In species with separate sexes, the selection on males causes evolutionary change in female traits values (and vice versa) via genetic correlations, which has far-reaching consequences for adaptation. Here, we utilize a sex-specific form of Robertson's Secondary Theorem of Natural Selection to estimate the expected response to selection for 474 organismal-level traits and similar to 28,000 gene expression traits measured in the Drosophila Genetic Reference Panel (DGRP). Across organismal-level traits, selection acting on males produced a larger predicted evolutionary response than did selection acting on females, even for female traits; while for transcriptome traits selection on each sex produced a roughly equal average evolutionary response. For most traits, the selection on males and females was predicted to move average trait values in the same direction, though for some traits, the selection on one sex increased trait values while the selection on the other sex decreased them, implying intralocus sexual conflict. Our results provide support for the hypothesis that males experience stronger selection than females, potentially accelerating adaptation in females. Furthermore, sex-opposite responses to selection appear to exist for only a small proportion of traits, consistent with observations that the intersex genetic correlation for fitness is positive but less than one in most populations so far studied.
Human activities are affecting marine biodiversity globally by accelerating extinction rates, altering ecosystem conditions and changing community structures. These changes can only be understood through establishing the ecosystem state prior to significant anthropogenic impact and by disentangling the anthropogenic effect from natural climatic changes. Here, we reconstruct marine biodiversity in Iceland across three millennia (1315 BCE-1785 CE), encompassing periods of climatic fluctuation and human settlement, to explore the comparative effect of natural and anthropogenic forces on marine biodiversity. We performed 18S metabarcoding of ancient environmental DNA from two sediment cores collected from northern Icelandic shelf seas, integrating local climatic records, population estimates and zooarchaeological remains from published sources to estimate the influence of climatic and anthropogenic impacts. Against the backdrop of increasing human populations and marine exploitation, we observe no large-scale taxonomic shifts or anthropogenic biodiversity changes across the period. In contrast, we found a positive correlation between herring (Clupea harengus) detection rates and proxy-reconstructed sea surface temperature, suggesting a role for climate in shaping marine biodiversity. Overall, our data suggest that despite impacts on terrestrial ecosystems and the development of a substantial export fishery across the study period, Icelandic society may have had a limited effect on marine biodiversity.This article is part of the theme issue 'Shifting seas: understanding deep-time human impacts on marine ecosystems'.
Effective biodiversity survey methods are crucial for monitoring ecosystems threatened by climatic fluctuations and anthropogenic pressures. Here we advance methods for the collection of a novel source of biodiversity data - airborne environmental DNA (eDNA) - and investigate whether it yields habitat- and season-specific signatures of terrestrial vertebrate communities. Using portable and low budget samplers, we sampled airborne eDNA in three protected nature areas across Denmark and show that air filters with a large surface area and the widest range of particle retention sizes yield detections of higher numbers of vertebrate taxa and show higher community homogeneity across samples. Further, we show that increased airflow rate and dry storage of filters − 20°C yield detections of more diverse and consistent vertebrate communities. Overall, we demonstrate that airborne eDNA yields robust detections of spatio-temporal dynamics across terrestrial vertebrate classes, which can be adapted by conservation programs to monitor terrestrial biodiversity across the globe.
ABSTRACT The condition of ancient marine ecosystems provides context for contemporary biodiversity changes in human‐impacted oceans. Sequencing sedimentary ancient DNA (sedaDNA) is an emerging method for generating high‐resolution biodiversity time‐series data, offering insights into past ecosystems. However, few studies directly compare the two predominant sedaDNA sequencing approaches: metabarcoding and shotgun‐metagenomics, and it remains unclear if these methodological differences affect diversity metrics. We compared these methods using sedaDNA from an archived marine sediment record sampled in the Skagerrak, North Sea, spanning almost 8000 years. We performed metabarcoding of a eukaryotic 18S rRNA region (V9) and sequenced 153–229 million metagenomic reads per sample. Our results show limited overlap between metabarcoding and metagenomics, with only three metazoan genera detected by both methods. For overlapping taxa, metabarcoding detections became inconsistent for samples older than 2000 years, while metagenomics detected taxa throughout the time series. We observed divergent patterns of alpha diversity, with metagenomics indicating decreased richness towards the present and metabarcoding showing an increase. However, beta diversity patterns were similar between methods, with discrepancies only in metazoan data comparisons. Our findings demonstrate that the choice of sequencing method significantly impacts detected biodiversity in an ancient marine sediment record. While we stress that studies with limited variation in DNA degradation among samples may not be strongly affected, researchers should exonerate methodological explanations for observed biodiversity changes in marine sediment cores, particularly when considering alpha diversity, before making ecological interpretations.
Central European forests have been shaped by complex human interactions throughout the Holocene, with significant changes following the introduction of domesticated animals in the Neolithic (∼7.5-6.0 ka before present [BP]). However, understanding early pastoral practices and their impact on forests is limited by methods for detecting animal movement across past landscapes. Here, we examine ancient sedimentary DNA (sedaDNA) preserved at the Velký Mamuťák rock shelter in northern Bohemia (Czech Republic), which has been a forested enclave since the early Holocene. We find that domesticated animals, their associated microbiomes, and plants potentially gathered for fodder have clear representation by the Late Neolithic, around 6.0 ka BP, and persist throughout the Bronze Age into recent times. We identify a change in dominant grazing species from sheep to pigs in the Bronze Age (∼4.1-3.0 ka BP) and interpret the impact this had in the mid-Holocene retrogressions that still define the structure of Central European forests today. This study highlights the ability of ancient metagenomics to bridge archaeological and paleoecological methods and provide an enhanced perspective on the roots of the "Anthropocene."
RNA sequencing (RNAseq) methodology has experienced a burst of technological developments in the last decade, which has opened up opportunities for studying the mechanisms of adaptation to environmental factors at both the organismal and cellular level. Selecting the most suitable experimental approach for specific research questions and model systems can, however, be a challenge and researchers in ecology and evolution are commonly faced with the choice of whether to study gene expression variation in whole bodies, specific tissues, and/or single cells. A wide range of sometimes polarised opinions exists over which approach is best. Here, we highlight the advantages and disadvantages of each of these approaches to provide a guide to help researchers make informed decisions and maximise the power of their study. Using illustrative examples of various ecological and evolutionary research questions, we guide the readers through the different RNAseq approaches and help them identify the most suitable design for their own projects.
Uncovering the drivers that shape biodiversity patterns is critical to understand fundamental ecological and evolutionary processes, but also to assist biodiversity managers and conservation agencies. Despite evidence that biodiversity composition is influenced by processes at different spatial scales, little is known about the role of fine-scale oceanographic processes in controlling marine biodiversity patterns. This is particularly important in biodiversity hotspot regions, where small changes in local conditions may facilitate introductions of novel species, local extirpation, or even extinction. Here, we conducted oceanographic modelling and environmental DNA (eDNA) metabarcoding to investigate how fine-scale oceanographic processes shape marine biogeographic patterns across the Galápagos Islands. We found that eDNA data confirmed previously reported biogeographic regionalization, and demonstrated significant differences in community structure across the highly diverse oceanographic seascape of the Galápagos Islands. We then tested the effect of local current systems with a novel metric, termed oceanographic resistance, measuring the cumulative seawater flow resistance between pairs of geographic sites. Oceanographic resistance explained a significant proportion of variation in eDNA-measured beta dissimilarity between sites (2.0% of total), comparable in influence to some of the most important abiotic drivers, such as temperature (2.9%) and geographic distance between sites (11.5%). This indicates that oceanographic resistance can be a useful metric to understand the effects of current systems on marine biota. Taken together, our results indicate that marine communities are particularly sensitive to changes in local current systems, and suggest that fine-scale oceanographic processes may have an underappreciated role in structuring marine communities globally.### Competing Interest StatementThe authors have declared no competing interest.
There is a great diversity of eDNA metabarcoding studies in the literature and identifying how to design a survey to best suit your needs can be challenging. Design considerations are particularly important given that eDNA metabarcoding can be used to survey biodiversity across a breadth of environments and identifying taxa across the tree of life. Here, we highlight eight burgeoning areas of eDNA metabarcoding research: air, plant-pollinators, soil, diet, microbiome, freshwater, estuarine and marine. We highlight design considerations that are important for specific contexts, while also identifying common denominators across all eDNA metabarcoding surveys. In doing so, we hope to provide both a valuable introduction into eDNA metabarcoding survey design for beginners, gold standards of survey design, and fertile ground for collaboration between research areas which all fall under the umbrella of eDNA metabarcoding.
Selection varies between categories of individuals, with far-reaching ramifications: Sex-specific selection can impede or accelerate adaptation, and differences in selection between young and old individuals are ultimately responsible for senescence. Here, we measure early- and late-life fitness in adults of both sexes from the Drosophila genetic reference panel and perform quantitative genetic and transcriptomic analyses. Fitness was heritable, showed positive pleiotropy across sexes and age classes, and appeared to be influenced by very large numbers of loci with small effects plus a smaller number with moderate effects. Most loci affected male and female fitness in the same direction; relatively few candidate sexually antagonistic loci were found, though these were enriched on the X chromosome as predicted by theory. The expression level of many genes showed an opposite correlation with fitness in males and females, consistent with unresolved sexual conflict over transcription. The load of deleterious mutations correlated negatively with fitness across genotypes, and we found some evidence for the mutation accumulation (but not the antagonistic pleiotropy) theory of aging.
Central European forests have been shaped by complex human interactions throughout the Holocene, with significant changes following the introduction of domesticated animals in the Neolithic (∼7.5 – 6.0 kyr BP). However, understanding early pastoral practices and their impact on forests is limited by methods for detecting animal movement across past landscapes. Here we examine ancient sedimentary DNA ( seda DNA) preserved at the Velký Mamuťák rock shelter, in northern Bohemia (Czech Republic), which has been a forested enclave since the early Holocene. We find that domesticated animals, their associated microbiomes, and plants potentially gathered for fodder, have clear representation by the Late Neolithic, around 6.0 kyr BP, and persist throughout the Bronze Age into recent times. We identify a change in dominant grazing species from sheep to pigs in the Bronze Age (∼4.1 – 3.0 kyr BP) and interpret the impact this had in the mid-Holocene retrogressions that still define the structure of Central European forests today. This study highlights the ability of ancient metagenomics to bridge archaeological and paleoecological methods and provide an enhanced perspective on the roots of the Anthropocene.
How does nature change through time and across space? How might it change in the future? While time travel has long been the domain of science fiction, scientists have approached these questions using techniques that examine the traces of the past remaining in today's environment. The use of ancient environmental DNA (ancient eDNA) is the latest method for paleoenvironmental reconstruction in a line of ancient biomolecular research, with the first research into DNA barcoding appearing near the turn of the last century (Willerslev et al. 2003). This field has principally advanced through a combination of milestone discoveries and a technological revolution that ultimately transformed genetic and genomic analyses into the Big Data Science we recognise today (Fig. 13.1). But what has been the trajectory of this development, and perhaps more importantly, what future potential lies ahead for this research area?
Sex differences in the fitness effects of genetic variants can influence the rate of adaptation and the maintenance of genetic variation. For example, “sexually antagonistic” (SA) variants, which are beneficial for one sex and harmful for the other, can both constrain adaptation and increase genetic variability for fitness components such as survival, fertility, and disease susceptibility. However, detecting variants with sex-differential fitness effects is difficult, requiring genome sequences and fitness measurements from large numbers of individuals. Here, we develop new theory for studying sex-differential selection across a complete life cycle and test our models with genotypic and reproductive success data from approximately 250,000 UK Biobank individuals. We uncover polygenic signals of sex-differential selection affecting survival, reproductive success, and overall fitness, with signals of sex-differential reproductive selection reflecting a combination of SA polymorphisms and sexually concordant polymorphisms in which the strength of selection differs between the sexes. Moreover, these signals hold up to rigorous controls that minimise the contributions of potential confounders, including sequence mapping errors, population structure, and ascertainment bias. Functional analyses reveal that sex-differentiated sites are enriched in phenotype-altering genomic regions, including coding regions and loci affecting a range of quantitative traits. Population genetic analyses show that sex-differentiated sites exhibit evolutionary histories dominated by genetic drift and/or transient balancing selection, but not long-term balancing selection, which is consistent with theoretical predictions of effectively weak SA balancing selection in historically small populations. Overall, our results are consistent with polygenic sex-differential—including SA—selection in humans. Evidence for sex-differential selection is particularly strong for variants affecting reproductive success, in which the potential contributions of nonrandom sampling to signals of sex differentiation can be excluded.
Metagenomic data generated from environmental samples is increasingly common in the analysis of modern and ancient biological communities. To obtain taxonomic profiles from this type of data, DNA sequences are aligned against large genomic reference databases and the lowest common ancestor (LCA) needs to be inferred for each sequence with multiple alignments. To date, efforts have mainly focused on improving the speed, sensitivity and specificity of alignment tools, and little effort has been applied to the LCA algorithm that generates the taxonomic profiles from alignments. We present ngsLCA, a command‐line toolkit with two separate modules: the main program (in C/C++) performing LCA inference, and an R package for generating tables and visualisations of the taxonomic profiles. ngsLCA processed large datasets in BAM/SAM alignment format 4–11 times faster and used less memory compared to other available programs. It is compatible with the NCBI taxonomy and has flexible parameter settings. Furthermore, the toolkit offers functions for filtering, contamination removal, taxonomic clustering, and multiple ways of visualising the generated taxonomic profiles. ngsLCA bridges a gap in current metagenomic analyses by supplying a computationally light, easy‐to‐use, accurate, fast and flexible LCA algorithm with R functions for processing and illustrating the taxonomic profiles
The use of molecular tools to manage natural resources is increasingly common. However, DNA-based methods are seldom used to understand the spatial and temporal dynamics of species' range shifts. This is important when managing range shifting species such as non-native species (NNS), which can have negative impacts on biotic communities. Here, we investigated the ascidian NNS Ciona robusta, Clavelina lepadiformis, Microcosmus squamiger and Styela plicata using a combined methodological approach. We first conducted non-molecular biodiversity surveys for these NNS along the South African coastline, and compared the results with historical surveys. We detected no consistent change in range size across species, with some displaying range stability and others showing range shifts. We then sequenced a section of cytochrome c oxidase subunit I (COI) from tissue samples and found genetic differences along the coastline but no change over recent times. Finally, we found that environmental DNA metabarcoding data showed broad congruence with both the biodiversity survey and the COI datasets, but failed to capture the complete incidence of all NNS. Overall, we demonstrated how a combined methodological approach can effectively detect spatial and temporal variation in genetic composition and range size, which is key for managing both thriving NNS and threatened species. This article is part of the theme issue 'Species' ranges in the face of changing environments (part I)'.
Animals living in large colonies are especially vulnerable to infectious pathogens and may therefore have evolved additional defences. Eusocial insects supplement their physiological immune systems with ‘social immunity’, a set of adaptations that impedes the entrance, establishment, and spread of pathogens in the colony. We here find that honey bee workers ( Apis mellifera ) that had been experimentally immune-challenged with bacterial lipopolysaccharide (LPS) often exited the hive and subsequently died; some individuals were dragged out by other workers, while others appeared to leave voluntarily. In a second experiment, we found that healthy workers treated with surface chemicals from LPS-treated bees were evicted from the hive more often than controls, indicating that immune-challenged bees produce chemical cues or signals that elicit their eviction. Thirdly, we observed pairs of bees under lab conditions, and found that pairs spent more time apart when one member of the pair had received LPS, relative to controls. Our findings suggest that immune-challenged bees altruistically banish themselves, and that workers evict sick individuals which they identify using olfactory cues, putatively because of (kin) selection to limit the spread of pathogens within colonies. Significance statement Just as in humans, animals living in large groups must contend with infectious diseases. Social insects such as honey bees have evolved a range of behavioural and organisational defences against disease, collectively termed ‘social immunity’. Here, we describe experiments in which we introduced immune-stimulated bee workers into hives to study social immunity. We find that bees that were wounded or immune-challenged were more likely to leave the hive—resulting in their death—compared to healthy controls. Some of the bees leaving the hive were ejected by other workers, while some left the hive seemingly by choice: we thus find evidence for both ‘banishment’ of immune-challenged bees and self-imposed exile. Furthermore, using experiments transferring chemical signals between healthy and immune stimulated bees, we establish that the latter are identified for banishment by the chemicals present on their body surface.
© 2022 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. Correction to: ‘Managing humanmediatedrange shifts: understanding spatial,temporal and genetic variation in marinenon-native species’ (2022) by Holman et al.
AbstractThe detection of species using environmental DNA (eDNA) relies on our capacity to identify DNA from the sampled environment. Once eDNA is released into the environment, the physical degradation of individual eDNA molecules over time directly affects our ability to detect species (eDNA decay). Therefore, interpreting eDNA data requires an explicit understanding of eDNA decay to accurately infer contemporary presence or absence of a given species in the study ecosystem. Most research to date on eDNA decay has focused on single‐species assays (predominantly quantitative PCR), and thus little is known on how eDNA decay affects the interpretation of metabarcoding datasets. Here, we used eDNA metabarcoding (targeting a section of the eukaryotic cytochrome c oxidase subunit I gene) of water samples from controlled tanks to examine eDNA decay in a wide variety of marine metazoan species. After the stocked organisms were removed from these tanks, we observed a sharp decrease in amplicon sequence variant (ASV) richness within the first 48 hours. Furthermore, there was a substantial change in beta diversity between 24 and 48 hours, and after 48 hours, most stocked species became undetectable. Interestingly, the estimated decay rate for each study species, calculated using a linear regression of reads over time, differed across organisms, with up to 2–3‐fold difference among species. Our results showed that, for marine temperate species, the most substantial change in eDNA metabarcoding detectability occurred within the first 48 h, and after that, eDNA from several taxa became undetectable. These findings inform the ecological interpretation of metabarcoding datasets and provide estimates of eDNA decay rate that are valuable for both simulation studies and the design of future ecological surveys.
Although considerable research progress on the effects of anthropogenic disturbance in the deep sea has been made in recent years, our understanding of these impacts at community level remains limited. Here, we studied deep-sea assemblages of Sicily (Mediterranean Sea) subject to different intensities of benthic trawling using environmental DNA (eDNA) metabarcoding and taxonomic identification of meiofauna communities. Firstly, eDNA metabarcoding data did not detect trawling impacts using alpha diversity whereas meiofauna data detected a significant effect of trawling. Secondly, both eDNA and meiofauna data detected significantly different communities across distinct levels of trawling intensity when we examined beta diversity. Taxonomic assignment of the eDNA data revealed that Bryozoa was present only at untrawled sites, highlighting their vulnerability to trawling. Our results provide evidence for community-wide impacts of trawling, with different trawling intensities leading to distinct deep-sea communities. Finally, we highlight the need for further studies to unravel understudied deep-sea biodiversity.
Sexual selection and sexual conflict are expected to affect all aspects of the phenotype, not only traits that are directly involved in reproduction. Here, we show coordinated evolution of multiple physiological and life-history traits in response to long-term experimental manipulation of the mating system in populations of Drosophila pseudoobscura. Development time was extended under polyandry relative to monogamy in both sexes, potentially due to higher investment in traits linked to sexual selection and sexual conflict. Individuals (especially males) evolving under polyandry had higher metabolic rates and locomotor activity than those evolving under monogamy. Polyandry individuals also invested more in metabolites associated with increased endurance capacity and efficient energy metabolism and regulation, namely lipids and glycogen. Finally, polyandry males were less desiccation- and starvation resistant than monogamy males, suggesting trade-offs between resistance and sexually selected traits. Our results provide experimental evidence that mating systems can impose selection that influences the evolution of non-sexual phenotypes such as development, activity, metabolism and nutrient homeostasis.