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Phenotypic homogenization and potential fitness constraints following non-native introgression in an endemic sportfish

Introgressive hybridization may lead to contrasting evolutionary outcomes that are difficult to predict since they depend on the fitness effects of endogenous genomic interactions and environmental factors. Conservation of endemic biodiversity may be more effective with require direct measurement of introgressed ancestry and fitness in wild populations, especially for keystone taxa at risk of hybridization following species introductions. We assessed the relationship of non-native ancestry with growth and body condition in the basin-restricted Neosho Bass ( Micropterus velox ; NB), focussing on two streams in the NB native range that are admixed extensively with non-native Smallmouth Bass ( M. dolomieu ; SMB). We quantified the genetic composition of 116 fish from Big Sugar Creek ( N = 46) and Elk River ( N = 70) at 14 microsatellite loci. Using back-calculated total length-at-age estimated from sagittal otoliths, we assessed whether genetic ancestry explained variation in von Bertalanffy growth model parameters, accounting for sex and stream effects. We then assessed the relationship between ancestry and body condition. We found no differences in growth parameters by sex, stream, or ancestry, suggesting phenotypic homogenization which could be mediated by selection on body size. We found a negative correlation between SMB ancestry and condition, including lower condition in Big Sugar Creek, possibly reflecting a trade-off between maximum length and condition with respect to overall fitness. We show that ongoing non-native introgression, which may be augmented by anthropogenic SMB introductions, may attenuate evolutionary differentiation between species and directly influence fitness, possibly having critical implications for long-term persistence and management of adaptive potential in a popular and ecologically important endemic sportfish.

Journal of Evolutionary Biology

The relationship between female brooding and male nestling provisioning: does climate underlie geographic variation in sex roles?

Comparative studies of populations occupying different environments can provide insights into the ecological conditions affecting differences in parental strategies, including the relative contributions of males and females. Male and female parental strategies reflect the interplay between ecological conditions, the contributions of the social mate, and the needs of offspring. Climate is expected to underlie geographic variation in incubation and brooding behavior, and can thereby affect both the absolute and relative contributions of each sex to other aspects of parental care such as offspring provisioning. However, geographic variation in brooding behavior has received much less attention than variation in incubation attentiveness or provisioning rates. We compared parental behavior during the nestling period in populations of orange-crowned warblers Oreothlypis celata near the northern (64°N) and southern (33°N) boundaries of the breeding range. In Alaska, we found that males were responsible for the majority of food delivery whereas the sexes contributed equally to provisioning in California. Higher male provisioning in Alaska appeared to facilitate a higher proportion of time females spent brooding the nestlings. Surprisingly, differences in brooding between populations could not be explained by variation in ambient temperature, which was similar between populations during the nestling period. While these results represent a single population contrast, they suggest additional hypotheses for the ecological correlates and evolutionary drivers of geographic variation in brooding behavior, and the factors that shape the contributions of each sex.

Journal of Avian Biology

Genetic tools for wildlife management

Granted interim status in November, 2013, The Wildlife Society’s (TWS) Molecular Ecology Working Group aims to promote scientific advancement by applying molecular techniques to wildlife ecology, management, and conservation. The working group—composed of sci - entists from diverse backgrounds—met for the first time in Pittsburgh at the TWS Annual Conference held in October. Our overarching goal is to enhance awareness of molecular ecology and genetic applica - tions to wildlife biology and act as an informational and networking resource. During the group’s interim status, which runs for three years, we intend to focus on a broad scope of molecular ecology that is applicable to wildlife including genetic and ge - nomic methods, conservation genetics, non-invasive genetic population monitoring, landscape genetics, evolutionary genetics, and molecular forensics

The Wildlife Professional

Hybridization among Arctic white-headed gulls (Larus spp.) obscures the genetic legacy of the Pleistocene

We studied the influence of glacial oscillations on the genetic structure of seven species of white-headed gull that breed at high latitudes ( Larus argentatus, L. canus, L. glaucescens, L. glaucoides, L. hyperboreus, L. schistisagus, and L. thayeri ). We evaluated localities hypothesized as ice-free areas or glacial refugia in other Arctic vertebrates using molecular data from 11 microsatellite loci, mitochondrial DNA (mtDNA) control region, and six nuclear introns for 32 populations across the Holarctic. Moderate levels of genetic structure were observed for microsatellites ( F ST = 0.129), introns ( Φ ST = 0.185), and mtDNA control region ( Φ ST = 0.461), with among-group variation maximized when populations were grouped based on subspecific classification. Two haplotype and at least two allele groups were observed across all loci. However, no haplotype/allele group was composed solely of individuals of a single species, a pattern consistent with recent divergence. Furthermore, northernmost populations were not well differentiated and among-group variation was maximized when L. argentatus and L. hyberboreus populations were grouped by locality rather than species, indicating recent hybridization. Four populations are located in putative Pleistocene glacial refugia and had larger t estimates than the other 28 populations. However, we were unable to substantiate these putative refugia using coalescent theory, as all populations had genetic signatures of stability based on mtDNA. The extent of haplotype and allele sharing among Arctic white-headed gull species is noteworthy. Studies of other Arctic taxa have generally revealed species-specific clusters as well as genetic structure within species, usually correlated with geography. Aspects of white-headed gull behavioral biology, such as colonization ability and propensity to hybridize, as well as their recent evolutionary history, have likely played a large role in the limited genetic structure observed.

Ecology and Evolution

Multiple hypotheses testing of fish incidence patterns in an urbanized ecosystem

Ecological and evolutionary theories have focused traditionally on natural processes with little attempt to incorporate anthropogenic influences despite the fact that humans are such an integral part of virtually all ecosystems. A series of alternate models that incorporated anthropogenic factors and traditional ecological mechanisms of invasion to account for fish incidence patterns in urban lakes was tested. The models were based on fish biology, human intervention, and habitat characteristics. However, the only models to account for empirical patterns were those that included fish invasiveness, which incorporated species-specific information about overall tolerance and fecundity. This suggests that species-specific characteristics are more important in general distributional patterns than human-mediated dispersal. Better information of illegal stocking activities is needed to improve human-mediated models, and more insight into basic life history of ubiquitous species is needed to truly understand underlying mechanisms of biotic homogenization. ?? Springer 2005.

Aquatic Ecology

Legacy introductions and climatic variation explain spatiotemporal patterns of invasive hybridization in a native trout

Hybridization between invasive and native species, a significant threat to worldwide biodiversity, is predicted to increase due to climate-induced expansions of invasive species. Long-term research and monitoring are crucial for understanding the ecological and evolutionary processes that modulate the effects of invasive species. Using a large, multi-decade genetics dataset (N = 582 sites, 12,878 individuals) with high-resolution climate predictions and extensive stocking records, we evaluate the spatiotemporal dynamics of hybridization between native cutthroat trout and invasive rainbow trout, the world’s most widely introduced invasive fish, across the northern Rocky Mountains of the United States. Historical effects of stocking and contemporary patterns of climatic variation were strongly related to the spread of hybridization across space and time. The probability of occurrence, extent of, and temporal changes in hybridization increased at sites in close proximity to historical stocking locations with greater rainbow trout propagule pressure, warmer water temperatures, and lower spring precipitation. Although locations with warmer water temperatures were more prone to hybridization, cold sites were not protected from invasion; 58% of hybridized sites had cold mean summer water temperatures (<11 ° C). Despite cessation of stocking over 40 years ago, hybridization increased over time at half (50%) of the locations with long-term data, the vast majority of which (74%) were initially non-hybridized, emphasizing the chronic, negative impacts of human-mediated hybridization. These results show that effects of climate change on biodiversity must be analyzed in the context of historical human impacts that set ecological and evolutionary trajectories.

Global Change Biology

Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems

It is difficult to find references to fire in general textbooks on ecology, conservation biology or biogeography, in spite of the fact that large parts of the world burn on a regular basis, and that there is a considerable literature on the ecology of fire and its use for managing ecosystems. Fire has been burning ecosystems for hundreds of millions of years, helping to shape global biome distribution and to maintain the structure and function of fire-prone communities. Fire is also a significant evolutionary force, and is one of the first tools that humans used to re-shape their world. Here, we review the recent literature, drawing parallels between fire and herbivores as alternative consumers of vegetation. We point to the common questions, and some surprisingly different answers, that emerge from viewing fire as a globally significant consumer that is analogous to herbivory.

Trends in Ecology and Evolution

Molecular sexing of birds using quantitative PCR (qPCR) of sex-linked genes and logistic regression models

The ability to sex individuals is an important component of many behavioural and ecological investigations and provides information for demographic models used in conservation and species management. However, many birds are difficult to sex using morphological characters or traditional molecular sexing methods. In this study, we developed probabilistic models for sexing birds using quantitative PCR (qPCR) data. First, we quantified distributions of gene copy numbers at a set of six sex-linked genes, including the sex-determining gene DMRT1 , for individuals across 17 species and seven orders of birds ( n = 150). Using these data, we built predictive logistic models for sex identification and tested their performance with independent samples from 51 species and 13 orders ( n = 209). Models using the two loci most highly correlated with sex had greater accuracy than models using the full set of sex-linked loci, across all taxonomic levels of analysis. Sex identification was highly accurate when individuals to be assigned were of species used in model building. Our analytical approach was widely applicable across diverse neognath bird lineages spanning millions of years of evolutionary divergence. Unlike previous methods, our probabilistic framework incorporates uncertainty around qPCR measurements as well as biological variation within species into decision-making rules. We anticipate that this method will be useful for sexing birds, including those of high conservation concern and/or subsistence value, that have proven difficult to sex using traditional approaches. Additionally, the general analytical framework presented in this paper may also be applicable to other organisms with sex chromosomes.

Molecular Ecology Resources

Genotyping-by-sequencing illuminates high levels of divergence among sympatric forms of coregonines in the Laurentian Great Lakes

Effective resource management depends on our ability to partition diversity into biologically meaningful units. Recent evolutionary divergence, however, can often lead to ambiguity in morphological and genetic differentiation, complicating the delineation of valid conservation units. Such is the case with the "coregonine problem," where recent postglacial radiations of coregonines into lacustrine habitats resulted in the evolution of numerous species flocks, often with ambiguous taxonomy. The application of genomics methods is beginning to shed light on this problem and the evolutionary mechanisms underlying divergence in these ecologically and economically important fishes. Here, we used restriction site-associated DNA (RAD) sequencing to examine genetic diversity and differentiation among sympatric forms in the Coregonus artedi complex in the Apostle Islands of Lake Superior, the largest lake in the Laurentian Great Lakes. Using 29,068 SNPs, we were able to clearly distinguish among the three most common forms for the first time, as well as identify putative hybrids and potentially misidentified specimens. Population assignment rates for these forms using our RAD data were 93%-100% with the only mis-assignments arising from putative hybrids, an improvement from 62% to 77% using microsatellites. Estimates of pairwise differentiation ( F ST : 0.045-0.056) were large given the detection of hybrids, suggesting that reduced fitness of hybrid individuals may be a potential mechanism for the maintenance of differentiation. We also used a newly built C. artedi linkage map to look for islands of genetic divergence among forms and found widespread differentiation across the genome, a pattern indicative of long-term drift, suggesting that these forms have been reproductively isolated for a substantial amount of time. The results of this study provide valuable information that can be applied to develop well-informed management strategies and stress the importance of re-evaluating conservation units with genomic tools to ensure they accurately reflect species diversity.

Wisconsin

The bee microbiome: Impact on bee health and model for evolution and ecology of host-microbe interactions

As pollinators, bees are cornerstones for terrestrial ecosystem stability and key components in agricultural productivity. All animals, including bees, are associated with a diverse community of microbes, commonly referred to as the microbiome. The bee microbiome is likely to be a crucial factor affecting host health. However, with the exception of a few pathogens, the impacts of most members of the bee microbiome on host health are poorly understood. Further, the evolutionary and ecological forces that shape and change the microbiome are unclear. Here, we discuss recent progress in our understanding of the bee microbiome, and we present challenges associated with its investigation. We conclude that global coordination of research efforts is needed to fully understand the complex and highly dynamic nature of the interplay between the bee microbiome, its host, and the environment. High-throughput sequencing technologies are ideal for exploring complex biological systems, including host-microbe interactions. To maximize their value and to improve assessment of the factors affecting bee health, sequence data should be archived, curated, and analyzed in ways that promote the synthesis of different studies. To this end, the BeeBiome consortium aims to develop an online database which would provide reference sequences, archive metadata, and host analytical resources. The goal would be to support applied and fundamental research on bees and their associated microbes and to provide a collaborative framework for sharing primary data from different research programs, thus furthering our understanding of the bee microbiome and its impact on pollinator health.

mBio

Ecological acclimation: A framework to integrate fast and slow responses to climate change

Ecological responses to climate change occur across vastly different time-scales, from minutes for physiological plasticity to decades or centuries for community turnover and evolutionary adaptation. Accurately predicting the range of ecosystem trajectories will require models that incorporate both fast processes that may keep pace with climate change and slower ones likely to lag behind and generate disequilibrium dynamics. However, the knowledge necessary for this integration is currently fragmented across disciplines. We develop ‘ecological acclimation’ as a unifying framework to emphasize the similarity of dynamics driven by processes operating on dramatically different time-scales and levels of biological organization. The framework focuses on ecoclimate sensitivities, measured as the change in an ecological response variable per unit of climate change. Acclimation processes acting at different time-scales cause these sensitivities to shift in magnitude and even direction over time. We highlight shifting ecoclimate sensitivities in case studies from diverse ecosystems, including terrestrial plant communities, coral reefs and soil microbiomes. Models predicting future ecosystem states inevitably make assumptions about acclimation processes; these assumptions must be explicit for users to evaluate whether a model is appropriate for a given forecast horizon. Similarly, decision frameworks that clearly account for multiple acclimation processes and their distinct time-scales will help natural resource managers plan for ecological impacts of climate change from years to many decades into the future. We outline a synthetic research programme focused on the time-scales of ecological acclimation to reduce uncertainty in ecological forecasts.

Functional Ecology

Assessing models of speciation under different biogeographic scenarios; An empirical study using multi-locus and RNA-seq analyses

Evolutionary biology often seeks to decipher the drivers of speciation, and much debate persists over the relative importance of isolation and gene flow in the formation of new species. Genetic studies of closely related species can assess if gene flow was present during speciation, because signatures of past introgression often persist in the genome. We test hypotheses on which mechanisms of speciation drove diversity among three distinct lineages of desert tortoise in the genus Gopherus . These lineages offer a powerful system to study speciation, because different biogeographic patterns (physical vs. ecological segregation) are observed at opposing ends of their distributions. We use 82 samples collected from 38 sites, representing the entire species' distribution and generate sequence data for mtDNA and four nuclear loci. A multilocus phylogenetic analysis in *BEAST estimates the species tree. RNA‐seq data yield 20,126 synonymous variants from 7665 contigs from two individuals of each of the three lineages. Analyses of these data using the demographic inference package ∂a∂i serve to test the null hypothesis of no gene flow during divergence. The best‐fit demographic model for the three taxa is concordant with the *BEAST species tree, and the ∂a∂i analysis does not indicate gene flow among any of the three lineages during their divergence. These analyses suggest that divergence among the lineages occurred in the absence of gene flow and in this scenario the genetic signature of ecological isolation (parapatric model) cannot be differentiated from geographic isolation (allopatric model).

Ecology and Evolution

Overview of emerging amphibian pathogens and modeling advances for conservation-related decisions

One of the leading causes of global amphibian decline is emerging infectious disease. We summarize the disease ecology of four major emerging amphibian infectious agents: chytrids, ranaviruses, trematodes, and Perkinsea. We focus on recently developed quantitative advances that build on well-established ecological theories and aid in studying epizootic and enzootic disease dynamics. For example, we identify ecological and evolutionary selective forces that determine disease outcomes and transmission pathways by borrowing ideas from population and community ecology theory. We outline three topics of general interest in disease ecology: (i) the relationship between biodiversity and disease risk, (ii) individual, species, or environmental transmission heterogeneity, and (iii) pathogen coinfections. Finally, we identify specific knowledge gaps impeding the success of conservation-related decisions for disease mitigation and the future of amphibian conservation success.

Biological Conservation

High site fidelity does not equate to population genetic structure for common goldeneye and Barrow's goldeneye in North America

Delineation of population structure provides valuable information for conservation and management of species, as levels of demographic and genetic connectivity not only affect population dynamics but also have important implications for adaptability and resiliency of populations and species. Here, we measure population genetic structure and connectivity across the ranges of two sister species of sea ducks: Barrow's goldeneye Bucephala islandica and common goldeneye B. clangula . We use two different marker types: 7–8 nuclear microsatellite loci assayed across 229 samples and 3678 double digest restriction‐site associated DNA sequencing (ddRAD‐seq) loci assayed across 61 samples. First, both datasets found no evidence of genetic structure within common or Barrow's goldeneye, including between North American and European samples of common goldeneye. These results are in contrast with previous mitochondrial DNA, band recovery and telemetry data which suggest that goldeneyes are structured across their range. We posit that the discordance between autosomal genetic markers and other data types suggests that males, possibly subadult males, may be maintaining genetic connectivity across each species' respective ranges. Next, although mate choice consequences resulting from inter‐specific brood parasitism was hypothesized to cause some level of gene flow between goldeneye species, we only identified a single F1 hybrid with no further evidence of contemporary or historical gene flow. Despite ddRAD‐seq demographic analyses which recovered an optimum evolutionary model of split‐with‐migration (i.e. secondary contact), estimates of gene flow were <<1 migrant per generation in both directions. Together, we conclude that either strong ecological barriers or assortative mating are likely playing a role in preventing further backcrossing. Finally, demographic analyses estimated a relatively deep divergence time between Barrow's goldeneye and common goldeneye of ~1.6 million years before present and suggests that the genomes of both species have been under similar evolutionary constraints.

Journal of Avian Biology

The conservation genetics juggling act: Integrating genetics and ecology, science and policy

The field of conservation genetics, when properly implemented, is a constant juggling act integrating molecular genetics, ecology, and demography with applied aspects concerning managing declining species or implementing conservation laws and policies. This young field has grown substantially since the 1980&rsquo;s following development of the polymerase chain reaction and now into the genomics era. Our lab has &ldquo;grown up&rdquo; with the field, having worked on these issues for over three decades. Our multi-disciplinary approach entails understanding the behavior and ecology of species as well as the underlying processes that contribute to genetic viability. Taking this holistic approach provides a comprehensive understanding of factors that influence species persistence and evolutionary potential while considering annual challenges that occur throughout their life cycle. As a federal lab, we are often addressing the needs of the U.S. Fish and Wildlife Service in their efforts to list, de-list or recover species. Nevertheless, there remains an overall communication gap between research geneticists and biologists who are charged with implementing their results. Therefore, we outline the need for a National Center for Small Population Biology to ameliorate this problem and provide organizations charged with making status decisions firmer ground from which to make their critical decisions.

Evolutionary Applications

Representing plant diversity in land models: An evolutionary approach to make ‘Functional Types’ more functional

Plants are critical mediators of terrestrial mass and energy fluxes, and their structural and functional traits have profound impacts on local and global climate, biogeochemistry, biodiversity, and hydrology. Yet Earth System Models (ESMs), our most powerful tools for predicting the effects of humans on the coupled biosphere-atmosphere system, simplify the incredible diversity of land plants into a handful of coarse categories of ‘Plant Functional Types’ (PFTs) that often fail to capture ecological dynamics such as biome distributions. The inclusion of more realistic functional diversity is a recognized goal for ESMs, yet there is currently no consistent, widely accepted way to add diversity to models, i.e. to determine what new PFTs to add and with what data to constrain their parameters. We review approaches to representing plant diversity in ESMs and draw on recent ecological and evolutionary findings to present an evolution-based functional type approach for further disaggregating functional diversity. Specifically, the prevalence of niche conservatism, or the tendency of closely related taxa to retain similar ecological and functional attributes through evolutionary time, reveals that evolutionary relatedness is a powerful framework for summarizing functional similarities and differences among plant types. We advocate that Plant Functional Types based on dominant evolutionary lineages (‘Lineage Functional Types’) will provide an ecologically defensible, tractable, and scalable framework for representing plant diversity in next-generation ESMs, with the potential to improve parameterization, process representation, and model benchmarking. We highlight how the importance of evolutionary history for plant function can unify the work of disparate fields to improve predictive modeling of the Earth system.

Global Change Biology

The Beringian coevolution project: Holistic collections of mammals and associated parasites reveal novel perspectives on evolutionary and environmental change in the North

The Beringian Coevolution Project (BCP), a field program underway in the high northern latitudes since 1999, has focused on building key scientific infrastructure for integrated specimen-based studies on mammals and their associated parasites. BCP has contributed new insights across temporal and spatial scales into how ancient climate and environmental change have shaped faunas, emphasizing processes of assembly, persistence, and diversification across the vast Beringian region. BCP collections also represent baseline records of biotic diversity from across the northern high latitudes at a time of accelerated environmental change. These specimens and associated data form an unmatched resource for identifying hidden diversity, interpreting past responses to climate oscillations, documenting contemporary conditions, and anticipating outcomes for complex biological systems in a regime of ecological perturbation. Because of its dual focus on hosts and parasites, the BCP record also provides a foundation for comparative analyses that can document the effects of dynamic change on the geographic distribution, transmission dynamics, and emergence of pathogens. By using specific examples from carnivores, shrews, lagomorphs, rodents and their associated parasites, we demonstrate how broad, integrated field collections provide permanent infrastructure that informs policy decisions regarding human impact and the effect of climate change on natural populations.

Arctic Science

Hybridization between Yellowstone cutthroat trout and rainbow trout alters the expression of muscle growth-related genes and their relationships with growth patterns

Hybridization creates novel gene combinations that may generate important evolutionary novelty, but may also reduce existing adaptation by interrupting inherent biological processes, such as genotype-environment interactions. Hybridization often causes substantial change in patterns of gene expression, which, in turn, may cause phenotypic change. Rainbow trout ( Oncorhynchus mykiss ) and cutthroat trout ( O . clarkii ) produce viable hybrids in the wild, and introgressive hybridization with introduced rainbow trout is a major conservation concern for native cutthroat trout. The two species differ in body shape, which is likely an evolutionary adaptation to their native environments, and their hybrids tend to show intermediate morphology. The characterization of gene expression patterns may provide insights on the genetic basis of hybrid and parental morphologies, as well as on the ecological performance of hybrids in the wild. Here, we evaluated the expression of eight growth-related genes (MSTN-1a, MSTN-1b, MyoD1a, MyoD1b, MRF-4, IGF-1, IGF-2, and CAST-L) and the relationship of these genes with growth traits (length, weight, and condition factor) in six line crosses: both parental species, both reciprocal F1 hybrids, and both first-generation backcrosses (F1 x rainbow trout and F1 x cutthroat trout). Four of these genes were differentially expressed among rainbow, cutthroat, and their hybrids. Transcript abundance was significantly correlated with growth traits across the parent species, but not across hybrids. Our findings suggest that rainbow and cutthroat trout exhibit differences in muscle growth regulation, that transcriptional networks may be modified by hybridization, and that hybridization disrupts intrinsic relationships between gene expression and growth patterns that may be functionally important for phenotypic adaptations.

PLoS ONE