Opposing Responses to Scarcity Emerge from Functionally Unique Sociality Drivers.

AbstractFrom biofilms to whale pods, organisms across taxa live in groups, thereby accruing numerous diverse benefits of sociality. All social organisms, however, pay the inherent cost of increased resource competition. One expects that when resources become scarce, this cost will increase, causing group sizes to decrease. Indeed, this occurs in some species, but there are also species for which group sizes remain stable or even increase under scarcity. What accounts for these opposing responses? We present a conceptual framework, literature review, and theoretical model demonstrating that differing responses to sudden resource shifts can be explained by which sociality benefit exerts the strongest selection pressure on a particular species. We categorize resource-related benefits of sociality into six functionally distinct classes and model their effect on the survival of individuals foraging in groups under different resource conditions. We find that whether, and to what degree, the optimal group size (or correlates thereof) increases, decreases, or remains constant when resource abundance declines depends strongly on the dominant sociality mechanism. Existing data, although limited, support our model predictions. Overall, we show that across a wide diversity of taxa, differences in how group size shifts in response to resource declines can be driven by differences in the primary benefits of sociality.

How genomics can help biodiversity conservation.

The availability of public genomic resources can greatly assist biodiversity assessment, conservation, and restoration efforts by providing evidence for scientifically informed management decisions. Here we survey the main approaches and applications in biodiversity and conservation genomics, considering practical factors, such as cost, time, prerequisite skills, and current shortcomings of applications. Most approaches perform best in combination with reference genomes from the target species or closely related species. We review case studies to illustrate how reference genomes can facilitate biodiversity research and conservation across the tree of life. We conclude that the time is ripe to view reference genomes as fundamental resources and to integrate their use as a best practice in conservation genomics.

Warming Accelerates the Onset of the Molecular Stress Response and Increases Mortality of Larval Atlantic Cod.

Temperature profoundly affects ectotherm physiology. Although differential thermal responses influence fitness, thus driving population dynamics and species distributions, our understanding of the molecular architecture underlying these responses is limited, especially during the critical larval stage. Here, using RNA-sequencing of laboratory-reared Atlantic cod (Gadus morhua) larvae of wild origin, we find changes in gene expression in thousands of transcripts consistent with a severe cellular stress response at both ambient and projected (+2°C and +4°C) temperatures. In addition, specific responses to stress, heat, and hypoxia were commonly identified in gene ontology enrichment analyses and 33 of the 44 genes comprising the minimum stress proteome of all organisms were upregulated. Earlier onset of the stress response was evident at higher temperatures; concomitant increased growth and mortality suggests a reduction in fitness. Temporal differences in gene expression levels do not correspond to differences in growing degree days, suggesting negative physiological consequences of warming beyond accelerated development. Because gene expression is costly, we infer that the upregulation of thousands of transcripts in response to warming in larval cod might act as an energetic drain. We hypothesize that the energetically costly stress response, coupled with increased growth rate at warmer temperatures, leads to faster depletion of energy reserves and increased risk of mortality in larval cod. As sea surface temperatures continue to rise over the next century, reduced fitness of Atlantic cod larvae might lead to population declines in this ecologically and socioeconomically important species. Further, our findings expand our understanding of transcriptomic responses to temperature by ectothermic vertebrate larvae beyond the critical first-feeding stage, a time when organisms begin balancing the energetic demands of growth, foraging, development, and maintenance. Linking the molecular basis of a thermal response to key fitness-related traits is fundamentally important to predicting how global warming will affect ectotherms.

Genomic reaction norms inform predictions of plastic and adaptive responses to climate change.

Genomic reaction norms represent the range of gene expression phenotypes (usually mRNA transcript levels) expressed by a genotype along an environmental gradient. Reaction norms derived from common-garden experiments are powerful approaches for disentangling plastic and adaptive responses to environmental change in natural populations. By treating gene expression as a phenotype in itself, genomic reaction norms represent invaluable tools for exploring causal mechanisms underlying organismal responses to climate change across multiple levels of biodiversity. Our goal is to provide the context, framework and motivation for applying genomic reaction norms to study the responses of natural populations to climate change. Here, we describe the utility of integrating genomics with common-garden-gradient experiments under a reaction norm analytical framework to answer fundamental questions about phenotypic plasticity, local adaptation, their interaction (i.e. genetic variation in plasticity) and future adaptive potential. An experimental and analytical framework for constructing and analysing genomic reaction norms is presented within the context of polygenic climate change responses of structured populations with gene flow. Intended for a broad eco-evo readership, we first briefly review adaptation with gene flow and the importance of understanding the genomic basis and spatial scale of adaptation for conservation and management of structured populations under anthropogenic change. Then, within a high-dimensional reaction norm framework, we illustrate how to distinguish plastic, differentially expressed (difference in reaction norm intercepts) and differentially plastic (difference in reaction norm slopes) genes, highlighting the areas of opportunity for applying these concepts. We conclude by discussing how genomic reaction norms can be incorporated into a holistic framework to understand the eco-evolutionary dynamics of climate change responses from molecules to ecosystems. We aim to inspire researchers to integrate gene expression measurements into common-garden experimental designs to investigate the genomics of climate change responses as sequencing costs become increasingly accessible.

FishSizer: Software solution for efficiently measuring larval fish size.

Length and depth of fish larvae are part of the fundamental measurements in many marine ecology studies involving early fish life history. Until now, obtaining these measurements has required intensive manual labor and the risk of inter- and intra-observer variability.We developed an open-source software solution to semi-automate the measurement process and thereby reduce both time consumption and technical variability. Using contrast-based edge detection, the software segments images of a fish larva into "larva" and "background." Length and depth are extracted from the "larva" segmentation while taking curvature of the larva into consideration. The graphical user interface optimizes workflow and ease of usage, thereby reducing time consumption for both training and analysis. The software allows for visual verification of all measurements.A comparison of measurement methods on a set of larva images showed that this software reduces measurement time by 66%-78% relative to commonly used software.Using this software instead of the commonly used manual approach has the potential to save researchers from many hours of monotonous work. No adjustment was necessary for 89% of the images regarding length (70% for depth). Hence, the only workload on most images was the visual inspection. As the visual inspection and manual dimension extraction works in the same way as currently used software, we expect no loss in accuracy.

The era of reference genomes in conservation genomics.

Progress in genome sequencing now enables the large-scale generation of reference genomes. Various international initiatives aim to generate reference genomes representing global biodiversity. These genomes provide unique insights into genomic diversity and architecture, thereby enabling comprehensive analyses of population and functional genomics, and are expected to revolutionize conservation genomics.

Preprinting is positively associated with early career researcher status in ecology and evolution.

The usage of preprint servers in ecology and evolution is increasing, allowing research to be rapidly disseminated and available through open access at no cost. Early Career Researchers (ECRs) often have limited experience with the peer review process, which can be challenging when trying to build publication records and demonstrate research ability for funding opportunities, scholarships, grants, or faculty positions. ECRs face different challenges relative to researchers with permanent positions and established research programs. These challenges might also vary according to institution size and country, which are factors associated with the availability of funding for open access journals. We predicted that the career stage and institution size impact the relative usage of preprint servers among researchers in ecology and evolution. Using data collected from 500 articles (100 from each of two open access journals, two closed access journals, and a preprint server), we showed that ECRs generated more preprints relative to non-ECRs, for both first and last authors. We speculate that this pattern is reflective of the advantages of quick and open access research that is disproportionately beneficial to ECRs. There is also a marginal association between first author, institution size, and preprint usage, whereby the number of preprints tends to increase with institution size for ECRs. The United States and United Kingdom contributed the greatest number of preprints by ECRs, whereas non-Western countries contributed relatively fewer preprints. This empirical evidence that preprint usage varies with the career stage, institution size, and country helps to identify barriers surrounding large-scale adoption of preprinting in ecology and evolution.

Consequences of Single-Locus and Tightly Linked Genomic Architectures for Evolutionary Responses to Environmental Change.

Genetic and genomic architectures of traits under selection are key factors influencing evolutionary responses. Yet, knowledge of their impacts has been limited by a widespread assumption that most traits are controlled by unlinked polygenic architectures. Recent advances in genome sequencing and eco-evolutionary modeling are unlocking the potential for integrating genomic information into predictions of population responses to environmental change. Using eco-evolutionary simulations, we demonstrate that hypothetical single-locus control of a life history trait produces highly variable and unpredictable harvesting-induced evolution relative to the classically applied multilocus model. Single-locus control of complex traits is thought to be uncommon, yet blocks of linked genes, such as those associated with some types of structural genomic variation, have emerged as taxonomically widespread phenomena. Inheritance of linked architectures resembles that of single loci, thus enabling single-locus-like modeling of polygenic adaptation. Yet, the number of loci, their effect sizes, and the degree of linkage among them all occur along a continuum. We review how linked architectures are often associated, directly or indirectly, with traits expected to be under selection from anthropogenic stressors and are likely to play a large role in adaptation to environmental disturbance. We suggest using single-locus models to explore evolutionary extremes and uncertainties when the trait architecture is unknown, refining parameters as genomic information becomes available, and explicitly incorporating linkage among loci when possible. By overestimating the complexity (e.g., number of independent loci) of the genomic architecture of traits under selection, we risk underestimating the complexity (e.g., nonlinearity) of their evolutionary dynamics.

A Roadmap for Understanding the Evolutionary Significance of Structural Genomic Variation.

Structural genomic variants (SVs) are ubiquitous and play a major role in adaptation and speciation. Yet, comparative and population genomics have focused predominantly on gene duplications and large-effect inversions. The lack of a common framework for studying all SVs is hampering progress towards a more systematic assessment of their evolutionary significance. Here we (i) review how different types of SVs affect ecological and evolutionary processes; (ii) suggest unifying definitions and recommendations for future studies; and (iii) provide a roadmap for the integration of SVs in ecoevolutionary studies. In doing so, we lay the foundation for population genomics, theoretical, and experimental approaches to understand how the full spectrum of SVs impacts ecological and evolutionary processes.

Fine-scale population differences in Atlantic cod reproductive success: A potential mechanism for ecological speciation in a marine fish.

Successful resource-management and conservation outcomes ideally depend on matching the spatial scales of population demography, local adaptation, and threat mitigation. For marine fish with high dispersal capabilities, this remains a fundamental challenge. Based on daily parentage assignments of more than 4,000 offspring, we document fine-scaled temporal differences in individual reproductive success for two spatially adjacent (<10 km) populations of a broadcast-spawning marine fish. Distinguished by differences in genetics and life history, Atlantic cod (Gadus morhua) from inner- and outer-fjord populations were allowed to compete for mating and reproductive opportunities. After accounting for phenotypic variability in several traits, reproductive success of outer-fjord cod was significantly lower than that of inner-fjord cod. This finding, given that genomically different cod ecotypes inhabit inner- and outer-fjord waters, raises the intriguing hypothesis that the populations might be diverging because of ecological speciation. Individual reproductive success, skewed within both sexes (more so among males), was positively affected by body size, which also influenced the timing of reproduction, larger individuals spawning later among females but earlier among males. Our work suggests that spatial mismatches between management and biological units exist in marine fishes and that studies of reproductive interactions between putative populations or ecotypes can provide an informative basis on which determination of the scale of local adaptation can be ascertained.

Variation in spawning time promotes genetic variability in population responses to environmental change in a marine fish.

The level of phenotypic plasticity displayed within a population (i.e. the slope of the reaction norm) reflects the short-term response of a population to environmental change, while variation in reaction norm slopes among populations reflects spatial variation in these responses. Thus far, studies of thermal reaction norm variation have focused on geographically driven adaptation among different latitudes, altitudes or habitats. Yet, thermal variability is a function of both space and time. For organisms that reproduce at different times of year, such variation has the potential to promote adaptive variability in thermal responses for critical early life stages. Using common-garden experiments, we examined the spatial scale of genetic variation in thermal plasticity for early life-history traits among five populations of endangered Atlantic cod (Gadus morhua) that spawn at different times of year. Patterns of plasticity for larval growth and survival suggest that population responses to climate change will differ substantially, with increasing water temperatures posing a considerably greater threat to autumn-spawning cod than to those that spawn in winter or spring. Adaptation to seasonal cooling or warming experienced during the larval stage is suggested as a possible cause. Furthermore, populations that experience relatively cold temperatures during early life might be more sensitive to changes in temperature. Substantial divergence in adaptive traits was evident at a smaller spatial scale than has previously been shown for a marine fish with no apparent physical barriers to gene flow (∼200 km). Our findings highlight the need to consider the impact of intraspecific variation in reproductive timing on thermal adaptation when forecasting the effects of climate change on animal populations.

Comparison of 454 pyrosequencing methods for characterizing the major histocompatibility complex of nonmodel species and the advantages of ultra deep coverage.

Characterization and population genetic analysis of multilocus genes, such as those found in the major histocompatibility complex (MHC) is challenging in nonmodel vertebrates. The traditional method of extensive cloning and Sanger sequencing is costly and time-intensive and indirect methods of assessment often underestimate total variation. Here, we explored the suitability of 454 pyrosequencing for characterizing multilocus genes for use in population genetic studies. We compared two sample tagging protocols and two bioinformatic procedures for 454 sequencing through characterization of a 185-bp fragment of MHC DRB exon 2 in wolverines (Gulo gulo) and further compared the results with those from cloning and Sanger sequencing. We found 10 putative DRB alleles in the 88 individuals screened with between two and four alleles per individual, suggesting amplification of a duplicated DRB gene. In addition to the putative alleles, all individuals possessed an easily identifiable pseudogene. In our system, sequence variants with a frequency below 6% in an individual sample were usually artefacts. However, we found that sample preparation and data processing procedures can greatly affect variant frequencies in addition to the complexity of the multilocus system. Therefore, we recommend determining a per-amplicon-variant frequency threshold for each unique system. The extremely deep coverage obtained in our study (approximately 5000×) coupled with the semi-quantitative nature of pyrosequencing enabled us to assign all putative alleles to the two DRB loci, which is generally not possible using traditional methods. Our method of obtaining locus-specific MHC genotypes will enhance population genetic analyses and studies on disease susceptibility in nonmodel wildlife species.

Mitochondrial evidence for panmixia despite perceived barriers to gene flow in a widely distributed waterbird.

We examined the mitochondrial genetic structure of American white pelicans (Pelecanus erythrorhynchos) to: 1) verify or refute whether American white pelicans are panmictic and 2) understand if any lack of genetic structure is the result of contemporary processes or historical phenomena. Sequence analysis of mitochondrial DNA control region haplotypes of 367 individuals from 19 colonies located across their North American range revealed a lack of population genetic or phylogeographic structure. This lack of structure was unexpected because: 1) Major geographic barriers such as the North American Continental Divide are thought to limit dispersal; 2) Differences in migratory behavior are expected to promote population differentiation; and 3) Many widespread North American migratory bird species show historic patterns of differentiation resulting from having inhabited multiple glacial refugia. Further, high haplotype diversity and many rare haplotypes are maintained across the species' distribution, despite frequent local extinctions and recolonizations that are expected to decrease diversity. Our findings suggest that American white pelicans have a high effective population size and low natal philopatry. We suggest that the rangewide panmixia we observed in American white pelicans is due to high historical and contemporary gene flow, enabled by high mobility and a lack of effective physical or behavioral barriers.