Genome-wide parallelism underlies contemporary adaptation in urban lizards

Abstract

Urbanization drastically transforms landscapes, resulting in fragmentation, degradation, and the loss of local biodiversity. Yet, urban environments also offer opportunities to observe rapid evolutionary change in wild populations that survive and even thrive in these novel habitats. In many ways, cities represent replicated “natural experiments” in which geographically separated populations adaptively respond to similar selection pressures over rapid evolutionary timescales. Little is known, however, about the genetic basis of adaptive phenotypic differentiation in urban populations nor the extent to which phenotypic parallelism is reflected at the genomic level with signatures of parallel selection. Here, we analyzed the genomic underpinnings of parallel urban-associated phenotypic change in Anolis cristatellus , a small-bodied neotropical lizard found abundantly in both urbanized and forested environments. We show that phenotypic parallelism in response to parallel urban environmental change is underlain by genomic parallelism and identify candidate loci across the Anolis genome associated with this adaptive morphological divergence. Our findings point to polygenic selection on standing genetic variation as a key process to effectuate rapid morphological adaptation. Identified candidate loci represent several functions associated with skeletomuscular development, morphology, and human disease. Taken together, these results shed light on the genomic basis of complex morphological adaptations, provide insight into the role of contingency and determinism in adaptation to novel environments, and underscore the value of urban environments to address fundamental evolutionary questions.

The genomic response to urbanization in the damselfly Ischnura elegans

“…Overall, parallel adaptation to urbanization is common at the phenotypic level (Santangelo et al, 2020). The parallel response has also been detected at the genomic level, both at individual SNPs (Campbell et al, 2014;Theodorou et al, 2018) and in genes and genomic regions (Mueller et al, 2013;Winchell et al, 2023). However, typically both parallel and region-specific signals are detected in genomic scans (Reid et al, 2016;Salmón et al, 2021), and some studies detected little evidence for parallel genomic response to urbanization (Caizergues et al, 2022;Mueller et al, 2020).…”

Genetic depletion does not prevent rapid evolution in island‐introduced lizards

“…Studies of “evolution in action” in wild populations have shown that dramatic phenotypic changes can emerge in just a few generations (Hendry, 2016 ; Messer et al., 2016 ), for example, in response to environmental perturbations (Campbell‐Staton et al., 2017 ; Eloy de Amorim et al., 2017 ; Franks et al., 2016 ; Grant & Grant, 2002 ; Winchell et al., 2023 ) or following species introductions (Colautti & Lau, 2015 ; Prentis et al., 2008 ). Species on islands often show particularly fast evolutionary rates compared to mainland populations (Millien, 2006 ).…”

Genomic signatures of adaptation in native lizards exposed to human-introduced fire ants

“…Across ecosystems, evidence for rapid adaptation to human-induced environmental changes continues to build (Strauss et al 2006; Shaw and Etterson 2012; Sullivan et al 2017; McCulloch and Waters 2023). A few illustrative examples include the water flea Daphnia showing signals of adaptation for resistance to salinization derived from human activity (Wersebe and Weider 2023), and independent populations of crested anoles ( Anolis cristatellus ) carrying signatures of convergent genetic adaptation to urbanization (Winchell et al 2023). Meanwhile, human-commensal house sparrows ( Passer domesticus ) have signatures of positive selection overlapping an amylase gene, which encodes an enzyme involved in starch digestion (Ravinet et al 2018), and poaching of African elephants for ivory appears to have resulted in rapid adaptation for a tuskless phenotype (Campbell-Staton et al 2021).…”