What makes a bird successful in the city? Jakob Mueller and colleagues first attempted to answer this question in blackbirds, finding genomic signatures of selection in the SERT gene associated with harm avoidance. Now, building on only a handful of studies to explore the genomic basis of urban adaptive responses, Mueller and colleagues tackle this topic in burrowing owls, Athene cunicularia, in their most recent paper: “Genes acting in synapses and neuron projections are early targets of selection during urban colonization“. This work also builds on their previous work on urban population genetics in burrowing owls, which demonstrated urban associated variation in population size and standing genetic variation.
Mueller and colleagues tested for repeated signatures of natural selection at the genomic level associated with urbanization among 213 burrowing owls from three paired urban-rural populations in Argentina. The group analyzed whole genome sequences and employed four complementary tests for selection at the genomic level: (1) consistent allele frequency shifts, (2) allele frequency shifts over time since urban colonization, (3) selective sweeps, and (4) genome-wide associations with harm-avoidance behavior (flight initiation distance, “FID”).
Genome-wide signatures of selection
Mueller et al. identified genome-wide signatures of natural selection in urban burrowing owls by employing a series of complementary linear models assessing genotypic associations with urbanization, behavioral phenotype, and time since urban colonization, as well as scans for selective sweeps. The authors then analyzed the common set of genes that were outliers in each of the genetic association tests with a gene enrichment analysis used to identify associated organismal functions. This GO enrichment analysis highlighted synaptic function and neuron development as key associations of genes under selection in urban burrowing owls.
A closer look at SERT and DRD4
The authors also took a closer look at two genes that have been identified in other bird species as an important for urban persistence and harm-avoidance behavior. This genome-wide association analysis revealed urban-habitat associations in SERT but not DRD4. Moreover, regions of SERT associated with urban habitat use were also associated with variation in flight initiation distance, suggesting a genomic basis in the SERT gene underlying urban shifts in this behavioral trait. Interestingly, this gene region appears to be homologous to the region of SERT previously analyzed in urban blackbirds with respect to harm-avoidance behavior.
Together, Mueller and team’s new findings suggest that the urban environment imposes strong selection pressures on cognition, brain function, and harm-avoidance evident at the genomic level. Brain function and behavioral responses thus continue to stand out among urban birds as critical for urban colonization and likely targets of urban natural selection.
Featured image: Burrowing owl, by iNaturalist user Rob Klotz (CC-BY-NC)
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