Limited directional selection but coevolutionary signals among imprinted genes in A. lyrata

  1. Audrey Le veve
  2. Ömer Iltas
  3. Julien Dutheil
  4. Clement Lafon Placette

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Abstract

Genomic imprinting is a form of gene regulation leading to the unequal expression of maternal and paternal alleles. The main hypothesis invoked to explain the evolution of imprinted genes is the kinship theory, which posits a conflict between parental genomes over resource allocation in progeny. According to this theory, such conflicts select for parent-of-origin–dependent expression of genes involved in resource allocation. How such conflicts translate into signatures of selection at coding or regulatory sequences remains model-dependent and is not explicitly predicted by the kinship theory. However, most studies addressing selection in imprinted genes in flowering plants, particularly those based on population-genomic or phylogenetic analyses, have focused on self-fertilizing species, where conflicts over resource allocation are predicted to be weak. Consequently, the impact of the kinship theory on the evolution of imprinted genes remains largely unexplored in systems where parental conflict is expected to be strong. Furthermore, potential coevolution between antagonistically acting imprinted genes, as proposed in extensions of parental conflict models, has not yet been tested empirically. Using combined phylogenetic and population genomic approaches, we investigated signatures of selection on imprinted genes across the Brassicaceae family and in autogamous and allogamous populations of Arabidopsis lyrata, and searched for evidence of coevolution among imprinted genes. We found that endosperm-expressed genes exhibited signals of balancing selection across Brassicaceae and within allogamous populations, consistent with models of unresolved intralocus conflict. These population-level signals varied with the mating system, in line with expectations that parental conflict is reduced under self-fertilization. Moreover, phylogenetic analyses indicated signatures of purifying (negative) selection acting on imprinted genes. However, the population-level signatures of selection were independent of the mating system and showed limited concordance with kinship predictions, possibly due to stronger selection acting on expression than on coding sequences. Finally, we identified coevolution between imprinted genes, although not at specific sites, suggesting that interactions beyond protein sequence may contribute to this process.

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  1. Version published to 10.24072/pcjournal.702
  2. Peer Community in Evolutionary Biology

    I have now read the comments from two reviewers, and based on their assessments I would recommend a thorough revision of the pre-print. 

    Reviewer 1 raised a very conceptual point, as they state that the sexual antagonism theory cannot meaningfully be applied to endosperm imprinting, because endosperm has no sex differentiation. While not my main expertise, but my understanding is, that the sexual antagonism theory of genomic imprinting relies on differences in selection between male and female offspring, predicting that patrigenes will be enriched for alleles that benefit males and matrigenes for those that benefit females. Because endosperm is a nutritive tissue without sexual differentiation, there are no sex-specific fitness optima for selection to act upon. Consequently, the fundamental premise of sexual antagonism theory does not apply to endosperm, and imprinting in this tissue is instead best explained by kinship (parental conflict) theory, which accounts for divergent maternal and paternal interests over resource allocation to developing embryos. Please consider framing the study in relation to kinship theory as this seems to be more appropriate. 

    Reviewer 1 also suggests to refine predictions of the kinship theory to avoid overemphasizing the arms-race narrative. Finally, they suggest to strengthen the discussion of the result that imprinted genes show higher correlated evolutionary rates across Brassicaceae, emphasizing its implications for broader patterns of selection and constraint.

    Several points were raised by reviewer 2, who found that the preprint would benefit from improvements in clarity, structure, and consistency. In particular, they called for clearer and more consistent writing, with a better separation of hypotheses and alignment between introduction, discussion and conclusions. 

    They also found that the interpretation of molecular evolutionary analyses should be presented more cautiously, with consideration of alternative explanations. Statistical comparisons need to address sample size imbalances and focus on effect sizes rather than significance alone, while potential artifacts in extreme values should be examined. Finally, the study would benefit from broader engagement with recent literature on imprinting in outcrossing taxa to strengthen its evolutionary context.

    Both reviewers have provided detailed comments that I hope will help in the revision of the manuscript.

  3. Peer Community in Evolutionary Biology

    The paper by Le Veve and colleagues attempts to discriminate between the kinship and sexual antagonism theories for the evolution of genomic imprinting by a study of the molecular evolution of imprinted and unimprinted genes in the endosperm of Arabidopsis lyrata and then in broad comparisons across the Brassicaceae. It is many years since I have played close attention to these issues but I will attempt to make helpful comments and hope I do not make foolish errors.

    The kinship theory was initially developed with endosperm in mind, and was subsequently applied to mammalian development, whereas the sexual antagonism theory was developed thinking about animals with two sexes. In the sexual antagonism theory, dams preferentially transmit female-beneficial alleles because they have survived to reproduce and sires preferentially transmit male-beneficial alleles to offspring of both sexes. Sires are proposed to benefit from down-regulating the male-beneficial alleles they transmits to their daughters. Dams are proposed to benefit from down-regulating the female-beneficial alleles they transmits to their sons. Endosperms do not exist as two different sexes (sons and daughters) in hermaphroditic plants. Therefore, I do not think the sexual antagonism theory applies to imprinted gene expression in endosperm.

    The initial models of the kinship theory explained the evolution of imprinted expresion as the resolution of a conflict between matrigenic and patrigenic alleles which corresponded to an evolutionarily stable strategy (ESS) in game theory. In these models, evolution stops when the ESS is achieved. However, the antagonistic phenotypic effects of maternally-expressed genes (MEGs) and paternally-expressed genes (PEGs) led several authors to predict a history of ongoing antagonistic coevolution (with positive selection) for imprinted genes. One could also make an argument for stronger negative selection acting on imprinted genes because their expression has large effects on fitness and individual alleles are directly exposed to haploid selection because only one allele is expressed within a generation. An ‘arms race’ may occur under some conditions but I think of this as a second-order prediction of the kinship theory rather than the first-order prediction about expression levels. 

    If an arms race occurs it is expected to be more intense in allogamous (outcrossing) taxa than in autogamous (self-fertilizing) taxa. For this reason, Le Veve and colleagues have looked at evolution of imprinted genes in allogamous Arabidopsis lyrata as a comparison to predominantly autogamous Arabidopsis thaliana.

    One conclusion of the authors is that there is greater evidence of balancing selection for unimprinted endosperm genes than for MEGs and PEGs (based on higher values of Tajima’s D). This is interpreted as evidence of unresolved intralocus conflict as in the sexual antagonism theory. I would suggest an alternative interpretation. Unimprinted genes are biallelically expressed and can maintain a balanced polymorphism by heterozygote advantage. Imprinted genes are monoallelically expressed and the conditions for a balanced polymorphism are more constrained.

    An intriguing result was that imprinted genes appeared to show higher correlations in their rates of evolution across the phylogeny of Brassicaceae than did unimprinted genes.

  4. Peer Community in Evolutionary Biology

    This manuscript by Le Veve et al. represents a quite ambitious attempt to test evolutionary theories accounting for genomic imprinting (that is, the parent-of-origin-dependent expression of alleles), here in the context of flowering plants, where genomic imprinting mainly occurs in the endosperm during early seed development.

    To this end, the authors draw on several published studies, and I think it is important to be cognizant of these data sources and their potential limitations. The data regarding which genes are considered to be imprinted in Arabidopsis lyrata are taken from Klosinska et al. 2016 (Nature Plants). Their results were based on reciprocal crosses between plants obtained from a single location in Europe and a single location in Michigan. In other words, these crosses are between the European subspecies (petraea) and the North American subspecies (lyrata), and no within-lineage data on imprinting in A. lyrata seem to exist. However, both source populations should have an outcrossing mating system.

    A second source of data is Willi et al. 2018 (Mol. Biol. Evol.). These authors sampled many North American populations, a mixture of both outcrossing and largely selfing ones. Data from 18 of these populations (9 + 9) are used in the present manuscript and re-analyzed to estimate levels of nucleotide diversity (pi) at synonymous, nonsynonymous, and all sites, as well as a summary of the site-frequency spectrum per gene, Tajima’s D. One caveat that should be kept in mind is that Willi et al. (2018) sequenced pools of 25 individuals per population (1 sequencing library per population), which implies that all estimates of nucleotide diversity and the site frequency spectra are not based on single sequences (haplotypes) but on estimates of population allele frequencies, with necessary cutoff values to ‘distinguish’ between sequencing errors and legitimate, low-frequency alleles. I recognize that this has been standard practice, but with such data it is impossible to distinguish genuine singletons from doubletons (etc.), which have large impacts on estimates of Tajima’s D. This argues for extra caution in interpreting slight differences between groups of that statistic.

    A third data source is the author’s own recent publication, Iltas et al. 2024 (Plant Cell Physiol.). They used seeds/plants from one selfing population in Ontario and from one outcrossing population from the Czech Republic and generated gene expression data from multiple reproductive and nonreproductive tissues (RNA-seq). These data are here used to inform about expression levels for both selfing (autogamous) and outcrossing (allogamous) populations.

    General Remarks

    1)     Given the senior author’s prior work and reputation in the field, I had high hopes when agreeing to referee this manuscript. However, I must say that the quality of the writing is astonishingly poor, so poor in fact that understanding and following the authors’ logic is really impaired by it. This encompasses all elements such as plural/singular, past/present tense, passive/active voice, typos, grammar, and plain logic. The Introduction, in particular, is also very poorly structured and reasoned, moving back and forth between aspects of the two competing hypotheses in a very convoluted manner.

    Some examples of poor logic: “Signals of balancing selection promoted by kinship theory in endosperm genes” (1st section heading of Discussion); “The kinship and sexual antagonism theories are together expected to promote directional selection on imprinted genes…” (start of paragraph in section “PEGs are associated with signals expected under kinship theory”).

    2)     The authors themselves appear to be unsure about their take-home message, to go by the respective endings of their Introduction and Discussion. The end of the Introduction states “Our findings suggest that the sexual antagonism theory is the more adapted to explain the evolution of the imprinted genes and that the shift for autogamy promotes relaxation on these genes”. The end of the Discussion (“Conclusions”) states “Thus, kinship theory appears to be the best hypothesis to explain the evolution of imprinted genes in A. lyrata populations”. A close examination of Table 1 reveals that the vast majority of the criteria (aspects of empirical data) in column 1 are not informative to distinguish between the 2 theories.

    3)     I think that the molecular evolutionary analyses are interpreted in quite rigid fashion by the authors. For one, we are never given the actual levels of nucleotide diversity (pi) for the various classes of sites, but only their ratios in the context of looking for signals of past directional and/or negative (= purifying) selection. The most obvious signal of recent directional selection should be markedly lower pi across all site types and across both coding and noncoding regions (compared to control genes), while a higher D_ns/D_s might be due to long-term directional selection, but could also be due to other processes such as weaker purifying selection due to smaller effective population size (among other possibilities). As it stands, demographic explanations as possible alternatives to the patterns found are never entertained.

    The same issue is also true for estimates of Tajima’s D, where only the different types of natural selection are mentioned as “making D higher or lower than expected under neutrality” – no alternatives based on demographic history are mentioned. Given my opening remarks on the consequences of looking at Pool-seq data, more caution regarding small differences in Tajima’s D between gene groups seems warranted.

    4)     The comparison of groups of genes always involves small numbers of MEGs and PEGs versus a higher number of control genes and a much higher number of endosperm genes (Figures 1-3). Although some comparisons are always significant across the various entities, could the much higher number of endosperm genes drive this?  After all, what should be of interest are the effect sizes (if any), not statistical significance per se. In particular, I note the very high variance of the endosperm genes for “length of branches” and “DNS/DS” in Fig. 2, with many outlier genes having absurdly high estimates. One possibility that comes to mind is that uneven quality of the reference genome assemblies (and/or alignment quality?) might yield such artifacts; other potential sources of error surely exist.

    5)  At the end of the Discussion and a bit earlier, the authors mention that studies of genomic imprinting in flowering plants have focused on mainly selfing species such as A. thaliana or Capsella rubella, where parental conflict should be weak or even (near) absent. Likewise, the available data suggest that imprinting seems stable over large time frames at only a handful of loci (e.g. maize vs. rice, or dicots vs. monocots), with variability of a gene’s imprinting status even within biological species. In this context it seems like a strange oversight that recent, relevant work on largely outcrossing, evolutionary model taxa such as Solanum and Mimulus is not cited and incorporated into this study.

     

  5. Peer Community in Evolutionary Biology

    Dear Audrey and co-authors

    Thank you for submitting the revised manuscript. I appreciate the thorough revision, and I think the revision of the focal hypotheses has greatly  improved tha clarity of the manuscript.

    I have obtained one review from a new reviewer, since the opriginal two reveiwers unfortunately were unable to assess the revised manuscript. The reviewer has proposed clarifications and some streamlining mainly in relation to the statistical analyses and reporting. Please see their detailed comments and suggestions below. I find the comments in relation to clarity and presentation relevant, and I hope you will find their comments constructive for the revision of your article.

    Best wishes

    Trine Bilde

     

     

     

  6. Peer Community in Evolutionary Biology

    Title and abstractDoes the title clearly reflect the content of the article? [ ] Yes, 


    Does the abstract present the main findings of the study? [ ] Yes


    Does the introduction build on relevant research in the field? [ ] Yes


    Materials and methodsAre the methods and analyses sufficiently detailed to allow replication by other researchers? [ ] I don’t know: Most of the details are given but, for instance, scripts are given without an explanations of the equations used.

    If applicable (for empirical studies), are sample sizes are clearly justified? [ ] Yes


    Are the methods and statistical analyses appropriate and well described?  [ ] I don’t know: some of the tests are appropriate while in some cases tests have not been performed.


    ResultsIn the case of negative results, is there a statistical power analysis (or an adequate Bayesian analysis or equivalence testing)? [ ] I don’t know

    Are the results described and interpreted correctly?  [ ] No: it is likeley that some of the results are coundaded by other factors and these have not been taken into account.

    DiscussionHave the authors appropriately emphasized the strengths and limitations of their study/theory/methods/argument? [ ] I don’t know: limitations should have been emphasised more


    Are the conclusions adequately supported by the results (without overstating the implications of the findings)? [ ] No: as mentioned above, some results are not entirrely convicing.

     

    This is my full review.

     

    In this work Authors searched for signatures for selection and co-evolution on imprinted genes in A. lyrata and across the Brassicaceae family. Their results suggest signals of unresolved intralocus conflict marked by balancing selection, among other events.

    My comments are on the data analysis rather than on the biological foundations on this study which are outside of my expertise. I also note the extensive changes from the originally submitted study. Finally, I acknowledge that I read and considered the previous reviewers’ comments and the authors’ replies. I agree that the manuscript is now more coherent although there are still some visible differences in analytical style between sections.

    The introduction is well written, with a gentle explanation of the main hypotheses and then more detailed information on specific systems and loci. The knowledge gap is explained. Results are repetitive and do not take into account all possible confounding factors. There are also lots of potential data and bioinformatic artifacts that may drive these signals. Therefore, the conclusions are not fully supported by the results.

    Main comments

    Line 114: what are the expectations on the proportions of MEG and PEG? Why shouldn’t they deviate from expectations in the first place? Same for the next sentence on upregulation. What is the expected distribution and where do the observed values lie? Overall, it is not clear to me the reasoning behind these tests at this stage of the manuscript if Authors don’t make it explicit what expectations are (for instance based on prior knowledge or studies).

    Line 121: how have these 100 random genes been chosen? Completely random or did the Authors try to match some features of the test set like chromosomal location, average physical/genetic distance between pairs of genes, average gene length, proportion of intronic/exonic, etc etc, if these (or other) features may be considered confounding factors.

    Lines 157-160: no statistical tests are done here; I don’t suggest to do tests all the time but the approach here is different from the previous section where several statistical tests have been done; also if “significantly” is used then one would expect some statistical support. This is true for the rest of the section.

    Line 160: how have these differences been taken into account for next results in practice? Shouldn’t they be correct for somehow or does it suggest that a better-matched set of control genes is necessary?

    Line 205: I wonder if a better choice is to impose a minimum number of SNPs rather than the SNP density. In the latter case, set is filtered out of low-diversity genes by construction. This may be conservative and that would be fine, I suppose.

    Figures are very similar, with different measures compared across groups. The variety of analyses is limited.

    Various factors influence summary statistics used in addition to selection. While these are acknowledged in the discussion, no convincing attempts to test against these competing scenarios have been performed.

    Line 264: what is the reasoning behind this test?

    Correlations between diversity, branch lengths and RF distances could be due to a number of reasons in addition to co-evolution. How is it possible to disentangle all these factors? Are there references to justify this approach? The clustering approach seems to be the most convincing one.

    Line 347: on ancient balancing selection, what is the time of selection? If long-term, we expect trans-species SNPs. Also, if balancing selection is old the genomic signal is very narrow. Has this been discussed or acknowledged?

    “Tajima’s D is a relatively weak statistic for detecting selection in pooled sequencing data (Korneliussen et al., 2013)”, I am not sure this is the most correct reference.

    Minor comment

    Line 98: authors could briefly state how they are testing for co-evolution in point (3) in the same way as done for points (1) and (2).

    The introduction may end with a single sentence on the key take-away message.

    Line 114: unusual presentation of numerical significance in 1^e-04; at least the “e” is not needed if already presented as exponential.

    Figure 1 is hard to read, especially I can’t see well the red dots.

    Figure 2 has low resolution.

    Line 197: title could be better phrased

    Line 207: for “both” but three statistics are mentioned.

    Line 690: q-score of 60 is impressively high; is there a reason or a reference for being so strict?

    Line 704: how did you estimate them? Providing a script is good but an explanation of the equations used is needed.

    In the Methods, a lot of github repos are mentioned, often multiple times. A single repo should be given. Also the scripts are not provided in a user-friendly manner with lots of hardcoded parameters.

     

  7. Peer Community in Evolutionary Biology

    Dear Audrey

     

    Thank you very much for the the revision of your manuscript. Because the previous reveiwer stated that the conceptual foundation of the study was outside their core expertise, and I find myself in a similar situation, I opted to obtain another review with focus on the theoretical framework. Please find their detailed review and annotated comments to the manuscript attached.

    The reviewer has detailed that the intralocus sexual conflict model by Day and Bondurianski is presented as an alternative to the kinship theory by Haig, and therefore emphaises that it is not clear how these models reconcile (please see their detailed argument in the review). The reviewer suggests to revise the manuscript to better distinguish the theories and their different predictions, and to revise the interpretations accordingly. 

    I fully acknowledge that the evaluation of your preprint has taken longer than it should, the reason being that it has consistently been very hard to find first a recommender and then reviewers (despite a major effort to find suitable reviewers). Nevertheless, it is particularly important to be clear on the theoretical foundation, and I think that the latest reviewer has highlighted the differences between the two models in a way that clarifies the expectations. The reviewer has also listed a number of points to clarify the manuscript.

    I look forward to receiving the revised version of the manauscriupt.

     

    Best wishes

    Trine

     

  8. Peer Community in Evolutionary Biology

    While considering the recommendation of this ms, it appeared that some important issues had been overlooked in the previous round of review. 
    In particular, a reviewer of the first version stated that s.he did " not think the sexual antagonism theory applies to imprinted gene expression in endosperm."
    The reviewer of the second version made clear that s.he did not comment on such aspects of the ms. Unfortunately, I think the revision has not correctly addressed the original criticism, and that this raises serious concerns about the overall message of the ms. 

    To be more specific, consider the following sentence from the first paragraph of the Introduction:

    "This conflict is expected to drive intralocus conflict between growth-promoting and growth-limiting genes (Haig and Graham 1991; Moore and Haig 1991; Wilkins and Haig 2001), consequently leaving signatures of balancing selection, such as reduced divergence across species and increased polymorphism within populations (Day and Bonduriansky 2004; Kasimatis et al., 2017)."

    This is hard to follow because the citations of Haig's papers  (broadly described as "the kinship theory" in the ms) do not support the statements made here. The conclusions of those papers concern conditions where imprinting of genes involved in offspring provisioning is selected, whereby a single allele is differentially expressed according to parent of origin. This per se has no reason to leave signatures of balancing selection on the imprinted locus. To support its claim, the quoted sentence refers to the notion of intralocus conflict in Day and Bonduriansky 2004 and Kasimatis et al., 2017. However, Day and Bondurianski emphatically frame their intralocus sexual conflict model as an alternative to Haig's theory ("Importantly, our hypothesis differs fundamentally from previous hypotheses such as the parental conflict hypothesis by focusing on the evolution of the
    locus causing the imprinting rather than on the locus that is imprinted"), so it is not clear how any of D&B's claims is applicable to the kinship theory. B&D's model rests on different alleles having opposite effects in the two sexes in a dioecious species ("Our theory is based on a very simple idea. Given that the individuals that are successful in transmitting their alleles to the next generation (i.e., sires and dams) are those that have passed the tests of sex-specific selection, it follows that sires are more likely to transmit high male-fitness alleles to their offspring, whereas dams are more likely to transmit high female-fitness alleles to their offspring..."), while the original kinship theory is about a differential expression of possibly the same allele within a single individual who may even be hermaphroditic (as is the case of Arabidopsis lyrata in the present ms). Likewise, Kasimatis et al. do not refer to the kinship theory but rather to B&D's model when they consider "intralocus conflict". 

    Therefore, I feel the ms should be revised to better distinguish the theories and their different predictions, and that the authors should revise their interpretations throughout the ms. more recent work than Kasimatis et al (e.g. Flintham et al, doi: 10.1093/evlett/qrae059 ) may have to be considered in this revision. 

    The authors should take this opportunity to clarify a few other statements. See specific comments below. They should also carefully check to ms for any language issue, as I noted a number of grammatical glitches and undefined acronyms, some of which are highlighted in the attached version of the ms.

    Specific comments:

    l. 15-16 "However, most studies addressing selection in imprinted genes have focused on self-fertilizing species, where conflicts over resource allocation are predicted to be weak." Do you mean studies of genomic diversity patterns in plants? That should be clarified, because some other studies in plants have cared about contrasting autogamous and allogamous populations, and beyond that, the not self-fertilizing mouse is a classical experimental model for imprinting.  

    l.83-84 "Indeed, a central debate has emphasized that kinship theory may concern selection on the optimal expression levels of genes between maternal and paternal genomes, and not on alleles (Patten et al., 2014)." This sentence is obscure. Alleles at loci controlling expression of other loci are still "alleles" concerned by selection.

    First paragraph of Results: it would be nice to clarify the precise concept of "genes" used here. (cf further comment on l.467)

    l.142 (double checking for potential confusion): do you really mean the 90% central range or do you actually used 2.5-97.5% range ?

    l.167 The statistical models being compared have not yet been described as far as I can see. Are these linear regression models ? 

    The expression "... was this that..." occurs recurrently and appears non-idiomatic. I would expect "was the one that"

    l. 290 "contrasts in Tajima’s D or πNS/πS for the imprinted genes": contrast... compared to what ? Does this refer to results in the next paragraph?

    l. 467 "The kinship theory is expected to promote directional selection on imprinted genes". Beyond my general criticism of this interpretation of the theory, I doubt "genes" is here a precise word with the same meaning as in the first paragraph of Results, so more precise language should be used. One can conceive selection on alleles more or less sensitive to imprinting at the imprinted locus, or on alleles at another locus controlling the imprinting at the imprinted locus. 

    Focusing on supplementary Table S7, I struggled to understand the legend, which refers to numbers in red and blue, but I don't see such coloring ; and which states that 
    "The significance was tested by binomial test based on the proportion of genes studied in endosperm and in control. specified." without the hypothesis tested being clearly specified (the main text is more clear).

  9. Peer Community in Evolutionary Biology

    Data editor's report

    Date: 29-10-2025

    Data editor: Cecilia Baldoni

     

    1. Data and metadata must be archived and adhere to FAIR guiding principles

    [X] Data are in a public repository

    [X] Data repository has a persistent identifier (e.g., a DOI)

    [X] Data are cited in the manuscript (in data availability statement or similar, as well as in the Literature Cited)

    [X] Data repository has a license

    [X] All necessary data files are present in the repository

         [x] All raw data present

         [X] All processed data present

    [X] Data are contained in an interoperable format

         [X] Tabular data - csv, tsv

    [X] Metadata present (including README file)

    [X] Metadata adequate (including README file)

     

    2. Archived data corresponds with the data reported in the manuscript

    [X] Variables used in analysis present in the data

    [X] The structure of the data presented matches the manuscript (e.g., it is the right size)

     

    3. Code and metadata must be archived and adhere to FAIR guiding principles

    [X] Code has a repository

    [X] Code repository has a DOI 

    [X] Code is cited in the manuscript

    [X] Code repository has a license

    [X] Code files are present in the repository

    [X] Code is contained in an interoperable format

    [X] Metadata present (README file and annotations in code) 

    [X] Metadata adequate

     

    4. Archived code matches the manuscript

    [X] Code is present for all analyses in the manuscript, along with code used to produce figures/tables where appropriate

     

    5. Archived code runs with the archived data

    [X] Runs without errors

     

    6. Results can be computationally reproduced by running the archived code 

    [X] Numeric results (in table or text)

    [X] Figures

    --------


    Comments from the data editor: The authors did a great job implementing the suggestions.

     

  10. Peer Community in Evolutionary Biology

    In angiosperms, endosperm provides nutrition for the developing embryo and is ideal for studying imprinting because this tissue integrates distinct maternal and paternal genomic contributions within a single developmental context. Genomic imprinting - where maternal and paternal alleles are expressed unequally - has often been interpreted through the lens of kinship theory, which emphasizes that mothers and fathers can differ in their evolutionary interests over how resources are allocated among seeds (Haig, 2000; Patten et al., 2014). When the same maternal plant produces offspring with different fathers, this asymmetry in relatedness can favour allele‑specific expression that shifts endosperm growth and nutrient flow towards one parent’s evolutionary interest (Haig, 2000).

    Under this framework, imprinting is viewed as a product of parental conflict: maternally and paternally inherited alleles experience different fitness payoffs from embryo and endosperm growth, so selection drives allele‑specific expression toward distinct optima. What remains uncertain is where the most informative genomic footprints lie: within protein‑coding sequence or in the regulatory sequences that govern dosage, timing, and tissue specificity of expression. Empirical studies have focused largely on predominantly selfing lineages, where low variance in paternity and kin structure dampen conflict. Therefore, we have limited understanding of imprinting dynamics in outcrossing systems, where multiple paternity can intensify antagonism between parental genomes.

    To address this gap, Le Veve and colleagues (2026) integrate phylogenetic comparisons across the Brassicaceae with population genomic analyses in Arabidopsis lyrata lineages that vary in their mating system. They ask whether imprinted loci bear the signatures predicted under parental conflict scenarios and whether antagonistic maternal–paternal interactions leave traces of coordinated evolutionary change. Across tissues, the set of genes active in the endosperm shows patterns consistent with long‑standing competitive pressures within the seed environment, indicative of forces that maintain alternative alleles over time rather than fix a single favoured variant. By contrast, when the evolutionary history of imprinted loci is traced across related species, their protein‑coding sequences mostly reflect constraint, pointing to a predominance of purifying forces rather than recurrent fixation of novel amino‑acid changes.

    Population‑level patterns did not track mating system and aligned only weakly with simple kinship predictions, suggesting that parental conflict is expressed primarily via regulation of gene activity rather than amino‑acid change. Coevolution among imprinted genes was evident, but diffuse across networks rather than concentrated at particular sites. By jointly analysing Brassicaceae phylogeny and both outcrossing and selfing lineages of A. lyrata, the study complements earlier reports of coding‑sequence selection in autogamous systems into a broader framework that incorporates mating‑system variation. The study clarifies where kinship‑theory signals are most likely to be detected and complements expression‑focused studies and imprinting datasets. Finally, the study emphasizes regulatory coupling and gene‑network architecture as the most promising targets for future tests.

     

    References

    Haig, D. (2000). The Kinship Theory of Genomic Imprinting. Annual Review of Ecology and Systematics, 31, 9–32. http://www.jstor.org/stable/221723

    Patten, M., Ross, L., Curley, J. et al. The evolution of genomic imprinting: theories, predictions and empirical tests. Heredity 113, 119–128 (2014). https://doi.org/10.1038/hdy.2014.29

    Audrey Le Veve, Omar Iltas, Julien Dutheil, Clement Lafon Placette (2026) Limited directional selection but coevolutionary signals among imprinted genes in A. lyrata.. bioRxiv, ver.6 peer-reviewed and recommended by PCI Evolutionary Biology https://doi.org/10.1101/2024.08.01.606153

  11. Version published to 10.1101/2024.08.01.606153 on bioRxiv