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  • 1.
    Bachmann, Jörg A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Tedder, Andrew
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Steige, Kim A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Targeted Long-Read Sequencing of a Locus Under Long-Term Balancing Selection in Capsella2018In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 8, no 4, p. 1327-1333Article in journal (Refereed)
    Abstract [en]

    Rapid advances in short-read DNA sequencing technologies have revolutionized population genomic studies, but there are genomic regions where this technology reaches its limits. Limitations mostly arise due to the difficulties in assembly or alignment to genomic regions of high sequence divergence and high repeat content, which are typical characteristics for loci under strong long-term balancing selection. Studying genetic diversity at such loci therefore remains challenging. Here, we investigate the feasibility and error rates associated with targeted long-read sequencing of a locus under balancing selection. For this purpose, we generated bacterial artificial chromosomes (BACs) containing the Brassicaceae S-locus, a region under strong negative frequency-dependent selection which has previously proven difficult to assemble in its entirety using short reads. We sequence S-locus BACs with single-molecule long-read sequencing technology and conduct de novo assembly of these S-locus haplotypes. By comparing repeated assemblies resulting from independent long-read sequencing runs on the same BAC clone we do not detect any structural errors, suggesting that reliable assemblies are generated, but we estimate an indel error rate of 5.7x10(-5). A similar error rate was estimated based on comparison of Illumina short-read sequences and BAC assemblies. Our results show that, until de novo assembly of multiple individuals using long-read sequencing becomes feasible, targeted long-read sequencing of loci under balancing selection is a viable option with low error rates for single nucleotide polymorphisms or structural variation. We further find that short-read sequencing is a valuable complement, allowing correction of the relatively high rate of indel errors that result from this approach.

  • 2. Desamore, Aurelie
    et al.
    Patino, Jairo
    Mardulyn, Patrick
    Mcdaniel, Stuart F.
    Zanatta, Florian
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). University of Liège, Belgium.
    Vanderpoorten, Alain
    High migration rates shape the postglacial history of amphi-Atlantic bryophytes2016In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 25, no 21, p. 5568-5584Article in journal (Refereed)
    Abstract [en]

    Paleontological evidence and current patterns of angiosperm species richness suggest that European biota experienced more severe bottlenecks than North American ones during the last glacial maximum. How well this pattern fits other plant species is less clear. Bryophytes offer a unique opportunity to contrast the impact of the last glacial maximum in North America and Europe because about 60% of the European bryoflora is shared with North America. Here, we use population genetic analyses based on approximate Bayesian computation on eight amphi-Atlantic species to test the hypothesis that North American populations were less impacted by the last glacial maximum, exhibiting higher levels of genetic diversity than European ones and ultimately serving as a refugium for the postglacial recolonization of Europe. In contrast with this hypothesis, the best-fit demographic model involved similar patterns of population size contractions, comparable levels of genetic diversity and balanced migration rates between European and North American populations. Our results thus suggest that bryophytes have experienced comparable demographic glacial histories on both sides of the Atlantic. Although a weak, but significant genetic structure was systematically recovered between European and North American populations, evidence for migration from and towards both continents suggests that amphi-Atlantic bryophyte population may function as a metapopulation network. Reconstructing the biogeographic history of either North American or European bryophyte populations therefore requires a large, trans-Atlantic geographic framework.

  • 3. Désamoré, Aurélie
    et al.
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Miller, Kelly B.
    Bergsten, Johannes
    Early burst in body size evolution is uncoupled from species diversification in diving beetles (Dytiscidae)2018In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, no 4, p. 979-993Article in journal (Refereed)
    Abstract [en]

    Changes in morphology are often thought to be linked to changes in species diversification, which is expected to leave a signal of early burst (EB) in phenotypic traits. However, such signal is rarely recovered in empirical phylogenies, even for groups with well-known adaptive radiation. Using a comprehensive phylogenetic approach in Dytiscidae, which harbours similar to 4,300 species with as much as 50-fold variation in body size among them, we ask whether pattern of species diversification correlates with morphological evolution. Additionally, we test whether the large variation in body size is linked to habitat preference and whether the latter influences species turnover. We found, in sharp contrast to most animal groups, that Dytiscidae body size evolution follows an early-burst model with subsequent high phylogenetic conservatism. However, we found no evidence for associated shifts in species diversification, which point to an uncoupled evolution of morphology and species diversification. We recovered the ancestral habitat of Dytiscidae as lentic (standing water), with many transitions to lotic habitat (running water) that are concomitant to a decrease in body size. Finally, we found no evidence for difference in net diversification rates between habitats nor difference in turnover in lentic and lotic species. This result, together with recent findings in dragonflies, contrasts with some theoretical expectations of the habitat stability hypothesis. Thus, a thorough reassessment of the impact of dispersal, gene flow and range size on the speciation process is needed to fully encompass the evolutionary consequences of the lentic-lotic divide for freshwater fauna.

  • 4. Gil-Lopez, Manuel J.
    et al.
    Segarra-Moragues, Jose G.
    Desamore, Aurelie
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Ojeda, Fernando
    Different historical backgrounds determine contrasting phylogeographical patterns in two co-distributed Erica species (Ericaceae) across the Strait of Gibraltar2017In: Botanical journal of the Linnean Society, ISSN 0024-4074, E-ISSN 1095-8339, Vol. 185, no 3, p. 359-375Article in journal (Refereed)
    Abstract [en]

    Erica australis and Erica arborea are morphologically and ecologically similar heather species. Erica australis is restricted to the western Mediterranean Basin where it overlaps with the westernmost distribution of E. arborea. Here we investigate the role of the Strait of Gibraltar (SG) as a potential biogeographical barrier to dispersal and/or as glacial refugium in these two Erica spp. in the western Mediterranean (WMed) region with contrasting geographical origins and distributions. Samples were collected from 55 and 54 populations of E. australis and E. arborea, respectively. One individual each of 52 and 45 populations of E. australis and E. arborea, respectively, were sequenced for plastid DNA regions, and 1304 and 1214 individuals from 44 and 42 populations of E. australis and E. arborea, respectively, were genotyped using nuclear microsatellites (SSRs). Plastid DNA sequences were used to estimate divergence time of lineages and to construct haplotype networks. SSR data helped to infer population genetic diversity and fixation indices and genetic structure patterns through Bayesian analysis, analysis of molecular variance and isolation by distance. Plastid haplotype diversity of E. australis was higher in the SG than in the WMed area, whereas the opposite was found in E. arborea. SSRs revealed high genetic diversity within populations of both species and population genetic structure patterns were consistent with those retrieved from plastid DNA. The SG was identified as the likely area of origin and diversification for E. australis in the late Pliocene-Pleistocene, where it survived the Last Glacial Maximum (LGM) and expanded northwards into the western Iberian Peninsula. In contrast, two separate evolutionary lineages were found for E. arborea in the Iberian Peninsula. The SG and southern WMed areas represent the western Mediterranean expansion limit of an E. arborea lineage from East Africa/Arabia in the late Pliocene-Pleistocene, whereas the northern WMed populations were relicts from an older refugium that survived LGM in north-western Iberia. This study illustrates how geographical range and origin explain differences in the phylogeographical structure of co-distributed Mediterranean plants and highlights the role of the SG as a Pleistocene refugium and biogeographical crossroads in the Mediterranean.

  • 5. Hatorangan, Marcelinus R.
    et al.
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Steige, Kim A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). Uppsala University, Sweden.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Kohler, Claudia
    Rapid Evolution of Genomic Imprinting in Two Species of the Brassicaceae2016In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 28, no 8, p. 1815-1827Article in journal (Refereed)
    Abstract [en]

    Genomic imprinting is an epigenetic phenomenon occurring in mammals and flowering plants that causes genes to adopt a parent-of-origin-specific mode of expression. While the imprinting status of genes is well conserved in mammals, clear estimates for the degree of conservation were lacking in plants. We therefore analyzed the genome-wide imprinting status of Capsella rubella, which shared a common recent ancestor with Arabidopsis thaliana similar to 10 to 14 million years ago. However, only similar to 14% of maternally expressed genes (MEGs) and similar to 29% of paternally expressed genes (PEGs) in C. rubella were commonly imprinted in both species, revealing that genomic imprinting is a rapidly evolving phenomenon in plants. Nevertheless, conserved PEGs exhibited signs of selection, suggesting that a subset of imprinted genes play an important functional role and are therefore maintained in plants. Like in Arabidopsis, PEGs in C. rubella are frequently associated with the presence of transposable elements that preferentially belong to helitron and MuDR families. Our data further reveal that MEGs and PEGs differ in their targeting by 24-nucleotide small RNAs and asymmetric DNA methylation, suggesting different mechanisms establishing DNA methylation at MEGs and PEGs.

  • 6.
    Laenen, Benjamin
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). University of Liège, Belgium.
    Machac, Antonin
    Gradstein, S. Robbert
    Shaw, Blanka
    Patino, Jairo
    Desamore, Aurelie
    Goffinet, Bernard
    Cox, Cymon J.
    Shaw, A. Jonathan
    Vanderpoorten, Alain
    Increased diversification rates follow shifts to bisexuality in liverworts2016In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 210, no 3, p. 1121-1129Article in journal (Refereed)
    Abstract [en]

    Shifts in sexual systems are one of the key drivers of species diversification. In contrast to angiosperms, unisexuality prevails in bryophytes. Here, we test the hypotheses that bisexuality evolved from an ancestral unisexual condition and is a key innovation in liverworts. We investigate whether shifts in sexual systems influence diversification using hidden state speciation and extinction analysis (HiSSE). This new method compares the effects of the variable of interest to the best-fitting latent variable, yielding robust and conservative tests. We find that the transitions in sexual systems are significantly biased toward unisexuality, even though bisexuality is coupled with increased diversification. Sexual systems are strongly conserved deep within the liverwort tree but become much more labile toward the present. Bisexuality appears to be a key innovation in liverworts. Its effects on diversification are presumably mediated by the interplay of high fertilization rates, massive spore production and long-distance dispersal, which may separately or together have facilitated liverwort speciation, suppressed their extinction, or both. Importantly, shifts in liverwort sexual systems have the opposite effect when compared to angiosperms, leading to contrasting diversification patterns between the two groups. The high prevalence of unisexuality among liverworts suggests, however, a strong selection for sexual dimorphism.

  • 7.
    Laenen, Benjamin
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). University of Liège, Belgium.
    Machac, Antonin
    Gradstein, S. Robbert
    Shaw, Blanka
    Patino, Jairo
    Desamore, Aurelie
    Goffinet, Bernard
    Cox, Cymon J.
    Shaw, Jonathan
    Vanderpoorten, Alain
    Geographical range in liverworts: does sex really matter?2016In: Journal of Biogeography, ISSN 0305-0270, E-ISSN 1365-2699, Vol. 43, no 3, p. 627-635Article in journal (Refereed)
    Abstract [en]

    AimWhy some species exhibit larger geographical ranges than others remains a fundamental, but largely unanswered, question in ecology and biogeography. In plants, a relationship between range size and mating system was proposed over a century ago and subsequently formalized in Baker's Law. Here, we take advantage of the extensive variation in sexual systems of liverworts to test the hypothesis that dioecious species compensate for limited fertilization by producing vegetative propagules more commonly than monoecious species. As spores are assumed to contribute to random long-distance dispersal, whereas vegetative propagules contribute to colony maintenance and frequent short-distance dispersal, we further test the hypothesis that monoecious species exhibit larger geographical ranges than dioecious ones. LocationWorldwide. MethodsWe used comparative phylogenetic methods to assess the correlation between range size and life history traits related to dispersal, including mating systems, spore size and production of specialized vegetative propagules. ResultsNo significant correlation was found between dioecy and production of vegetative propagules. However, production of vegetative propagules is correlated with the size of geographical ranges across the liverwort tree of life, whereas sexuality and spores size are not. Moreover, variation in sexual systems did not have an influence on the correlation between geographical range and production of asexual propagules. Main conclusionsOur results challenge the long-held notion that spores, and not vegetative propagules, are involved in long-distance dispersal. Asexual reproduction seems to play a major role in shaping the global distribution patterns of liverworts, so that monoecious species do not tend to display, on average, broader distribution ranges than dioecious ones. Our results call for further investigation on the spatial genetic structure of bryophyte populations at different geographical scales depending on their mating systems to assess the dispersal capacities of spores and asexual propagules and determine their contribution in shaping species distribution ranges.

  • 8.
    Laenen, Benjamin
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Patino, Jairo
    Hagborg, Anders
    Désamoré, Aurélie
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Wang, Jian
    Shaw, A.
    Goffinet, Bernard
    Vanderpoorten, Alain
    Evolutionary origin of the latitudinal diversity gradient in liverworts2018In: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 127, p. 606-612Article in journal (Refereed)
    Abstract [en]

    A latitudinal diversity gradient towards the tropics appears as one most recurrent patterns in ecology, but the mechanisms underlying this pattern remain an area of controversy. In angiosperms, the tropical conservatism hypothesis proposes that most groups originated in the tropics and are adapted to a tropical climatic regime, and that relatively few species have evolved physiological adaptations to cold, dry or unpredictable climates. This mechanism is, however, unlikely to apply across land plants, and in particular, to liverworts, a group of about 7500 species, whose ability to withstand cold much better than their tracheophyte counterparts is at odds with the tropical conservatism hypothesis. Molecular dating, diversification rate analyses and ancestral area reconstructions were employed to explore the evolutionary mechanisms that account for the latitudinal diversity gradient in liverworts. As opposed to angiosperms, tropical liverwort genera are not older than their extratropical counterparts (median stem age of tropical and extra-tropical liverwort genera of 24.35 +/- 39.65 Ma and 39.57 +/- 49.07 Ma, respectively), weakening the `time for speciation hypothesis'. Models of ancestral area reconstructions with equal migration rates between tropical and extra-tropical regions outperformed models with asymmetrical migration rates in either direction. The symmetry and intensity of migrations between tropical and extra-tropical regions suggested by the lack of resolution in ancestral area reconstructions towards the deepest nodes are at odds with the tropical niche conservatism hypothesis. In turn, tropical genera exhibited significantly higher net diversification rates than extra-tropical ones, suggesting that the observed latitudinal diversity gradient results from either higher extinction rates in extra-tropical lineages or higher speciation rates in the tropics. We discuss a series of experiments to help deciphering the underlying evolutionary mechanisms.

  • 9.
    Laenen, Benjamin
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Tedder, Andrew
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Nowak, Michael D.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Toräng, Per
    Wunder, Jörg
    Wötzel, Stefan
    Steige, Kim A.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Kourmpetis, Yiannis
    Odong, Thomas
    Drouzas, Andreas D.
    Bink, Marco C. A. M.
    Ågren, Jon
    Coupland, George
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina2018In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 115, no 4, p. 816-821Article in journal (Refereed)
    Abstract [en]

    Plant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population-genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles, whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.

  • 10. Patino, Jairo
    et al.
    Wang, Jian
    Renner, Matt A. M.
    Gradstein, S. Robbert
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Devos, Nicolas
    Shaw, A. Jonathan
    Vanderpoorten, Alain
    Range size heritability and diversification patterns in the liverwort genus Radula2017In: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 106, p. 73-85Article in journal (Refereed)
    Abstract [en]

    Why some species exhibit larger geographical ranges than others, and to what extent does variation in range size affect diversification rates, remains a fundamental, but largely unanswered question in ecology and evolution. Here, we implement phylogenetic comparative analyses and ancestral area estimations in Radula, a liverwort genus of Cretaceous origin, to investigate the mechanisms that explain differences in geographical range size and diversification rates among lineages. Range size was phylogenetically constrained in the two sub-genera characterized by their almost complete Australasian and Neotropical endemicity, respectively. The congruence between the divergence time of these lineages and continental split suggests that plate tectonics could have played a major role in their present distribution, suggesting that a strong imprint of vicariance can still be found in extant distribution patterns in these highly mobile organisms. Amentuloradula, Volutoradula and Metaradula species did not appear to exhibit losses of dispersal capacities in terms of dispersal life-history traits, but evidence for significant phylogenetic signal in macroecological niche traits suggests that niche conservatism accounts for their restricted geographic ranges. Despite their greatly restricted distribution to Australasia and Neotropics respectively, Amentuloradula and Volutoradula did not exhibit significantly lower diversification rates than more widespread lineages, in contrast with the hypothesis that the probability of speciation increases with range size by promoting geographic isolation and increasing the rate at which novel habitats are encountered. We suggest that stochastic long-distance dispersal events may balance allele frequencies across large spatial scales, leading to low genetic structure among geographically distant areas or even continents, ultimately decreasing the diversification rates in highly mobile, widespread lineages.

  • 11. Sim-Sim, Manuela
    et al.
    Afonina, Olga M.
    Almeida, Tereza
    Desamore, Aurelie
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
    Garcia, Cesar Augusto
    Gonzalez-Mancebo, Juana M.
    Stech, Michael
    Integrative taxonomy reveals too extensive lumping and a new species in the moss genus Amphidium (Bryophyta)2017In: Systematics and Biodiversity, ISSN 1477-2000, E-ISSN 1478-0933, Vol. 15, no 5, p. 451-463Article in journal (Refereed)
    Abstract [en]

    An integrative taxonomic approach, including molecular phylogenetic reconstructions based on plastid rps4-trnF and nuclear ITS sequences, statistical analysis of morphological-anatomical characters, and classical taxonomy, indicates that the reduction of 13 Amphidium species to three in a recent morphological revision represents a case of too extensive lumping. Instead, six Amphidium species can be distinguished based on molecular and morphological data, the widespread Amphidium lapponicum, A. mougeotii, and A. tortuosum, as well as the Macaronesian endemic A. curvipes, the North American endemic A. californicum, and a newly discovered species from Central Asia (southern Siberia and northern Mongolia), A. asiaticum sp. nov. Diagnostic morphological characters for all six species are discussed. The present data confirm that species diversity of Amphidium is highest in the Holarctic, where all six species occur.

  • 12.
    Steige, Kim A.
    et al.
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). Uppsala University, Sweden.
    Laenen, Benjamin
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab).
    Reimegård, Johan
    Scofield, Douglas G.
    Slotte, Tanja
    Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Science for Life Laboratory (SciLifeLab). Uppsala University, Sweden.
    Genomic analysis reveals major determinants of cis-regulatory variation in Capsella grandiflora2017In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 114, no 5, p. 1087-1092Article in journal (Refereed)
    Abstract [en]

    Understanding the causes of cis-regulatory variation is a long-standing aim in evolutionary biology. Although cis-regulatory variation has long been considered important for adaptation, we still have a limited understanding of the selective importance and genomic determinants of standing cis-regulatory variation. To address these questions, we studied the prevalence, genomic determinants, and selective forces shaping cis-regulatory variation in the outcrossing plant Capsella grandiflora. We first identified a set of 1,010 genes with common cis-regulatory variation using analyses of allele-specific expression (ASE). Population genomic analyses of whole-genome sequences from 32 individuals showed that genes with common cis-regulatory variation (i) are underweaker purifying selection and (ii) undergo less frequent positive selection than other genes. We further identified genomic determinants of cis-regulatory variation. Gene body methylation (gbM) was a major factor constraining cis-regulatory variation, whereas presence of nearby transposable elements (TEs) and tissue specificity of expression increased the odds of ASE. Our results suggest that most common cis-regulatory variation in C. grandiflora is under weak purifying selection, and that gene-specific functional constraints are more important for the maintenance of cis-regulatory variation than genome-scale variation in the intensity of selection. Our results agree with previous findings that suggest TE silencing affects nearby gene expression, and provide evidence for a link between gbM and cis-regulatory constraint, possibly reflecting greater dosage sensitivity of body-methylated genes. Given the extensive conservation of gbM in flowering plants, this suggests that gbM could be an important predictor of cis-regulatory variation in a wide range of plant species.

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