We are soliciting nominations 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, Scott Edwards, Victoria Sork, Fuwen Wei, and Kerstin Johannesson.
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 Joanna Freeland (firstname.lastname@example.org) by Friday, March 31, 2023. 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.
In a recent paper in Molecular Ecology, Szukala et al. quantified the degree of gene expression and functional parallelism across polytopic divergence of montane and alpine ecotypes of in Heliosperma pusillum (Caryophyllaceae) and gained insights into the architecture of adaptive traits. They performed RNA-seq analyses of plants grown in a common garden and detected a large proportion of differentially expressed genes in each replicate ecotype pair. Functional enrichment of these genes, however, revealed that the traits affected by significant expression divergence are largely consistent across ecotype pairs, suggesting a polygenic architecture for the diverged adaptive traits and multiple routes for adaptation. A new genome assembly for H. pusillum was also presented in this study.
We sent a number of questions to lead authors of this work, Aglaia Szukala and Ovidiu Paun, to get more detail on this study.
What led to your interest in this topic / what was the motivation for this study?
We are fascinated by the concept of parallel evolution and the molecular mechanisms behind this process. Given that drift is a major driver of evolution and due to the traditional focus on mono- or oligogenic traits, parallel evolution has been considered to be a rare process until recently. However, together with the increasing understanding of polygenic adaptation (Barghi et al., 2020), it has become clear that parallel evolution is relatively frequent, with implications across evolutionary biology and ecology. Specifically, for our study, previous works (Trucchi et al., 2017; Bertel et al., 2018) reported some evidence that altitudinal ecotypes in H. pusillum diverged in parallel. We wanted to rigorously test this hypothesis using demographic modeling and understand the level of molecular parallelism, with regard to divergent gene expression and outlier SNPs.
What difficulties did you run into along the way?
For several reasons related to the planning of field work and the development of the wider project over years, we had to deal with uneven sampling sizes across populations, which needed to be taken into account, especially for the demographic modeling analyses. Fun fact: in reciprocal translocation experiments of a complementary study (Szukala et al., 2022) on the same species, whose data is also included in the present paper, we chose to use alpine microsites to plant our accessions that were fairly flat (in an otherwise steep area) and free of other plants. At the end of the vegetation season, those sites proved to be resting places for chamois which squeezed and munched most of our plants, while overfertilizing them. In previous years, when reciprocal transplantations were performed as preparation for this study, we faced droughts, poor germination and survival rates at some sites, leading to uneven sampling sizes across sites. Take-home message: experiments in the wild are always a challenge.
What is the biggest or most surprising innovation highlighted in this study?
It is unclear how much overlap of divergence outliers is to be expected across natural evolutionary replicates. Our study showed a surprisingly low amount of shared molecular differentiation, which we did not expect given that the geographic range considered is relatively small and our study system is in a phase of incipient speciation with no reproductive isolation detectable (Bertel et al., 2016). The extremely low sharing of differentially expressed genes and outlier SNPs, but high similarity of GO terms involved across independent divergence events, indicates that the polygenic architecture of traits is relevant for adaptation of these populations to distinct altitudinal zones in the Alps.
Moving forward, what are the next steps in this area of research?
We further investigated the role of phenotypic plasticity for the development of parallel evolution in our system (Szukala et al., 2022) towards a better understanding of the relative role of genetic and environmentally-induced phenotypic variation in such replicated divergence events. We are also interested if other molecular mechanisms, which are sensitive to environmental input, such as epigenetic signals, could play an important role in parallel evolution. Further, we wish to understand how polygenic adaptation affects signatures of parallel evolution. Very interesting is to question if adaptation can use different genes to produce similar outcomes even in very closely related lineages, and how frequent this process takes place compared to the re-use of standing variation.
What would your message be for students about to start developing or using novel techniques in Molecular Ecology?
Being curious and exploiting the most advanced and newest methods is good, but don´t forget to be robust, careful, and bias-aware when it comes to the interpretation of results.
What have you learned about methods and resource development over the course of this project?
It is often difficult to quantify and describe results relative to expectations in an objective way, because it is hard to formulate objective expectations in natural systems.
Describe the significance of this research for the general scientific community in one sentence.
Repeated evolution of similar phenotypes can involve different sets of genes.
Describe the significance of this research for your scientific community in one sentence.
Polygenic traits offer different genetic substrates for parallel evolution of similar phenotypes.
Barghi N, Hermisson J, Schlötterer C. 2020. Polygenic adaptation: a unifying framework to understand positive selection. Nature Reviews Genetics 21: 769–781.
Bertel C, Hülber K, Frajman B, Schönswetter P. 2016. No evidence of intrinsic reproductive isolation between two reciprocally non-monophyletic, ecologically differentiated mountain plants at an early stage of speciation. Evolutionary Ecology 30: 1031–1042.
Bertel C, Rešetnik I, Frajman B, Erschbamer B, Hülber K, Schönswetter P. 2018. Natural selection drives parallel divergence in the mountain plant Heliosperma pusillum s.l. Oikos 127: 1355–1367.
Trucchi E, Frajman B, Haverkamp THA, Schönswetter P, Paun O. 2017. Genomic analyses suggest parallel ecological divergence in Heliosperma pusillum (Caryophyllaceae). New Phytologist 216: 267–278.
Szukala A, Bertel C, Frajman B, Schönswetter P, Paun O. 2022. Parallel adaptation to lower altitudes is associated with enhanced plasticity in Heliosperma pusillum (Caryophyllaceae). bioRxiv 2022.05.28.493825; doi: 10.1101/2022.05.28.493825.
Szukala A, Lovegrove-Walsh J, Luqman H, Fior S, Wolfe TM, Frajman B, Schönswetter P, Paun O. 2022. Polygenic routes lead to parallel altitudinal adaptation in Heliosperma pusillum (Caryophyllaceae). Molecular Ecology. https://doi.org/10.1111/mec.16356.
In a recent paper in Molecular Ecology, Singh et al. used genome sequencing, bioinformatics and population genetic analyses to gain insight into the genetics and evolution of a fascinating mating system. The species in question, Lamprologous callipterus, exhibits a mating system with two males morphs. Large “bourgeois” males carry empty snail shells that are inhabited and used as nests by the females. An alternate male morph, much smaller than the “bourgeois” males, also exists and inhabits shells along with the females. Previous genetic work had established that this mating system was Y-linked and that the male body size was a Mendelian trait, but the sex-determining locus had not been identified until this study.
We sent some questions to Pooja Singh, the author who led this work, to get more detail on this study.
What is the biggest or most surprising innovation highlighted in this study?
The most novel aspect of this study is that we found an example of a young sex chromosome that may have evolved due to sexual antagonism over body size. While the sexual antagonism theory is considered the classical model of sex chromosome evolution, few empirical examples exist to support it. The other exciting finding was that the candidate body size/dwarfism gene that we propose for L. callipterus, GHRHR, is a well-known dwarfism gene in mammals. Fish and mammals shared a common ancestor over 440 million years ago, so the body size development pathway is genetically constrained through deep evolutionary time.
What difficulties did you run into along the way?
The major challenge for me was that I knew little about sex chromosome evolution when I started this project, so I really had to do a lot of groundwork reading relevant literature and researching methods to be able to get things going. I had to start thinking beyond the classical XY and WZ old sex systems and familiarize myself with the workings of early stages of sex chromosome evolution.
When I read your paper, I had never heard of the fascinating mating system of these cichlids. They reminded me of the ruff, and the multiple inversions that seem to be involved in the different reproductive strategies in that system. You mention in the paper that you were not able to identify inversions based on the bioinformatic approaches you used. Is there a sense for how much chromosome evolution during the radiation? Could the use of the divergent reference genome have anything to do with the lack of a signal of inversions?
To my knowledge the broad scale chromosomal structure of African cichlid species is similar. However, small scale structural variations (inversions, indels, translocations etc.) have not been investigated systematically. So yes, it is totally possible that our short read data and the divergent (and fragmented) reference genome assembly may have hindered our ability to detect inversions. The system really needs a long-read de novo genome assembly to resolve the inversion question.
In the Discussion, you talk about the possibility of different male Y-haplotypes. Is your data sufficiently high resolution that you could examine insertion/deletion polymorphisms in your dataset?
Yes, we could technically identify small insertions/deletions in our data. Might certainly be something to investigate in the future, in combination with long-read Y assembly.
A recently proposed model of sex-chromosome evolution indicates that gene expression differences may predominate at the early stages of sex chromosome evolution (Lenormand and Roze 2022 Science – https://doi.org/10.1126/science.abj1813). This is intriguing given that you didn’t find any smoking gun loci with signals of sexual antagonism. Do you have plans to look at patterns of gene expression across the different morphs?
While Lenormand and Roze’s theory is certainly exciting for the field of sex chromosome evolution, I think it is less plausible for the L. callipterus mating system because antagonistic body sizes in females and males are crucial shell-brooding success and fitness. And because we found the candidate sex-determining gene and body-size gene to be physically linked. I am certainly not a proponent of the ‘one classical theory explains all’ narrative and I really look forward to seeing what RNA-seq data reveal about sex chromosome evolution in this species. It would be especially interesting to see the landscape of cis/trans eQTLs of genes in our proposed L. callipterus sex chromosome and how much it reflects the expectations from Lenormand and Roze’s model. Beyond just this species, cichlid fishes are an excellent system to test the sexual antagonism vs gene regulation models of sex chromosome evolution.
Regarding the coverage analysis you used to identify the putative sex-linked locus. Given the hypothesis that the divergence of the sex chromosomes is recent, reads sampled from Y-linked regions may still map well to the orthologous region on the putative X-chromosome. Did you tweak mapping quality filters at all?
I did run a less stringent mapping analysis, which overall had slightly higher mapping statistics, but the reduced coverage pattern on the L. callipterus sex chromosome was still significant.
Could you describe the significance of this research for the general scientific community in one sentence?
Sexual antagonism over body-size may have driven sex chromosome evolution in a shell-brooding cichlid fish where giant and dwarf male reproductive types have evolved.
Moving forward, what are the next steps in this area of research (unless otherwise covered)?
Our main priority right now is to keep the L. callipterus dwarf males alive and breeding. Our fish were recently moved from the University of Bern in Switzerland to the University of Graz in Austria, and it has proved difficult to get the dwarf males happy and breeding in the new facility. This is (probably) the only collection in the world of L. callipterus dwarf males outside Lake Tanganyika so they are very precious. Our next step is to write a convincing grant to get funding to build a long-read improved genome assembly, conduct RNA-seq, and sample and sequence more individuals from natural populations. I would like to use the RNA-seq data to map expression QTLs and investigate the regulatory interactions of candidate genes related to sex, morphology, physiology, and behaviour that we found in or around the L. callipterus sex region. It would also be interesting to study sex chromosomes in related lamprologine species, as our pre-liminary analysis in this manuscript suggests that the sex region may be shared across the lamprologine tribe