Interview with the authors: response to amphibian-killing fungus is altered by temperature

Recently, Drs. Ellison, Zamudio, Lips, and Muletz-Wolz published their work focused on some of the ways amphibians respond to an infection by Batrachochytrium dendrobatidis (Bd). Bd is a fungus that is causing devastating worldwide decline of amphibians, meaning that understanding how some species manage the infection is important for conservation of myriad species. Using an elegant experimental set up and subsequent RNA sequencing data, Dr. Ellison and co-authors suggests that the variation in amphibian susceptibility to the fungus, which is related to temperature, occurs due concurrent temperature-dependent shifts in immune system function; lower temperatures were associated with an inflammatory response while higher temperatures with an adaptive immune response. Understanding exactly how and when this fungus alters wild amphibian populations is important for conservation of these often imperiled species. For more information, please see the full article and the interview with Dr. Ellison below. 

Eastern red-backed salamander (Plethodon cinereus). Photo credit: Alberto Lopez.

What led to your interest in this topic / what was the motivation for this study? I have always been fascinated with how parasites and pathogens influence fitness and shape host populations, particularly generalists infecting a wide range of host species. The pathogenic chytrid, Batrachochytrium dendrobatidis (Bd), is arguably one of the most generalist pathogens known to science, capable of infecting hundreds of amphibian species globally. However, even within a single host species, disease outcome (e.g. succumbing to or clearing infection) is highly variable and is often temperature-dependent. Given the devastating impacts Bd has already had on amphibian populations, the recent discovery of another amphibian-killing chytrid (B. salamandivorans), and the ever-pressing threat of climate change, we were driven to uncover how amphibian gene expression responses to chytrid infections vary under different temperatures.

What difficulties did you run into along the way? For me, it was the sheer scale of the sequencing dataset. Plethodon salamanders, notorious for their large genome sizes, had yet to have a published genome or transcriptome to use as a reference for RNAseq studies such as ours. Therefore, we had to ensure sufficient sequencing to de novo assemble the transcriptome, and enough per-sample depth to capture potentially subtle but important changes in gene expression due to temperature and infection. With multiple temperature treatments and multiple disease outcomes at each temperature, this resulted in relatively large RNAseq dataset of over 2 billion reads. Thankfully, having returned to Wales from the US by the time we received our sequence data, I had access to Supercomputing Wales, a nationwide high-powered computing initiative that allowed me to handle the computationally intensive analyses. More importantly, without the hard work of the other authors to carefully design and execute the highly-controlled animal experiments to generate the tissue samples, this study would simply not be possible.

What is the biggest or most surprising innovation highlighted in this study? I think that, within a relatively narrow thermal range, the substantial shifts in the types of immune genes being expressed in response to infection is really important to our understanding chytrid infection dynamics. The finding that adaptive immune transcripts (particularly those involved in MHC pathways) are more highly expressed at warmer temperatures – where amphibians tend to survive infection better – is most exciting. Given the growing evidence for the importance of certain MHC allele variants in Bd resistance, our results suggest it is not only be what MHC genotype amphibians possess, but how they express them during infection that dictates survival.

Moving forward, what are the next steps in this area of research? This study, while providing new insights into how temperature influences Bd-amphibian interactions, has generated many further questions. Some of the authors on this study have recently shown both temperature and Bd has a significant impact amphibian skin microbiome communities, a potentially critical line of defense against infections. It is currently unknown whether temperature-dependent host immune expression responses to Bd shapes skin microbiomes during infection or if skin bacteria are influencing host responses (or a combination of both). Work to directly assess host gene expression under different microbial community compositions would be an exciting future avenue of research. In addition, further investigation of both MHC genotype and expression phenotype simultaneously could be highly relevant to understanding intraspecific variation in chytrid resistance. Finally, we have previously developed methods to quantify Bd gene expression in vivo; it would be fascinating to couple our current findings with how Bd genes are expressed in-host under different temperatures.

Dr Carly Muletz-Wolz field sampling. Photo credit: Karen Lips.

What would your message be for students about to start developing or using novel techniques in Molecular Ecology? Many others on this blog have already highlighted the importance of well thought out experimental designs, and the need to grips with the theory before embarking on a project, that I can only echo. Although having now worked on many transcriptomic datasets in non-model organisms, I still sometimes get overwhelmed with the amount of information that could be potentially conveyed in a manuscript, particularly with more complex experimental designs such as this study. I recommend periodically taking a step back from your analyses, share it with colleagues to gauge the most important “headline” results, and finally, don’t worry that some things have to go as supplemental material; they can still be gems of information that kick-off an exciting new line of inquiry for someone!

What have you learned about methods and resources development over the course of this project? With high-throughput sequencing methods becoming ever more accessible and the explosion of innovative ways to analyse and present NGS data, it is all too easy to feel your project is not “cutting-edge” enough. It’s all very well having billions of sequences and a slick set of figures, but a research team most importantly needs to be able to provide meaningful biological/ecological interpretation. That’s why it has been great to be part of a collaborative team of amphibian ecologists and geneticists, which was critical to the development of this new resource of information on salamander transcriptomic responses to temperature and infection.

Describe the significance of this research for the general scientific community in one sentence. The thermally-altered transcriptional responses of salamanders to fungal pathogen infection is an important component to understanding observed seasonal and climatic patterns of chytrid disease outbreaks. 

Describe the significance of this research for your scientific community in one sentence. Our results suggest shifts from inflammatory to adaptive immune gene expression responses to Bd infection at warmer temperatures are a key component to thermal and/or seasonal patterns of amphibian chytridiomycosis.

Eastern red-backed salamander (Plethodon cinereus). Photo credit: Dr Carly Muletz-Wolz.

Ellison A, Zamudio K, Lips K. Muletz-Wolz C. 2019. Temperature-mediated shifts in salamander transcriptomic responses to the amphibian-killing fungus. Molecular Ecology 28:50586-5102.

Interview with the author: Creating the SPIKEPIPE metagenomic pipeline

Reliable abundance estimates is a significant challenge for eDNA metagenomic studies. One important issue is that sequencing introduces multiple sources of noise that can significantly alter the accuracy of abundance estimates. Here we interview Douglas Yu, a professor at the University of East Anglia, about the SPIKEPIPE pipeline recently published in Molecular Ecology Resources. This method is particularly exciting as it can use either short read barcodes or mitogenome data to estimate species abundances by accounting for sequencing noise using correction factors. They test this eDNA pipeline on arthropod samples taken from the High Arctic in Greenland and show that this approach can produce remarkably accurate species abundance estimates compared to samples of known composition. Read the full article here and get the code to run this pipeline here.

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The 5 steps of SPIKEPIPE.

What led to your interest in this topic / what was the motivation for this study? 

We very much want to know how a heating climate is affecting biodiversity. Greenland is a direct window into this, both because heating has progressed very fast here, and because local species richness is manageable for study:  375 known aboveground arthropod species at the Zackenberg research station. Equally important, the Danish research station at Zackenberg had had the foresight to systematically collect arthropods starting in 1996, and those samples were sitting in ethanol in a warehouse in Denmark. The main obstacle to using them had been that no one could identify the hundreds of thousands of individuals to species level. Luckily, Helena Wirta and Tomas Roslin had in parallel carried out a DNA barcoding campaign at Zackenberg. Put together, we had in our hands a complete time series of community dynamics over a stretch of time during which summer had almost doubled in length. 

What difficulties did you run into along the way? 

When we started, we were all set to use metabarcoding. However, we soon learned (not surprisingly) that the sample-handling protocols had not been designed with molecular methods in mind:  the trap water was reused across time periods, the collecting net was used across traps, and the sorting trays were not bleached between samples. We thus needed a protocol that would be robust to cross-sample contamination and would ideally return quantitative information, since we wanted to detect change in population dynamics. This is why we turned to mitochondrial metagenomics (Tang et al. 2015, Crampton-Platt et al. 2016) and came up with SPIKEPIPE, which combines read-mapping, a percent-coverage detection threshold, and a spike-in to correct for pipeline stochasticity. 

What is the biggest or most surprising innovation highlighted in this study? 

The individual elements of SPIKEPIPE were reasonably well known, but what we hadn’t anticipated is just how accurate the results were when combined in a single pipeline. With mock samples, we found no false-positive species detections (when the percent-coverage threshold is applied) and recovered highly accurate estimates of intraspecific abundances (in terms of DNA mass). With resequenced environmental samples, we found high repeatability of abundance estimates across sample repeats, even though DNA extraction and Illumina library prep, sequencing, and base-calling all inject stochasticity into datafile sizes.

Also very gratifying was finding that SPIKEPIPE returned useful data even when mapping reads only to short DNA barcodes, as originally presaged by Xin et al. (2013). This means that we can make use of the existing vast DNA-barcode reference library.

Moving forward, what are the next steps in this area of research?

SPIKEPIPE is of course only the means to an end, and our next goal is the statistical analysis of community change in a rapidly heating ecosystem. Nerea Abrego and Otso Ovaskainen are now applying joint species distribution modelling (with the R package Hmsc, Tikhonov et al. 2019) to the dataset of 712 pitfall-trap samples. One important question is to quantify how much of the year-to-year variation in species abundances can be attributed to species interactions, as opposed to climate variables. 

More broadly, the result that SPIKEPIPE can be used with DNA barcodes makes possible an intriguing strategy:   one may now generate both the species reference database and the sample-by-species table from the same set of samples. We are using Greenfield et al.’s (2019) Kelpie software to carry out targeted assembly of DNA barcodes from shotgun-sequenced bulk samples, which we compile into a single DNA-barcode reference database, against which we then map reads from each sample to generate the data table. 

What would your message be for students about to start developing or using novel techniques in Molecular Ecology? 

Build in a lot of testing:  multiple, complex mock samples for pipeline development, repeat environmental samples to measure repeatability, realistically complex positive controls, many negative controls, and many sanity checks as you work through your bioinformatic code. 

You are likely to be learning to code at the same time that you write your first pipelines. Take the extra time *now* to learn and apply robust coding techniques, even if there are easier but less robust methods available. 

Read Jenny Bryan’s tutorial on file naming:  https://speakerdeck.com/jennybc/how-to-name-files

What have you learned about methods and resources development over the course of this project? 

A great way to inspire new methods is to talk with non-molecular researchers about their scientific questions, currently used methods, and available sample types. Our team includes arctic ecologists, molecular ecologists, and a mathematician.

For one’s method to have impact, it will need to be useful for years after one first thinks of it. Stay up to date with technology trends, including costs, to avoid rapid obsolescence.

Describe the significance of this research for the general scientific community in one sentence.

We can use DNA sequencing to quantify how insect and spider communities respond to environmental change.

Describe the significance of this research for your scientific community in one sentence.

Mitochondrial metagenomics is a viable alternative to amplicon sequencing for characterising arthropod communities. 

Summary from the authors: telomere length predicts remaining lifespan

Close-up of an adult common tern with its prey. Photo credit: Andrea Parisi

Telomeres are DNA structures located at the end of chromosomes. They protect the chromosome, but shorten at each cell division. When telomeres get too short, the normal functioning of cells can be impaired. An individual’s telomere length may therefore predict its future lifespan, and understanding individual telomere dynamics could help to understand ageing in general.

Telomere shortening can be accelerated due to stress, thereby acting as a biomarker of an individual’s health status. However, some studies suggest that individual differences in telomere length are already determined at birth, and largely consistent over life.

We investigated individual telomere dynamics in a long-lived seabird, the common tern. The telomere lengths of 387 individuals, aged from 2 to 24 years, were repeatedly sampled across 10 years. We found that an individual’s telomeres shortened as they got older. Telomere shortening was also slightly increased if individuals had produced more chicks in the previous year. However, the correlation between repeated measures of an individual’s telomere length was very high, even with 6 years between measures. Nevertheless, an individual’s telomere length positively predicted its remaining lifespan, leaving the question of whether lifespan is already partly determined at the start of life.

Full article: Bichet C, Bouwhuis S, Bauch C, Verhulst S, Becker PH, Vedder O. 2019. Telomere length is repeatable, shortens with age and reproductive success, and predicts remaining lifespan in a long-lived seabird. Molecular ecology. https://doi.org/10.1111/mec.15331

CRISPR-Cas Diagnostics for Environmental Monitoring

In a special blog post, Molly-Ann Williams(@WilliamsMolly_9) and Anne Parle-McDermott (@anne_parle) from the School of Biotechnology and DCU Water Institute, Dublin City University provide an overview of how CRISPR-Cas works and how it can be applied to ecology and monitoring in particular. Read their recently published Molecular Ecology Resources paper here.

The field of CRISPR-Cas for genome editing has simply exploded since its introduction in 2012. The discovery of many different Cas enzymes with additional natural or genetically engineered functionalities, is resulting in an increase in CRISPR-Cas applications across all fields from food security to medicine. 

Number of Scopus search results for query “CRISPR” in given year. Search performed on 21 November 2019 .

So how can we join the revolution and apply CRISPR-Cas to the field of Ecology?

CRISPR-Cas systems consist of two main elements: a guide and a nuclease. Guides (made of RNA) direct the nuclease (Cas enzyme) to specific nucleic acid sequences (DNA or RNA). Upon target recognition the nuclease carries out the desired response, most commonly cleavage of the target sequence. The initially discovered CRISPR-Cas system relied on a nuclease called Cas9. This enzyme is involved in highly specific cleavage of target sequences that allow genome editing to occur by activating the natural repair system of the cell. More recently the applications of this system have been expanded beyond genome editing by the discovery of several new Cas enzymes with a secondary function i.e., the indiscriminate cleavage of single stranded nucleic acids upon target recognition. The discovery of these Cas enzymes has revolutionised nucleic acid diagnostics due to two main features:

Two main elements of a CRISPR-Cas diagnostic system: Cas enzyme and guide RNA effector complex and single stranded (ss) nucleic acid reporter molecule. In this example, the nuclease is Cas12a specific to DNA detection downstream from a TTTV PAM site. Adapted from Williams MA et al (2019).
  1. Protein-guide and cleavage molecules (Cas): able to specifically recognise target nucleic acids, cleave the target sequence and subsequently cleave other non-specific nucleic acids.
  2. Nucleic acids as reporters: the non-specific nucleic acids can be designed as a reporter molecule that releases measurable signal when cleaved. This allows us to visualise when the initial target sequence has been detected and apply it to diagnostics and species monitoring.

Two main elements of a CRISPR-Cas diagnostic system: Cas enzyme and guide RNA effector complex and single stranded (ss) nucleic acid reporter molecule. In this example, the nuclease is Cas12a specific to DNA detection downstream from a TTTV PAM site.

The three main Cas enzymes of interest for diagnostics are Cas12, Cas13 and Cas14 each with unique functions applicable to different types of tests (for a more detailed discussion of these enzymes visit this blog).

The Cas enzyme most relevant for single species detection from environmental DNA is the enzyme Cas12a. This nuclease can detect both ssDNA and dsDNA but can only recognise DNA sequences downstream from a TTTV protospacer adjacent motif (PAM). Importantly, Cas12a cannot detect DNA sequences missing this PAM site. This is vital when designing single species detection assays.

Do you have two closely related species that you want to distinguish? Searching your target species sequence for a site downstream of a PAM site found ONLY in your target, and not in sympatric species, will ensure highly specific recognition and prevent detection of non-target species.

What if you work with environmental RNA? Well there is a CRISPR-Cas system for you too! The Cas enzyme Cas13 differs from Cas12a in that it recognises single stranded RNA molecules with non-specific cleavage of ssRNA following target cleavage i.e., it works the same as Cas12a but targets RNA rather than DNA.

The world of CRISPR diagnostics is still in its early stages but with the discovery of new CRISPR-Cas systems with unique functions, there is no reason ecologists cannot utilise these diagnostic tools to enhance environmental monitoring using molecular techniques. For more information on using CRISPR-Cas diagnostics for single species detection from environmental DNA read our paper here.

Summary from the authors: genetic architecture of sexual dimorphism in an interspecific cross

The evolution of differences among females and males or sexual dimorphism (SD) is very common in animals but rare in plants. These differences emerge because there is a conflict of interests between sexes to maximize their reproductive success. Thus,  moving genes of reproductive traits to low recombining regions such as the sex chromosomes might be one way to solve this conflict at the genomic level. Closely related species with young sex chromosomes, which differ in the degree of SD, are ideal systems to explore the underlining genetic architecture of SD. We have crossed a female from Silene latifolia with marked SD with a male from S. dioica with less SD. We performed a QTL analysis of reproductive and vegetative traits in the F2 hybrids to find out if sexually dimorphic traits are located on the sex chromosomes, and how they contribute to species differences. Our results support that evolutionary young sex chromosomes are important for the expression of both SD and species differences. Moreover, transgressive segregation (traits with extreme values) and a reversal of SD in the F2s indicated that SD is constrained within the species but not in the recombinant hybrids. Sexual selection can, thus, contribute to speciation.

Full article: Baena-Díaz F, Zemp N, Widmar A. 2019. Insights into the genetic architecture of sexual dimorphism from an interspecific cross between two diverging Silene (Caryophyllaceae) species. Molecular ecology. https://doi.org/10.1111/mec.15271

Interview with the authors: Massive introgression of major histocompatibility complex (MHC) genes in newt hybrid zones

Hybridization is a mechanism by which adaptive alleles can cross species boundaries and possibly boost the adaptive potential of hybridizing species. This may be especially true for alleles that confer a selective advantage when rare, which is common among major histocompatibility complex (MHC) genes involved in pathogen defense. We therefore would expect MHC genes to introgress across hybridizing species relatively easily, though there exists relatively few examples supporting this hypothesis. In this paper from Molecular Ecology, Katarzyna Dudek, Tomasz Gaczorek, Piotr Zieliński, and Wiesław Babik document the extent of introgression in MHC variants across two hybridizing European newts across replicated transects. Read below for a behind-the-scenes look at their paper!

Link to the study: https://onlinelibrary.wiley.com/doi/full/10.1111/mec.15254

F1 hybrid male. Photo from M. Niedzicka

What led to your interest in this topic / what was the motivation for this study? 
The evolutionary significance of adaptive introgression is increasingly appreciated and many examples have been described, but few generalizations are available. There is a relatively well understood mechanism – novel/rare allele advantage – which should promote introgression of genes evolving under balancing selection (a prime example of these are MHC genes). However balancing selection itself produces signatures resembling introgression, so convincing demonstration of introgression in genes under balancing selection is difficult. Hybrid zones, especially in the form of replicated transect, are among the best tools you can imagine for such a project. And we’ve been studying these newts for some time – in a way this study was motivated by our long standing interest in adaptive introgression, but it’s an off-shoot of another project (see the paper in the same issue of Mol. Ecol.).

What difficulties did you run into along the way? 
The most difficult part was the design and justification of simulations that we used to rule out explanations alternative to introgression. Because MHC in newts is multi-locus and shows extensive copy number variation, it’s been difficult to design simulations that would at the same be time realistic and feasible. This may sound surprising, but genotyping and interpretation of MHC variation has not been a major problem, although the system is quite complicated. It seems that the field has matured enough that exon-based genotyping of MHC variation has become a standard. Another frontier would be population genetic analysis of entire MHC haplotypes, extremely interesting but currently beyond reach in non-model (and most model) taxa.

Field sampling. Photo from M. Liana

What is the biggest or most surprising finding from this study? 
The scale of apparently adaptive introgression. It’s not only that MHC variants introgress – we have suspected this before. One could expect that a single or a handful of novel, introgressed MHC haplotypes would be favoured in the recipient species, but we found massive introgression, apparently involving tens or more haplotypes, most likely in both directions. It’s been quite a surprise for us – this suggests that introgression can really remodel MHC variation in hybridizing species – an influx of large amount of variation may cause species to share, at least locally, pool of MHC variation.

Moving forward, what are the next steps for this research?
A natural next step is to test generality of our findings. The mechanism of novel/rare allele advantage should operate rather universally. If so, we expect that MHC genes will be among the last genes to stop introgressing between species that still hybridize, but are strongly reproductively isolated genome-wide. In other words we expect MHC introgression should be detectable (and perhaps strong) in systems, where despite hybridization, there is very little genome-wide introgression. We’ve been lucky to obtain funding for a collaborative project, in which we are going to test this prediction using over twenty hybrid zones from major vertebrate groups. We’d also like to look at the process at the level of entire haplotypes, but this would need to wait until technologies mature.

Albino L. montandoni male. Photo from W. Babik

What would your message be for students about to start their first research projects in this topic?
The most important would probably be: have your questions worked out and if you find a system that is good to address them – go for it. Try to understand the available theory, there’s nothing more practical than good theory to guide you and to save countless hours of your precious time. And finally, start writing before you think you’re ready. Writing is the best way to have your ideas clear, to spot weak points and see things you didn’t realized before.

What have you learned about science over the course of this project? 
Over and over again – that science is unpredictable. That reality mocks your well laid out ideas and plans, twisting and turning your paths, but if you recognize and follow the opportunities that appear on the way, everything will be fine :). For example something that appears as an offshoot of a major project may turn out at least equally interesting and important. Two key components are good and diverse collaboration and the scale of research appropriate to your question – that is just large enough to provide sound answers, but not necessarily larger.

Field sampling pt 2. Photo from W. Babik

Describe the significance of this research for the general scientific community in one sentence.
Our research suggests that MHC introgression may be a widespread process that introduces novel and restores previously lost variation, boosting the adaptive potential of hybridizing taxa.

Citation
Dudek, K., Gaczorek, T.S., Zieliński, P. and Babik, W., 2019. Massive introgression of MHC genes in newt hybrid zones. Molecular Ecology. 28(21). 4798-4810. https://onlinelibrary.wiley.com/doi/full/10.1111/mec.15254

Interview with the authors: RAD‐sequencing for estimating genomic relatedness matrix‐based heritability in the wild: A case study in roe deer

Working on non-model organisms comes with both challenges and rewards. While the joy and satisfaction of uncovering knowledge in wild populations drives many scientists, the lack of genomic resources can be a roadblock for many important research themes, such as determining the extent of evolutionary potential and response to selection. In this paper from Molecular Ecology Resources, Laura Gervais and co-authors demonstrate the potential for RAD-sequencing to overcome these challenges and estimate heritability and evolutionary potential in wild populations, even for non-model organisms without many existing genomic resources. Read below for a behind-the-scenes look at their paper!

Link to the study: https://onlinelibrary.wiley.com/doi/full/10.1111/1755-0998.13031

Image result for Capreolus capreolus
Photo of male and female roe deer (Capreolous capreolus) from Wikimedia Commons

What led to your interest in this topic / what was the motivation for this study? 
We are interested in how natural populations adapt to environmental changes. These changes occur rapidly and there is an urge to accumulate results on wild populations’ capacity of adaption for a wide range of species. Traditionally, measuring the evolutionary potential of a trait required long-term field surveys of phenotypic data and genetic relatedness obtained from a multi-generational pedigree. This is challenging to obtain because many free-ranging populations are hard to sample with the intensity required for pedigree reconstruction. We believe that genome-wide data and in particular RAD-sequencing data might be an opportunity to overcome this issue but we still lack an accessible practical framework to go from genomic data to the estimation of a population’s evolutionary potential.

What difficulties did you run into along the way? 
We had to overcome two main methodological difficulties. First, to investigate the effects of the sequencing strategy and the SNP calling/filtering procedure ultimately on GRM-based heritability, we had to run a considerable amount of bioinformatic and quantitative genetic analyses, which both proved to be time consuming. Secondly, there was not much methodology available on how to implement genomic relatedness matrix in a quantitative genetic linear mixed model. We hope that our work will make this approach more easily accessible.

What is the biggest or most surprising finding from this study? 
When we started the study, we did not expect that it would be possible to run genomic quantitative genetic analyses with only a few hundred individuals. Most of our colleagues were skeptical when we mentioned that we found significant heritability (at the beginning with only 170 genotyped individuals). Our results give hope that evolutionary potential studies in the wild might be virtually accessible for any natural population when using the appropriate sampling and sequencing design.

Moving forward, what are the next steps for this research?
We are working to combine genome-wide data with intensive bio-logging technology (data on animal movement) and high-resolution habitat information. The synergy between these three high-density data technologies offers a great opportunity to understand how species adapt to environmental changes across complex landscapes.

What would your message be for students about to start their first research projects in this topic?
Our message would be to never hesitate to contact people and surround yourself with all the necessary help. This is a domain that evolves rapidly and that is very exciting but may be quite disconcerting. It seems essential to remain informed and open-minded. Lastly, I would say that self-learning is really rewarding but that there is always the opportunity to ask for help to learn and get over a problem efficiently.

What have you learned about science over the course of this project? 
We have learned that more interdisciplinary exchanges between ecologists, molecular biologists and bioinformaticians are useful and can help to build such an integrative approach. This may be challenging as they often have different views on different issues that need to be conciliated. There is a need to meet and exchange ideas to get the most out of this type of projects.

Describe the significance of this research for the general scientific community in one sentence.
This study sheds light on a unique opportunity to evaluate whether species have the genetic potential to adapt to environmental changes, and this for virtually any non-model organism.

Citation
Gervais, L., Perrier, C., Bernard, M., Merlet, J., Pemberton, J. M., Pujol, B., & Quéméré, E. RAD‐sequencing for estimating genomic relatedness matrix‐based heritability in the wild: A case study in roe deer. Molecular Ecology Resources. 19(5). 1205-1217. https://onlinelibrary.wiley.com/doi/abs/10.1111/1755-0998.13031