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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.
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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 of A. sagrei. A highly-complete chromosome-scale genome assembly of the brown anole, Anolis sagrei, provides insight into the evolution of sex chromosomes and is a crucial resource for this model lizard species.
Repeated evolution can provide insight into the mechanisms that facilitate adaptation to novel or changing environments. Here we study adaptation to altitude in two tropical butterflies, Heliconius erato and H. melpomene , which have repeatedly and independently adapted to montane habitats on either side of the Andes. We sequenced 518 whole genomes from altitudinal transects and found many regions differentiated between highland (~ 1200 m) and lowland (~ 200 m) populations. We show repeated genetic differentiation across replicate populations within species, including allopatric comparisons. In contrast, there is little molecular parallelism between the two species. By sampling five close relatives, we find that a large proportion of divergent regions identified within species have arisen from standing variation and putative adaptive introgression from high-altitude specialist species. Taken together our study supports a role for both standing genetic variation and gene flow from independently adapted species in promoting parallel local adaptation to the environment.
Urbanization is the dominant trend of global land use change. The replicated nature of environmental change associated with urbanization should drive parallel evolution, yet insight into the repeatability of evolutionary processes in urban areas has been limited by a lack of multi-city studies. Here we leverage community science data on coat color in > 60,000 eastern gray squirrels (Sciurus carolinensis) across 43 North American cities to test for parallel clines in melanism, a genetically based trait associated with thermoregulation and crypsis. We show the prevalence of melanism was positively associated with urbanization as measured by impervious cover. Urban–rural clines in melanism were strongest in the largest cities with extensive forest cover and weakest or absent in cities with warmer winter temperatures, where thermal selection likely limits the prevalence of melanism. Our results suggest that novel traits can evolve in a highly repeatable manner among urban areas, modified by factors intrinsic to individual cities, including their size, land cover, and climate.
Bone strength and the incidence and severity of skeletal disorders vary significantly among human populations, due in part to underlying genetic differentiation. While clinical models predict that this variation is largely deleterious, natural population variation unrelated to disease can go unnoticed, altering our perception of how natural selection has shaped bone morphologies over deep and recent time periods. Here, we conduct the first comparative population-based genetic analysis of the main bone structural protein gene, collagen type I α 1 (COL1A1), in clinical and 1000 Genomes Project datasets in humans, and in natural populations of chimpanzees. Contrary to predictions from clinical studies, we reveal abundant COL1A1 amino acid variation, predicted to have little association with disease in the natural population. We also find signatures of positive selection associated with intron haplotype structure, linkage disequilibrium, and population differentiation in regions of known gene expression regulation in humans and chimpanzees. These results recall how recent and deep evolutionary regimes can be linked, in that bone morphology differences that developed among vertebrates over 450 million years of evolution are the result of positive selection on subtle type I collagen functional variation segregating within populations over time.
Urbanisation is increasing worldwide, and there is now ample evidence of phenotypic changes in wild organisms in response to this novel environment. Yet, the genetic changes and genomic architecture underlying these adaptations are poorly understood. Here, we genotype 192 great tits ( Parus major ) from nine European cities, each paired with an adjacent rural site, to address this major knowledge gap in our understanding of wildlife urban adaptation. We find that a combination of polygenic allele frequency shifts and recurrent selective sweeps are associated with the adaptation of great tits to urban environments. While haplotypes under selection are rarely shared across urban populations, selective sweeps occur within the same genes, mostly linked to neural function and development. Collectively, we show that urban adaptation in a widespread songbird occurs through unique and shared selective sweeps in a core-set of behaviour-linked genes.
Background:
SAMtools and BCFtools are widely used programs for processing and analysing high-throughput sequencing data. They include tools for file format conversion and manipulation, sorting, querying, statistics, variant calling, and effect analysis amongst other methods.
Findings:
The first version appeared online 12 years ago and has been maintained and further developed ever since, with many new features and improvements added over the years. The SAMtools and BCFtools packages represent a unique collection of tools that have been used in numerous other software projects and countless genomic pipelines.
Conclusion:
Both SAMtools and BCFtools are freely available on GitHub under the permissive MIT licence, free for both non-commercial and commercial use. Both packages have been installed >1 million times via Bioconda. The source code and documentation are available from https://www.htslib.org.
Urbanization has recently emerged as an exciting new direction for evolutionary research founded on our growing understanding of rapid evolution paired with the expansion of novel urban habitats. Urbanization can influence adaptive and nonadaptive evolution in urban‐dwelling species, but generalized patterns and the predictability of urban evolutionary responses within populations remain unclear. This editorial introduces the special feature “Evolution in Urban Environments” and addresses four major emerging themes, which include: (a) adaptive evolution and phenotypic plasticity via physiological responses to urban climate, (b) adaptive evolution via phenotype–environment relationships in urban habitats, (c) population connectivity and genetic drift in urban landscapes, and (d) human–wildlife interactions in urban spaces. Here, we present the 16 articles (12 empirical, 3 review, 1 capstone) within this issue and how they represent each of these four emerging themes in urban evolutionary biology. Finally, we discuss how these articles address previous questions and have now raised new ones, highlighting important new directions for the field.
Brown rats (Rattus norvegicus) thrive in urban environments by navigating the anthropocentric environment and taking advantage of human resources and by-products. From the human perspective, rats are a chronic problem that causes billions of dollars in damage to agriculture, health and infrastructure. Did genetic adaptation play a role in the spread of rats in cities? To approach this question, we collected whole-genome sequences from 29 brown rats from New York City (NYC) and scanned for genetic signatures of adaptation. We tested for (i) high-frequency, extended haplotypes that could indicate selective sweeps and (ii) loci of extreme genetic differentiation between the NYC sample and a sample from the presumed ancestral range of brown rats in northeast China. We found candidate selective sweeps near or inside genes associated with metabolism, diet, the nervous system and locomotory behavior. Patterns of differentiation between NYC and Chinese rats at putative sweep loci suggest that many sweeps began after the split from the ancestral population. Together, our results suggest several hypotheses on adaptation in rats living in close proximity to humans.
Cities are uniquely complex systems regulated by interactions and feedbacks between natural and social processes. Characteristics of human society – including culture, economics, technology, and politics – underlie social patterns and activity, creating a heterogeneous environment that can influence and be influenced by both ecological and evolutionary processes. Increasing interest in urban ecology and evolutionary biology has coincided with growing interest in eco‐evolutionary dynamics, which encompasses the interactions and reciprocal feedbacks between evolution and ecology. Research on both urban evolutionary biology and eco‐evolutionary dynamics frequently focuses on contemporary evolution of species that have potentially substantial ecological – and even social – significance. Still, little research fully integrates urban evolutionary biology and eco‐evolutionary dynamics, and rarely do researchers in either of these fields fully consider the role of human social patterns and processes. Because cities are fundamentally regulated by human activities, are inherently interconnected, and are frequently undergoing social and economic transformation, they represent an opportunity for ecologists and evolutionary biologists to study urban “socio‐eco‐evolutionary dynamics.” Through this new framework, we encourage researchers of urban ecology and evolution to fully integrate human social drivers and feedbacks to increase understanding and conservation of ecosystems, their functions, and their contributions to people within and outside cities.
When a species colonizes an urban habitat, differences in the environment can create novel selection pressures. Successful colonization will further lead to demographic perturbations and genetic drift, which can interfere with selection. Here, we test for consistent urban selection signals in multiple populations of the burrowing owl (Athene cunicularia), a species that colonized South American cities just a few decades ago. We sequenced 213 owls from three urban‐rural population pairs and performed a genome‐wide comparison of urban against rural birds. We further studied genome‐wide associations with flight initiation distance (FID), a measure of harm avoidance in which urban and rural birds are known to differ. Based on four samples taken over nine years from one of the urban populations, we investigated temporal allele frequency changes. The genomic data were also used to identify urban‐specific signatures of selective sweeps. Single genomic sites did not reach genome‐wide significance for any association. However, a gene‐set analysis on the strongest signals from these four selection scans suggests a significant enrichment of genes with known functions related to synapses and neuron projections. We identified 98 genes predominantly expressed in the brain, of which many may play a role in the modulation of brain connectivity and consequently in cognitive function and motivational behavior during urbanization. Furthermore, polymorphisms in the promotor region of the synaptic SERT gene – one of the two candidates known to correlate with urban colonization in birds ‐ associated with the habitat in which individuals lived (urban vs. rural).
Only recently have we begun to understand the ecological and evolutionary effects of urbanization on species, with studies revealing drastic impacts on community composition, gene flow, behaviour, morphology and physiology. However, our understanding of how adaptive evolution allows species to persist, and even thrive, in urban landscapes is still nascent. Here, we examine phenotypic, genomic and regulatory impacts of urbanization on a widespread lizard, the Puerto Rican crested anole (Anolis cristatellus). We find that urban lizards endure higher environmental temperatures and display greater heat tolerance than their forest counterparts. A single non-synonymous polymorphism within a protein synthesis gene (RARS) is associated with heat tolerance plasticity within urban heat islands and displays parallel signatures of selection in cities. Additionally, we identify groups of differentially expressed genes between habitats showing elevated genetic divergence in multiple urban–forest comparisons. These genes display evidence of adaptive regulatory evolution within cities and disproportionately cluster within regulatory modules associated with heat tolerance. This study provides evidence of temperature-mediated selection in urban heat islands with repeatable impacts on physiological evolution at multiple levels of biological hierarchy. Analysing phenotypic and genomic differences between urban and rural lizards, the authors identify a single non-synonymous polymorphism associated with heat tolerance plasticity that may explain how urban lizards can endure higher temperatures compared to those in forests.
IQ-TREE (http://www.iqtree.org, last accessed February 6, 2020) is a user-friendly and widely used software package for phylogenetic inference using maximum likelihood. Since the release of version 1 in 2014, we have continuously expanded IQ-TREE to integrate a plethora of new models of sequence evolution and efficient computational approaches of phylogenetic inference to deal with genomic data. Here, we describe notable features of IQ-TREE version 2 and highlight the key advantages over other software.
Urbanization is accelerating worldwide and creates novel habitat conditions including increases in environmental temperature and changes in presence and abundance of predators, prey and parasites. For species that use urban habitats, these changes can have strong impacts on phenotypes. Anolis lizards commonly exploit urban habitats and, as ectotherms, are likely to experience pressures from these novel environments. Previous research shows that anoles may adapt to some aspects of urban habitats, but we lack an understanding of the breadth of traits that may shift in response to urbanization and how widespread these changes may be. To assess effects of urban habitat use on anole phenotypes, we measured morphology, thermal preference and parasitism in brown anoles (Anolis sagrei) and crested anoles (Anolis cristatellus) from urban and natural habitats within the Miami metropolitan area (FL, USA). In urban areas, individuals of both species were larger, but did not show any differences in preferred body temperatures. These results agree with other studies showing increased body size in anoles inhabiting urban areas, but the mechanisms underlying this pattern are unclear. Brown anoles experienced higher levels of parasite infection intensity in urban habitats, but crested anoles showed no differences between urban and natural sites. Increased infection intensity in urban brown anoles suggests that exploiting urban habitats may have costs and shows that urbanization can lead to species-specific changes in ecologically similar congeners. Understanding how urban habitats alter phenotypes of organisms that exploit these areas will be important in predicting costs of and adaptive responses to future urbanization.
Urban ecosystems are rapidly expanding throughout the world, but how urban growth affects the evolutionary ecology of species living in urban areas remains largely unknown. Urban ecology has advanced our understanding of how the development of cities and towns changes environmental conditions and alters ecological processes and patterns. However, despite decades of research in urban ecology, the extent to which urbanization influences evolutionary and eco‐evolutionary change has received little attention. The nascent field of urban evolutionary ecology seeks to understand how urbanization affects the evolution of populations, and how those evolutionary changes in turn influence the ecological dynamics of populations, communities, and ecosystems. Following a brief history of this emerging field, this Perspective article provides a research agenda and roadmap for future research aimed at advancing our understanding of the interplay between ecology and evolution of urban‐dwelling organisms. We identify six key questions that, if addressed, would significantly increase our understanding of how urbanization influences evolutionary processes. These questions consider how urbanization affects non‐adaptive evolution, natural selection, and convergent evolution, in addition to the role of urban environmental heterogeneity on species evolution, and the roles of phenotypic plasticity vs adaptation on species’ abundance in cities. Our final question examines the impact of urbanization on evolutionary diversification. For each of these six questions, we suggest avenues for future research that will help advance the field of urban evolutionary ecology. Lastly, we highlight the importance of integrating urban evolutionary ecology into urban planning, conservation practice, pest management, and public engagement.
This article is protected by copyright. All rights reserved.
Rapid urbanization has become an area of crucial concern in conservation owing to the radical changes in habitat structure and loss of species engendered by urban and suburban development. Here, we draw on recent mechanistic ecological studies to argue that, in addition to altered habitat structure, three major processes contribute to the patterns of reduced species diversity and elevated abundance of many species in urban environments. These activities, in turn, lead to changes in animal behavior, morphology and genetics, as well as in selection pressures on animals and plants. Thus, the key to understanding urban patterns is to balance studying processes at the individual level with an integrated examination of environmental forces at the ecosystem scale.
We created a new dataset of spatially interpolated monthly climate data for global land areas at a very high spatial resolution (approximately 1 km 2). We included monthly temperature (minimum, maximum and average), precipitation, solar radiation, vapour pressure and wind speed, aggregated across a target temporal range of 1970–2000, using data from between 9000 and 60 000 weather stations. Weather station data were interpolated using thin-plate splines with covariates including elevation, distance to the coast and three satellite-derived covariates: maximum and minimum land surface temperature as well as cloud cover, obtained with the MODIS satellite platform. Interpolation was done for 23 regions of varying size depending on station density. Satellite data improved prediction accuracy for temperature variables 5–15% (0.07–0.17 ∘ C), particularly for areas with a low station density, although prediction error remained high in such regions for all climate variables. Contributions of satellite covariates were mostly negligible for the other variables, although their importance varied by region. In contrast to the common approach to use a single model formulation for the entire world, we constructed the final product by selecting the best performing model for each region and variable. Global cross-validation correlations were ≥ 0.99 for temperature and humidity, 0.86 for precipitation and 0.76 for wind speed. The fact that most of our climate surface estimates were only marginally improved by use of satellite covariates highlights the importance having a dense, high-quality network of climate station data.
Significance
Rare recessive monogenic diseases are often found in isolated populations. In one such population, we identified a child carrying a homozygous nonsense mutation in an understudied smooth muscle-restricted gene called Leiomodin1 ( LMOD1 ). Heterozygous parents showed no disease; however, the child died shortly after birth from a rare condition known as megacystis microcolon intestinal hypoperistalsis syndrome. A mouse model with a similar Lmod1 mutation, engineered with CRISPR-Cas9 genome editing, exhibited the same gastrointestinal and urinary bladder phenotypes as seen in the newborn child. Phenotyping revealed insights into the underlying cause of the disease. Results demonstrate the conserved function of LMOD1 in human and mice and the importance of this protein in the molecular regulation of contractility in visceral smooth muscle cells.
Significance
Ecoevolutionary feedbacks on contemporary timescales were hypothesized over half a century ago, but only recently has evidence begun to emerge. The role that human activity plays in such dynamics is still unclear. Through a metaanalysis of >1,600 phenotypic changes in species across regions and ecosystem types, we examine the evidence that the rate of phenotypic change has an urban signature. Our findings indicate greater phenotypic change in urbanizing systems compared with natural and nonurban anthropogenic systems. By explicitly linking urban development to trait changes that might affect ecosystem function, we provide insights into the potential ecoevolutionary implications for maintaining ecosystem function and the sustainability of human well-being.
With over 9000 species, squamates, which include lizards and snakes, are the largest group of reptiles and second-largest order of vertebrates, spanning a vast array of appendicular skeletal morphology. As such, they provide a promising system for examining developmental and molecular processes underlying limb morphology. Using the central bearded dragon (Pogona vitticeps) as the primary study model, we examined limb morphometry throughout embryonic development and characterized the expression of three known developmental genes (GHR, Pitx1 and Shh) from early embryonic stage through to hatchling stage via reverse transcription quantitative polymerase chain reaction (RT-qPCR) and immunohistochemistry (IHC). In this study, all genes were found to be transcribed in both the forelimbs and hindlimbs of P. vitticeps. While the highest level of GHR expression occurred at the hatchling stage, Pitx1 and Shh expression was greatest earlier during embryogenesis, which coincides with the onset of the differentiation between forelimb and hindlimb length. We compared our finding of Pitx1 expression—a hindlimb-determining gene—in the forelimbs of P. vitticeps to that in a closely related Australian agamid lizard, Ctenophorus pictus, where we found Pitx1 expression to be more highly expressed in the hindlimb compared with the forelimb during early and late morphogenesis—a result consistent with that found across other tetrapods. Expression of Pitx1 in forelimbs has only rarely been documented, including via in situ hybridization in a chicken and a frog. Our findings from both RT-qPCR and IHC indicate that further research across a wider range of tetrapods is needed to more fully understand evolutionary variation in molecular processes underlying limb morphology.
Research on the evolutionary ecology of urban areas reveals how human-induced evolutionary changes affect biodiversity and essential ecosystem services. In a rapidly urbanizing world imposing many selective pressures, a time-sensitive goal is to identify the emergent issues and research priorities that affect the ecology and evolution of species within cities. Here, we report the results of a horizon scan of research questions in urban evolutionary ecology submitted by 100 interdisciplinary scholars. We identified 30 top questions organized into six themes that highlight priorities for future research. These research questions will require methodological advances and interdisciplinary collaborations, with continued revision as the field of urban evolutionary ecology expands with the rapid growth of cities.
Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.
Differentiation of multi-potent mesenchymal stromal cells (MSCs) is directed by the activities of lineage-specific transcription factors and co-factors. A subset of these proteins controls the accessibility of chromatin by recruiting histone acetyl transferases or deacetylases that regulate acetylation of the N-termini of H3 and H4 histone proteins. Bromodomain (BRD) proteins recognize these acetylation marks and recruit the RNA pol II containing transcriptional machinery. Our previous studies have shown that Brd4 is required for osteoblast differentiation in vitro. Here, we investigated the role of Brd4 on endochondral ossification in C57BL/6 mice and chondrogenic differentiation in cell culture models. Conditional loss of Brd4 in the mesenchyme (Brd4 cKO, Brd4fl/fl: Prrx1-Cre) yields smaller mice that exhibit alteration in endochondral ossification. Importantly, abnormal growth plate morphology and delayed long bone formation is observed in juvenile Brd4 cKO mice. One week old Brd4 cKO mice have reduced proliferative and hypertrophic zones within the physis and exhibit a delay in the formation of the secondary ossification center. At the cellular level, Brd4 function is required for chondrogenic differentiation and maturation of both ATDC5 cells and immature mouse articular chondrocytes. Mechanistically, Brd4 loss suppresses Sox9 levels and reduces expression of Sox9 and Runx2 responsive endochondral genes (e.g., Col2a1, Acan, Mmp13 and Sp7/Osx). Collectively, our results indicate that Brd4 is a key epigenetic regulator required for normal chondrogenesis and endochondral ossification.
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.
The field of urban ecology has provided many fascinating examples of organisms that display novel biological features in urban environments compared to natural habitats. Quantitative genetics provides a framework that can be used to investigate whether this phenotypic differentiation between urban and natural habitats is adaptive and is the result of heritable changes in response to divergent selection. New generation sequencing tools offer unique opportunities to expand our understanding of the genes and genetic mechanisms implicated in evolution in urban environments. This chapter first reviews quantitative genetics studies investigating the mechanisms of evolution in the city. It then reviews pioneering genomic studies that have shed light on the genes and genetic mechanisms implicated in urban microevolution. The authors discuss how further use of cost-effective high-resolution genomic approaches may improve the comprehension of both genomic and epigenomic mechanisms implicated in such evolution. Finally, the chapter provides an overview of how the integrated use of quantitative genetics, field experiments, and genomics could expand our knowledge of the processes leading to urban evolution.
Organisms living in urban environments are exposed to many novel, sometimes beneficial, but most often challenging conditions. These conditions include increased exposure to chemical pollution, artificial light at night, noise, altered pathogen and predator communities, increased abundance of often poor quality food, increased temperature, and increased human presence and disturbances. Given the central role of a variety of physiological responses in coping with challenges such as these, the authors of the chapter expect that the range of physiological phenotypes expressed by individuals and species will dramatically influence their ability to persist in urban habitat and cope with urban challenges. They also expect that plasticity in components of these physiological systems will be an important target of selection imposed by the challenges confronting urban populations. The chapter takes a closer look at three fundamental physiological systems in animals that are central components of coping responses to environmental challenges, namely detoxification, and endocrine and metabolic systems.
The structural habitat of terrestrial urban environments can differ drastically from environments less impacted by human activities. Whether or not urban species use anthropogenic structures, they are subject to novel selection pressures to effectively locomote. Urban environments are distinctly more open than non-urban habitats, they offer few refuges, and habitat space is patchy with clustered perches. Animals must either change their behaviour to use only natural substrates or contend with manufactured substrates. Arboreal species are particularly impacted because the anthropogenic structures with which they interact, even if infrequently, differ from trees in structural, material, and surface properties. The chapter explores potential adaptive responses to the spatial structure and properties of climbing substrates in urban environments relevant to terrestrial and climbing locomotion. For each, the authors first discuss differences between urban and non-urban terrestrial habitats relevant to locomotion. They then discuss how these differences influence behaviour and locomotor demands, providing a mechanism through which natural selection shapes morphology. Lastly, they discuss the morphological traits most likely to be impacted by these altered demands and predict how natural selection may affect these traits in urban environments based on biomechanical principles. As there have been very few studies investigating urban morphological adaptation related to locomotion, the chapter draws on trait–environment relationships in natural environments. The discussion provides a starting point for developing rigorous hypotheses about functionally relevant trait shifts in urban environments and future directions for investigating locomotor adaptations in urban species.
Urbanization is one of the most drastic alterations of natural habitats, causing sudden adaptive mismatches that make population persistence difficult for many organisms. Urban contexts may be challenging for adaptation, particularly for animals with long generation times with slow evolutionary responses. This chapter argues that cognition may play a major role in facilitating evolutionary adaptation of animals to the urban environment. By regulating how animals gather, preserve, and use information, cognition can influence adaptive evolution in urban areas by (1) allowing individuals to choose the habitats and resources that better match their phenotypes, and (2) helping animals to construct learned responses to challenges they have never or rarely experienced before. These cognitive processes can weaken the strength of selection. However, they can also facilitate adaptive evolution by reducing the risk of population extinction and by ensuring that individuals are more gradually exposed to the new conditions. In addition, cognitive processes can maintain genetic diversity for selection to act upon in the future as well as promoting local adaptation by reducing gene flow with nearby non-urban populations. Finally, learned behaviours can allow the population to move close to the realm of attraction of new adaptive peaks, driving evolution toward novel directions. Cognition itself may also evolve in urban areas—particularly in long-lived generalists—if it exhibits enough heritable variation. Echoing recent suggestions in cognitive ecology, the chapter highlights the need to design and carry out experiments explicitly designed to assess the evolutionary consequences of cognition in urban populations.
As humans continue to modify the climatic conditions organisms encounter, downstream effects on the phenotypes of organisms are likely to arise. In particular, the worldwide proliferation of human settlements rapidly generates pockets of localized warming across the landscape. These urban heat island effects are frequently intense, especially for moderate to larger sized cities, where urban centres can be several degrees Celsius warmer compared with nearby non-urban areas. Although organisms likely ameliorate the effects of warming through phenotypic plasticity, the evolution of thermally sensitive traits may be an important yet underappreciated means of survival. Recent work suggests the potential for contemporary evolutionary change in association with urban heat islands across a diverse suite of traits from morphology to physiological tolerance, growth rate, and metabolism. This chapter reviews and synthesizes this work. It first develops a comprehensive set of predictions for adaptive evolutionary changes in morphology, physiology, and life-history traits driven by urban heat islands. It then evaluates these predictions with regard to the burgeoning literature on urban evolution of thermally sensitive traits.
Urban environments represent globally replicated, large-scale disturbances to the landscape, providing an ideal opportunity to study parallel evolution in natural populations on a large scale. In recent years, there has been a rapid increase in the number of studies investigating evolutionary responses of a diverse range of taxa across multiple cities. Although parallel evolutionary responses across independent urban environments will depend on the extent to which urban environments converge on similar biotic and abiotic environments, the extent to which cities are environmentally similar has not yet fully been integrated into studies of urban evolution. This chapter begins by asking: Do species display parallel evolutionary responses across independent urban environments? It then briefly reviews a subset of the environmental factors that have driven parallel responses to cities (heat islands, pollution, and habitat fragmentation) and discusses some of the potential causes of non-parallelism. Finally, it ends with practical considerations for the design of future studies aiming to examine parallel evolutionary responses to urbanization. Understanding the shared and unique features of urban environments and identifying parallel species responses to rapid and ongoing urban development will provide important insight into the ubiquity of parallel evolution in nature.
R package pcadapt is a user-friendly R package for performing genome scans for local adaptation. Here we present version 4 of pcadapt which substantially improves computational efficiency while providing similar results. This improvement is made possible by using a different format for storing genotypes and a different algorithm for computing principal components of the genotype matrix, which is the most computationally demanding step in method pcadapt. These changes are seamlessly integrated into the existing pcadapt package, and users will experience a large reduction in computation time (by a factor of 20 to 60 in our analyses) as compared to previous versions.
There are many compelling examples of molecular convergence at individual genes. However, the prevalence and the relative importance of adaptive genome-wide convergence remains largely unknown. Many recent works have reported striking examples of excess genome-wide convergence, but some of these studies have been called into question because of the use of inappropriate null models. Here, we sequenced and compared the genomes of twelve species of anole lizards that have independently converged on suites of adaptive behavioral and morphological traits. Despite extensive searches for a genome-wide signature of molecular convergence, we found no evidence supporting molecular convergence at specific amino acids either at individual genes or at genome-wide comparisons; we also uncovered no evidence supporting an excess of adaptive convergence in the rates of amino acid substitutions within genes. Our findings indicate that comprehensive phenotypic convergence is not mirrored at genome-wide protein-coding levels in anoles, and therefore that adaptive phenotypic convergence is likely not constrained by the evolution of many specific protein sequences or structures.
Genomic studies in African populations provide unique opportunities to understand disease etiology, human diversity, and population history. In the largest study of its kind, comprising genome-wide data from 6,400 individuals and whole-genome sequences from 1,978 individuals from rural Uganda, we find evidence of geographically correlated fine-scale population substructure. Historically, the ancestry of modern Ugandans was best represented by a mixture of ancient East African pastoralists. We demonstrate the value of the largest sequence panel from Africa to date as an imputation resource. Examining 34 cardiometabolic traits, we show systematic differences in trait heritability between European and African populations, probably reflecting the differential impact of genes and environment. In a multi-trait pan-African GWAS of up to 14,126 individuals, we identify novel loci associated with anthropometric, hematological, lipid, and glycemic traits. We find that several functionally important signals are driven by Africa-specific variants, highlighting the value of studying diverse populations across the region.
Evidence is growing that human modification of landscapes has dramatically altered evolutionary processes. In urban population genetic studies, urbanization is typically predicted to act as a barrier that isolates populations of species, leading to increased genetic drift within populations and reduced gene flow between populations. However, urbanization may also facilitate dispersal among populations, leading to higher genetic diversity within and lower differentiation between urban populations. We reviewed the literature on non‐adaptive urban evolution to evaluate the support for each of these urban fragmentation and facilitation models. In a review of the literature with supporting quantitative analyses of 167 published urban population genetics studies, we found a weak signature of reduced within‐population genetic diversity, and no evidence of consistently increased between‐population genetic differentiation associated with urbanization. In addition, we found that urban landscape features act as barriers or conduits to gene flow, depending on the species and city in question. Thus, we speculate that dispersal ability of species and environmental heterogeneity between cities contribute to the variation exhibited in our results. However, greater than 90% of published studies reviewed here showed an association of urbanization with genetic drift or gene flow, highlighting the strong impact of urbanization on non‐adaptive evolution. It is clear that organism biology and city heterogeneity obscure patterns of genetic drift and gene flow in a quantitative analysis. Thus, we suggest that future research makes comparisons of multiple cities and nonurban habitats, and takes into consideration species' natural history, environmental variation, spatial modelling, and marker selection. This article is protected by copyright. All rights reserved.
The Genomic Data Storage (GDS) format provides efficient storage and retrieval of genotypes measured by microarrays and sequencing. We developed GENESIS to perform various single- and aggregate-variant association tests using genotype data stored in GDS format. GENESIS implements highly flexible mixed models, allowing for different link functions, multiple variance components, and phenotypic heteroskedasticity. GENESIS integrates cohesively with other R/Bioconductor packages to build a complete genomic analysis workflow entirely within the R environment.
Availability and implementation:
https://bioconductor.org/packages/GENESIS; vignettes included.
Supplementary information:
Supplementary tables and figures are available at Bioinformatics online.
Convergent adaptation is the independent evolution of similar traits conferring a fitness advantage in two or more lineages. Cases of convergent adaptation inform our ideas about the ecological and molecular basis of adaptation. In judging the degree to which putative cases of convergent adaptation provide an independent replication of the process of adaptation, it is necessary to establish the degree to which the evolutionary change is unexpected under null models and to show that selection has repeatedly, independently driven these changes. Here, we discuss the issues that arise from these questions particularly for closely related populations, where gene flow and standing variation add additional layers of complexity. We outline a conceptual framework to guide intuition as to the extent to which evolutionary change represents the independent gain of information owing to selection and show that this is a measure of how surprised we should be by convergence. Additionally, we summarize the ways population and quantitative genetics and genomics may help us address questions related to convergent adaptation, as well as open new questions and avenues of research.
This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.
The urea cycle is a metabolic pathway for the disposal of excess nitrogen, which arises primarily as ammonia. Nitrogen is essential for growth and life-maintenance, but excessive ammonia leads to life-threatening conditions. The urea cycle disorders (UCDs) comprise diseases presenting with hyperammonemia that arise in either the neonatal period (about 50% of cases) or later. Congenital defects of the enzymes or transporters of the urea cycle cause the disease. This cycle utilizes five enzymes, two of which, carbamoylphosphate synthetase 1 and ornithine transcarbamylase are present in the mitochondrial matrix, whereas the others (argininosuccinate synthetase, argininosuccinate lyase and arginase 1) are present in the cytoplasm. In addition, N-acetylglutamate synthase and at least two transporter proteins are essential to urea cycle function. Severity and age of onset depend on residual enzyme or transporter function and are related to the respective gene mutations. The strategy for therapy is to prevent the irreversible toxicity of high-ammonia exposure to the brain. The pathogenesis and natural course are poorly understood because of the rarity of the disease, so an international registry system and novel clinical trials are much needed. We review here the current concepts of the pathogenesis, diagnostics, including genetics and treatment of UCDs.
Animals that live in cities face a number of challenges particular to the urban environment that may impact on overall health and survival. Nevertheless, relatively few studies have investigated injury and health in urban species. We measured body condition, injury rate and fluctuating asymmetry in urban and forest populations of the tropical lizard Anolis cristatellus. We found that although there were strong differences in body condition between urban and forest populations, the direction of this difference varied between municipalities. We also found that injury rates (amputated digits and bone fractures) were slightly, but significantly, more common in urban populations; this phenomenon may be due to changes in intraspecific interactions or predation pressure in urban sites. Contrary to our expectations, we found that fluctuating asymmetry was greater in forest compared to urban populations. Because our data were collected from adults, this may be a sign of stronger natural selection on the symmetry of functional traits in urban than in forest environments. Finally, we found no persuasive evidence that city living is inherently detrimental to individuals of this species despite a slightly higher rate of injury. Being able to overcome the challenges of city life may be integral to urban persistence and a step along the path to urban adaptation.
Principal component analysis (PCA) is often used to describe overall population structure—patterns of relatedness arising from past demographic history—among a set of genomes. Here, Li and Ralph describe how the patterns uncovered by....
Population structure leads to systematic patterns in measures of mean relatedness between individuals in large genomic data sets, which are often discovered and visualized using dimension reduction techniques such as principal component analysis (PCA). Mean relatedness is an average of the relationships across locus-specific genealogical trees, which can be strongly affected on intermediate genomic scales by linked selection and other factors. We show how to use local PCA to describe this intermediate-scale heterogeneity in patterns of relatedness, and apply the method to genomic data from three species, finding in each that the effect of population structure can vary substantially across only a few megabases. In a global human data set, localized heterogeneity is likely explained by polymorphic chromosomal inversions. In a range-wide data set of Medicago truncatula, factors that produce heterogeneity are shared between chromosomes, correlate with local gene density, and may be caused by linked selection, such as background selection or local adaptation. In a data set of primarily African Drosophila melanogaster, large-scale heterogeneity across each chromosome arm is explained by known chromosomal inversions thought to be under recent selection and, after removing samples carrying inversions, remaining heterogeneity is correlated with recombination rate and gene density, again suggesting a role for linked selection. The visualization method provides a flexible new way to discover biological drivers of genetic variation, and its application to data highlights the strong effects that linked selection and chromosomal inversions can have on observed patterns of genetic variation.
Parallel evolution across replicate populations has provided evolutionary biologists with iconic examples of adaptation. When multiple populations colonize seemingly similar habitats, they may evolve similar genes, traits, or functions. Yet, replicated evolution in nature or in the laboratory often yields inconsistent outcomes: Some replicate populations evolve along highly similar trajectories, whereas other replicate populations evolve to different extents or in distinct directions. To understand these heterogeneous outcomes, biologists are increasingly treating parallel evolution not as a binary phenomenon but rather as a quantitative continuum ranging from parallel to nonparallel. By measuring replicate populations' positions along this (non)parallel continuum, we can test hypotheses about evolutionary and ecological factors that influence the extent of repeatable evolution. We review evidence regarding the manifestation of (non)parallel evolution in the laboratory, in natural populations, and in applied contexts such as cancer. We enumerate the many genetic, ecological, and evolutionary processes that contribute to variation in the extent of parallel evolution.
House sparrows (Passer domesticus) are a hugely successful anthrodependent species; occurring on nearly every continent. Yet, despite their ubiquity and familiarity to humans, surprisingly little is known about their origins. We sought to investigate the evolutionary history of the house sparrow and identify the processes involved in its transition to a human-commensal niche. We used a whole genome resequencing dataset of 120 individuals from three Eurasian species, including three populations of Bactrianus sparrows, a non-commensal, divergent house sparrow lineage occurring in the Near East. Coalescent modelling supports a split between house and Bactrianus sparrow 11 Kya and an expansion in the house sparrow at 6 Kya, consistent with the spread of agriculture following the Neolithic revolution. Commensal house sparrows therefore likely moved into Europe with the spread of agriculture following this period. Using the Bactrianus sparrow as a proxy for a pre-commensal, ancestral house population, we performed a comparative genome scan to identify genes potentially involved with adaptation to an anthropogenic niche. We identified potential signatures of recent, positive selection in the genome of the commensal house sparrow that are absent in Bactrianus populations. The strongest selected region encompasses two major candidate genes; COL11A-which regulates craniofacial and skull development and AMY2A, part of the amylase gene family which has previously been linked to adaptation to high-starch diets in humans and dogs. Our work examines human-commensalism in an evolutionary framework, identifies genomic regions likely involved in rapid adaptation to this new niche and ties the evolution of this species to the development of modern human civilization.
Urban habitats are drastically modified from their natural state, creating unique challenges and selection pressures for organisms that reside in them. We compared locomotor performance of Anolis lizards from urban and forest habitats on tracks differing in angle and substrate, and found that using artificial substrates came at a cost: lizards ran substantially slower and frequently lost traction on man-made surfaces compared to bark. We found that various morphological traits were positively correlated with sprint speed and that these same traits were significantly larger in urban compared to forest lizards. We found that urban lizards ran faster on both man-made and natural surfaces, suggesting similar mechanisms improve locomotor performance on both classes of substrate. Thus, lizards in urban areas may be under selection to run faster on all flat surfaces, while forest lizards face competing demands of running, jumping and clinging to narrow perches. Novel locomotor challenges posed by urban habitats likely have fitness consequences for lizards that cannot effectively use man-made surfaces, providing a mechanistic basis for observed phenotypic shifts in urban populations of this species.
Background
-Angiogenesis is integral for embryogenesis, and targeting angiogenesis improves the outcome of many pathological conditions in patients. TBX20 is a crucial transcription factor for embryonic development, and its deficiency is associated with congenital heart disease. However, the role of TBX20 in angiogenesis has not been described.
Methods
-Loss- and gain-of-function approaches were used to explore the role of TBX20 in angiogenesis bothin vitroandin vivoAngiogenesis gene array was used to identify key downstream targets of TBX20.
Results
-Unbiased gene array survey showed thatTBX20knockdown profoundly reduced angiogenesis-associatedPROK2gene expression. Indeed, loss of TBX20 hindered endothelial cell migration andin vitroangiogenesis. In a murine angiogenesis model using subcutaneously implanted matrigel plugs, we observed that TBX20 deficiency markedly reduced PROK2 expression and restricted intra-plug angiogenesis. Furthermore, recombinant PROK2 administration enhanced angiogenesis and blood flow recovery in murine hindlimb ischemia. In zebrafish, transient knockdown oftbx20by morpholino antisense oligos (MO) or genetic disruption oftbx20by CRISPR/Cas9 impaired angiogenesis. Furthermore, loss ofprok2or its cognate receptorprokr1aalso limited angiogenesis. In contrast, overexpression ofprok2orprokr1arescued the impaired angiogenesis intbx20deficient animals.
Conclusions
-Our study identifies TBX20 as a novel transcription factor regulating angiogenesis through the PROK2-PROKR1 pathway in both development and disease, and reveals a novel mode of angiogenic regulation whereby the TBX20-PROK2-PROKR1 signaling cascade may act as a "biological capacitor" to relay and sustain the pro-angiogenic effect of VEGF. This pathway may be a therapeutic target in the treatment of diseases with dysregulated angiogenesis.
Our planet is an increasingly urbanized landscape, with over half of the human population residing in cities. Despite advances in urban ecology, we do not adequately understand how urbanization affects the evolution of organisms, nor how this evolution may affect ecosystems and human health. Here, we review evidence for the effects of urbanization on the evolution of microbes, plants, and animals that inhabit cities. Urbanization affects adaptive and nonadaptive evolutionary processes that shape the genetic diversity within and between populations. Rapid adaptation has facilitated the success of some native species in urban areas, but it has also allowed human pests and disease to spread more rapidly. The nascent field of urban evolution brings together efforts to understand evolution in response to environmental change while developing new hypotheses concerning adaptation to urban infrastructure and human socioeconomic activity. The next generation of research on urban evolution will provide critical insight into the importance of evolution for sustainable interactions between humans and our city environments.
We present two new cases of Warsaw Breakage Syndrome (WABS), an autosomal recessive cohesinopathy, in sisters aged 13 and 11 years who both had compound heterozygous mutations in DDX11. After exclusion of Fanconi anemia, Bloom syndrome and Nijmegen breakage syndrome, whole exome sequencing revealed two novel variants—c.1523T>G, predicting (p.Leu508Arg) and c.1949-1G>A (IVS19-1G>A), that were confirmed with Sanger sequencing in both affected individuals. DDX11 encodes an iron-sulfur-containing DNA helicase, and mutations in this gene have been reported in the five WABS cases previously identified to date. The sisters reported here display the distinguishing clinical features of WABS: pre- and post-natal growth restriction, microcephaly, intellectual disability, sensorineural hearing loss with cochlear abnormalities, and facial dysmorphic features. In addition, our cases had early menarche at 8 and 10 years of age, bilateral small thumbs, and the younger, more severely affected sister had small fibulae. These findings broaden the WABS phenotype and the limb malformations demonstrate further clinical overlap with Fanconi anemia and other cohesinopathies, such as Roberts Syndrome.
Aim
We examine the influence of fluctuating sea levels in a land‐bridge archipelago on the apportioning of intraspecific genetic diversity and divergence in the widespread Puerto Rican crested anole (Anolis cristatellus). We compare three alternative scenarios for genetic diversification in an archipelagic species that contrast the relative influences of periodic isolation versus island connectedness driven by fluctuating sea levels. Our approach combines information from geography and population genetics to assess the influence of island size, island isolation, island historical geography, and population genetic processes such as drift on the contemporary distribution of genetic variation within and among islands.
Location
The Puerto Rico Bank in the Caribbean focusing primarily on the Spanish, British and U.S. Virgin Islands.
Methods
We used nuclear and mitochondrial DNA sequences and microsatellite genotypes sampled from A. cristatellus populations to investigate: (1) the broad‐scale pattern of phylogeographical divergence across Puerto Rico Bank islands and (2) diversification within the Virgin Islands archipelago. For the first component, we used sequence data to reconstruct the relationships among 542 samples from across the species range. For the second component, we examined the relative influences of island size, isolation, and population genetic processes on the distribution of genetic diversity across the Virgin Islands.
Results
In the Virgin Islands, A. cristatellus is represented by a monophyletic clade except on the island of Vieques, where two divergent clades coexist. We found evidence for non‐equilibrium dynamics in the Virgin Islands, suggesting spatial population expansion during intraglacial periods of low sea level.
Main conclusions
We found limited evidence that periods of island isolation affected patterns of genetic diversity and differentiation. Instead, we found that the patterns of genetic diversity and divergence in A. cristatellus in the Virgin Islands archipelago are likely shaped by long‐term persistence in the region and periods of population spatial expansion.
Model-based molecular phylogenetics plays an important role in comparisons of genomic data, and model selection is a key step in all such analyses. We present ModelFinder, a fast model-selection method that greatly improves the accuracy of phylogenetic estimates by incorporating a model of rate heterogeneity across sites not previously considered in this context and by allowing concurrent searches of model space and tree space.
The zinc-finger SWIM domain-containing protein 6 (ZSWIM6) is a protein of unknown function that has been associated with schizophrenia and limited educational attainment by three independent genome-wide association studies. Additionally, a putatively causal point mutation in ZSWIM6 has been identified in several cases of acromelic frontonasal dysostosis with severe intellectual disability. Despite the growing number of studies implicating ZSWIM6 as an important regulator of brain development, its role in this process has never been examined. Here, we report the generation of Zswim6 knockout mice and provide a detailed anatomical and behavioral characterization of the resulting phenotype. We show that Zswim6 is initially expressed widely during embryonic brain development but becomes restricted to the striatum postnatally. Loss of Zswim6 causes a reduction in striatal volume and changes in medium spiny neuron morphology. These changes are associated with alterations in motor control, including hyperactivity, impaired rotarod performance, repetitive movements, and behavioral hyperresponsiveness to amphetamine. Together, our results show that Zswim6 is indispensable to normal brain function and support the notion that Zswim6 might serve as an important contributor to the pathogenesis of schizophrenia and other neurodevelopmental disorders.
The R package pcadapt performs genome scans to detect genes under selection based on population genomic data. It assumes that candidate markers are outliers with respect to how they are related to population structure. Because population structure is ascertained with principal component analysis, the package is fast and works with large-scale data. It can handle missing data and pooled sequencing data. By contrast to population-based approaches, the package handle admixed individuals and does not require grouping individuals into populations. Since its first release, pcadapt has evolved in terms of both statistical approach and software implementation. We present results obtained with robust Mahalanobis distance, which is a new statistic for genome scans available in the 2.0 and later versions of the package. When hierarchical population structure occurs, Mahalanobis distance is more powerful than the communality statistic that was implemented in the first version of the package. Using simulated data, we compare pcadapt to other computer programs for genome scans (BayeScan, hapflk, OutFLANK, sNMF). We find that the proportion of false discoveries is around a nominal false discovery rate set at 10% with the exception of BayeScan that generates 40% of false discoveries. We also find that the power of BayeScan is severely impacted by the presence of admixed individuals whereas pcadapt is not impacted. Last, we find that pcadapt and hapflk are the most powerful in scenarios of population divergence and range expansion. Because pcadapt handles next-generation sequencing data, it is a valuable tool for data analysis in molecular ecology.