Nominations are now open for the annual Molecular Ecology Prize.
The field of molecular ecology is young and inherently interdisciplinary. As a consequence, research in molecular ecology is not currently represented by a single scientific society, so there is no body that actively promotes the discipline or recognizes its pioneers. The editorial board of the journal Molecular Ecology therefore created the Molecular Ecology Prize in order to fill this void, and recognize significant contributions to this area of research. The prize selection committee is independent of the journal and its editorial board.
The prize will go to an outstanding scientist who has made significant contributions to molecular ecology. These contributions would mostly be scientific, but the door is open for other kinds of contributions that were crucial to the development of the field. The previous winners are: Godfrey Hewitt, John Avise, Pierre Taberlet, Harry Smith, Terry Burke, Josephine Pemberton, Deborah Charlesworth, Craig Moritz, Laurent Excoffier, Johanna Schmitt, Fred Allendorf, Louis Bernatchez, Nancy Moran, Robin Waples, and Scott Edwards.
Please send your nomination with a short supporting statement (no more than 250 words; longer submissions will not be accepted) and the candidate’s CV directly to Andrea Sweigart (email@example.com) by Thursday, April 2, 2020. Organized campaigns to submit multiple nominations for the same person are not necessary and can be counterproductive. Also, note that nominations from previous years do not roll over.
With thanks on behalf of the Molecular Ecology Prize Selection Committee
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!
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.
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.
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.
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.
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!
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
Recent work has suggested that background selection (BGS) may lead to incorrect inferences in FST outlier studies, generating substantial concern given the prevalence of these studies in evolutionary biology. In their recent Molecular Ecology publication, Matthey‐Doret and Whitlock investigate the effects of BGS on FST outlier tests using biologically realistic simulations, and find minimal effects. Matthey-Doret and Whitlock suggest that previous studies used unrealistic parameter values in simulations, leading to an overestimate of the effects of BGS in real studies. Read the full article here: https://onlinelibrary.wiley.com/doi/pdf/10.1111/mec.15197, and get a behind-the-scenes look at this work below.
What led to your interest in this topic / what was the motivation for this study? It all started with a paper by Cruickshank and Hahn (2014), in which they highlight a fear that background selection could be a confounding factor to local adaptation in FST outlier studies. Curious about this issue, Mike and I investigated the question further and quickly figured that many of these fears were based on misinterpretation of Charlesworth et al. (1997). Indeed, Charlesworth et al. (1997) demonstrated that background selection can cause FST peaks for extreme and unrealistic parameter sets only. They highlighted that their parameter choice was unrealistic as their goal was to find extreme effects, but this important limitation of their study was sadly often ignored by their readers. We therefore decided to perform simulations of background selection with realistic parameter choices.
What difficulties did you run into along the way? The main difficulty was technical. We tried to run these simulations with a number of popular simulation softwares but none of them were fast enough for our needs. We quickly realized that we had to write our own simulation software (SimBit) that would have a very high performance especially for simulations with a lot of genetic diversity.
What is the biggest or most surprising finding from this study? Starting the study, I was actually expecting that background selection would have a stronger effect on FST and that it would bias FST outlier methods to detect local adaptation. Our finding was a surprise to us, but it was also comforting to realize that the results of the many studies using FST outlier methods were probably not affected by background selection.
Moving forward, what are the next steps for this research? I think there is a need for a clarified view of the relative importance of positive and negative selection in explaining patterns of genetic diversity within and between populations. Also, I would wish to investigate further the interaction between selection coefficient and migration rate and how it affects within and between population genetic diversity. Such an endeavor would likely require a mixture of empirical and theoretical work.
What would your message be for students about to start their first research projects in this topic? I think there is a lot of intuition about the effect of linked selection in structured populations that has not been published. Talk to smart people! They may have some expectation about how background selection can affect the coalescent tree in structured populations that needs to be studied and written out.
What have you learned about science over the course of this project? I learned that a lot of the numeric tools that we use to analyse genetic data contain bugs (one of which is detailed in our article) and untold (or somewhat neglected) assumptions. One must always be very careful to have a good understanding about a particular statistical software before using it.
Describe the significance of this research for the general scientific community in one sentence. We found that background selection does not cause peaks of population differentiation and therefore that methods that use population differentiation to detect positive selection should be safe to be used without worry of background selection being a confounding factor.
Describe the significance of this research for your scientific community in one sentence. We found that background selection does not cause much variation in locus-to-locus variation in FST and therefore FST outlier methods to detect positive selection should be safe to be used without worry of background selection being a confounding factor.
Matthey‐Doret R, Whitlock MC. Background selection and FST: Consequences for detecting local adaptation. Mol Ecol. 2019;28:3902–3914. https://doi.org/10.1111/mec.15197.
Our ability to detect rapid evolution at the level of the genome has improved dramatically over the past decades, driven in part by advances in sequencing technology. It is now possible to detect small genetic differences in a population in just a few generations. This ability has stimulated many questions surrounding the causes and processes of rapid evolution. For example, how is the evolutionary trajectory of a species affected by the diversity of the surrounding community? In their recent Molecular Ecology paper, Dr. Sofia J. van Moorsel and colleagues quantify genetic and epigenetic differences across a set of plant species in the long-term Jena Experiment in Germany, which aims to test the effects of biodiversity on ecosystem functioning. Read below for a behind-the-scenes look at their study.
What led to your interest in this topic / what was the motivation for this study? Previously we had found that offspring of plants from the same species that had been growing either in monoculture or mixture for an extended period of time showed clear phenotypic differences in common environments. We thought that selection in response to community diversity was driving these observations. If selection was occurring, we would find genetic differences between individuals of the same species either from a monoculture or mixture background. However, at the time it was suggested that potentially epigenetics were the source of the observed effects (Tilman & Snell-Rodd 2014). Considering the current interest in the potential role of epigenetics in ecology we wanted to state an example by analyzing our monoculture and mixture phenotypes with a new combined method.
What difficulties did you run into along the way? In terms of the lab work and bioinformatic analysis, the method we used was still very new, so we needed to update and improve it along the way. Also, we focused perhaps too much on the hypothesis that the observed evolutionary differentiations could have “simply reflected epigenetic effects”. However, when we found clear genetic effects, we realized that this makes it more difficult to detect independent epigenetic effects, in particular because we could not analyze whole epi-/genomes. Further this research was a collaboration between two labs from two different countries. Consequently, we had to organized exchange visits to do lab work and discuss results. Lastly, the publication process is always accompanied with frustrations and hurdles, but thanks to fantastic teamwork and a healthy dose of perseverance we made it!
What is the biggest or most surprising finding from this study? The most surprising finding was that for four out of five perennial (!) plant species selected in monoculture vs. mixture were genetically distinct already after 10 years (with at least two experimentally ensured reproductive cycles). We showed that rapid evolution can happen in plant communities after only a small number of generations. Previously it was thought that evolution happening at ecological time scales was either largely limited to organisms with very short generation times (i.e., microbial species) or in macro-organisms like plants limited to non-genetic effects. Even though some of us were critical about the role of epigenetics to start with, most of us were still intrigued that genetic divergence was so clear and that it could explain almost all epigenetic variation.
Moving forward, what are the next steps for this research? Reduced-representation sequencing will never be able to exclude with certainty that epigenetic effects are entirely due to genetic differences at a place in the genome far away and thus possibly not sequenced. Ideally, we could do whole-genome bisulfite sequencing to get more to the bottom of all of this. We only sequenced about 2% of the genome, so potentially we have overlooked some important genes affecting DNA methylation. One next step would be selection experiments with clonal replicates of our perennial plants. However, this would also set epigenetic variation to zero and selection would have to use variation arising by new epigenetic mutations, whereas it may be more conceivable that epigenetic differentiation results from “sorting out” standing epigenetic variation.
What would your message be for students about to start their first research projects in this topic? First of all: forge collaborations. This paper would not have been possible, if we had not met at a conference. If you hear a talk of somebody at a conference or at your department, even if you do not see an immediate potential for collaboration, approach the speaker and tell them about your research. They are likely equally interested in your things as you are in theirs. Further, following the more unconventional research avenue pays off, even when it sometimes might take a little longer getting a paper accepted for publication. Specific to our topic, we would definitely recommend adding an evolutionary twist to classic plant community ecology, it’s an emerging field and it’s always exciting to be among the first researchers to enter a new topic.
What have you learned about science over the course of this project? Interdisciplinarity, even the small one between ecologists, molecular biologists and bioinformaticians is challenging but highly rewarding. Clearly, hot topics, such as epigenetics in ecology, are not free from differences in beliefs. Here we were juggling many different perspectives both among co-authors and among reviewers. It forced us to find a balance, which is also testimony for the importance of a broad-scale review process (five reviewers and a very engaged associate editor).
Describe the significance of this research for the general scientific community in one sentence. Rapid genetic but not epigenetic adaptation among plant species in mixtures means that we cannot predict community functioning by studying species in isolation and that we should conserve and restore entire communities and not individual species.
Arid environments are ecosystems of energetic stringency. Their typical high temperatures, low primary productivity, and unpredictable water availability prove physiologically challenging for birds. How these vertebrates cope with such harshness remains a conundrum in physiological evolutionary biology. While physiological adaptation likely involves energetic metabolic phenotypes, the underlying mechanisms (plasticity, genetics) are largely uncharacterized. To explore this, we developed a intra-specific level framework (Figure 1) that links environmental conditions, phenotypes and genotypes in a passerine bird whose range spans an aridity gradient. We found variation in energetic physiology phenotypes (a measure of energy expenditure) and gut microbiota composition (involved in energy retrieval from food) to be associated with environmental features and identified a small list of candidate adaptive genes. By working at the interface of physiology and genomics, we suggest that selective pressures on energetic physiology mediated by genes related to energy homeostasis and possibly with contribution of gut microbiota may facilitate adaptation to local conditions. Ultimately, our findings offer a possible explanation to the high avian intra-specific divergence observed in harsh environments, raises awareness that accounting for intra-specific variation is fundamental when modeling physiological responses to climate change, and provides a stepping-stone for further research into the mechanisms of phenotypic adaptation to aridity.
Ribeiro ÂM, Puetz L, Pattinson NB, Dálen L, Deng Y, Zhang G, da Fonseca RR, Smit B, Gilbert MT. (2019). 31° South: The physiology of adaptation to arid conditions in a passerine bird. Molecular Ecology. 2019. 28-16. 3709-3721.
Estimated to be around 17,000 years old, the Paleolithic paintings in the Lascaux cave of southwestern France give us a rare insight into the history and culture of communities that existed long before modern society. The conservation of caves such as Lascaux is a high priority for historians, scientists, and the general public. The anthropization, or human use, of caves may have dramatic effects on cave-dwelling macro- and micro-organisms, though few studies have been conducted on this topic. By comparing ‘pristine’ caves with anthropized caves frequently visited by humans, Dr. Lise Alonso and colleagues demonstrate that the anthropization of caves is associated with reduced microbial diversity for bacteria and archaea living on cave walls, though microeukaryotes and arthropods were not as strongly affected. In this post, we go behind-the-scenes with Dr. Yvan Moënne-Loccoz on their recent publication in Molecular Ecology and talk about the importance and challenges of working in cave ecosystems.
What led to your interest in this topic / what was the motivation for this study? Cave conservation is an important issue, especially when dealing with caves displaying Paleolithic artwork, as engravings and particularly paintings can be very fragile. There are many of these caves in Dordogne (South-West of France), some of them listed on the UNESCO World Heritage List (https://whc.unesco.org/en/list/85). The most famous Paleolithic cave in Dordogne is the Lascaux Cave, which was closed to the public in the 1960s for conservation reasons. To guide conservation efforts, it is important to understand the ecology and functioning of these caves, especially at the levels of microorganisms and arthropods, which form the main communities present. Against this background, the project was carried out to understand better the biotic communities residing in Lascaux Cave.
What difficulties did you run into along the way? When dealing with microorganisms and arthropods populating soils, sediments or water, in a majority of cases it is rather straightforward to collect samples and there is no restriction on sample size. In caves, taking samples from walls for microbial analyses, using a scalpel, may leave long-lasting marks. This is an issue in all caves, and particularly so in Paleolithic caves. In the Lascaux Cave, the sample list was prepared after discussions with the cave staff and approved by the cave conservator, and the samples were collected (away from ornate surfaces) by qualified restorers, under the guidance of microbial ecologists, so as to avoid any marks on the wall. It also means that only minute samples were available. Restrictions also apply for the type and location of arthropods traps, as sediments at the bottom of caves might contain historical artefacts.
What is the biggest or most surprising finding from this study? Caves are oligotrophic environments, so it is always a surprise to find diversified, rather large microbial communities on cave walls. In this study, the Lascaux Cave was compared with eight other caves from the same region, and these caves were quite different from one another in terms of size, architecture, distance from the soil surface, presence/absence of stream underground, human frequentation patterns, etc. Yet, there were clear distinctions in terms of microbial and arthropod communities when comparing anthropized caves versus non-anthropized (almost pristine) caves, which suggests that anthropization was more influential than these cave-specific features. Finally, we were rather surprised to find that prokaryotes (bacteria and archaea) were comparatively more impacted than eukaryotic residents (fungi, other micro-eukaryotes, arthropods) by cave anthropization.
Moving forward, what are the next steps for this research? This work was carried out with the Lascaux Cave and eight other caves from Dordogne, which corresponds to a relatively small area. There were at the most 35 km between two caves in this study. Therefore, it remains to be seen whether the results of the current investigation are also relevant elsewhere. At a larger geographic scale, several differences in cave properties can be expected, for instance in geological features (e.g. limestone type) and climatic conditions, which have the potential to influence cave biotic communities. In addition, we evidenced parallel variations in the diversity of microbial and arthropod communities, and it will be important to explore and understand better the ecological interactions between both types of cave inhabitants.
What would your message be for students about to start their first research projects in this topic? First of all, the underground world and the interface between ecology and artwork conservation issues are fascinating, so welcome to the field! More importantly, each cave is different and represents a complex situation of its own, so one can be very busy focusing on a single cave only. This is reflected by the literature on cave microbial ecology, where often a single cave is considered at a time. However, we found that the comparison of different caves, following the path of various groups (e.g. Campbell et al. 2011 J Cave Karst Stud 73:75 ; Hathaway et al. 2014 Geomicrobiol J 31:205 ; De Mandal et al. 2017 BMC Microbiol 17:90 ; Pfendler et al. 2018 Sci Tot Environ 615:1207), brought very interesting insights, so comparative assessments are worth the effort.
What have you learned about science over the course of this project? The majority of participants to this project usually work on soil or aquatic ecosystems, and we found (once again) that concepts and methodology are applicable across different types of ecosystems. More specifically, we realized that underground systems represent interesting models to investigate ecological perturbations, because they are rather confined environments, where community fluctuations in response to mild environmental variations can be documented.
Describe the significance of this research for the general scientific community in one sentence. This research shows that microbiome diversity can be used as a bioindicator of the level of cave anthropization.
Citation Alonso L, Pommier T, Kaufmann B, Dubost A, Chapulliot D, Doré J, Douady CJ, Moënne‐Loccoz Y. Anthropization level of Lascaux Cave microbiome shown by regional‐scale comparisons of pristine and anthropized caves. Molecular Ecology, 28(14), 3383-3394. https://onlinelibrary.wiley.com/doi/10.1111/mec.15144