradburd 2014), yet controlling for neutral genetic structure in RDA approaches may result in a high loss of power to detect signals of selection without necessarily reducing the rate of false positives (Forester et al.2018). RDA outliers linked to functional genes suggest, however, a role for selective pressures in shaping allele frequencies in potentially adaptive loci in the newly colonized habitat. Among the functions associated to detected candidate genes, at least two (ABCB6 and KCNQ4) seem particularly relevant in anthropogenic environments. The ABCB6 gene shows significant sequence identity to HMT-1 (heavy metal tolerance factor 1) proteins, whose evolutionarily conserved role is to confer tolerance to heavy metals through the intracellular sequestration of metal complexes (Rakvács et al. 2019). Several studies have reported negative effects of metals (such as cadmium, copper, lead, mercury, nickel and selenium) on fitness traits of birds occurring in anthropogenic habitats (Burger & Gochfeld 1988; Eeva & Lehikoinen 1996; Geens et al. 2010; Takekawa et al. 2002). In turn, KCNQ4 encodes a protein that forms a voltage-gated potassium channel for the regulation of electrical signaling, expressed in the sensory receptors of the auditory system of all vertebrates (Kharkovets et al. 2000). KCNQ4 has also been found to be involved in high-frequency hearing in echolocating bats (Eriksson & Wiktelius 2011). A significantly higher minimum frequency in the vocal signaling of the UCSD juncos with respect to natural habitats have been previously reported (Cardoso & Atwell 2010, 2011; Reichard et al. 2020; Slabbekoorn et al. 2007), arguably as a strategy to reduce masking by anthropogenic low-frequency noise. Importantly, both genes showed high levels of divergence with respect to pinosus , as evidenced by F ST values. Other genes showing signs of differentiation between these two groups were involved in thrombopoiesis, DNA damage repair, or egg laying performance and quality, which could also be involved in adaptive processes driving differentiation between pinosus and UCSD juncos. These results suggest a specific role for anthropogenic selective pressures in shaping adaptive variability among UCSD and forest Oregon juncos, which in combination with extreme founding conditions, may have resulted in an exceptionally fast process of differentiation at both functional and neutral loci in the resident juncos at UCSD.