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02 May 2025
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Experimental evidence for short term directional selection of epigenetic trait variation

Transgenerationally-transmitted epigenetic variation responds to phenotypic selection – results from a novel selection methodology

Recommended by ORCID_LOGO based on reviews by Leandro Quadrana and Sophie Brunel Muguet

The breeder’s equation is a classical equation in evolutionary theory, and basically states that the response of a trait to selection is equal to the strength of selection on this trait multiplied by the heritability of the trait. There can be several reasons why reality does not conform to a narrow interpretation of this equation, but in spite of that, let us actually indulge in a broad interpretation of the equation. Typically, the heritability of a trait is interpreted to refer to the genetic basis of a trait (the additive genetic variance). However, a broad interpretation of the breeder’s equation would be that if selection acts on a trait and that trait is somehow heritable, we should expect to observe an evolutionary change in that trait. In other words, the source and mechanism of inheritance does not matter for the breeder’s equation to have applicability.

In this paper, Pujol et al. (2025) follow this rationale for epigenetic variation, and more specifically for differentially methylated regions in the model plant Arabidopsis thaliana. They used 120 lines which vary across 126 differentially methylated regions of the genome, but are genetically identical, thereby eliminating additive genetic variance from the heritability component of the breeder’s equation. Previous studies have already shown that these differentially methylated regions are associated with different phenotypes, suggesting they somehow functionally affect the development of the plants. Previous studies have also shown that these differentially methylated regions are stably transmitted across generation, i.e., that they are heritable. This predicts that if one selects for different phenotypes, there should be an evolutionary response in the phenotypes, and an associated shift in the differentially methylated regions that are responsible for the phenotypic variation.

By and large, this is what Pujol et al. (2025) found. They selected divergently on four different plants traits (biomass, rosette size, flowering time, and height at first fruit), in two different populations, and with two different selection strengths. For most traits they found a phenotypic shift, and this largely corresponded with associated shifts in the differentially methylated regions. The patterns were very congruent between the different selection strengths, and very similar for the two different populations. We can therefore confidently conclude that epigenetic variation has effects on fitness-relevant phenotypic traits, that therefore natural selection can act on this epigenetic variation, and if so that this would cause an evolutionary change in the phenotypes under selection and in the differentially methylated regions causing this phenotypic variation. I.e., the breeder’s equation can indeed by applied to more than just genetically heritable variation, it can also be applied to non-genetically heritable variation. 

While this seems like a very obvious result, there are still very few studies that show how selection on non-genetic heritable variation results in a between-generation shift in this non-genetic heritable variation. In that sense, this study can function as a case in favour of a broader interpretation of evolution; to refer to a heritable between-generation change in the composition of a population, independent of whether the heredity is genetic or non-genetic. Critics might say that this study has only limited validity, since the epigenetic variation has been artificially increased in the used plant lines, and may not reflect naturally occurring variation. Indeed, more studies on natural selection on epigenetic variation are called for, but these will have the added complication that they need to correct for genetic variation, which is often correlated to epigenetic variation. Here, the authors could exclude genetic variation by working with epigenetically different lines that were genetically identical.

The study stands out in yet another respect – it uses a highly unusual and apparently novel selection design (although the authors do not know for sure if their idea is actually novel). Typically, in a selection study only a subset of parents is allowed to reproduce out of the total set of potential parents. If one wants to select for different traits separately, or with different selection strengths, separate selection studies need to be undertaken. Here the authors took a different approach. They let all their parents reproduce (3 offspring per plant), and phenotyped all offspring. They then, virtually, selected for different traits or for different selection strengths in the parents by excluding from their dataset the offspring of parents that are selected not to reproduce – after they had actually already reproduced! It is almost as if selection acts with a time delay, destroying not only the selected parents but also their offspring. This has the benefit that a single dataset is generated (all phenotyped offspring of all parents), and then selection can be exerted as often as one wants, for example for distinct types of selection, or on different (combinations) of traits. While the initial effort to phenotype offspring of all potential parents is large, and exponentially so if multiple generations are selected, the subsequent evaluation of distinct types of selection on any of the phenotyped traits is virtually effortless. For example, the authors applied divergent selection, but could reuse their dataset to apply stabilising selection. This novel selection design may therefore be a very attractive approach for many other researchers.

References

Benoit Pujol, Mathieu Latutrie, Pierick Mouginot, Nelia Luviano- Aparicio, Jésaëlle Piquet, Sara Marin, and Stéphane Maury (2025) Experimental evidence for short term directional selection of epigenetic trait variation. Zenodo, ver.2 peer-reviewed and recommended by PCI Evolutionary Biology https://doi.org/10.5281/zenodo.15227609

Experimental evidence for short term directional selection of epigenetic trait variationBenoit Pujol, Mathieu Latutrie, Pierick Mouginot, Nelia Luviano- Aparicio, Jésaëlle Piquet, Sara Marin, and Stéphane Maury<p>Evolution by natural selection can occur when organisms harbor genetically inherited phenotypic variation, and phenotypic variants have differential fitness. Stable transgenerational epigenetic variation also exists for fitness-related traits a...Morphological Evolution, Non Genetic InheritancePim Edelaar2024-07-17 16:07:37 View
26 Aug 2021
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Impact of ploidy and pathogen life cycle on resistance durability

Durability of plant resistance to diploid pathogen

Recommended by based on reviews by Loup Rimbaud and 1 anonymous reviewer

​​Durability of plant resistance to diploid pathogen Hirohisa Kishino Based on the population genetic and epidemiologic model, Saubin et al. (2021) report that the resistant hosts generated by the breeding based on the gene-for-gene interaction is durable much longer against diploid pathogens than haploid pathogens. The avr allele of pathogen that confers the resistance is genetically recessive. The heterozygotes are not recognized by the resistant hosts and only the avr/avr homozygote is adaptive. As a result, the trajectory of avr allele frequency becomes more stochastic due to genetic drift. Although the paper focuses on the evolution of standing polymorphism, it seems obvious that the adaptive mutations in pathogen have much larger probability of being deleted from the population because the individuals own the avr allele mostly in the form of heterozygote at the initial phase after the mutation. Since only few among many models of plant resistance deployment study the case of diploid pathogen and the contribution of the pathogen life cycle, this work will add an important intellect to the literature (Rimbaud et al. 2021).

From the study of host-parasite interaction in flax rust Melampsora lini, Flor (1942, 1955) showed that the host resistance is formed by the interaction of a host resistance gene and a corresponding pathogen gene. This gene-for-gene hypothesis has been supported by experimental evidence and has served as a basis of the methods of molecular breeding targeting the dominant R genes. However, modern agriculture provides the pathogen populations with the homogeneous environments and laid strong selection pressure on them. As a result, the newly developed resistant plants face the risk of immediate resistance breakdown (Möller and Stukenbrock 2017).

Currently, quantitative resistance is getting attention as characters as a potential target for long-life (mild) resistant breeds (Lannou, 2012). They are polygenic and controlled partly by the same genes that mediate qualitative resistance but mostly by the genes that encode defense-related outputs such as strengthening of the cell wall or defense compound biosynthesis (Corwin and Kliebenstein, 2017). Progress of molecular genetics may overcome the technical difficulty (Bakkeren and Szabo, 2020). Saubin et al. (2021) notes that the pattern of genetic inheritance of the pathogen counterparts that respond to the host traits is crucial regarding with the durability of the resistant hosts. The resistance traits for which avr alleles are predicted to be recessive may be the targets of breeding.

References

Bakkeren, G., and Szabo, L. J. (2020) Progress on molecular genetics and manipulation of rust fungi. Phytopathology, 110, 532-543. https://doi.org/10.1094/PHYTO-07-19-0228-IA

Corwin, J. A., and Kliebenstein, D. J. (2017) Quantitative resistance: more than just perception of a pathogen. The Plant Cell, 29, 655-665. https://doi.org/10.1105/tpc.16.00915

Flor, H. H. (1942) Inheritance of pathogenicity in a cross between physiological races 22 and 24 of Melampsova lini. Phytopathology, 35. Abstract.

Flor, H. H. (1955) Host-parasite interactions in flax rust-its genetics and other implications. Phytopathology, 45, 680-685.

Lannou, C. (2012) Variation and selection of quantitative traits in plant pathogens. Annual review of phytopathology, 50, 319-338. https://doi.org/10.1146/annurev-phyto-081211-173031

Möller, M. and Stukenbrock, E. H. (2017) Evolution and genome architecture in fungal plant pathogens. Nature Reviews Microbiology. 15, 756–771. https://doi.org/10.1038/nrmicro.2017.76

Rimbaud, L., Fabre, F., Papaïx, J., Moury, B., Lannou, C., Barrett, L. G., and Thrall, P. H. (2021) Models of Plant Resistance Deployment. Annual Review of Phytopathology, 59. https://doi.org/10.1146/annurev-phyto-020620-122134

Saubin, M., De Mita, S., Zhu, X., Sudret, B. and Halkett, F. (2021) Impact of ploidy and pathogen life cycle on resistance durability. bioRxiv, 2021.05.28.446112, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.05.28.446112

Impact of ploidy and pathogen life cycle on resistance durabilityMéline Saubin, Stephane De Mita, Xujia Zhu, Bruno Sudret, Fabien Halkett<p>The breeding of resistant hosts based on the gene-for-gene interaction is crucial to address epidemics of plant pathogens in agroecosystems. Resistant host deployment strategies are developed and studied worldwide to decrease the probability of...Evolutionary Applications, Evolutionary EpidemiologyHirohisa Kishino2021-06-03 07:58:16 View
04 Sep 2019
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The discernible and hidden effects of clonality on the genotypic and genetic states of populations: improving our estimation of clonal rates

How to estimate clonality from genetic data: use large samples and consider the biology of the species

Recommended by ORCID_LOGO based on reviews by David Macaya-Sanz, Marcela Van Loo and 1 anonymous reviewer

Population geneticists frequently use the genetic and genotypic information of a population sample of individuals to make inferences on the reproductive system of a species. The detection of clones, i.e. individuals with the same genotype, can give information on whether there is clonal (vegetative) reproduction in the species. If clonality is detected, population geneticists typically use genotypic richness R, the number of distinct genotypes relative to the sample size, to estimate the rate of clonality c, which can be defined as the proportion of reproductive events that are clonal. Estimating the rate of clonality based on genotypic richness is however problematic because, to date, there is no analytical, nor simulation-based, characterization of this relationship. Furthermore, the effect of sampling on this relationship has never been critically examined.
The paper by Stoeckel, Porro and Arnaud-Haond [1] contributes significantly to the characterization of the relationship between rate of clonality and genetic and genotypic parameters in a population. The authors use an extensive individual-based simulation approach to assess the effects of rate of clonality (fully sexual, fully clonal and a range of intermediate levels of clonality, i.e., partial clonality) on genetic and genotypic parameters, considering variable population size, sample size, and numbers of generations elapsed since population initiation. Based on their simulations, they derive empirical formulae that link for the first time the rate of clonality to the genotypic richness and to the size distribution of clones (genotypic parameters), as well as to the population inbreeding coefficient and to a metric of linkage disequilibrium (genetic parameters). They then use the simulated data to assess the accuracy of their predictions. In a second phase, the authors use a Bayesian supervised learning algorithm to estimate rates of clonality from the simulated data.
The authors show that the relationship between rate of clonality and genotypic richness is not linear: genotypic richness decreases slowly with increasing clonality, a large drop in genotypic richness is only seen for rates of clonality ≥ 0.90. Genetic parameters are only sensitive to high rates of clonality. The practical implications of these results are that genotypic and genetic parameters can complement each other for the estimation of rates of clonality, with genotypic parameters most useful throughout most of the range of clonality values and with genetic parameters complementing them meaningfully at higher values. The most meaningful practical result of the paper is the demonstration of sampling bias on the estimation of genotypic richness. Commonly used population sample sizes in population genetics studies (n ≤ 50) lead to great overestimation of genotypic richness, which consequently leads to a severe underestimation of the rate of clonality in most systems, irrespectively of whether they have reached stationary equilibrium. Only in small populations, these effects are attenuated.
Biologists interested in the estimation of the rate of clonality will find this paper highly useful to design their sampling, and to choose their statistics for inference in a meaningful way. This paper also calls for a careful reappraisal of previously published works that infer rates of clonality from genetic data, and highlights the prime importance of complementary information on species life history data for a correct understanding of partial clonality.

References

[1] Stoeckel, S., Porro, B., and Arnaud-Haond, S. (2019). The discernible and hidden effects of clonality on the genotypic and genetic states of populations: improving our estimation of clonal rates. ArXiv:1902.09365 [q-Bio] v4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. Retrieved from http://arxiv.org/abs/1902.09365v4

The discernible and hidden effects of clonality on the genotypic and genetic states of populations: improving our estimation of clonal ratesSolenn Stoeckel, Barbara Porro, Sophie Arnaud-Haond<p>Partial clonality is widespread across the tree of life, but most population genetics models are conceived for exclusively clonal or sexual organisms. This gap hampers our understanding of the influence of clonality on evolutionary trajectories...Population Genetics / Genomics, Reproduction and SexMyriam Heuertz2019-02-28 10:10:56 View
29 Sep 2022
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How many sirtuin genes are out there? evolution of sirtuin genes in vertebrates with a description of a new family member

Making sense of vertebrate sirtuin genes

Recommended by based on reviews by Filipe Castro, Nicolas Leurs and 1 anonymous reviewer

Sirtuin proteins are class III histone deacetylases that are involved in a variety of fundamental biological functions mostly related to aging. These proteins are located in different subcellular compartments and are associated with different biological functions such as metabolic regulation, stress response, and cell cycle control [1]. In mammals, the sirtuin gene family is composed of seven paralogs (SIRT1-7) grouped into four classes [2]. Due to their involvement in maintaining cell cycle integrity, sirtuins have been studied as a way to understand fundamental mechanisms governing longevity [1]. Indeed, the downregulation of sirtuin genes with aging seems to explain much of the pathophysiology that accumulates with aging [3]. Biomedical studies have thus explored the potential therapeutic implications of sirtuins [4] but whether they can effectively be used as molecular targets for the treatment of human diseases remains to be demonstrated [1]. Despite this biomedical interest and some phylogenetic analyses of sirtuin paralogs mostly conducted in mammals, a comprehensive evolutionary analysis of the sirtuin gene family at the scale of vertebrates was still lacking.

In this preprint, Opazo and collaborators [5] took advantage of the increasing availability of whole-genome sequences for species representing all main groups of vertebrates to unravel the evolution of the sirtuin gene family. To do so, they undertook a phylogenomic approach in its original sense aimed at improving functional predictions by evolutionary analysis [6] in order to inventory the full vertebrate sirtuin gene repertoire and reconstruct its precise duplication history. Harvesting genomic databases, they extracted all predicted sirtuin proteins and performed phylogenetic analyses based on probabilistic inference methods. Maximum likelihood and Bayesian analyses resulted in well-resolved and congruent phylogenetic trees dividing vertebrate sirtuin genes into three major clades. These analyses also revealed an additional eighth paralog that was previously overlooked because of its restricted phyletic distribution. This newly identified sirtuin family member (named SIRT8) was recovered with unambiguous statistical support as a sister-group to the SIRT3 clade. Comparative genomic analyses based on conserved gene synteny confirmed that SIRT8 was present in all sampled non-amniote vertebrate genomes (cartilaginous fish, bony fish, coelacanth, lungfish, and amphibians) except cyclostomes. SIRT8 has thus most likely been lost in the last common ancestor of amniotes (mammals, reptiles, and birds). Discovery of such previously unknown genes in vertebrates is not completely surprising given the plethora of high-quality genomes now available. However, this study highlights the importance of considering a broad taxonomic sampling to infer evolutionary patterns of gene families that have been mostly studied in mammals because of their potential importance for human biology.

Based on its phylogenetic position as closely related to SIRT3 within class I, it could be predicted that the newly identified SIRT8 paralog likely has a deacetylase activity and is probably located in mitochondria. To test these evolutionary predictions, Opazo and collaborators [5] conducted further bioinformatics analyses and functional experiments using the elephant shark (Callorhinchus milii) as a model species. RNAseq expression data were analyzed to determine tissue-specific transcription of sirtuin genes in vertebrates, including SIRT8 found to be mainly expressed in the ovary, which suggests a potential role in biological processes associated with reproduction. The elephant shark SIRT8 protein sequence was used with other vertebrates for comparative analyses of protein structure modeling and subcellular localization prediction both pointing to a probable mitochondrial localization. The protein localization and its function were further characterized by immunolocalization in transfected cells, and enzymatic and functional assays, which all confirmed the prediction that SIRT8 proteins are targeted to the mitochondria and have deacetylase activity. The extensive experimental efforts made in this study to shed light on the function of this newly discovered gene are both rare and highly commendable.

Overall, this work by Opazo and collaborators [5] provides a comprehensive phylogenomic study of the sirtuin gene family in vertebrates based on detailed evolutionary analyses using state-of-the-art phylogenetic reconstruction methods. It also illustrates the power of adopting an integrative comparative approach supplementing the reconstruction of the duplication history of the gene family with complementary functional experiments in order to elucidate the function of the newly discovered SIRT8 family member. These results provide a reference phylogenetic framework for the evolution of sirtuin genes and the further functional characterization of the eight vertebrate paralogs with potential relevance for understanding the cellular biology of aging and its associated diseases in human.

References

[1] Vassilopoulos A, Fritz KS, Petersen DR, Gius D (2011) The human sirtuin family: Evolutionary divergences and functions. Human Genomics, 5, 485. https://doi.org/10.1186/1479-7364-5-5-485

[2] Yamamoto H, Schoonjans K, Auwerx J (2007) Sirtuin Functions in Health and Disease. Molecular Endocrinology, 21, 1745–1755. https://doi.org/10.1210/me.2007-0079

[3] Morris BJ (2013) Seven sirtuins for seven deadly diseases ofaging. Free Radical Biology and Medicine, 56, 133–171. https://doi.org/10.1016/j.freeradbiomed.2012.10.525

[4] Bordo D Structure and Evolution of Human Sirtuins. Current Drug Targets, 14, 662–665. http://dx.doi.org/10.2174/1389450111314060007

[5] Opazo JC, Vandewege MW, Hoffmann FG, Zavala K, Meléndez C, Luchsinger C, Cavieres VA, Vargas-Chacoff L, Morera FJ, Burgos PV, Tapia-Rojas C, Mardones GA (2022) How many sirtuin genes are out there? evolution of sirtuin genes in vertebrates with a description of a new family member. bioRxiv, 2020.07.17.209510, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology.  https://doi.org/10.1101/2020.07.17.209510

[6] Eisen JA (1998) Phylogenomics: Improving Functional Predictions for Uncharacterized Genes by Evolutionary Analysis. Genome Research, 8, 163–167. https://doi.org/10.1101/gr.8.3.163

How many sirtuin genes are out there? evolution of sirtuin genes in vertebrates with a description of a new family memberJuan C. Opazo, Michael W. Vandewege, Federico G. Hoffmann, Kattina Zavala, Catalina Meléndez, Charlotte Luchsinger, Viviana A. Cavieres, Luis Vargas-Chacoff, Francisco J. Morera, Patricia V. Burgos, Cheril Tapia-Rojas, Gonzalo A. Mardones<p style="text-align: justify;">Studying the evolutionary history of gene families is a challenging and exciting task with a wide range of implications. In addition to exploring fundamental questions about the origin and evolution of genes, disent...Molecular EvolutionFrédéric Delsuc Filipe Castro, Anonymous, Nicolas Leurs2022-05-12 16:06:04 View
09 Dec 2019
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Systematics and geographical distribution of Galba species, a group of cryptic and worldwide freshwater snails

The challenge of delineating species when they are hidden

Recommended by based on reviews by Pavel Matos, Christelle Fraïsse and Niklas Wahlberg

The science of naming species (taxonomy) has been renewed with the developments of molecular sequencing, digitization of museum specimens, and novel analytical tools. However, naming species can be highly subjective, sometimes considered as an art [1], because it is based on human-based criteria that vary among taxonomists. Nonetheless, taxonomists often argue that species names are hypotheses, which are therefore testable and refutable as new evidence is provided. This challenge comes with a more and more recognized and critical need for rigorously delineated species not only for producing accurate species inventories, but more importantly many questions in evolutionary biology (e.g. speciation), ecology (e.g. ecosystem structure and functioning), conservation biology (e.g. targeting priorities) or biogeography (e.g. diversification processes) depend in part on those species inventories and our knowledge of species [2-3]. Inaccurate species boundaries or diversity estimates may lead us to deliver biased answers to those questions, exactly as phylogenetic trees must be reconstructed rigorously and analyzed critically because they are a first step toward discussing broader questions [2-3]. In this context, biological diversity needs to be studied from multiple and complementary perspectives requiring the collaboration of morphologists, molecular biologists, biogeographers, and modelers [4-5]. Integrative taxonomy has been proposed as a solution to tackle the challenge of delimiting species [2], especially in highly diverse and undocumented groups of organisms.
In an elegant study that harbors all the characteristics of an integrative approach, Alda et al. [6] tackle the delimitation of species within the snail genus Galba (Lymnaeidae). Snails of this genus represent a peculiar case study for species delineation with a long and convoluted taxonomic history in which previous works recognized a number of species ranging from 4 to 30. The confusion is likely due to a loose morphology (labile shell features and high plasticity), which makes the identification and naming of species very unstable and likely subjective. An integrative taxonomic approach was needed. After two decades of taxon sampling and visits of type localities, the authors present an impressively dense taxon sampling at a global scale for the genus, which includes all described species. When it comes to delineate species, taxon sampling is often the key if we want to embrace the genetic and morphological diversity. Molecular data was obtained for several types of markers (microsatellites and DNA sequences for four genes), which were combined to morphology of shell and of internal organs, and to geographic distribution. All the data are thoroughly analyzed with cutting-edge methods starting from Bayesian phylogenetic reconstructions using multispecies coalescent models, followed by models of species delimitation based on the molecular specimen-level phylogeny, and then Bayesian divergence time estimates. They also used probabilistic models of ancestral state estimation to infer the ancestral phenotypic state of the Galba ancestors.
Their numerous phylogenetic and delimitation analyses allow to redefine the species boundaries that indicate that the genus Galba comprises six species. Interestingly, four of these species are morphologically cryptic and likely constitute species with extensive genetic diversity and widespread geographic distribution. The other two species have more geographically restricted distributions and exhibit an alternative morphology that is more phylogenetically derived than the cryptic one. Although further genomic studies would be required to strengthen some species status, this novel delimitation of Galba species has important implications for our understanding of convergence and morphological stasis, or the role for stabilizing selection in amphibious habitats; topics that are rarely addressed with invertebrate groups. For instance, in terms of macroevolutionary history, it is striking that an invertebrate clade of that age (22 million years ago) has only given birth to six species today. Including 30 (ancient taxonomy) or 6 (integrative taxonomy) species in a similar amount of evolutionary time does not tell us the same story when studying the diversification processes [7]. Here, Alda et al. [6] present a convincing case study that should foster similar studies following their approach, which will provide stimulating perspectives for testing the concepts of species and their effects on evolutionary biology.

References

[1] Ohl, M. (2018). The art of naming. MIT Press.
[2] Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society, 85(3), 407–415. doi: 10.1111/j.1095-8312.2005.00503.x
[3] De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56(6), 879–886. doi: 10.1080/10635150701701083
[4] Padial, J. M., Miralles, A., De la Riva, I., and Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology, 7(1), 16. doi: 10.1186/1742-9994-7-16
[5] Schlick-Steiner, B. C., Steiner, F. M., Seifert, B., Stauffer, C., Christian, E., and Crozier, R. H. (2010). Integrative taxonomy: A multisource approach to exploring biodiversity. Annual Review of Entomology, 55(1), 421–438. doi: 10.1146/annurev-ento-112408-085432
[6] Alda, P. et al. (2019). Systematics and geographical distribution of Galba species, a group of cryptic and worldwide freshwater snails. BioRxiv, 647867, v3 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/647867
[7] Ruane, S., Bryson, R. W., Pyron, R. A., and Burbrink, F. T. (2014). Coalescent species delimitation in milksnakes (Genus Lampropeltis) and impacts on phylogenetic comparative analyses. Systematic Biology, 63(2), 231–250. doi: 10.1093/sysbio/syt099

Systematics and geographical distribution of Galba species, a group of cryptic and worldwide freshwater snailsPilar Alda, Manon Lounnas, Antonio Alejandro Vázquez, Rolando Ayaqui, Manuel Calvopina, Maritza Celi-Erazo, Robert Dillon, Luisa Carolina González Ramírez, Eric S. Loker, Jenny Muzzio-Aroca, Alberto Orlando Nárvaez, Oscar Noya, Andrés Esteban Pere...<p>Cryptic species can present a significant challenge to the application of systematic and biogeographic principles, especially if they are invasive or transmit parasites or pathogens. Detecting cryptic species requires a pluralistic approach in ...Phylogeography & Biogeography, Systematics / TaxonomyFabien Condamine Pavel Matos, Christelle Fraïsse2019-05-25 10:34:57 View
28 Sep 2020
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Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage

Evolutionary insights into disassortative mating and its association to an ecologically relevant supergene

Recommended by ORCID_LOGO based on reviews by Tom Van Dooren and 2 anonymous reviewers

*Heliconius* butterflies are famous for their colorful wing patterns acting as a warning of their chemical defenses [1]. Most species are involved in Müllerian mimicry assemblies, as predators learn to associate common wing patterns with unpalatability and preferentially target rare variants. Such positive-frequency dependent selection homogenizes wing patterns at different localities, and in several species, all individuals within a community belong to the same morph [2]. In this respect, *H. numata* stands out. This species shows stable local polymorphism across multiple localities, with local populations home to up to seven distinct morphs [2]. Although a balance between migration and local positive-frequency dependent selection can allow some degree of local polymorphism, theory suggests that this occurs only when migration is within a narrow window [3]. One factor that potentially enhances local polymorphism in *H. numata* is disassortative mating. Mate choice assays have in fact revealed that females of this species tend to reject males with the same wing pattern [4]. However the evolution of such mating behavior and its effect on polymorphism remain unclear when selection is locally positive-frequency dependent. Using a mathematical model, Maisonneuve *et al.* [5] clarify the conditions that favor the evolution of disassortative mating in the complicated system of *H. numata*. In particular, they investigate whether the genetic basis of wing colour can favor the emergence of disassortative mating. Variation in wing pattern in *H. numata* is controlled by the supergene P, which is a single genomic region harboring multiple protein coding genes that have ceased to recombine due to chromosomal inversions [6]. If such remarkable genetic configuration allows for the co-adaptation of multiple loci participating to a complex phenotype such as wing color pattern, the absence of recombination can also result in the accumulation of deleterious mutations [7]. In fact, alleles at the P locus have been associated with a recessive genetic load, leading to a fitness advantage for heterozygotes at this locus [8]. Can this fitness advantage to heterozygotes lead to the evolution of disassortative mating? And if so, can such evolution lead to the maintenance of local polymorphism in spite of strong positive frequency-dependent selection? To investigate these questions, Maisonneuve *et al.* [5] model evolution at two loci, one is the P locus for wing pattern, and the other influences mating behavior. The population is divided among two connected patches that differ in their butterfly communities, so that different alleles at the P locus are favored by positive frequency-dependent selection in different patches. The different alleles at the P locus are ordered in dominance relationships such that the most dominant over wing color pattern are also those with the highest load. By tracking the dynamics of haplotype frequencies in the population, the authors first show that disassortative mating readily evolves via the invasion of an allele causing females carrying it to reject males that resemble them phenotypically. Such “self-referencing” mechanism of mate choice, however, has never been reported and has been argued to be rare due to its complicated nature [9]. Maisonneuve *et al.* [5] then compare the evolution of disassortative mating via two alternative mechanisms: attraction and rejection. In these cases, alleles at the mating locus determine attraction to or rejection of specific phenotypes (e.g., under attraction rule, allele “B” encodes attraction to males with phenotype B). With the P and mating loci fully linked, disassortative mating can evolve under all three mechanisms (self-referencing, attraction and rejection), but tends to be less prevalent at equilibrium under attraction rule. This in turn results in the maintenance of less genetic variation under attraction compared to the other mating mechanisms. The loss of variation that occurs under attraction rules is due to a combination of dominance relationships between alleles at the P locus and the searching cost to females in finding rare types of males. When a particular wing pattern, say B, is only expressed in homozygotic form, B males are relatively rare. Females that carry the allele at the mating locus causing them to be attracted to such males then suffer a fitness cost due to lost mating opportunities. This mating allele is therefore purged, and in turn so is the recessive allele for B phenotype at the P locus. Under self-referencing and rejection rules, however, choosy females only reject males of a specific phenotype. They can therefore potentially mate with larger pool of males than females attracted to a single type. As a result, self-referencing and rejection rules are less sensitive to demographic effects and so are more conducive to disassortative mating evolution. In their final analysis, Maisonneuve *et al.* [5] investigate the influence of recombination among the P and mating loci. They show that recombination has different effects on disassortative mating evolution depending on the mechanism of mate choice. Under the self-referencing rule, loose linkage leads to higher levels of disassortative mating and polymorphism than when linkage is tight. Under attraction or rejection rule, however, even very limited recombination completely inhibits the evolution of disassortative mating. This is because, with alleles at the mating locus coding for attraction/rejection to specific males, recombination breaks the association between the P and mating loci necessary for disassortative mating. By contrast, disassortative mating via a self-referencing rule does not depend on the linkage among the P and mating loci: females choose males that are different to themselves independently from the alleles they carry at the P locus. Taken together, Maisonneuve *et al.*’s analyses [5] show that disassortative mating can readily evolve in a system like *H. numata*, but that this evolution depends on the genetic architecture of mating behavior. The architectures that are more conducive to the evolution of disassortative mating are: (1) epistatic interactions among the P and mating loci such that females are able to recognize their own phenotype and base their mating decision upon this information (self-referencing rule); and (2) full linkage among the P supergene and a mating locus that triggers rejection of a specific color pattern. While the mechanisms behind disassortative mating remain to be elucidated, assortative mating seems to rely on alleles triggering attraction to specific cues with variation in attraction and cues linked together [10]. These observations support the notion that disassortative mating is due to alleles causing rejection, in tight linkage to the P locus. If so, mating loci would in fact be part of the P supergene, thus controlling not only intricate wing color pattern but also mating behavior. Beyond the specific system of *H. numata*, Maisonneuve *et al.*’s study [5] helps understand the evolution of disassortative mating and its association with the genetic architecture of correlated traits. In particular, Maisonneuve *et al.* [5] expands the role of supergenes for ecologically relevant traits to mating behavior, further bolstering the relevance of these remarkable genetic elements in the maintenance of variation in complex and elaborate phenotypes. **References** [1] Merrill, R M, K K Dasmahapatra, J W Davey, D D Dell'Aglio, J J Hanly, B Huber, C D Jiggins, et al. (2015). The Diversification of Heliconius butterflies: What Have We Learned in 150 Years? Journal of Evolutionary Biology 28 (8), 1417–38. [https://doi.org/10.1111/jeb.12672.](https://doi.org/10.1111/jeb.12672.) [2] Joron M, IR Wynne, G Lamas, and J Mallet (1999). Variable selection and the coexistence of multiple mimetic forms of the butterfly Heliconius numata. Evolutionary Ecology 13, 721– 754. [https://doi.org/10.1023/A:1010875213123](https://doi.org/10.1023/A:1010875213123) [3] Joron M and Y Iwasa (2005). The evolution of a Müllerian mimic in a spatially distributed community. Journal of Theoretical Biology 237, 87–103. [https://doi.org/10.1016/j.jtbi.2005.04.005](https://doi.org/10.1016/j.jtbi.2005.04.005) [4] Chouteau M, V Llaurens, F Piron-Prunier, and M Joron (2017). Polymorphism at a mimicry su- pergene maintained by opposing frequency-dependent selection pressures. Proceedings of the National Academy of Sciences 114, 8325–8329. [https://doi.org/10.1073/pnas.1702482114](https://doi.org/10.1073/pnas.1702482114) [5] Maisonneuve, L, Chouteau, M, Joron, M and Llaurens, V. (2020). Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage. bioRxiv, 616409, ver. 9 peer-reviewed and recommended by PCI Evolutionary Biology. [https://doi.org/10.1101/616409](https://doi.org/10.1101/616409) [6] Joron M, L Frezal, RT Jones, NL Chamberlain, SF Lee, CR Haag, A Whibley, M Becuwe, SW Baxter, L Ferguson, et al. (2011). Chromosomal rearrangements maintain a polymorphic super- gene controlling butterfly mimicry. Nature 477, 203. [https://doi.org/10.1038/nature10341](https://doi.org/10.1038/nature10341) [7] Schwander T, R Libbrecht, and L Keller (2014). Supergenes and Complex Phenotypes.” Current Biology. 24 (7), 288–94. [https://doi.org/10.1016/j.cub.2014.01.056.](https://doi.org/10.1016/j.cub.2014.01.056.) [8] Jay P, M Chouteau, A Whibley, H Bastide, V Llaurens, H Parrinello, and M Joron (2019). Mutation accumulation in chromosomal inversions maintains wing pattern polymorphism in a butterfly. bioRxiv. [https://doi.org/ 10.1101/736504. ](https://doi.org/ 10.1101/736504. ) [9] Kopp M, MR Servedio, TC Mendelson, RJ Safran, RL Rodrıguez, ME Hauber, EC Scordato, LB Symes, CN Balakrishnan, DM Zonana, et al. (2018). Mechanisms of assortative mating in speciation with gene flow: connecting theory and empirical research. The American Naturalist 191, 1–20. [https://doi.org/10.1086/694889](https://doi.org/10.1086/694889) [10] Merrill RM, P Rastas, SH Martin, MC Melo, S Barker, J Davey, WO McMillan, and CD Jiggins (2019). Genetic dissection of assortative mating behavior. PLoS biology 17, e2005902. [https://doi.org/10.1371/journal.pbio.2005902](https://doi.org/10.1371/journal.pbio.2005902)

Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantageLudovic Maisonneuve, Mathieu Joron, Mathieu Chouteau and Violaine Llaurens<p>The evolution of mate preferences may depend on natural selection acting on the mating cues and on the underlying genetic architecture. While the evolution of assortative mating with respect to locally adapted traits has been well-characterized...Evolutionary Theory, Population Genetics / Genomics, Reproduction and Sex, Sexual SelectionCharles Mullon2019-10-29 09:55:18 View
11 May 2023
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Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages

Flexibility in Aphid Endosymbiosis: Dual Symbioses Have Evolved Anew at Least Six Times

Recommended by based on reviews by Alex C. C. Wilson and 1 anonymous reviewer

In this intriguing study (Manzano-Marín et al. 2022) by Alejandro Manzano-Marin and his colleagues, the association between aphids and their symbionts is investigated through meta-genomic analysis of new samples. These associations have been previously described as leading to fascinating genomic evolution in the symbiont (McCutcheon and Moran 2012). The bacterial genomes exhibit a significant reduction in size and the range of functions performed. They typically lose the ability to produce many metabolites or biobricks created by the host, and instead, streamline their metabolism by focusing on the amino acids that the host cannot produce. This level of co-evolution suggests a stable association between the two partners.

However, the new data suggests a much more complex pattern as multiple independent acquisitions of co-symbionts are observed. Co-symbiont acquisition leads to a partition of the functions carried out on the bacterial side, with the new co-symbiont taking over some of the functions previously performed by Buchnera. In most cases, the new co-symbiont also brings the ability to produce B1 vitamin. Various facultative symbiotic taxa are recruited to be co-symbionts, with the frequency of acquisition related to the bacterial niche and lifestyle.
Despite this diversity of associations, the evolution of co-obligate symbiosis in aphids commonly involves just a handful of nutritional pathways. These include tryptophan biosynthesis (twice), histidine biosynthesis, riboflavin biosynthesis (six times), and biotin biosynthesis (five times). Microscopy analyses suggest that some co-symbionts colonize different bacteriocytes. Yet, a few traces of horizontal gene transfers in Buchnera suggest that some contact with other bacteria may occasionally occur.
The emergence of multiple co-symbioses highlights the success of a "menage à trois". However, this success is achieved by adding a new co-symbiont to an already established pair. It is possible that the slow but irreversible decay of the bacterial genome under symbiosis may lead to a degradation of the partnership, creating a niche for the acquisition of new bacteria to maintain the symbiosis.

REFERENCES

Manzano-Marín, Alejandro, Armelle Coeur D’acier, Anne-Laure Clamens, Corinne Cruaud, Valérie Barbe, and Emmanuelle Jousselin. 2023. “Co-Obligate Symbioses Have Repeatedly Evolved across Aphids, but Partner Identity and Nutritional Contributions Vary across Lineages.” bioRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.08.28.505559.

McCutcheon, John P., and Nancy A. Moran. 2012. “Extreme Genome Reduction in Symbiotic Bacteria.” Nature Reviews Microbiology 10 (1): 13–26. https://doi.org/10.1038/nrmicro2670.

Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineagesAlejandro Manzano-Marín, Armelle Coeur d'acier, Anne-Laure Clamens, Corinne Cruaud, Valérie Barbe, Emmanuelle Jousselin<p style="text-align: justify;">Aphids are a large family of phloem-sap feeders. They typically rely on a single bacterial endosymbiont, <em>Buchnera aphidicola</em>, to supply them with essential nutrients lacking in their diet. This association ...Genome Evolution, Other, Species interactionsOlivier Tenaillon2022-11-16 10:13:37 View
13 Nov 2023
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Color polymorphism and conspicuousness do not increase speciation rates in Lacertids

Colour polymorphism does not increase diversification rates in lizards

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

The striking differences in species richness among lineages in the Tree of Life have long attracted much research interest. In particular, researchers have asked whether certain traits are associated with greater diversification, with a particular focus on traits under sexual selection given their direct link to mating isolation.

Polymorphism, defined as the presence of co-occurring, heritable morphs within a population, has been proposed to influence diversification rates although the effect has been proposed as both promoting or alternatively impeding speciation. The effect of polymorphism may be positive, that is facilitating speciation if polymorphism allows to broaden the ecological niche, thus enabling range expansion, or enabling maintenance of populations in variable environments. Specialized ectomorphs have been observed in several species (e.g. Kusche et al. 2015, Lattanzio and Miles 2016, Whitney et al. 2018, Scali et al. 2016). Polymorphism may also facilitate speciation if a morph is lost during the colonization of a novel area or niche, resulting in rapid divergence of the remaining morphs and reproductive isolation from the ancestral population, known as the morph speciation hypothesis (West-Eberhard 1986, Corl et al. 2010). On the other hand, polymorphism may hamper speciation through disassortative maintaining by morph, which may maintain the polymorphism through the speciation process (Jamie and Meier 2020). An example of such a process is Heliconius numata where disassortative mate preferences based on color hampers ecological speciation (Chouteau et al. 2017). Previous evidence in birds and lizards suggests polymorphism favors diversification (Corl et al. 2010b, 2012, Hugall and Stuart-Fox 2012, Brock et al. 2021).

Here, de Solan et al. (2023) test the effect of polymorphism on diversification in Lacertidae, a family of lizards containing more than 300 species distributed across Europe, Africa and Asia. The group offers a good model system to test the effect of polymorphism on speciation as it contains several species with colour polymorphism, sometimes present in both sexes but restricted to males when present in the flank. Using coloration data from the literature as well as photographs of live specimens for 295 species the authors tested whether the presence of polymorphism is associated with higher diversification rates.

While undertaking their project, another group independently tackled the same question (Brock et al. 2021), using the same model system but coming to very different conclusions. Therefore, de Solan et al. (2023) decided to also contrast their results with those of Brock et al. (2021) to determine the factors responsible for the contrasting results of both studies. The latter I consider one of the strengths of the work, given the careful re-analyses to determine the causes of the discrepancies between both studies. De Solan et al. (2023) found no association between the presence of polymorphism and diversification rates, even though they used different analytical approaches. Thus, this study is interesting as it provides results that do not support a positive effect of polymorphism on species richness. The use of a phylogeny with more limited species sampling (García-Porta et al. 2019) implied that the authors had to manually add 75 species, of which 17 were added to the tree based on information from previously published trees and 68 were added at random locations within the genus. To control for potential biases the authors repeated the analyses using a sample of trees with the imputed taxa, results were broadly concordant across the set of trees. The careful re-analysis contrasting Brock et al. (2021) and de Solan et al. (2023) results suggests the difference is mainly due to a difference in how species were coded as presenting polymorphism, which differed between the two studies, as well as a difference in the package version used to run the state-dependent diversification models. Interestingly non-parametric analyses yielded similar results across both datasets. 
 
References
 
Brock, K.M., McTavish, E.J., Edwards, D.L. 2021. Colour polymorphism is a driver of diversification in the lizard family Lacertidae. Systematic Biology. 71: 24-39. https://doi.org/10.1093/sysbio/syab046
 
Chouteau, M., Llaurens, V., Piron-Prunier, F., Joron, M. 2017. Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures. Proceedings of the National Academy of Sciences. 114: 8325-8329. https://doi.org/10.1073/pnas.1702482114
 
Corl, A., Davis, A.R., Kuchta, S.R., Comendant, T., Sinervo, B. 2010a. Alternative mating strategies and the evolution of sexual dimorphism in the side-blotched lizard, Uta stansburiana: a population-level comparative analysis. Evolution. 64: 79-96. https://doi.org/10.1111/j.1558-5646.2009.00791.x 
 
Corl, A., Davis, A.R., Kuchta, S.R., Sinervo, B. 2010b. Selective loss of polymorphic mating types is associated with rapid phenotypic evolution during morphic speciation. Proceedings of the National Academy of Sciences. 107: 4254-4259. https://doi.org/10.1073/pnas.0909480107
 
Corl, A., Lancaster, L.T., Sinervo, B. 2012. Rapid formation of reproductive isolation between two populations of side-blotched lizards, Uta stansburiana. Copeia. 2012: 593-602. https://doi.org/10.1643/CH-11-166

Garcia-Porta, J., Irisarri, I., Kirchner, M. et al. 2019. Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards. Nature Communications. 10: 4077. https://doi.org/10.1038/s41467-019-11943-x
 
Hugall, A.F., Stuart-Fox, D. 2012. Accelerated speciation in colour-polymorphic birds. Nature. 485: 631-634. https://doi.org/10.1038/nature11050
 
Jamie, G.A. and Meier, J.I. 2020. The persistence of polymorphisms across species radiations. Trends in Ecology and Evolution. 35: 795-808. https://doi.org/10.1016/j.tree.2020.04.007
 
Kusche, H., Elmer, K.R., Meyer, A. 2015. Sympatric ecological divergence associated with a colour polymorphism. BMC Biology, 13: 82. https://doi.org/10.1186/s12915-015-0192-7
 
Lattanzio, M.S. and Miles, D.B. 2016. Trophic niche divergence among colour morphs that exhibit alternative mating tactics. Royal Society Open Science. 3: 150531. https://doi.org/10.1098/rsos.150531
 
Scali, S., Sacchi, R., Mangiacotti, M., Pupin, F., Gentilli, A., Zucchi, C. Scannolo, M., Pavesi, M., Zuffi, M.A.L. 2016. Does a polymorphic species have a ‘polymorphic’ diet? A case study from a lacertid lizard. Biologcial Journal of the Linnean Society. 117: 492-502. https://doi.org/10.1111/bij.12652

de Solan T, Sinervo B, Geniez P, David P, Crochet P-A (2023) Colour polymorphism and conspicuousness do not increase speciation rates in Lacertids. bioRxiv, 2023.02.15.528678, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.02.15.528678

West-Eberhard, M.J. 1986. Alternative adaptations, speciation, and phylogeny (A review). Proceedings of the National Academy of Sciences. 83: 1388-1392. https://doi.org/10.1073/pnas.83.5.1388
 
Whitney, J.L., Donahue, M.J., Karl, S.A. 2018. Niche divergence along a fine-scale ecological gradient in sympatric colour morphs of a coral reef fish. Ecosphere. 9: e02015. https://doi.org/10.1002/ecs2.2015

Color polymorphism and conspicuousness do not increase speciation rates in LacertidsThomas de Solan, Barry Sinervo, Philippe Geniez, Patrice David, Pierre-André Crochet<p style="text-align: justify;">Conspicuous body colors and color polymorphism have been hypothesized to increase rates of speciation. Conspicuous colors are evolutionary labile, and often involved in intraspecific sexual signaling and thus may pr...Evolutionary Ecology, Macroevolution, SpeciationAlejandro Gonzalez-Voyer2023-02-22 10:05:03 View
31 Mar 2022
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Gene network robustness as a multivariate character

Genetic and environmental robustness are distinct yet correlated evolvable traits in a gene network

Recommended by ORCID_LOGO based on reviews by Diogo Melo, Charles Mullon and Charles Rocabert

Organisms often show robustness to genetic or environmental perturbations. Whether these two components of robustness can evolve separately is the focus of the paper by Le Rouzic [1]. Using theoretical analysis and individual-based computer simulations of a gene regulatory network model, he shows that multiple aspects of robustness can be investigated as a set of pleiotropically linked quantitative traits. While genetically correlated, various robustness components (e.g., mutational, developmental, homeostasis) of gene expression in the regulatory network evolved more or less independently from each other under directional selection. The quantitative approach of Le Rouzic could explain both how unselected robustness components can respond to selection on other components and why various robustness-related features seem to have their own evolutionary history. Moreover, he shows that all components were evolvable, but not all to the same extent. Robustness to environmental disturbances and gene expression stability showed the largest responses while increased robustness to genetic disturbances was slower. Interestingly, all components were positively correlated and remained so after selection for increased or decreased robustness.

This study is an important contribution to the discussion of the evolution of robustness in biological systems. While it has long been recognized that organisms possess the ability to buffer genetic and environmental perturbations to maintain homeostasis (e.g., canalization [2]), the genetic basis and evolutionary routes to robustness and canalization are still not well understood. Models of regulatory gene networks have often been used to address aspects of robustness evolution (e.g., [3]). Le Rouzic [1] used a gene regulatory network model derived from Wagner’s model [4]. The model has as end product the expression level of a set of genes influenced by a set of regulatory elements (e.g., transcription factors). The level and stability of expression are a property of the regulatory interactions in the network.

Le Rouzic made an important contribution to the study of such gene regulation models by using a quantitative genetics approach to the evolution of robustness. He crafted a way to assess the mutational variability and selection response of the components of robustness he was interested in. Le Rouzic’s approach opens avenues to investigate further aspects of gene network evolutionary properties, for instance to understand the evolution of phenotypic plasticity.

Le Rouzic also discusses ways to measure his different robustness components in empirical studies. As the model is about gene expression levels at a set of protein-coding genes influenced by a set of regulatory elements, it naturally points to the possibility of using RNA sequencing to measure the variation of gene expression in know gene networks and assess their robustness. Robustness could then be studied as a multidimensional quantitative trait in an experimental setting.

References

[1] Le Rouzic, A (2022) Gene network robustness as a multivariate character. arXiv: 2101.01564, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://arxiv.org/abs/2101.01564

[2] Waddington CH (1942) Canalization of Development and the Inheritance of Acquired Characters. Nature, 150, 563–565. https://doi.org/10.1038/150563a0

[3] Draghi J, Whitlock M (2015) Robustness to noise in gene expression evolves despite epistatic constraints in a model of gene networks. Evolution, 69, 2345–2358. https://doi.org/10.1111/evo.12732

[4] Wagner A (1994) Evolution of gene networks by gene duplications: a mathematical model and its implications on genome organization. Proceedings of the National Academy of Sciences, 91, 4387–4391. https://doi.org/10.1073/pnas.91.10.4387

Gene network robustness as a multivariate characterArnaud Le Rouzic<p style="text-align: justify;">Robustness to genetic or environmental disturbances is often considered as a key property of living systems. Yet, in spite of being discussed since the 1950s, how robustness emerges from the complexity of genetic ar...Bioinformatics & Computational Biology, Evolutionary Theory, Genotype-Phenotype, Quantitative GeneticsFrédéric Guillaume Charles Mullon, Charles Rocabert, Diogo Melo2021-01-11 17:48:20 View
14 May 2020
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Potential adaptive divergence between subspecies and populations of snapdragon plants inferred from QST – FST comparisons

From populations to subspecies… to species? Contrasting patterns of local adaptation in closely-related taxa and their potential contribution to species divergence

Recommended by based on reviews by Sophie Karrenberg, Santiago C. Gonzalez-Martinez and 1 anonymous reviewer

Elevation gradients are convenient and widely used natural setups to study local adaptation, particularly in these times of rapid climate change [e.g. 1]. Marin and her collaborators [2] did not follow the mainstream, however. Instead of tackling adaptation to climate change, they used elevation gradients to address another crucial evolutionary question [3]: could adaptation to altitude lead to ecological speciation, i.e. reproductive isolation between populations in spite of gene flow? More specifically, they examined how much local adaptation to environmental variation differed among closely-related, recently diverged subspecies. They studied several populations of two subspecies of snapdragon (Antirrhinum majus), with adjacent geographical distributions. Using common garden experiments and the classical, but still useful, QST-FST comparison, they demonstrate contrasting patterns of local adaptation to altitude between the two subspecies, with several traits under divergent selection in A. majus striatum but none in A. majus pseudomajus. These differences in local adaptation may contribute to species divergence, and open many stimulating questions on the underlying mechanisms, such as the identity of environmental drivers or contribution of reproductive isolation involving flower color polymorphism.

References

[1] Anderson, J. T., and Wadgymar, S. M. (2020). Climate change disrupts local adaptation and favours upslope migration. Ecology letters, 23(1), 181-192. doi: 10.1111/ele.13427
[2] Marin, S., Gibert, A., Archambeau, J., Bonhomme, V., Lascoste, M., and Pujol, B. (2020). Potential adaptive divergence between subspecies and populations of snapdragon plants inferred from QST – FST comparisons. Zenodo, 3628168, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. doi: 10.5281/zenodo.3628168
[3] Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science, 323(5915), 737-741. doi: 10.1126/science.1160006

Potential adaptive divergence between subspecies and populations of snapdragon plants inferred from QST – FST comparisonsSara Marin, Anaïs Gibert, Juliette Archambeau, Vincent Bonhomme, Mylène Lascoste and Benoit Pujol<p>Phenotypic divergence among natural populations can be explained by natural selection or by neutral processes such as drift. Many examples in the literature compare putatively neutral (FST) and quantitative genetic (QST) differentiation in mult...Adaptation, Evolutionary Ecology, Genotype-Phenotype, Morphological Evolution, Quantitative GeneticsEmmanuelle Porcher2018-08-05 15:34:30 View