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  1. The idea that changing environmental conditions drive adaptive evolution is a pillar of evolutionary ecology. But, the opposite—that adaptive evolution alters ecological processes—has received far less attention yet is critical for eco-evolutionary dynamics. We assessed the ecological impact of divergent values in a key adaptive trait using 16 populations of the brown anole lizard ( Anolis sagrei ). Mirroring natural variation, we established islands with short- or long-limbed lizards at both low and high densities. We then monitored changes in lower trophic levels, finding that on islands with a high density of short-limbed lizards, web-spider densities decreased and plants grew more via an indirect positive effect, likely through an herbivore-mediated trophic cascade. Our experiment provides strong support for evolution-to-ecology connections in nature, likely closing an otherwise well-characterized eco-evolutionary feedback loop. 
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    Free, publicly-accessible full text available June 13, 2024
  2. 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. 
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  3. Abstract

    As anthropogenic activities are increasing the frequency and severity of droughts, understanding whether and how fast populations can adapt to sudden changes in their hydric environment is critically important. Here, we capitalize on the introduction of the Cuban brown anole lizard (Anolis sagrei) in North America to assess the contemporary evolution of a widespread terrestrial vertebrate to an abrupt climatic niche shift. We characterized hydric balance in 30 populations along a large climatic gradient. We found that while evaporative and cutaneous water loss varied widely, there was no climatic cline, as would be expected under adaptation. Furthermore, the skin of lizards from more arid environments was covered with smaller scales, a condition thought to limit water conservation and thus be maladaptive. In contrast to environmental conditions, genome-averaged ancestry was a significant predictor of water loss. This was reinforced by our genome-wide association analyses, which indicated a significant ancestry-specific effect for water loss at one locus. Thus, our study indicates that the water balance of invasive brown anoles is dictated by an environment-independent introduction and hybridization history and highlights genetic interactions or genetic correlations as factors that might forestall adaptation. Alternative water conservation strategies, including behavioral mitigation, may influence the brown anole invasion success and require future examination.

     
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  4. Abstract

    Introductions of invasive species to new environments often result in rapid rates of trait evolution. While in some cases these evolutionary transitions are adaptive and driven by natural selection, they can also result from patterns of genetic and phenotypic variation associated with the invasion history. Here, we examined the brown anole (Anolis sagrei), a widespread invasive lizard for which genetic data have helped trace the sources of non‐native populations. We focused on the dewlap, a complex signalling trait known to be subject to multiple selective pressures. We measured dewlap reflectance, pattern and size in 30 non‐native populations across the southeastern United States. As well, we quantified environmental variables known to influence dewlap signal effectiveness, such as canopy openness. Further, we used genome‐wide data to estimate genetic ancestry, perform association mapping and test for signatures of selection. We found that among‐population variation in dewlap characteristics was best explained by genetic ancestry. This result was supported by genome‐wide association mapping, which identified several ancestry‐specific loci associated with dewlap traits. Despite the strong imprint of this aspect of the invasion history on dewlap variation, we also detected significant relationships between dewlap traits and local environmental conditions. However, we found limited evidence that dewlap‐associated genetic variants have been subject to selection. Our study emphasizes the importance of genetic ancestry and admixture in shaping phenotypes during biological invasion, while leaving the role of selection unresolved, likely due to the polygenic genetic architecture of dewlaps and selection acting on many genes of small effect.

     
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  5. Determining whether and how evolution is predictable is an important goal, particularly as anthropogenic disturbances lead to novel species interactions that could modify selective pres- sures. Here, we use a multigeneration field experiment with brown anole lizards (Anolis sagrei) to test hypotheses about the predictabil- ity of evolution. We manipulated the presence/absence of predators and competitors of A. sagrei across 16 islands in the Bahamas that had preexisting brown anole populations. Before the experiment and again after roughly five generations, we measured traits related to locomotor performance and habitat use by brown anoles and used double-digest restriction enzyme–associated DNA sequencing to estimate genome-wide changes in allele frequencies. Although previous work showed that predators and competitors had characteristic effects on brown anole behavior, diet, and population sizes, we found that evolutionary change at both phenotypic and genomic levels was difficult to forecast. Phenotypic changes were contingent on sex and hab- itat use, whereas genetic change was unpredictable and not measur- ably correlated with phenotypic changes, experimental treatments, or other environmental factors. Our work shows how differences in ecological context can alter evolutionary outcomes over short timescales and underscores the difficulty of forecasting evolutionary responses to multispecies interactions in natural conditions, even in a well-studied system with ample supporting ecological information. 
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  6. Abstract

    Research conducted during the past two decades has demonstrated that biological invasions are excellent models of rapid evolution. Even so, characteristics of invasive populations such as a short time for recombination to assemble optimal combinations of alleles may occasionally limit adaptation to new environments. Here, we investigated such genetic constraints to adaptation in the invasive brown anole (Anolis sagrei)—a tropical ectotherm that was introduced to the southeastern United States, a region with a much colder climate than in its native Caribbean range. We examined thermal physiology for 30 invasive populations and tested for a climatic cline in cold tolerance. Also, we used genomics to identify mechanisms that may limit adaptation. We found no support for a climatic cline, indicating that thermal tolerance did not shift adaptively. Concomitantly, population genomic results were consistent with the occurrence of recombination cold spots that comprise more than half of the genome and maintain long‐range associations among alleles in invasive populations. These genomic regions overlap with both candidate thermal tolerance loci that we identified using a standard genome‐wide association test. Moreover, we found that recombination cold spots do not have a large contribution to population differentiation in the invasive range, contrary to observations in the native range. We suggest that limited recombination is constraining the contribution of large swaths of the genome to adaptation in invasive brown anoles. Our study provides an example of evolutionary stasis during invasion and highlights the possibility that reduced recombination occasionally slows down adaptation in invasive populations.

     
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  7. Abstract

    Rapid technological improvements are democratizing access to high quality, chromosome-scale genome assemblies. No longer the domain of only the most highly studied model organisms, now non-traditional and emerging model species can be genome-enabled using a combination of sequencing technologies and assembly software. Consequently, old ideas built on sparse sampling across the tree of life have recently been amended in the face of genomic data drawn from a growing number of high-quality reference genomes. Arguably the most valuable are those long-studied species for which much is already known about their biology; what many term emerging model species. Here, we report a highly complete chromosome-scale genome assembly for the brown anole,Anolis sagrei– a lizard species widely studied across a variety of disciplines and for which a high-quality reference genome was long overdue. This assembly exceeds the vast majority of existing reptile and snake genomes in contiguity (N50 = 253.6 Mb) and annotation completeness. Through the analysis of this genome and population resequence data, we examine the history of repetitive element accumulation, identify the X chromosome, and propose a hypothesis for the evolutionary history of fusions between autosomes and the X that led to the sex chromosomes ofA. sagrei.

     
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  8. Oceanic islands are known as test tubes of evolution. Isolated and colonized by relatively few species, islands are home to many of nature’s most renowned radiations from the finches of the Galápagos to the silverswords of the Hawaiian Islands. Despite the evolutionary exuberance of insular life, island occupation has long been thought to be irreversible. In particular, the presumed much tougher competitive and predatory milieu in continental settings prevents colonization, much less evolutionary diversification, from islands back to mainlands. To test these predictions, we examined the ecological and morphological diversity of neotropicalAnolislizards, which originated in South America, colonized and radiated on various islands in the Caribbean, and then returned and diversified on the mainland. We focus in particular on what happens when mainland and island evolutionary radiations collide. We show that extensive continental radiations can result from island ancestors and that the incumbent and invading mainland clades achieve their ecological and morphological disparity in very different ways. Moreover, we show that when a mainland radiation derived from island ancestors comes into contact with an incumbent mainland radiation the ensuing interactions favor the island-derived clade.

     
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  10. Hybridization is among the evolutionary mechanisms most frequently hypothesized to drive the success of invasive species, in part because hybrids are common in invasive populations. One explanation for this pattern is that biological invasions coincide with a change in selection pressures that limit hybridization in the native range. To investigate this possibility, we studied the introduction of the brown anole (Anolis sagrei) in the southeastern United States. We find that native populations are highly genetically structured. In contrast, all invasive populations show evidence of hybridization among native-range lineages. Temporal sampling in the invasive range spanning 15 y showed that invasive genetic structure has stabilized, indicating that large-scale contemporary gene flow is limited among invasive populations and that hybrid ancestry is maintained. Additionally, our results are consistent with hybrid persistence in invasive populations resulting from changes in natural selection that occurred during invasion. Specifically, we identify a large-effect X chromosome locus associated with variation in limb length, a well-known adaptive trait in anoles, and show that this locus is often under selection in the native range, but rarely so in the invasive range. Moreover, we find that the effect size of alleles at this locus on limb length is much reduced in hybrids among divergent lineages, consistent with epistatic interactions. Thus, in the native range, epistasis manifested in hybrids can strengthen extrinsic postmating isolation. Together, our findings show how a change in natural selection can contribute to an increase in hybridization in invasive populations.

     
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