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Wayne, R. K.

Publications and source records attributed to Wayne, R. K..

16 recordsLinked to original sources

Whole genomes reveal how Andean climate history shapes genetic diversity and modern conservation risk in South American pumas

Climatic oscillations in the Andes have repeatedly reshaped habitats over millions of years, yet their long-term genomic consequences for wide-ranging carnivores remain unclear. We generated whole-genome sequences from pumas (Puma concolor) across ecologically distinct regions of Ecuador to test how paleoclimate shaped population structure, demography, and genetic load. We show that northwestern forest pumas persisted in long-term isolation within humid refugia, whereas northern Andean and southern Pacific populations reconnected intermittently during warm interglacial periods. Southern coastal pumas maintained persistently small effective population sizes, leading to elevated runs of homozygosity and increased burdens of homozygous loss-of-function variants. In contrast, northern populations historically remained larger but exhibit early signs of inbreeding in one individual, marked by long runs of homozygosity and a kinked tail phenotype. Our findings indicate that recent fragmentation may be disrupting historical connectivity. Restoring corridors around the western foothills could reestablish gene flow and reduce inbreeding risk, while targeted genetic rescue may support chronically isolated southern populations. By integrating paleoclimate history with genome-wide data, we provide a framework for region-specific conservation strategies that balance connectivity restoration with the preservation of local adaptation.

genomics↗

Urbanization drives genetic erosion and population structure in a historically connected carnivore population

Urbanization is a dominant driver of habitat fragmentation globally, creating small, isolated wildlife populations vulnerable to accelerated genetic drift, reduced genetic diversity, and increased population differentiation. We investigated how urban development affects the genetic composition and structure of caracals (Caracal caracal) in Cape Town, South Africa using microsatellites and mitochondrial DNA sequence data. Sampling across four geographically disparate urban and rural populations revealed contrasting temporal patterns: mitochondrial markers indicated historical genetic connectivity among populations, while microsatellite data demonstrated recent genetic structuring driven primarily by urbanization. An extensively isolated urban population showed reduced allelic richness and pronounced genetic differentiation, reflecting urbanization as a strong barrier to gene flow. Within the isolated urban population, GPS-collared caracals demonstrated a degree of spatial genetic organization, with related individuals maintaining significantly higher home range overlap despite inhabiting a severely fragmented urban landscape. This kin-structured space use occurred despite caracals in the system having large home ranges compressed within a relatively small, isolated environment. Our findings reveal that urbanization has rapidly disrupted gene flow in this otherwise geographically widespread and adaptable carnivore, imposing a sufficient barrier to generate detectable genetic consequences within contemporary timeframes. The contrasting signals from historical versus contemporary molecular markers highlight urbanizations role in fragmenting previously connected populations and demonstrates the value of multi-marker approaches for detecting anthropogenic impacts on wildlife populations. These results underscore urbanizations capacity to rapidly alter population genetic dynamics, even in a highly mobile and adaptable carnivore.

genetics↗

The distribution of fitness effects varies phylogenetically across animals

1The distribution of fitness effects (DFE) describes the selection coefficients (s) of newly arising mutations and fundamentally influences population genetic processes. However, the extent and mechanisms of DFE variation have not been systematically investigated across species with divergent phylogenetic histories and ecological functions. Here, we inferred the DFE in natural populations of eleven animal (sub)species, including humans, mice, fin whales, vaquitas, wolves, collared flycatchers, pied flycatchers, halictid bees, Drosophila, and mosquitoes. We find that the DFE co-varies with phylogeny, where the expected mutation effects are more similar in closely related species (Pagels{lambda} = 0.84, P = 0.01). Additionally, mammals have a higher proportion of strongly deleterious mutations (22% to 47% in mammals; 0.0% to 5.4% in insects and birds) and a lower proportion of weakly deleterious mutations than insects and birds. Population size is significantly negatively correlated with the expected impact of new deleterious mutations (PGLS{lambda}, P = 0.03), and the proportion of new beneficial mutations ([Formula], P < 0.001). These findings align with Fishers Geometric Model (FGM), which defines organismal complexity as the number of phenotypes under selection. Consistent with the FGMs predictions, we observe that mutations are more deleterious in complex organisms, while beneficial mutations occur more frequently in smaller populations to compensate for the drift load. Our study demonstrates strong phylogenetic constraints in the evolution of a fundamental population genetics parameter, and proposes that, through mechanisms of global epistasis, long-term population size and organismal complexity drive variation in the DFE across animals. 2 Significance StatementUnderstanding how mutations affect fitness is fundamental in evolution, but little is known about how and why the distribution of fitness effects (DFE) varies across species. In this study, we examine the DFE in diverse animal populations and show that closely related species exhibit similar patterns of mutation effects, with new mutations being more deleterious in mammals compared with birds and insects. Our findings corroborate Fishers Geometric Model, which explains the variation in the DFE across species as a function of organismal complexity and long-term population size. By connecting organismal complexity and population size with the DFE, we offer a phylogenetic view into the selective forces shaping species adaptation and evolution.

evolutionary biology↗

Genetic and anatomical determinants of olfaction in dogs and wild canids

Understanding the anatomical and genetic basis of complex phenotypic traits has long been a challenge for biological research. Domestic dogs offer a compelling model as they demonstrate more phenotypic variation than any other vertebrate species. Dogs have been intensely selected for specific traits and abilities, directly or indirectly, over the past 15,000 years since their initial domestication from the gray wolf. Because olfaction plays a central role in critical tasks, such as the detection of drugs, diseases, and explosives, as well as human rescue, we compared relative olfactory capacity across dog breeds and assessed changes to the canine olfactory system resulting from domestication. We conducted a cross-disciplinary survey of olfactory anatomy, olfactory receptor (OR) gene variation, and OR gene expression in domestic dogs. Through comparisons to their closest wild canid relatives, the gray wolf and coyote, we show that domestic dogs might have lost functional OR genes commensurate with a documented reduction in nasal morphology during domestication. Critically, within domestic dogs alone, we found no genetic or morphological profile shared among functional or genealogical breed groupings, such as scent hounds, that might indicate evidence of any human-directed selection for enhanced olfaction. Instead, our results suggest that superior scent detection dogs likely owe their success to advantageous behavioral traits and training rather than an "olfactory edge" provided by morphology or genes.

evolutionary biology↗

The influence of gene flow on population viability in an isolated urban caracal population

Wildlife populations are becoming increasingly fragmented by anthropogenic development. Such small and isolated populations often face an elevated risk of extinction, in part due to inbreeding depression. Here, we examine the genomic consequences of urbanization in a caracal (Caracal caracal) population that has become isolated in the Cape Peninsula region of the city of Cape Town, South Africa and is thought to number [~]50 individuals. We document low levels of migration into the population over the past [~]75 years, with an estimated rate of 1.3 effective migrants per generation. As a consequence of this isolation and small population size, levels of inbreeding are elevated in the contemporary Cape Peninsula population (mean FROH>1Mb=0.20). Inbreeding primarily manifests as long runs of homozygosity >10Mb, consistent with the effects of isolation due to the rapid recent growth of Cape Town. To explore how reduced migration and elevated inbreeding may impact future population dynamics, we parameterized an eco-evolutionary simulation model. We find that if migration rates do not change in the future, the population is expected to decline only slightly, with a low projected risk of extinction. However, if migration rates decline or anthropogenic mortality rates increase, the potential risk of extinction is greatly elevated. To avert a population decline, we suggest that translocating migrants into the Cape Peninsula to initiate a genetic rescue may be warranted in the near future. Our analysis highlights the utility of genomic datasets coupled with computational simulation models for investigating the influence of gene flow on population viability.

evolutionary biology↗

Environmental DNA reveals invasive crayfish microbial associates and ecosystem-wide biodiversity before and after eradication

Biodiversity monitoring in conservation projects is essential to understand environmental status and recovery. However, traditional field surveys can be expensive, time-consuming, biased towards visual detection, and focused on measuring a limited set of taxa. Environmental DNA (eDNA) methods provide a new approach to biodiversity monitoring that has the potential to sample a taxonomically broader set of organisms with similar effort, but many of these approaches are still in the early stages of development and testing. Here, we use multilocus eDNA metabarcoding to understand how the removal of invasive red swamp crayfish impacts local biodiversity of a desert oasis ecosystem, as well as to detect crayfish both directly and indirectly. We tracked crayfish DNA signatures, microbial DNA associated with crayfish, and biodiversity of plant, fungal, animal, and bacterial communities through time. We were unsuccessful in detecting crayfish directly in either control tanks or oases using targeted metabarcoding primers for invertebrates and eukaryotes, similar to previous studies which have shown variable levels of success in detecting crayfish from environmental samples. However, we were successful in discerning a suite of 90 crayfish-associated taxa to serve as candidate bioindicators of invasive presence using 16S and Fungal ITS2 metabarcoding. Ranking these 90 taxa by their geographic distribution in eDNA surveys and by evidence of crayfish-associations in the literature, we support 9 taxa to be high-ranking, and suggest they be prioritized in future biomonitoring. Biodiversity analyses from five metabarcode loci including plants, animals, and both prokaryotic and eukaryotic microbes showed that communities differed but that species richness remained relatively similar between oases through time. Our results reveal that, while there are limitations of eDNA approaches to detect crayfish and other invasive species, microbial bioindicators offer a largely untapped biomonitoring opportunity for invasive species management, adding a valuable resource to a conservation managers toolkit.

ecology↗

Genomic underpinnings of population persistence in Isle Royale moose

Island ecosystems provide models to assess the impacts of isolation on population persistence. However, most studies of persistence have focused on a single species, without comparisons to other organisms they interact with in the ecosystem. The simple predator-prey system of moose and gray wolves on Isle Royale provides allows a direct contrast of genetic variation in a prey species with their natural predator. Wolves on Isle Royale exhibited signs of severe inbreeding depression, which nearly drove the population to extinction in 2019. In the relative absence of wolves, the moose population has thrived and exhibits no obvious signs of inbreeding depression despite being isolated for [~]120 years and having low genetic diversity. Here, we examine the genomic underpinnings of population persistence in the Isle Royale moose population. We document high levels of inbreeding in the population, roughly as high as the wolf population at the time of its decline. However, inbreeding in the moose population manifests in the form of intermediate-length runs of homozygosity indicative of gradual inbreeding, contrasting with the severe recent inbreeding observed in the wolf population. Using simulations, we demonstrate that this more gradual inbreeding in the moose population has resulted in an estimated 50% purging of the inbreeding load, helping to explain the continued persistence of the population. However, we also document notable increases in genetic load, which could eventually threaten population viability over the long term. Finally, we document low diversity in mainland North American moose populations due to a severe founder event occurring near the end of the Holocene. Overall, our results demonstrate a complex relationship between inbreeding, genetic diversity, and population viability that highlights the importance of maintaining isolated populations at moderate size to avert extinction from genetic factors. Significance statementIsolated wildlife populations face a high risk of extinction due in part to the deleterious consequences of inbreeding. Whether purifying natural selection can overcome these negative impacts by "purging" harmful recessive mutations is a topic of active debate. We characterized the extent of purging in an isolated moose population. Our results demonstrate signatures of gradual inbreeding in the population, ideal circumstances to facilitate purging. Using simulations, we demonstrate substantial potential for purging in the population, though we also show that fitness is reduced by small population size and inbreeding. Our findings provide insight into the mechanisms enabling persistence in isolated populations, with implications for conserving the growing number of isolated populations worldwide.

evolutionary biology↗

Hibernation slows epigenetic aging in yellow-bellied marmots

Species that hibernate live longer than would be expected based solely on their body size. Hibernation is characterized by long periods of metabolic suppression (torpor) interspersed by short periods of increased metabolism (arousal). The torpor-arousal cycles occur multiple times during hibernation, and it has been suggested that processes controlling the transition between torpor and arousal states cause aging suppression. Metabolic rate is also a known correlate of longevity, we thus proposed the hibernation-aging hypothesis whereby aging is suspended during hibernation. We tested this hypothesis in a well-studied population of yellow-bellied marmots (Marmota flaviventer), which spend 7-8 months per year hibernating. We used two approaches to estimate epigenetic age: the epigenetic clock and the epigenetic pacemaker. Variation in epigenetic age of 149 samples collected throughout the life of 73 females were modeled using generalized additive mixed models (GAMM), where season (cyclic cubic spline) and chronological age (cubic spline) were fixed effects. As expected, the GAMM using epigenetic ages calculated from the epigenetic pacemaker was better able to detect nonlinear patterns in epigenetic age change over time. We observed a logarithmic curve of epigenetic age with time, where the epigenetic age increased at a higher rate until females reached sexual maturity (2-years old). With respect to circannual patterns, the epigenetic age increased during the summer and essentially stalled during the winter. Our enrichment analysis of age-related CpG sites revealed pathways related to development and cell differentiation, while the season-related CpGs enriched pathways related to central carbon metabolism, immune system, and circadian clock. Taken together, our results are consistent with the hibernation-aging hypothesis and may explain the enhanced longevity in hibernators.

evolutionary biology↗

From zero to infinity: minimum to maximum diversity of the planet by spatio-parametric Rao's quadratic entropy

AimThe majority of work done to gather information on Earth diversity has been carried out by in-situ data, with known issues related to epistemology (e.g., species determination and taxonomy), spatial uncertainty, logistics (time and costs), among others. An alternative way to gather information about spatial ecosystem variability is the use of satellite remote sensing. It works as a powerful tool for attaining rapid and standardized information. Several metrics used to calculate remotely sensed diversity of ecosystems are based on Shannons Information Theory, namely on the differences in relative abundance of pixel reflectances in a certain area. Additional metrics like the Raos quadratic entropy allow the use of spectral distance beside abundance, but they are point descriptors of diversity, namely they can account only for a part of the whole diversity continuum. The aim of this paper is thus to generalize the Raos quadratic entropy by proposing its parameterization for the first time. InnovationThe parametric Raos quadratic entropy, coded in R, i) allows to represent the whole continuum of potential diversity indices in one formula, and ii) starting from the Raos quadratic entropy, allows to explicitly make use of distances among pixel reflectance values, together with relative abundances. Main conclusionsThe proposed unifying measure is an integration between abundance- and distance-based algorithms to map the continuum of diversity given a satellite image at any spatial scale.

ecology↗

Experimental assessment of K locus effects on the gray wolf response to virus

In North American gray wolves, black coat color is dominantly inherited via a three base pair coding deletion in the canine beta defensin 3 (CBD103) gene. This three base pair deletion, called the KB allele, was introduced through hybridization with dogs and subsequently underwent a selective sweep that increased its frequency in wild wolves. Despite apparent positive selection, KBB wolves have significantly lower fitness than wolves with the KyB genotype, even though the two genotypes show no observable differences in black coat color. Thus, the KB allele is thought to have pleiotropic effects on as-yet unknown phenotypes. Given the role of skin-expressed CBD103 in innate immunity, we hypothesized that the KB allele influences the gene regulatory response to viral infection. To test this hypothesis, we developed a panel of primary epidermal keratinocyte cell cultures from 24 wild North American gray wolves (both Kyy and KyB genotypes) and generated immortalized Kyy and CBD103 knockout lines. We assessed the transcriptome-wide responses of wolf keratinocytes to polyinosinic:polycytidylic acid (polyI:C), which mimics infection by a double-stranded RNA virus, and to live canine distemper virus. Keratinocytes with the KyB genotype and with the Kyy genotype had similar gene regulatory responses to viral infection, suggesting that this response does not explain pleiotropic effects of the KB allele on fitness. This study supports the feasibility of using cell culture methods to investigate the phenotypic effects of naturally occurring genetic variation in wild mammals.

evolutionary biology↗

A Biodiversity Composition Map of California Derived from Environmental DNA Metabarcoding and Earth Observation

Unique ecosystems globally are under threat from ongoing anthropogenic environmental change. Effective conservation management requires more thorough biodiversity surveys that can reveal system-level patterns and that can be applied rapidly across space and time. We offer a way to use environmental DNA, community science and remote sensing together as methods to reduce the discrepancy between the magnitude of change and historical approaches to measure it. Taking advantages of modern ecological models, we integrate environmental DNA and Earth observations to evaluate regional biodiversity patterns for a snapshot of time, and provide critical community-level characterization. We collected 278 samples in Spring 2017 from coastal, shrub and lowland forest sites in California, a large-scale biodiversity hotspot. We applied gradient forest to model 915 family occurrences and community composition together with environmental variables and multi-scalar habitat classifications to produce a statewide biodiversity-based map. 16,118 taxonomic entries recovered were associated with environmental variables to test their predictive strength on alpha, beta, and zeta diversity. Local habitat classification was diagnostic of community composition, illuminating a characteristic of biodiversity hotspots. Using gradient forest models, environmental variables predicted 35% of the variance in eDNA patterns at the family level, with elevation, sand percentage, and greenness (NDVI32) as the top predictors. This predictive power was higher than we found in published literature at global scale. In addition to this indication of substantial environmental filtering, we also found a positive relationship between environmentally predicted families and their numbers of biotic interactions. In aggregate, these analyses showed that strong eDNA community-environment correlation is a general characteristic of temperate ecosystems, and may explain why communities easily destabilize under disturbances. Our study provides the first example of integrating citizen science based eDNA with biodiversity mapping across the tree of life, with promises to produce large scale, high resolution assessments that promote a more comprehensive and predictive understanding of the factors that influence biodiversity and enhance its maintenance.

ecology↗

Beach environmental DNA fills gaps in photographic biomonitoring to track spatiotemporal community turnover across 82 phyla

AbstractEnvironmental DNA (eDNA) metabarcoding is emerging as a biomonitoring tool available to the citizen science community that promises to augment or replace photographic observation. However, eDNA results and photographic observations have rarely been compared to document their individual or combined power. Here, we use eDNA multilocus metabarcoding, a method deployed by the CALeDNA Program, to inventory and evaluate biodiversity variation along the Pillar Point headland near Half Moon Bay, California. We describe variation in presence of 13,000 taxa spanning 82 phyla, analyze spatiotemporal patterns of beta diversity, and identify metacommunities. Inventory and measures of turnover across space and time from eDNA analysis are compared to the same measures from Global Biodiversity Information Facility (GBIF) data, which contain information largely contributed by iNaturalist photographic observations. We find eDNA depicts local signals with high seasonal turnover, especially in prokaryotes. We find a diverse community dense with pathogens and parasites in the embayment, and a State Marine Conservation Area (SMCA) with lower species richness than the rest of the beach peninsula, but with beta diversity signals showing resemblance to adjacent unprotected tidepools. The SMCA differs in observation density, with higher density of protozoans, and animals in Ascidiacea, Echinoidea, and Polycladida. Local contributions to beta diversity are elevated in a section of East-facing beach. GBIF observations are mostly from outside the SMCA, limiting some spatial comparisons. However, our findings suggest eDNA samples can link the SMCA sites to sites with better GBIF inventory, which may be useful for imputing species from one site given observations from another. Results additionally support >3800 largely novel biological interactions. This research, and accompanying interactive website support eDNA as a gap-filling tool to measure biodiversity that is available to community and citizen scientists.

ecology↗

High genetic diversity can contribute to extinction in small populations

Human-driven habitat fragmentation and loss have led to a proliferation of small and isolated plant and animal populations with high risk of extinction. One of the main threats to extinction in these populations is inbreeding depression, which is primarily caused by the exposure of recessive deleterious mutations as homozygous by inbreeding. The typical approach for managing these populations is to maintain high genetic diversity, often by translocating individuals from large populations to initiate a genetic rescue. However, the limitations of this approach have recently been highlighted by the demise of the gray wolf population on Isle Royale, which was driven to the brink of extinction soon after the arrival of a migrant from the large mainland wolf population. Here, we use a novel population genetic simulation framework to investigate the role of genetic diversity, deleterious variation, and demographic history in mediating extinction risk due to inbreeding depression in small populations. We show that, under realistic models of dominance, large populations harbor high levels of recessive strongly deleterious variation due to these mutations being hidden from selection in the heterozygous state. As a result, when large populations contract, they experience a substantially elevated risk of extinction after these strongly deleterious mutations are exposed by inbreeding. Moreover, we demonstrate that although translocating individuals to small populations is broadly effective as a means to reduce extinction risk, using small or moderate-sized source populations rather than large source populations can greatly increase the effectiveness of genetic rescue due to greater purging in these smaller populations. Our findings challenge the traditional conservation paradigm that focuses on maximizing genetic diversity to reduce extinction risk in favor of a view that emphasizes minimizing strongly deleterious variation. These insights have important implications for managing small and isolated populations in the increasingly fragmented landscape of the Anthropocene. Impact SummaryNumerous threats to extinction exist for small populations, including the detrimental effects of inbreeding. Although much of the focus in reducing these harmful effects in small populations has been on maintaining high genetic diversity, here we use simulations to demonstrate that emphasis should instead be placed on minimizing strongly deleterious variation. More specifically, we show that historically-large populations with high levels of genetic diversity also harbor elevated levels of recessive strongly deleterious mutations hidden in the heterozygous state. Thus, when these populations contract, inbreeding can expose these strongly deleterious mutations as homozygous and lead to severe inbreeding depression and rapid extinction. Moreover, we demonstrate that, although translocating individuals to these small populations to perform a genetic rescue is broadly beneficial, the effectiveness of this strategy can be greatly increased by targeting historically-smaller source populations where recessive strongly deleterious mutations have been purged. These results challenge long-standing views on how to best conserve small and isolated populations facing the threat of inbreeding depression, and have immediate implications for preserving biodiversity in the increasingly fragmented landscape of the Anthropocene.

evolutionary biology↗

Mountain lion genomes provide insights into genetic rescue of inbred populations

Introduction paragraph/AbstractAcross the geographic range of mountain lions, which includes much of North and South America, populations have become increasingly isolated due to human persecution and habitat loss. To explore the genomic consequences of these processes, we assembled a high-quality mountain lion genome and analyzed a panel of resequenced individuals from across their geographic range. We found strong geographical structure and signatures of severe inbreeding in all North American populations. Tracts of homozygosity were rarely shared among populations, suggesting that assisted gene flow would restore local genetic diversity. However, the genome of an admixed Florida panther that descended from a translocated individual from Central America had surprisingly long tracts of homozygosity, indicating that genomic gains from translocation were quickly lost by local inbreeding. Thus, to sustain diversity, genetic rescue will need to occur at regular intervals, through repeated translocations or restoring landscape connectivity. Mountain lions provide a rare opportunity to examine the potential to restore diversity through genetic rescue, and to observe the long-term effects of translocation. Our methods and results provide a framework for genome-wide analyses that can be applied to the management of small and isolated populations.

evolutionary biology↗

Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction

The observation that small, isolated populations often suffer reduced fitness as a result of inbreeding depression has guided conservation theory and practice for decades. However, investigating the genome-wide dynamics associated with inbreeding depression in natural populations is only now feasible with relatively inexpensive sequencing technology and annotated reference genomes. To characterize the genome-wide effects of intense inbreeding and isolation, we sequenced complete genomes from an iconic inbred population, the gray wolves (Canis lupus) of Isle Royale. Through comparison with other wolf genomes from a variety of demographic histories, we found that Isle Royale wolf genomes contain extensive runs of homozygosity, but neither the overall level of heterozygosity nor the number of deleterious variants per genome were reliable predictors of inbreeding depression. These findings are consistent with the hypothesis that severe inbreeding depression results from increased homozygosity of strongly deleterious recessive mutations, which are more prevalent in historically large source populations. Our results have particular relevance in light of the recently proposed reintroduction of wolves to Isle Royale, as well as broader implications for management of genetic variation in the fragmented landscape of the modern world.

evolutionary biology↗

Complex patterns of sex-biased demography in canines

INTRODUCTION INTRODUCTION RESULTS DISCUSSION METHODS Data availability REFERENCES Studies of genetic variation have shown that the demographic history of dogs has been extremely complex, involving multiple bottleneck and admixture events. However, existing studies have not explored the variance in the number of reproducing males and females, and whether it has changed across evolutionary time. While male-biased mating practices, such as male-biased migration and multiple paternity, have been observed in wolves, recent breeding practices could have led to female-biased mating patterns in breed dogs. In addition, breed dogs are thought to have experienced the popular sire effect, where a small number of males father many offspring with a large number of females. Here we use genetic variation data to test how widespr ...

evolutionary biology↗