Roses, a symbol of love and beauty, have a rich history of cultivation that spans millennia. While their aesthetic appeal has remained a constant, the genetic changes underlying their domestication and breeding remain intriguing. The manuscript titled "Dark side of the honeymoon: reconstructing the Asian x European rose breeding history through the lens of genomics" by Leroy et al. provides an unprecedented insight into the genomic shifts that accompanied the breeding history of roses in Europe during the 19th century. By leveraging on genotyping and whole-genome sequencing data from more than 200 accessions, this study reconstructs the genetic journey of roses from their European origins to their integration with Asian varieties.

This work is particularly fascinating for evolutionary biologists, geneticists, and horticulturists alike, as it sheds light on several critical aspects of plant breeding history. The study provides compelling evidence of a rapid transition from predominantly European to a near-Asian genetic background within a few generations. This shift highlights the strong influence of Asian roses in shaping modern cultivated varieties, particularly through the introduction of recurrent blooming traits, novel colors, and scents.

A striking finding is the reduction in genetic diversity that occurred during this transition, likely due to selective breeding practices that prioritized a narrow set of desirable traits. This discovery underscores the potential risks of genetic bottlenecks in cultivated plants and raises concerns about the long-term sustainability of modern rose breeding programs.

The study also features a robust methodological framework applied to a unique data set which includes 204 rose accessions, covering both botanically and historically significant varieties. Whole genome sequencing of 32 accessions provides high-resolution insights into genomic evolution. Comprehensive phenotypic characterization over multiple years further allows in-depth investigation of the genetic architecture of key horticultural traits such as petal number, flowering time, disease resistance, and scent composition, with the building of the largest GWAS catalog for roses to date.

Finally, the findings emphasize the need for sustainable breeding practices that balance genetic innovation with the preservation of historical diversity, by maintaining rose collections. Integrating ancient genetic resources into modern breeding programs could enhance resilience against diseases and environmental changes, while maintaining the aesthetic qualities that make roses so beloved.

Overall, the manuscript by Leroy et al. is a landmark contribution to our understanding of the genomic history of rose breeding. By merging historical records with cutting-edge genomic analysis, the study not only reconstructs a critical phase of horticultural evolution but also provides invaluable insights for future breeding strategies.

References

Thibault Leroy, Elise Albert, Tatiana Thouroude, Sylvie Baudino, Jean-Claude Caissard, Annie Chastellier, Jerome Chameau, Julien Jeauffre, Therese Loubert, Saretta Nindya Paramita, Alix Pernet, Vanessa Soufflet-Freslon, Cristiana Oghina-Pavie, Fabrice Foucher, Laurence Hibrand-Saint Oyant, Jeremy Clotault (2024) Dark side of the honeymoon: reconstructing the Asian x European rose breeding history through the lens of genomics. bioRxiv, ver.4 peer-reviewed and recommended by PCI Evol Biol https://doi.org/10.1101/2023.06.22.546162

In the 19th century, C. Darwin and F. Delpino engaged in a debate about the success of species with different reproduction modes, with the later favouring the idea that monoecious plants capable of autonomous selfing could spread more easily than dioecious plants (or self-incompatible hermaphroditic plants) if cross-pollination opportunities were limited [1]. Since then, debate has never faded about how natural selection is responsible for transitions to selfing and can explain the diversity and distribution of reproduction modes we observe in the natural world [2, 3].
Explanations for mating systems diversity, and transitions to selfing in particular, generally fall into two categories: either genetic or ecological. On the genetic side, many theoretical works showed a critical role for mutation load and inbreeding depression, transmission advantage and reproductive assurance in the evolution of selfing, e.g. [4]. Many experimental works were conducted to test theoretical hypotheses and predictions, especially regarding the magnitude of inbreeding depression; see [5] for a review. Ecologically, the presence of selfing populations is usually correlated with fragmented and harsh habitats, on the periphery of ancestral outcrossing populations. The cause of this distribution could be that selfers are better dispersers and colonizers than outcrossers, or variations in other life-history traits [6]. Yet, few experiments were run to assess whether selfing species or populations have effectively different ecological characteristics, and even scarcer are experiments evaluating both the roles of mutational load and life-history traits evolution. This is the aim of the present study by X. Yang et al [7].
The study of Yang et al [7], together with that of Petrone Mendoza et al. [8], supervised by S. Glémin and M. Lascoux, is probably one of the first to conduct experiments where the competitive abilities are compared between and within species. Using 4 species of the Capsella genus, annual plants from the mustard family, they tested the theoretical predictions that i) the transition from outcrossing to selfing resulted in reduced competitive ability at higher densities, because of the accumulation of deleterious mutations and/or the evolution of life-history traits in an open habitat and a colonization/dispersal trade-off; ii) that reduced competitive ability of selfers should be less pronounced in polyploid then diploid species because the effect of partially recessive deleterious mutations would be buffered; and iii) that competitive ability of selfers should decline with historical range expansion because of the expansion load [9].
Of the 4 Capsella species studied, only one of them, presumably the ancestral, is a diploid outcrosser with a small distribution but large population sizes. The three other species are selfers, two diploids with independent histories of transitions from outcrossing, and another, tetraploid, resulting from a recent hybridization between one of the diploid selfer and the diploid outcrossing ancestor. Many accessions from each species were sampled and individuals assayed for their competitive ability against a tester species or alone, for vegetative and reproductive traits. The measured vegetative traits (rosette surface at two stages, growth rate and flowering probability) showed no differentiation between selfers and outcrossers. To the contrary, reproductive traits (number of flowers) followed theoretical predictions: selfing species are more sensitive to competition than the outcrossing species, with polyploid selfing species being intermediate between the diploid selfers and the diploid outcrosser, and within the tetraploid selfing species (where sampling was quite significant across a large geographical range) sensitivity to competition increased with range expansion.
The study of Yang et al. [7] suffers from several limitations, such that alternative explanations cannot be discarded in the absence of further experimental data. They nonetheless provide the reader with a nice discussion and prospects on how to untwine the causes and the consequences of transitions to selfing. Their study also brings up to date questions about the joint evolution of mating system and life-history traits, which needs a renewed interest from an empirical and theoretical point of view. The results of Yang et al. raise for instance the question of whether it is indeed expected that only reproductive traits, and not vegetative traits, should evolve with the transition to selfing.
The recommandation and evaluation of this paper have been made in collaboration with Thomas Lesaffre.

References

[1] Darwin, C. R. (1876). The effects of cross and self fertilization in the vegetable kingdom. London: Murray. [2] Stebbins, G. L. (1957). Self fertilization and population variability in the higher plants. The American Naturalist, 91, 337-354. doi: 10.1086/281999
[3] Harder, L.D. & Barrett, S. C. H. (2006). Ecology and evolution of flowers. Oxford: Oxford University Press. [4] Porcher, E. & Lande, R. (2005). The evolution of self-fertilization and inbreeding depression under pollen discounting and pollen limitation. Journal of Evolutionary Biology, 18(3), 497-508. doi: 10.1111/j.1420-9101.2005.00905.x
[5] Winn, A.A., et al. (2011). Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution, 65(12), 3339-3359. doi: 10.1111/j.1558-5646.2011.01462.x
[6] Munoz, F., Violle, C. & Cheptou, P.-O. (2016). CSR ecological strategies and plant mating systems: outcrossing increases with competitiveness but stress-tolerance is related to mixed mating. Oikos, 125(9), 1296-1303. doi: 10.1111/oik.02328
[7] Yang, X., Lascoux, M. & Glémin, S (2018). Variation in competitive ability with mating system, ploidy and range expansion in four Capsella species. bioRxiv, 214866, ver. 5 recommended and peer-reviewed by PCI Evol Biol. doi: 10.1101/214866
[8] Petrone Mendoza, S., Lascoux, M. & Glémin, S. (2018). Competitive ability of Capsella species with different mating systems and ploidy levels. Annals of Botany 121(6), 1257-1264. doi: 10.1093/aob/mcy014
[9] Peischl, S. & Excoffier, L. (2015). Expansion load: recessive mutations and the role of standing genetic variation. Molecular Ecology, 24(9): 2084-2094. doi: 10.1111/mec.13154

Sex chromosomes are special in the genome because they are often highly differentiated over much of their lengths and marked by degenerative evolution of their gene content. Understanding why sex chromosomes differentiate requires deciphering the forces driving their recombination patterns. Suppression of recombination may be subject to selection, notably because of functional effects of locking together variation at different traits, as well as longer-term consequences of the inefficient purge of deleterious mutations, both of which may contribute to patterns of differentiation [1]. As an example, male and female functions may reveal intrinsic antagonisms over the optimal genotypes at certain genes or certain combinations of interacting genes. As a result, selection may favour the recruitment of rearrangements blocking recombination and maintaining the association of sex-antagonistic allele combinations with the sex-determining locus.
The hypothesis that sexually antagonistic selection might drive recombination suppression along the sex chromosomes is not new, but there are surprisingly few studies examining this empirically [1]. Support mainly comes from the study of guppy populations Poecilia reticulata in which the level of sexual dimorphism (notably due to male ornaments, subject to sexual selection) varies among populations, and was found to correlate with the length of the non-recombining region on the sex chromosome [2]. But the link is not always that clear. For instance in the fungus Microbotryum violaceum, the mating type loci is characterized by adjacent segments with recombination suppression, despite the near absence of functional differentiation between mating types [3].
In this study, Shearn and colleagues [4] explore the patterns of recombination suppression on the sex chromosomes of primates. X and Y chromosomes are strongly differentiated, except in a small region where they recombine with each other, the pseudoautosomal region (PAR). In the clade of apes and monkeys, including humans, large rearrangements have extended the non recombining region stepwise, eroding the PAR. Could this be driven by sexually antagonistic selection in a clade showing strong sexual differentiation?
To evaluate this idea, Shearn et al. have compared the structure of recombination in apes and monkeys to their sister clade with lower levels of sexual dimorphism, the lemurs and the lorises. If sexual antagonism was important in shaping recombination suppression, and assuming lower measures of sexual dimorphism reflect lower sexual antagonism [5], then lemurs and lorises would be predicted to show a shorter non-recombining region than apes and monkeys.
Lemurs and lorises were terra incognita in terms of genomic research on the sex chromosomes, so Shearn et al. have sequenced the genomes of males and females of different species. To assess whether sequences came from a recombining or non-recombining segment, they used coverage information in males vs females to identify sequences on the X whose copy on the Y is absent or too divergent to map, indicating long-term differentiation (absence of recombination). This approach reveals that the two lineages have undergone different recombination dynamics since they split from their common ancestor: regions which have undergone further structural rearrangements extending the non-recombining region in apes and monkeys, have continued to recombine normally in lemurs and lorises. Consistent with the prediction, macroevolutionary variation in the differentiation of males and females is indeed accompanied by variation in the size of the non-recombining region on the sex chromosome.
Sex chromosomes are excellent examples of how genomes are shaped by selection. By directly exploring recombination patterns on the sex chromosome across all extant primate groups, this study comes as a nice addition to the short series of empirical studies evaluating whether sexual antagonism may drive certain aspects of genome structure. The sexual selection causing sometimes spectacular morphological or behavioural differences between sexes in many animals may be the visible tip of the iceberg of all the antagonisms that characterise male vs. female functions generally [5]. Further research should bring insight into how different flavours or intensities of antagonistic selection can contribute to shape genome variation.

References

[1] Charlesworth D (2017) Evolution of recombination rates between sex chromosomes. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20160456. https://doi.org/10.1098/rstb.2016.0456
[2] Wright AE, Darolti I, Bloch NI, Oostra V, Sandkam B, Buechel SD, Kolm N, Breden F, Vicoso B, Mank JE (2017) Convergent recombination suppression suggests role of sexual selection in guppy sex chromosome formation. Nature Communications, 8, 14251. https://doi.org/10.1038/ncomms14251
[3] Branco S, Badouin H, Vega RCR de la, Gouzy J, Carpentier F, Aguileta G, Siguenza S, Brandenburg J-T, Coelho MA, Hood ME, Giraud T (2017) Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism. Proceedings of the National Academy of Sciences, 114, 7067–7072. https://doi.org/10.1073/pnas.1701658114
[4] Shearn R, Wright AE, Mousset S, Régis C, Penel S, Lemaitre J-F, Douay G, Crouau-Roy B, Lecompte E, Marais GAB (2020) Evolutionary stasis of the pseudoautosomal boundary in strepsirrhine primates. bioRxiv, 445072. https://doi.org/10.1101/445072
[5] Connallon T, Clark AG (2014) Evolutionary inevitability of sexual antagonism. Proceedings of the Royal Society B: Biological Sciences, 281, 20132123. https://doi.org/10.1098/rspb.2013.2123

There is a heavy body of literature on sex-biased gene expression, which can easily be tricky. One reason is that expression data are multi-dimensional, notoriously noisy, and highly sensitive to experimental conditions. Achieving reproducibility is, therefore, a challenge, especially in non-model organisms. Another reason is that the evolutionary forces shaping gene expression variation are complex, involving processes such as intra- and inter-locus conflicts between sexes, sex-chromosome evolution and degeneration, dosage compensation, cis vs. trans regulation, dominance, linkage, drift, etc... Not surprisingly, the field is rich in discordant studies, and a wide variety of situations have been described.

The three-spined stickleback is a good illustration. This widely-studied fish displays conspicuous sexual dimorphisms, both morphological and behavioural. Yet, the existing literature regarding which genes and tissues are involved is remarkably unclear due to the lack of a comprehensive data set. Sylvestre et al. (1) here fix this issue. They sampled 40 wild-caught individuals in each of the two sexes and performed high-throughput sequencing of the transcriptome in three somatic tissues, dissected and preserved in the exact same conditions. This is an impressive effort, well above current standards. Data analysis delivered a series of neat results: gene expression in the liver is particularly sex-biased; the brain, in contrast, is remarkably little sex-differentiated despite the presence of courtship and paternal care in this species; gills show significantly sex-biased gene expression, which had been unnoticed previously despite the importance of this organ in fish ecotoxicology; the relatively young sex-chromosomes, finally, do not seem to experience dosage compensation, and are therefore enriched in sex-biased genes.

Some of these results are consistent with previous studies in other fish species (2), here confirmed or demonstrated with a high degree of certainty. Others are new and worth considering in future studies of stickleback ecology and reproduction. We simply need more studies of this sort: well-conducted and clear-cut, recalling the career of its last author.

References

(1) Florent Sylvestre, Nadia Aubin-Horth, Louis Bernatchez (2024) Sex-biased gene expression across tissues reveals unexpected differentiation in the gills of the threespine stickleback. bioRxiv, ver.2 peer-reviewed and recommended by PCI Evol Biol https://doi.org/10.1101/2024.06.09.597944

(2) Iulia Darolti I, Judith E. Mank (2023). Sex-biased gene expression at single-cell resolution: cause and consequence of sexual dimorphism. Evolution Letters 7(3):148-156. https://doi.org/10.1093/evlett/qrad013

150 years after Darwin published ‘Descent of man and selection in relation to sex’ (Darwin, 1871), the evolutionary mechanism that he laid out in his treatise continues to fascinate us. Sexual selection is responsible for some of the most spectacular traits among animals, and plants, and it appeals to our interest in all things reproductive and sexual (Bell, 1982). In addition, sexual selection poses some of the more intractable problems in evolutionary biology: Its realm encompasses traits that are subject to markedly different selection pressures, particularly when distinct, yet associated, traits tend to be associated with males, e.g. courtship signals, and with females, e.g. preferences (cf. Ah-King & Ahnesjo, 2013). While separate, such traits cannot evolve independently of each other (Arnqvist & Rowe, 2005), and complex feedback loops and correlations between them are predicted (Greenfield et al., 2014). Traditionally, sexual selection has been modelled under simplifying assumptions, and quantitative genetic approaches that avoided evolutionary dynamics have prevailed. New computing methods may be able to free the field from these constraints, and a trio of theoreticians (Chevalier, De Coligny & Labonne 2020) describe here a novel application of a ‘demo-genetic agent (or individual) based model’, a mouthful hereafter termed DG-ABM, for arriving at a holistic picture of the sexual selection trajectory. The application is built on the premise that traits, e.g. courtship, preference, gamete investment, competitiveness for mates, can influence the genetic architecture, e.g. correlations, of those traits. In turn, the genetic architecture can influence the expression and evolvability of the traits. Much of this influence occurs via demographic features, i.e. social environment, generated by behavioral interactions during sexual advertisement, courtship, mate guarding, parental care, post-mating dispersal, etc.
The authors provide a lengthy verbal description of their model, specifying the genomic and behavioral parameters that can be set and how a ‘run’ may be initialized. There is a link to an internet site where users can then enter their own parameter values and begin exploring hypotheses. Back in the article several simulations illustrate simple tests; e.g. how gamete investment and preference jointly evolve given certain survival costs. One obvious test would have been the preference – courtship genetic correlation that represents the core of Fisherian runaway selection, and it is regrettable that it was not examined under a range of demographic parameters. As presented the author’s DG-ABM appears particularly geared toward mating systems in ‘higher’ vertebrates, where couples form during a discrete mating season and are responsible for most reproduction. It is not clear how applicable the model could be to a full range of mating systems and nuances, including those in arthropods and other invertebrates as well as plants.
What is the likely value of the DG-ABM for sexual selection researchers? We will not be able to evaluate its potential impact until readers with specialized understanding of a question and taxon begin exploring and comparing their results with prior expectations. Of course, lack of congruence with earlier predictions would not invalidate the model. Hopefully, some of these specialists will have opportunities for comparing results with pertinent empirical data.

References

Ah-King, M. and Ahnesjo, I. 2013. The ‘sex role’ concept: An overview and evaluation Evolutionary Biology, 40, 461-470. doi: https://doi.org/10.1007/s11692-013-9226-7
Arnqvist, G. and Rowe, L. 2005. Sexual Conflict. Princeton University Press, Princeton. doi: https://doi.org/10.1515/9781400850600
Bell, G. 1982. The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press, Berkeley.
Chevalier, L., De Coligny, F. and Labonne, J. (2020) A demogenetic individual based model for the evolution of traits and genome architecture under sexual selection. bioRxiv, 2020.04.01.014514, ver. 4 peer-reviewed and recommended by PCI Evol Biol. doi: https://doi.org/10.1101/2020.04.01.014514
Darwin, C. 1871. The Descent of Man and Selection in Relation to Sex. J. Murray, London.
Greenfield, M.D., Alem, S., Limousin, D. and Bailey, N.W. 2014. The dilemma of Fisherian sexual selection: Mate choice for indirect benefits despite rarity and overall weakness of trait-preference genetic correlation. Evolution, 68, 3524-3536. doi: https://doi.org/10.1111/evo.12542