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.