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Landscape community genomics: understanding eco-evolutionary processes in complex environments

Extrinsic factors influencing evolutionary processes are often categorically lumped into interactions that are environmentally (e.g., climate, landscape) or community-driven, with little consideration of the overlap or influence of one on the other. However, genomic variation is strongly influenced by complex and dynamic interactions between environmental and community effects. Failure to consider both effects on evolutionary dynamics simultaneously can lead to incomplete, spurious, or erroneous conclusions about the mechanisms driving genomic variation. We highlight the need for a landscape community genomics (LCG) framework to help to motivate and challenge scientists in diverse fields to consider a more holistic, interdisciplinary perspective on the genomic evolution of multi-species communities in complex environments.

Trends in Ecology and Evolution↗

Metamorphosis in an era of increasing climate variability

Most animals have complex life cycles including metamorphosis or other discrete life stage transitions during which individuals may be particularly vulnerable to environmental stressors. With climate change, individuals will be exposed to increasing thermal and hydrologic variability during metamorphosis, which may affect survival and performance through physiological, behavioral, and ecological mechanisms. Furthermore, because metamorphosis entails changes in traits and vital rates, it is likely to play an important role in how populations respond to increasing climate variability. To identify mechanisms underlying population responses and associated trait and life history evolution, we need new approaches to estimating changes in individual traits and performance throughout metamorphosis, and we need to integrate metamorphosis as an explicit life stage in analytical models.

Trends in Ecology & Evolution↗

Integrating Earth–life systems: A geogenomic approach

For centuries, scientists have recognized and worked to understand how Earth’s mutable landscape and climate shape the distribution and evolution of species. Here, we describe the emerging field of geogenomics, which uses the reciprocal and deep integration of geologic, climatic, and population genomic data to define and test cause–effect relationships between Earth and life at intermediate spatial and temporal scales (i.e., the mesoscale). Technological advances now power the detailed reconstruction of landscape and evolutionary histories, but transdisciplinary collaborations and new quantitative tools are needed to better integrate Earth–life data. Geogenomics can help build a more unified theory and characterize the boundary conditions under which geologic and climatic processes generate new biodiversity, how species’ responses differ, and why.

Trends in Ecology & Evolution↗

New uses for ancient middens: Bridging ecological and evolutionary perspectives

Rodent middens provide a fine-scale spatiotemporal record of plant and animal communities over the late Quaternary. In the Americas, middens have offered insight into biotic responses to past environmental changes and historical factors influencing the distribution and diversity of species. However, few studies have used middens to investigate genetic or ecosystem level responses. Integrating midden studies with neoecology and experimental evolution can help address these gaps and test mechanisms underlying eco-evolutionary patterns across biological and spatiotemporal scales. Fully realizing the potential of middens to answer cross-cutting ecological and evolutionary questions and inform conservation goals in the Anthropocene will require a collaborative research community to exploit existing midden archives and mount new campaigns to leverage midden records globally.

Trends in Ecology and Evolution↗

A comprehensive multilocus phylogeny for the wood-warblers and a revised classification of the Parulidae (Aves)

The birds in the family Parulidae-commonly termed the New World warblers or wood-warblers-are a classic model radiation for studies of ecological and behavioral differentiation. Although the monophyly of a 'core' wood-warbler clade is well established, no phylogenetic hypothesis for this group has included a full sampling of wood-warbler species diversity. We used parsimony, maximum likelihood, and Bayesian methods to reconstruct relationships among all genera and nearly all wood-warbler species, based on a matrix of mitochondrial DNA (5840 nucleotides) and nuclear DNA (6 loci, 4602 nucleotides) characters. The resulting phylogenetic hypotheses provide a highly congruent picture of wood-warbler relationships, and indicate that the traditional generic classification of these birds recognizes many non-monophyletic groups. We recommend a revised taxonomy in which each of 14 genera (Seiurus, Helmitheros, Mniotilta, Limnothlypis, Protonotaria, Parkesia, Vermivora, Oreothlypis, Geothlypis, Setophaga, Myioborus, Cardellina, Basileuterus, Myiothlypis) corresponds to a well-supported clade; these nomenclatural changes also involve subsuming a number of well-known, traditional wood-warbler genera (Catharopeza, Dendroica, Ergaticus, Euthlypis, Leucopeza, Oporornis, Parula, Phaeothlypis, Wilsonia). We provide a summary phylogenetic hypothesis that will be broadly applicable to investigations of the historical biogeography, processes of diversification, and evolution of trait variation in this well studied avian group. ?? 2010 Elsevier Inc.

Molecular Phylogenetics and Evolution↗

Lineage diversification of fringe-toed lizards (Phrynosomatidae: Uma notata complex) in the Colorado Desert: Delimiting species in the presence of gene flow

Multi-locus nuclear DNA data were used to delimit species of fringe-toed lizards of the Uma notata complex, which are specialized for living in wind-blown sand habitats in the deserts of southwestern North America, and to infer whether Quaternary glacial cycles or Tertiary geological events were important in shaping the historical biogeography of this group. We analyzed ten nuclear loci collected using Sanger sequencing and genome-wide sequence and single-nucleotide polymorphism (SNP) data collected using restriction-associated DNA (RAD) sequencing. A combination of species discovery methods (concatenated phylogenies, parametric and non-parametric clustering algorithms) and species validation approaches (coalescent-based species tree/isolation-with-migration models) were used to delimit species, infer phylogenetic relationships, and to estimate effective population sizes, migration rates, and speciation times. Uma notata , U. inornata , U. cowlesi , and an undescribed species from Mohawk Dunes, Arizona ( U. sp.) were supported as distinct in the concatenated analyses and by clustering algorithms, and all operational taxonomic units were decisively supported as distinct species by ranking hierarchical nested speciation models with Bayes factors based on coalescent-based species tree methods. However, significant unidirectional gene flow (2 NM >1) from U. cowlesi and U. notata into U. rufopunctata was detected under the isolation-with-migration model. Therefore, we conservatively delimit four species-level lineages within this complex ( U. inornata , U. notata , U. cowlesi , and U. sp.), treating U. rufopunctata as a hybrid population ( U. notata x cowlesi ). Both concatenated and coalescent-based estimates of speciation times support the hypotheses that speciation within the complex occurred during the late Pleistocene, and that the geological evolution of the Colorado River delta during this period was an important process shaping the observed phylogeographic patterns.

Molecular Phylogenetics and Evolution↗

Phylogenomic analyses reveal introgression and cryptic speciation in the globally distributed, vector-transmitted pathogen Plasmodium relictum

Establishing species limits is challenging, particularly for pathogens of wildlife. These pathogens can be difficult to sample and culture, and their genome sequencing must often be conducted in the presence of high levels of host DNA. Plasmodium relictum is a mosquito-vectored avian malaria pathogen that is a globally distributed host generalist, comprised of several genetic lineages. We used sequence capture data from 52 P. relictum infections originating from multiple continents to generate a genomic dataset of the pathogen. With this data, we established a robust phylogeny and determined species limits among P. relictum lineages. We generated phylogenomic trees by maximum likelihood and Bayesian methods with multi-species coalescent models and confirmed robustness of the topology by varying the amount of missing data in the analyses. Our results suggest the existence of two cryptic species among the infections we analyzed and provide evidence of genetic introgression between these species. One of the cryptic species, GRW4, devastated the endemic and immunologically naïve avifauna of Hawaii after its introduction to the islands ca. 100 years ago, and so was tested for positive selection in the GRW4 Hawaiian clade. Although we hypothesized it would be released from host selective pressures, we did not find evidence of positive selection in the Hawaiian GRW4 clade, and we discuss possible explanations. Overall, our results underscore the importance of genomic analyses for resolving pathogen species limits and understanding pathogen evolution.

Molecular Phylogenetics and Evolution↗

Links between worlds: Unraveling migratory connectivity

Migration is the regular seasonal movement of animals from one place to another, often from a breeding site to a nonbreeding site and back. Because the act of migration makes it difficult to follow individuals and populations year round, our understanding of the ecology and evolution of migrating organisms, particularly birds, has been severely impeded. Exciting new advances in satellite telemetry, genetic analyses and stable isotope chemistry are now making it possible to determine the population and geographical origin of individual birds. Here, we review these new approaches and consider the relevance of understanding migratory connectivity to ecological, evolutionary and conservation issues.

Trends in Ecology and Evolution↗

Trophic strategies, animal diversity and body size

A primary difference between predators and parasites is the number of victims that an individual attacks throughout a life-history stage. A key division within natural enemies is whether a successful attack eliminates the fitness of the prey or the host. A third distinctive axis for parasites is whether the host must die to further parasite development. The presence or absence of intensity-dependent pathology is a fourth factor that separates macroparasites from microparasites; this also distinguishes between social and solitary predators. Combining these four dichotomies defines seven types of parasitism, seven corresponding parasites, three forms of predation and, when one considers obligate and facultative combinations of these forms, four types of predator. Here, we argue that the energetics underlying the relative and absolute sizes of natural enemies and their victims is the primary selective factor responsible for the evolution of these different trophic strategies.

Trends in Ecology and Evolution↗

Best practices for genetic and genomic data archiving

Genetic and genomic data are collected for a vast array of scientific and applied purposes. Despite mandates for public archiving, data are typically used only by the generating authors. The reuse of genetic and genomic datasets remains uncommon because it is difficult, if not impossible, due to non-standard archiving practices and lack of contextual metadata. But as the new field of macrogenetics is demonstrating, if genetic data and their metadata were more accessible and FAIR (findable, accessible, interoperable and reusable) compliant, they could be reused for many additional purposes. We discuss the main challenges with existing genetic and genomic data archives, and suggest best practices for archiving genetic and genomic data. Recognizing that this is a longstanding issue due to little formal data management training within the fields of ecology and evolution, we highlight steps that research institutions and publishers could take to improve data archiving.

Nature, Ecology and Evolution↗

Parallel shifts in trout feeding morphology suggest rapid adaptation to alpine lake environments

Eco-evolutionary interactions following ecosystem change provide critical insight into the ability of organisms to adapt to shifting resource landscapes. Here we explore evidence for the rapid parallel evolution of trout feeding morphology following eco-evolutionary interactions with zooplankton in alpine lakes stocked at different points in time in the Wind River Range (Wyoming, USA). In this system, trout predation has altered the zooplankton species community and driven a decrease in average zooplankton size. In some lakes that were stocked decades ago, we find shifts in gill raker traits consistent with the hypothesis that trout have rapidly adapted to exploit available smaller-bodied zooplankton more effectively. We explore this morphological response in multiple lake populations across two species of trout (cutthroat trout, Oncorhynchus clarkii , and golden trout Oncorhynchus aguabonita ) and examine the impact of resource availability on morphological variation in gill raker number among lakes. Furthermore, we present genetic data to provide evidence that historically stocked cutthroat trout populations likely derive from multiple population sources, and incorporate variation from genomic relatedness in our exploration of environmental predictors of feeding morphology. These findings describe rapid adaptation and eco-evolutionary interactions in trout and document an evolutionary response to novel, contemporary ecosystem change.

Evolution↗

The role of ecology in allopatric speciation of darters in the Central Highlands, USA

Allopatric speciation is the predominant mode of speciation in riverine fishes. However, the relative importance of genetic drift versus natural selection in the allopatric speciation of these fishes remain uncertain. Here, we present a case study that demonstrates the role of ecology in the diversification of a group of imperiled freshwater fishes from the central United States. We integrate a phylogenomic dataset with analyses of streamwise distance, environmental variables, meristic and morphological traits, and diet to investigate the ecological context and outcomes of allopatric speciation within a species complex comprising the Slenderhead Darter Percina phoxocephala (Nelson), Ouachita Darter Percina brucethompsoni (Robison, Cashner, and Near), and Longnose Darter Percina nasuta (Bailey). We find that two of the species traditionally delimited based on disparity in snout length, P. phoxocephala and P. nasuta , are polyphyletic, revealing three instances of the parallel evolution of snout length disparity. We propose a revised taxonomy including the delimitation of six new species based on disparity in phenotypic traits and phylogenomic analyses. We find that morphological differences are not correlated with genetic divergence but are congruent with variations in diet and environmental niches, suggesting a role for ecological factors in allopatric speciation of riverine fishes.

Arkansas, Kansas, Missouri, Oklahoma↗

Deconstructing cardiovascular and coagulation-related traits links dietary ecology to multi-functional snake venom specificity

Animal venoms vary greatly in compositional complexity, where complex venoms are hypothesized to be maintained by greater dietary breadth. Beyond explaining venom composition, the dietary breadth hypothesis predicts that these more complex venoms should show greater functional breadth in terms of overall toxicity and by disrupting multiple prey physiological processes. We evaluate these predictions with six distinct physiological assays of cardiac and blood clotting functions and compared the effects of venoms from snake species with a range of taxonomic dietary diversity levels. We compared the taxonomic dietary generalists Agkistrodon piscivorus and Sistrurus miliarius to taxa with varying taxonomic specialization, namely Ag. contortrix and Crotalus adamanteus , and Azemiops feae . Comparing fish thrombocyte and mammal platelet aggregation and fibrin clot formation, only species with broader diets disrupted both fish and mammal hemostatic function. Venom of Ag. piscivorus , a uniquely fish-eating species, was the most disruptive of zebrafish heart rate, thrombocyte activation, vascular permeability, and clotting after injury. Sistrurus miliarius was also highly toxic, whereas mammal-specialists’ venoms scarcely altered zebrafish physiology. Our results support the hypothesis that dietary breadth selects functionally complex venoms. Understanding venom gene evolution, snakebite symptoms, and searching for therapeutics in venom should be guided by evolutionary ecology.

Evolution↗

Nanopore amplicon sequencing reveals molecular convergence and local adaptation of rhodopsin in Great Lakes salmonids

Local adaptation can drive diversification of closely related species across environmental gradients and promote convergence of distantly related taxa that experience similar conditions. We examined a potential case of adaptation to novel visual environments in a species flock (Great Lakes salmonids, genus Coregonus ) using a new amplicon genotyping protocol on the Oxford Nanopore Flongle and MinION. We sequenced five visual opsin genes for individuals of C. artedi , C. hoyi , C. kiyi , and C. zenithicus. Comparisons revealed species-specific differences in a key spectral tuning amino acid in rhodopsin (Tyr261Phe substitution), suggesting local adaptation of C. kiyi to the blue-shifted depths of Lake Superior. Ancestral state reconstruction demonstrates that parallel evolution and “toggling” at this amino acid residue has occurred several times across the fish tree of life, resulting in identical changes to the visual systems of distantly related taxa across replicated environmental gradients. Our results suggest that ecological differences and local adaptation to distinct visual environments are strong drivers of both evolutionary parallelism and diversification.

Lake Superior↗

Structured populations of Sulfolobus acidocaldarius with susceptibility to mobile genetic elements

The impact of a structured environment on genome evolution can be determined through comparative population genomics of species that live in the same habitat. Recent work comparing three genome sequences of Sulfolobus acidocaldarius suggested that highly structured, extreme, hot spring environments do not limit dispersal of this thermoacidophile, in contrast to other co-occurring Sulfolobus species. Instead, a high level of conservation among these three S. acidocaldarius genomes was hypothesized to result from rapid, global-scale dispersal promoted by low susceptibility to viruses that sets S. acidocaldarius apart from its sister Sulfolobus species. To test this hypothesis, we conducted a comparative analysis of 47 genomes of S. acidocaldarius from spatial and temporal sampling of two hot springs in Yellowstone National Park. While we confirm the low diversity in the core genome, we observe differentiation among S. acidocaldarius populations, likely resulting from low migration among hot spring “islands” in Yellowstone National Park. Patterns of genomic variation indicate that differing geological contexts result in the elimination or preservation of diversity among differentiated populations. We observe multiple deletions associated with a large genomic island rich in glycosyltransferases, differential integrations of the Sulfolobus turreted icosahedral virus, as well as two different plasmid elements. These data demonstrate that neither rapid dispersal nor lack of mobile genetic elements result in low diversity in the S. acidocaldarius genomes. We suggest instead that significant differences in the recent evolutionary history, or the intrinsic evolutionary rates, of sister Sulfolobus species result in the relatively low diversity of the S. acidocaldarius genome.

Genome Biology and Evolution↗

Identification of novel hepaciviruses and Sylvilagus-associated viruses via metatranscriptomics in North American lagomorphs

Cottontails ( Sylvilagus spp.) and jackrabbits ( Lepus spp.) within the Leporidae family are native to North America and are found in a wide range of habitats, including deserts, forests, and grasslands. Although there is a growing body of research describing the arrival of the highly virulent rabbit haemorrhagic disease virus 2 (RHDV2, GI.2) on this continent, and its impact on native lagomorphs, information about the natural virome and microbiome of healthy and deceased American lagomorphs is relatively limited. In this study, we used a meta-transcriptomics approach to conduct whole pathogen profiling on healthy and deceased animals in the USA. We analysed 48 matched liver and lung sample pools from apparently healthy cottontails and jackrabbits in Texas and an additional 48 liver samples from deceased animals from nine other US states. This approach enabled the discovery of three distinct new viruses and revealed additional new insights into the lung and liver microbiomes of North American lagomorphs. Of the three new viruses, a tetnovirus and a novel picorna-like virus were likely of insect origin and therefore considered environmental contaminants. Of particular interest was a new species of hepacivirus, with around 50% sequence identity to a known hepacivirus from a xeric four-striped grass rat ( Rhabdomys pumilio ). Phylogenetic analysis from 41 individual hepacivirus genomes recovered from our lagomorph samples revealed two distinct clades, corresponding with different cottontail species. No hepaciviruses were detected in any of the jackrabbit samples. This is the first description of a hepacivirus in lagomorphs. Our findings extend the Hepacivirus genus, provide new insights into its evolution, and describe the first baseline on microbial diversity in North American lagomorphs, an important step towards understanding the role of potential pathogens for population management and conservation.

Arizona, California, Iowa, Massachusetts, Montana,↗

Increasing virulence, but not infectivity, associated with serially emergent virus strains of a fish rhabdovirus

Surveillance and genetic typing of field isolates of a fish rhabdovirus, infectious hematopoietic necrosis virus (IHNV), has identified four dominant viral genotypes that were involved in serial viral emergence and displacement events in steelhead trout ( Oncorhynchus mykiss ) in western North America. To investigate drivers of these landscape-scale events, IHNV isolates designated 007, 111, 110, and 139, representing the four relevant genotypes, were compared for virulence and infectivity in controlled laboratory challenge studies in five relevant steelhead trout populations. Viral virulence was assessed as mortality using lethal dose estimates (LD50), survival kinetics, and proportional hazards analysis. A pattern of increasing virulence for isolates 007, 111, and 110 was consistent in all five host populations tested, and correlated with serial emergence and displacements in the virus-endemic lower Columbia River source region during 1980–2013. The fourth isolate, 139, did not have higher virulence than the previous isolate 110. However, the mG139M genotype displayed a conditional displacement phenotype in that it displaced type mG110M in coastal Washington, but not in the lower Columbia River region, indicating that factors other than evolution of higher viral virulence were involved in some displacement events. Viral infectivity, measured as infectious dose (ID50), did not correlate consistently with virulence or with viral emergence, and showed a narrow range of variation relative to the variation observed in virulence. Comparison among the five steelhead trout populations confirmed variation in resistance to IHNV, but correlations with previous history of virus exposure or with sites of viral emergence varied between IHNV source and sink regions. Overall, this study indicated increasing viral virulence over time as a potential driver for emergence and displacement events in the endemic Lower Columbia River source region where these IHNV genotypes originated, but not in adjacent sink regions.

Virus Evolution↗

Representing the acquisition and use of energy by individuals in agent-based models of animal populations

1. Agent-based models (ABMs) are widely used to predict how populations respond to changing environments. As the availability of food varies in space and time, individuals should have their own energy budgets, but there is no consensus as to how these should be modelled. Here, we use knowledge of physiological ecology to identify major issues confronting the modeller and to make recommendations about how energy budgets for use in ABMs should be constructed. 2. Our proposal is that modelled animals forage as necessary to supply their energy needs for maintenance, growth and reproduction. If there is sufficient energy intake, an animal allocates the energy obtained in the order: maintenance, growth, reproduction, energy storage, until its energy stores reach an optimal level. If there is a shortfall, the priorities for maintenance and growth/reproduction remain the same until reserves fall to a critical threshold below which all are allocated to maintenance. Rates of ingestion and allocation depend on body mass and temperature. We make suggestions for how each of these processes should be modelled mathematically. 3. Mortality rates vary with body mass and temperature according to known relationships, and these can be used to obtain estimates of background mortality rate. 4. If parameter values cannot be obtained directly, then values may provisionally be obtained by parameter borrowing, pattern-oriented modelling, artificial evolution or from allometric equations. 5. The development of ABMs incorporating individual energy budgets is essential for realistic modelling of populations affected by food availability. Such ABMs are already being used to guide conservation planning of nature reserves and shell fisheries, to assess environmental impacts of building proposals including wind farms and highways and to assess the effects on nontarget organisms of chemicals for the control of agricultural pests.

Methods in Ecology and Evolution↗