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Molecular and morphological data reveal non-monophyly and speciation in imperiled freshwater mussels (Anodontoides and Strophitus)

Accurate taxonomic placement is vital to conservation efforts considering many intrinsic biological characteristics of understudied species are inferred from closely related taxa. The rayed creekshell, Anodontoides radiatus (Conrad, 1834), exists in the Gulf of Mexico drainages from western Florida to Louisiana and has been petitioned for listing under the Endangered Species Act. We set out to resolve the evolutionary history of A. radiatus, primarily generic placement and species boundaries, using phylogenetic, morphometric, and geographic information. Our molecular matrix contained 3 loci: cytochrome c oxidase subunit I, NADH dehydrogenase subunit I, and the nuclear-encoded ribosomal internal transcribed spacer I. We employed maximum likelihood and Bayesian inference to estimate a phylogeny and test the monophyly of Anodontoides and Strophitus. We implemented two coalescent-based species delimitation models to test seven species models and evaluate species boundaries within A. radiatus. Concomitant to molecular data, we also employed linear morphometrics and geographic information to further evaluate species boundaries. Molecular and morphological evidence supports the inclusion of A. radiatus in the genus Strophitus, and we resurrect the binomial Strophitus radiatus to reflect their shared common ancestry. We also found strong support for polyphyly in Strophitus and advocate the resurrection of the genus Pseudodontoideus to represent ‘Strophitus’ connasaugaensis and ‘Strophitus’ subvexus. Strophitus radiatus exists in six well-supported clades that were distinguished as evolutionary independent lineages using Bayesian inference, maximum likelihood, and coalescent-based species delimitation models. Our integrative approach found evidence for as many as 4 evolutionary divergent clades within S. radiatus. Therefore, we formally describe two new species from the S. radiatus species complex (Strophitus williamsi and Strophitus pascagoulaensis) and recognize the potential for a third putative species (Strophitus sp. cf. pascagoulaensis). Our findings aid stakeholders in establishing conservation and management strategies for the members of Anodontoides, Strophitus, and Pseudodontoideus.

Alabama, Florida, Louisiana, Mississippi↗

Trait heritability and its implications for the management of an invasive vertebrate

Control methods that target specific traits of an invasive species can produce results contrary to the aims of management. If targeted phenotypes exhibit heritability, then it follows that the invasive species could evolve greater resistance to the applied control measures over time. Additional complications emerge if those traits targeted by control are also inversely related to reproductive success. Given this, prudent considerations for invasive species management are to quantify the heritability of traits selected through control measures and gauge their relationship with reproductive success. Herein we provide a case study utilizing long-term field data and a multi-generational pedigree of an experimentally-closed population of brown treesnakes (N = 426; Boiga irregularis ) on Guam. We employed an “animal model” to estimate the narrow-sense heritability ( h 2 ) for annual body condition, a trait related to both susceptibility to a primary tool used for brown treesnake control (i.e., live-lure traps) and annual reproductive success. Annual body condition displayed significant heritability [ h 2 = 0.149 (95% highest posterior density interval: 0.059–0.220)]. Considering a negative effect of body condition on susceptibility to trap capture but positive effect on reproductive success, significant heritability of body condition suggests the potential for live-lure traps to lose efficacy over time while also eliciting an undesirable effect on brown treesnake fecundity. Our results highlight the potential for negative repercussions that can stem from management actions, while also serving to underscore the evolutionary implications that are often overlooked but subsumed within invasive species control.

Biological Invasions↗

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↗

Using landscape genomics to delineate future adaptive potential for climate change in the Yosemite toad (Anaxyrus canorus)

An essential goal in conservation biology is delineating population units that maximize the probability of species persisting into the future and adapting to future environmental change. However, future-facing conservation concerns are often addressed using retrospective patterns that could be irrelevant. We recommend a novel landscape genomics framework for delineating future “Geminate Evolutionary Units” (GEUs) in a focal species: (1) identify loci under environmental selection, (2) model and map adaptive conservation units that may spawn future lineages, (3) forecast relative selection pressures on each future lineage, and (4) estimate their fitness and likelihood of persistence using geo-genomic simulations. Using this process, we delineated conservation units for the Yosemite toad ( Anaxyrus canorus ), a U.S. federally threatened species that is highly vulnerable to climate change. We used a genome-wide dataset, redundancy analysis, and Bayesian association methods to identify 24 candidate loci responding to climatic selection ( R 2 ranging from 0.09 to 0.52), after controlling for demographic structure. Candidate loci included genes such as MAP3K5, involved in cellular response to environmental change. We then forecasted future genomic response to climate change using the multivariate machine learning algorithm Gradient Forests. Based on all available evidence, we found three GEUs in Yosemite National Park, reflecting contrasting adaptive optima: YF-North (high winter snowpack with moderate summer rainfall), YF-East (low to moderate snowpack with high summer rainfall), and YF-Low-Elevation (low snowpack and rainfall). Simulations under the RCP 8.5 climate change scenario suggest that the species will decline by 29% over 90 years, but the highly diverse YF-East lineage will be least impacted for two reasons: (1) geographically it will be sheltered from the largest climatic selection pressures, and (2) its standing genetic diversity will promote a faster adaptive response. Our approach provides a comprehensive strategy for protecting imperiled non-model species with genomic data alone and has wide applicability to other declining species.

California↗

Divergence and gene flow in the globally distributed blue-winged ducks

The ability to disperse over long distances can result in a high propensity for colonizing new geographic regions, including uninhabited continents, and lead to lineage diversification via allopatric speciation. However, high vagility can also result in gene flow between otherwise allopatric populations, and in some cases, parapatric or divergence-with-gene-flow models might be more applicable to widely distributed lineages. Here, we use five nuclear introns and the mitochondrial control region along with Bayesian models of isolation with migration to examine divergence, gene flow, and phylogenetic relationships within a cosmopolitan lineage comprising six species, the blue-winged ducks (genus Anas), which inhabit all continents except Antarctica. We found two primary sub-lineages, the globally-distributed shoveler group and the New World blue-winged/cinnamon teal group. The blue-winged/cinnamon sub-lineage is composed of sister taxa from North America and South America, and taxa with parapatric distributions are characterized by low to moderate levels of gene flow. In contrast, our data support strict allopatry for most comparisons within the shovelers. However, we found evidence of gene flow from the migratory, Holarctic northern shoveler (A. clypeata) and the more sedentary, African Cape shoveler (A. smithii) into the Australasian shoveler (A. rhynchotis), although we could not reject strict allopatry. Given the diverse mechanisms of speciation within this complex, the shovelers and blue-winged/cinnamon teals can serve as an effective model system for examining how the genome diverges under different evolutionary processes and how genetic variation is partitioned among highly dispersive taxa.

Journal of Avian 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↗

Adjusting the lens of invasion biology to focus on the impacts of climate-driven range shifts

As Earth’s climate rapidly changes, species range shifts are considered key to species persistence. However, some range-shifting species will alter community structure and ecosystem processes. By adapting existing invasion risk assessment frameworks, we can identify characteristics shared with high-impact introductions and thus predict potential impacts. There are fundamental differences between introduced and range-shifting species, primarily shared evolutionary histories between range shifters and their new community. Nevertheless, impacts can occur via analogous mechanisms, such as wide dispersal, community disturbance and low biotic resistance. As ranges shift in response to climate change, we have an opportunity to develop plans to facilitate advantageous movements and limit those that are problematic.

Nature Climate Change↗

Insular biogeographic origins and high phylogenetic distinctiveness for a recently depleted lizard fauna from Christmas Island, Australia

Striking faunal turnover across Asia and Australasia, most famously along the eastern edge of the Sunda Shelf or ‘Wallace's Line’, has been a focus of biogeographic research for over 150 years. Here, we investigate the origins of a highly threatened endemic lizard fauna (four species) on Christmas Island. Despite occurring less 350 km south of the Sunda Shelf, this fauna mostly comprises species from clades centred on the more distant regions of Wallacea, the Pacific and Australia (more than 1000 km east). The three most divergent lineages show Miocene (approx. 23–5 Ma) divergences from sampled relatives; and have recently become extinct or extinct in the wild, likely owing to the recent introduction of a southeast Asian snake ( Lycodon capucinus ). Insular distributions, deep phylogenetic divergence and recent decline suggest that rather than dispersal ability or recent origins, environmental and biotic barriers have impeded these lineages from diversifying on the continental Sunda Shelf, and thereby, reinforced faunal differentiation across Wallace's Line. Our new phylogenetically informed perspective further highlights the rapid loss of ancient lineages that has occurred on Christmas Island, and underlines how the evolutionary divergence and vulnerability of many island-associated lineages may continue to be underestimated.

Christmas Island↗

The expectations and challenges of wildlife disease research in the era of genomics: Forecasting with a horizon scan-like exercise

The outbreak and transmission of disease-causing pathogens are contributing to the unprecedented rate of biodiversity decline. Recent advances in genomics have coalesced into powerful tools to monitor, detect, and reconstruct the role of pathogens impacting wildlife populations. Wildlife researchers are thus uniquely positioned to merge ecological and evolutionary studies with genomic technologies to exploit unprecedented ‘Big Data’ tools in disease research; however, many researchers lack the training and expertise required to use these computationally intensive methodologies. To address this disparity, the inaugural ‘Genomics of Disease in Wildlife’ workshop assembled early to mid-career professionals with expertise across scientific disciplines (e.g., genomics, wildlife biology, veterinary sciences, and conservation management) for training in the application of genomic tools to wildlife disease research. A horizon scanning-like exercise, an activity to identify forthcoming trends and challenges, performed by the workshop participants identified and discussed five themes considered to be the most pressing to the application of genomics in wildlife disease research: i) “Improving Communication”, ii) “Methodological and Analytical Advancements”, iii) “Translation into Practice”, iv) “Integrating Landscape Ecology and Genomics”, and v) “Emerging New Questions”. Wide-ranging solutions from the horizon scan were international in scope, itemized both deficiencies and strengths in wildlife genomic initiatives, promoted the use of genomic technologies to unite wildlife and human disease research, and advocated best practices for optimal use of genomic tools in wildlife disease projects. The results offer a glimpse of the potential revolution in human and wildlife disease research possible through multi-disciplinary collaborations at local, regional, and global scales.

Journal of Heredity↗

Long-term isolation of a highly mobile seabird on the Galapagos

The Galapagos Islands are renowned for their high degree of endemism. Marine taxa inhabiting the archipelago might be expected to be an exception, because of their utilization of pelagic habitats—the dispersal barrier for terrestrial taxa—as foraging grounds. Magnificent frigatebirds ( Fregata magnificens ) have a highly vagile lifestyle and wide geographical distribution around the South and Central American coasts. Given the potentially high levels of gene flow among populations, the species provides a good test of the effectiveness of the Galapagos ecosystem in isolating populations of highly dispersive marine species. We studied patterns of genetic (mitochondrial DNA, microsatellites and nuclear introns) and morphological variation across the distribution of magnificent frigatebirds. Concordant with predictions from life-history traits, we found signatures of extensive gene flow over most of the range, even across the Isthmus of Panama, which is a major barrier to gene flow in other tropical seabirds. In contrast, individuals from the Galapagos were strongly differentiated from all conspecifics, and have probably been isolated for several hundred thousand years. Our finding is a powerful testimony to the evolutionary uniqueness of the taxa inhabiting the Galapagos archipelago and its associated marine ecosystems.

Galapagos Islands↗

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↗

Conditions favouring Bromus tectorum dominance of endangered sagebrush steppe ecosystems

1. Ecosystem invasibility is determined by combinations of environmental variables, invader attributes, disturbance regimes, competitive abilities of resident species and evolutionary history between residents and disturbance regimes. Understanding the relative importance of each factor is critical to limiting future invasions and restoring ecosystems. 2. We investigated factors potentially controlling Bromus tectorum invasions into Artemisia tridentata ssp. wyomingensis communities across 75 sites in the Great Basin. We measured soil texture, cattle grazing intensity, gaps among perennial plants and plant cover including B. tectorum, biological soil crusts (BSCs) and bare soil. Using a priori knowledge, we developed a multivariate hypothesis of the susceptibility of Artemisia ecosystems to B. tectorum invasion and used the model to assess the relative importance of the factors driving the magnitude of such invasions. 3. Model results imply that bunchgrass community structure, abundance and composition, along with BSC cover, play important roles in controlling B. tectorum dominance. Evidence suggests abundant bunchgrasses limit invasions by limiting the size and connectivity of gaps between vegetation, and BSCs appear to limit invasions within gaps. Results also suggest that cattle grazing reduces invasion resistance by decreasing bunchgrass abundance, shifting bunchgrass composition, and thereby increasing connectivity of gaps between perennial plants while trampling further reduces resistance by reducing BSC. 4. Synthesis and applications. Grazing exacerbates Bromus tectorum dominance in one of North America's most endangered ecosystems by adversely impacting key mechanisms mediating resistance to invasion. If the goal is to conserve and restore resistance of these systems, managers should consider maintaining or restoring: (i) high bunchgrass cover and structure characterized by spatially dispersed bunchgrasses and small gaps between them; (ii) a diverse assemblage of bunchgrass species to maximize competitive interactions with B. tectorum in time and space; and (iii) biological soil crusts to limit B. tectorum establishment. Passive restoration by reducing cumulative cattle grazing may be one of the most effective means of achieving these three goals.

Journal of Applied Ecology↗

Thiamine deficiency in fishes: Causes, consequences, and potential solutions

Thiamine deficiency complex (TDC) is a disorder resulting from the inability to acquire or retain thiamine (vitamin B 1 ) and has been documented in organisms in aquatic ecosystems ranging from the Baltic Sea to the Laurentian Great Lakes. The biological mechanisms leading to TDC emergence may vary among systems, but in fishes, one common outcome is high mortality among early life stages. Here, we review the causes and consequences of thiamine deficiency in fishes and identify potential solutions. First, we examine the biochemical and physiological roles of thiamine in vertebrates and find that thiamine deficiency consistently results in impaired neurological function across diverse taxa. Next, we review natural producers of thiamine, which include bacteria, fungi, and plants, and suggest that thiamine is not currently limiting for most animal species inhabiting natural aquatic environments. A survey of historic occurrences of thiamine deficiency identifies consumption of a thiamine-degrading enzyme, thiaminase, as the primary explanation for low levels of thiamine in individuals and subsequent onset of TDC. Lastly, we review conservation and management strategies for TDC mitigation ranging from evolutionary rescue to managing for a diverse forage base. As recent evidence suggests occurrences of thiamine deficiency may be increasing in frequency, increased awareness and a better mechanistic understanding of the underlying causes associated with thiamine deficiency may help prevent further population declines.

Reviews in Fish Biology and Fisheries↗

DNA-based studies and genetic diversity indicator assessments are complementary approaches to conserving evolutionary potential

Genetic diversity is essential for maintaining healthy populations and ecosystems. Several approaches have recently been developed to evaluate population genetic trends without necessarily collecting new genetic data. Such “genetic diversity indicators” enable rapid, large-scale evaluation across dozens to thousands of species. Empirical genetic studies, when available, provide detailed information that is important for management, such as estimates of gene flow, inbreeding, genetic erosion and adaptation. In this article, we argue that the development and advancement of genetic diversity indicators is a complementary approach to genetic studies in conservation biology, but not a substitute. Genetic diversity indicators and empirical genetic data can provide different information for conserving genetic diversity. Genetic diversity indicators enable affordable tracking, reporting, prioritization and communication, although, being proxies, do not provide comprehensive evaluation of the genetic status of a species. Conversely, genetic methods offer detailed analysis of the genetic status of a given species or population, although they remain challenging to implement for most species globally, given current capacity and resourcing. We conclude that indicators and genetic studies are both important for genetic conservation actions and recommend they be used in combination for conserving and monitoring genetic diversity.

Conservation Genetics↗

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↗

Introduced species as evolutionary traps

Invasive species can alter environments in such a way that normal behavioural decision-making rules of native species are no longer adaptive. The evolutionary trap concept provides a useful framework for predicting and managing the impact of harmful invasive species. We discuss how native species can respond to changes in their selective regime via evolution or learning. We also propose novel management strategies to promote the long-term co-existence of native and introduced species in cases where the eradication of the latter is either economically or biologically unrealistic.

Ecology Letters↗

Closure of the Isthmus of Panama: The near-shore marine record of Costa Rica and western Panama

The final closure of the Isthmus of Panama at ∼3.5 Ma divided the American tropical ocean into two separate and different oceanographic regions. Consequences for the marine biota were profound, but, hitherto, correlation of the Pacific and Caribbean coastal sections has not been precise enough to track biologic patterns. We present here a correlation of 31 sections from the Pacific and Caribbean coasts of Costa Rica and western Panama. Using calcareous nannofossils and planktonic foraminifera at both the tops and bottoms of each formation, we estimate that the Caribbean section ranges from 8.2 Ma to 1.7 Ma; and the Pacific sequence, from 3.6 Ma to <1.7 Ma. These intervals bracket postulated dates for final closure of the Isthmus and provide the first well-dated record of middle and late Pliocene faunas from the region. The Caribbean and Pacific sections include very different environments of deposition, yet there is sufficient overlap and diversity of habitats to permit meaningful biological comparisons. On the Caribbean side, formations tied together by the overlap of the upper Pliocene markers Sphenolithus abies and Pseudoemiliana lacunosa (3.5 Ma to 3.6 Ma) range from very shallow to shallow inner shelf (<200 m) and upper slope (200-800 m). The Pacific coast sections were mostly deposited in a trench slope environment, which is absent on the Caribbean side. These sections fortuitously include abundant thick intra-formational slumps containing shallow-water fauna more appropriate for biological comparison with the Caribbean biota. Similarly, the ∼1.9 Ma to 1.5 Ma interval, well constrained by various taxa, includes middle- to outer-shelf, and inner-shelf to upper-slope deposits on the Caribbean side, and marginal-marine to inner-shelf deposits on the Pacific coast. Using our new biostratigraphic framework to correlate previously poorly constrained mollusc collections, we show that evolutionary divergence of the Pacific and Caribbean near-shore marine faunas had occurred by 3.5 Ma. This strongly suggests that the Isthmus was effectively closed by this time.

GSA Bulletin↗