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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. 

Urbanization, despite its destructive effects on natural habitats, offers species an opportunity to colonize novel niches. Previous research found that urban Anolis lizards in Puerto Rico had increased adhesive toepad area and more ventral toepad scales, traits that are likely adaptive and genetically based. We further investigated these phenotypic changes using geometric morphometrics to measure differences in toe shape, toepad shape, and lamellar morphology. Our results indicate that the increased toepad area of urban Anolis cristatellus lizards in Puerto Rico is not simply an isometric increase in toe size. Toes of urban populations exhibit multiple disproportional changes compared to forest lizards, with a larger proportion of the toe length covered in adhesive toepad. In addition, the toepads of urban lizards increase more in length than width. Lastly, lizards in urban populations exhibit both increased number of lamellae as well as increased spacing between individual lamellae. We also observed regional variation, with urban specimens having significantly more disparity, suggesting similar processes of urban adaptation are likely happening in parallel across the island, yet with region-specific idiosyncrasies, possibly generating more variation in toepad morphology across urban specimens as compared to forest specimens. Considering the use of geometric morphometrics, we found that specimen preparation, specifically how flat and straight toes are during imaging, to be an important factor affecting our data, more so than specimen size or any other meaningful morphological variation. In addition, we found that landmark and semilandmark data can be used to directly estimate toepad area, offering the opportunity to streamline future studies. In conclusion, our results highlight the value of considering toepad morphology in more detail beyond adhesive pad area or number of lamellae. Geometric morphometrics tools may be employed to elucidate subtle differences in shape to better allow researchers to connect changes in morphology to ecology and adhesive performance.

 

Abstract Human activity drastically transforms landscapes, generating novel habitats to which species must adaptively respond. Consequently, urbanization is increasingly recognized as a driver of phenotypic change. The structural environment of urban habitats presents a replicated natural experiment to examine trait–environment relationships and phenotypic variation related to locomotion. We use geometric morphometrics to examine claw morphology of five species of Anolis lizards in urban and forest habitats. We find that urban lizards undergo a shift in claw shape in the same direction but varying magnitude across species. Urban claws are overall taller, less curved, less pointed and shorter in length than those of forest lizards. These differences may enable more effective attachment or reduce interference with toepad function on smooth anthropogenic substrates. We also find an increase in shape disparity, a measurement of variation, in urban populations, suggesting relaxed selection or niche expansion rather than directional selection. This study expands our understanding of the relatively understudied trait of claw morphology and adds to a growing number of studies demonstrating phenotypic changes in urban lizards. The consistency in the direction of the shape changes we observed supports the intriguing possibility that urban environments may lead to predictable convergent adaptive change. 

Abstract Anolis lizards are well known for their specialist ecomorphs characterized by the convergent evolution of suites of traits linked to the use of particular microhabitats. Many of these same traits evolve rapidly in response to novel selection pressures and have been very well studied. In contrast, the tail crest, a feature present in a subset of lineages, has been almost entirely overlooked. Variation in tail crest morphology within and among species remains largely unstudied, as does the function of the trait. Here, we use the natural experiment provided by urbanization to ask whether tail crest size differs between urban and forest populations of the crested anole (Anolis cristatellus) across the Caribbean island of Puerto Rico. We find that tail crest size differs primarily between regions; however, within regions, crests are invariably larger in urban than in forest environments. This difference in size is correlated with the hotter, drier conditions and sparser distribution of perches that typify urban sites, leading to the intriguing possibility that the tail crest might be under differential natural selection for signalling and/or because of the thermoregulatory challenge of urban habitats. Further study is required to shed light on the functional significance and evolution of this under-studied trait.