Flowering plants show significant diversity in sexual strategies, profoundly impacting the evolution of sexual traits and associated genes. Sexual selection is one of the primary evolutionary forces driving sexual trait variation, particularly evident during pollen-pistil interactions, where pollen grains compete for fertilization and females select mating partners. Multiple mating may intensify competition among pollen donors for siring, while in contrast, self-fertilization reduces sire-sire competition, relaxing the sexual selection pressure. Traits involved in male-male competition and female choice are well described, and molecular mechanisms underlying pollen development and pollen-pistil interactions have been extensively studied in the model species Arabidopsis thaliana. However, whether these molecular mechanisms are involved in sexual selection in nature remains unclear. To address this gap, we measured intrinsic pollen performance and its interaction with female choice and investigated the associated gene expression patterns in a selfing and an outcrossing population of Arabidopsis lyrata. We found that pollen germination and pollen tube growth were significantly higher in outcrossers than selfers, and this difference was accompanied by changes in the expression of genes involved in vesicle transport and cytoskeleton. Outcrosser mother plants showed a negative impact on pollen tube growth compared to selfer mother plants, together with a difference of expression for genes involved in auxin and stress response, suggesting a potential mechanism for female choice through molecular cross talk at the post-pollination stage. Our study provides insight into the impact of sexual selection on the evolution of sexual gene expression in plants.

Department of Botany Faculty of Science Charles University Benátská 2 CZ 128 01 Prague Czech Republic

Department of Evolutionary Plant Biology Institute of Botany of the Czech Academy of Sciences Zámek 1 CZ 128 01 Průhonice Czech Republic

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Aloni  R., Aloni  E., Langhans  M. and Ullrich  C.I. (2006) Role of auxin in regulating PubMed

Alonzo  S.H. and Servedio  M.R. (2019) Grey zones of sexual selection: why is finding a modern definition so hard? PubMed PMC

Al-Shehbaz  I.A. and O’Kane  S.L. (2002) Taxonomy and phylogeny of PubMed PMC

Anders  S., Pyl  P.T. and Huber  W. (2015) HTSeq—a Python framework to work with high-throughput sequencing data. PubMed PMC

Arunkumar  R., Josephs  E.B., Williamson  R.J. and Wright  S.I. (2013) Pollen-specific, but not sperm-specific, genes show stronger purifying selection and higher rates of positive selection than sporophytic genes in PubMed

Austerlitz  F., Gleiser  G., Teixeira  S. and Bernasconi  G. (2012) The effects of inbreeding, genetic dissimilarity and phenotype on male reproductive success in a dioecious plant. PubMed PMC

Bates  D., Mächler  M., Bolker  B. and Walker  S. (2015) Fitting linear mixed-effects models using lme4.

Beaudry  F.E.G.  Rifkin  J.L., Barrett  S.C.H. and Wright  S.I. (2020) Evolutionary genomics of plant gametophytic selection. PubMed PMC

Bolger  A.M., Lohse  M. and Usadel  B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. PubMed PMC

Carleial  S., van Kleunen  M. and Stift  M. (2017) Small reductions in corolla size and pollen: ovule ratio, but no changes in flower shape in selfing populations of the North American PubMed

Cascallares  M., Setzes  N., Marchetti  F., López  G.A., Distéfano  A.M., Cainzos  M., et al. (2020) A complex journey: cell wall remodeling, interactions, and integrity during pollen tube growth. PubMed PMC

Chae  K. and Lord  E.M. (2011) Pollen tube growth and guidance: roles of small, secreted proteins. PubMed PMC

Chae  K., Zhang  K., Zhang  L., Morikis  D., Kim  S.T., Mollet  J.-C., et al. (2007) Two SCA (stigma/style cysteine-rich adhesin) isoforms show structural differences that correlate with their levels of PubMed

Chebli  Y. and Geitmann  A. (2024) Pectate lyase-like lubricates the male gametophyte’s path toward its mating partner. PubMed

Chen  D. and Zhao  J. (2008) Free IAA in stigmas and styles during pollen germination and pollen tube growth of PubMed

Cheung  A.Y., Wang  H. and Wu  H. (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. PubMed

Christopher  D.A., Mitchell  R.J. and Karron  J.D. (2020) Pollination intensity and paternity in flowering plants. PubMed PMC

Cole  R.A. and Fowler  J.E. (2006) Polarized growth: maintaining focus on the tip. PubMed

Connallon  T. and Hall  M.D. (2018) Genetic constraints on adaptation: a theoretical primer for the genomics era. PubMed

Cutter  A.D. (2019) Reproductive transitions in plants and animals: selfing syndrome, sexual selection and speciation. PubMed

Darwin  C.R. (1871) Principles of Sexual Selection.

Dean  R., Harrison  P.W., Wright  A.E., Zimmer  F. and Mank  J.E. (2015) Positive selection underlies Faster-z evolution of gene expression in birds. PubMed PMC

Delph  L.F., Johannsson  M.H. and Stephenson  A.G. (1997) How environmental factors affect pollen performance: ecological and evolutionary perspectives.

Delph  L.F., Weinig  C. and Sullivan  K. (1998) Why fast-growing pollen tubes give rise to vigorous progeny: the test of a new mechanism.

Dobin  A., Davis  C.A., Schlesinger  F., Drenkow  J., Zaleski  C., Jha  S., et al. (2013) STAR: ultrafast universal RNA-seq aligner. PubMed PMC

Dresselhaus  T. and Franklin-Tong  N. (2013) Male–female crosstalk during pollen germination, tube growth and guidance, and double fertilization. PubMed

Dresselhaus  T. and Márton  M.L. (2009) Micropylar pollen tube guidance and burst: adapted from defense mechanisms? PubMed

Eberhard  W.G. (1996)

Elleman  C.J. and Dickinson  H.G. (1999) Commonalities between pollen/stigma and host/pathogen interactions: calcium accumulation during stigmatic penetration by

Enami  K., Ichikawa  M., Uemura  T., Kutsuna  N., Hasezawa  S., Nakagawa  T., et al. (2009) Differential expression control and polarized distribution of plasma membrane-resident SYP1 SNAREs in PubMed

Erbar  C. (2003) Pollen tube transmitting tissue: place of competition of male gametophytes.

Foxe  J.P., Stift  M., Tedder  A., Haudry  A., Wright  S.I. and Mable  B.K. (2010) Reconstructing origins of loss of self-incompatibility and selfing in North American PubMed

Guo  F. and McCubbin  A.G. (2012) The pollen-specific R-SNARE/longin PiVAMP726 mediates fusion of endo- and exocytic compartments in pollen tube tip growth. PubMed PMC

Gutiérrez-Valencia  J., Fracassetti  M., Horvath  R., Laenen  B., Désamore  A., Drouzas  A.D., et al. (2022) Genomic signatures of sexual selection on pollen-expressed genes in PubMed PMC

Harrison  M.C., Mallon  E.B., Twell  D., Hammond  R.L. and Mank  J. (2019) Deleterious mutation accumulation in PubMed PMC

Harrison  P.W., Wright  A.E., Zimmer  F., Dean  R., Montgomery  S.H., Pointer  M.A., et al. (2015) Sexual selection drives evolution and rapid turnover of male gene expression. PubMed PMC

Heberle  H., Meirelles  G.V., Da Silva  F.R., Telles  G.P. and Minghim  R. (2015) InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. PubMed PMC

Heblack  J., Schepers  J.R. and Willi  Y. (2024) Evolutionary potential under heat and drought stress at the southern range edge of North American PubMed

Hedhly  A., Hormaza  J. and Herrero  M. (2004) Effect of temperature on pollen tube kinetics and dynamics in sweet cherry, PubMed

Hemp  A. (1996). Okologie, Verbreitung und Gesellschaftsanschluβ ausgewhlter Eiszeitrelikte (

Higashiyama  T. and Yang  W. (2017) Gametophytic pollen tube guidance: attractant peptides, gametic controls, and receptors. PubMed PMC

Hoebe  P.N., Stift  M., Tedder  A. and Mable  B.K. (2009) Multiple losses of self-incompatibility in North-American PubMed

Hove  A. and Mazer  S. (2013) Pollen performance in clarkia taxa with contrasting mating systems: implications for male gametophytic evolution in selfers and outcrossers. PubMed PMC

Hu  T.T., Pattyn  P., Bakker  E.G.  Cao  J., Cheng  J.-F., Clark  R.M., et al. (2011) The PubMed PMC

Huang  N., Lee  I., Marcotte  E.M., Hurles  M.E. and Schierup  M.H. (2010) Characterising and predicting haploinsufficiency in the human genome. PubMed PMC

Ichikawa  M., Hirano  T., Enami  K., Fuselier  T., Kato  N., Kwon  C., et al. (2014) Syntaxin of plant proteins SYP123 and SYP132 mediate root hair tip growth in PubMed

Johnson  M.A., Harper  J.F. and Palanivelu  R. (2019) A fruitful journey: pollen tube navigation from germination to fertilization. PubMed

Johnson  M.A. and Preuss  D. (2002) Plotting a course: multiple signals guide pollen tubes to their targets. PubMed

Jonsell  B., Kustås  K. and Nordal  I. (1995) Genetic variation in

Klosinska  M., Picard  C.L. and Gehring  M. (2016) Conserved imprinting associated with unique epigenetic signatures in the Arabidopsis genus. PubMed PMC

Kolesnikova  U.K., Scott  A.D., Van De Velde  J.D., Burns  R., Tikhomirov  N.P., Pfordt  U., et al. (2023) Transition to self-compatibility associated with dominant PubMed PMC

Kuznetsova  A., Brockhoff  P.B. and Christensen  R.H.B. (2017) lmerTest package: tests in linear mixed effects models.

Lankinen  Å. and Karlsson Green  K. (2015) Using theories of sexual selection and sexual conflict to improve our understanding of plant ecology and evolution. PubMed PMC

Li  Y., Mamonova  E., Köhler  N., van Kleunen  M. and Stift  M. (2023) Breakdown of self-incompatibility due to genetic interaction between a specific PubMed PMC

Liu  X., Xiao  Y., Zi  J., Yan  J., Li  C., Du  C., et al. (2023a) Differential effects of low and high temperature stress on pollen germination and tube length of mango ( PubMed PMC

Liu  X., Zhu  D., Zhao  F., Gao  Y., Li  J. and Li  Y. (2023b) VAMP726 and VAMP725 regulate vesicle secretion and pollen tube growth in PubMed

Love  M.I., Huber  W. and Anders  S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. PubMed PMC

Lovy‐Wheeler  A., Cárdenas  L., Kunkel  J.G. and Hepler  P.K. (2007) Differential organelle movement on the actin cytoskeleton in lily pollen tubes. PubMed

Mable  B.K., Robertson  A.V., Dart  S., Di Berardo  C. and Witham  L. (2005) Breakdown of self-incompatibility in the perennial PubMed

Macgregor  S.R., Beronilla  P.K.S. and Goring  D.R. (2023) The PubMed

Marshall  D.L., Hatfield  M.W.F.C. and Bennett  T. (1996) Does interference competition among pollen grains occur in wild radish? PubMed

Martin  M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads.

Mazer  S.J., Hendrickson  B.T., Chellew  J.P., Kim  L.J., Liu  J.W., Shu  J., et al. (2018) Divergence in pollen performance between PubMed

Mazer  S.J., Hove  A.A., Miller  B.S. and Barbet-Massin  M. (2010) The joint evolution of mating system and pollen performance: predictions regarding male gametophytic evolution in selfers vs. outcrossers.

Mollet  J.-C., Park  S.-Y., Nothnagel  E.A. and Lord  E.M. (2000) A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. PubMed PMC

Moore  J.C. and Pannell  J.R. (2011) Sexual selection in plants. PubMed

Németh  M.B. and Smith‐Huerta  N.L. (2003) Pollen deposition, pollen tube growth, seed production, and seedling performance in natural populations of

Nordborg  M. (1997) Structured coalescent processes on different time scales. PubMed PMC

O’Kane  S.L. and Al-Shehbaz  I.A. (1997) A synopsis of

Pannell  J.R. and Labouche  A.-M. (2013) The incidence and selection of multiple mating in plants. PubMed PMC

Park  S.-Y., Jauh  G.-Y., Mollet  J.-C., Eckard  K.J., Nothnagel  E.A., Walling  L.L., et al. (2000) A lipid transfer–like protein is necessary for lily pollen tube adhesion to an in vitro stylar matrix. PubMed PMC

Pasonen  H.L., Pulkkinen  P., Kapyla  M. and Blom  A. (1999) Pollen-tube growth rate and seed-siring success among

Pereira  A.M., Moreira  D., Coimbra  S. and Masiero  S. (2021) Paving the way for fertilization: the role of the transmitting tract. PubMed PMC

Price  P.D., Palmer Droguett  D.H., Taylor  J.A., Kim  D.W., Place  E.S., Rogers  T.F., et al. (2022) Detecting signatures of selection on gene expression. PubMed

Qin  Y. and Yang  Z. (2011) Rapid tip growth: insights from pollen tubes. PubMed PMC

Rawat  V., Abdelsamad  A., Pietzenuk  B., Seymour  D.K., Koenig  D., Weigel  D., et al. (2015) Improving the annotation of PubMed PMC

R Core Team . (2023) R Core Team R: A Language and Environment for Statistical Computing.

Rodríguez-Trelles  F., Tarrío  R. and Ayala  F. (2003) Evolution of cis-regulatory regions versus codifying regions. PubMed

Ross-Ibarra  J., Wright  S.I., Foxe  J.P., Kawabe  A., DeRose-Wilson  L., Gos  G., et al. (2008) Patterns of polymorphism and demographic history in natural populations of PubMed PMC

Ruan  H., Li  J., Wang  T. and Ren  H. (2021) Secretory vesicles targeted to plasma membrane during pollen germination and tube growth. PubMed PMC

Sanati Nezhad  A. and Geitmann  A. (2013) The cellular mechanics of an invasive lifestyle. PubMed

Schmickl  R., Jørgensen  M.H., Brysting  A.K. and Koch  M.A. (2010) The evolutionary history of the PubMed PMC

Scholz  P., Anstatt  J., Krawczyk  H.E. and Ischebeck  T. (2020) Signalling pinpointed to the tip: the complex regulatory network that allows pollen tube growth. PubMed PMC

Shi  D., Tang  C., Wang  R., Gu  C., Wu  X., Hu  S., et al. (2017) Transcriptome and phytohormone analysis reveals a comprehensive phytohormone and pathogen defence response in pear self-/cross-pollination. PubMed PMC

Shuker  D.M., Kvarnemo  C. and Simmons  L. (2021) The definition of sexual selection. PubMed PMC

Sicard  A., Kappel  C., Lee  Y.W., Woźniak  N.J., Marona  C., Stinchcombe  J.R., et al. (2016) Standing genetic variation in a tissue-specific enhancer underlies selfing-syndrome evolution in PubMed PMC

Signor  S.A. and Nuzhdin  S.V. (2018) The evolution of gene expression in PubMed PMC

Skogsmyr  I. and Lankinen  Å. (2002) Sexual selection: an evolutionary force in plants? PubMed

Slane  D., Reichardt  I., El Kasmi  F., Bayer  M. and Jürgens  G. (2017) Evolutionarily diverse SYP1 Qa-SNAREs jointly sustain pollen tube growth in PubMed

Smith-Huerta  N.L. (1996) Pollen germination and tube growth in selfing and outcrossing populations of

Smith-Huerta  N.L., Carrino-Kyker  S.R. and Huerta  A.J. (2007) The effects of maternal and paternal nutrient status on pollen performance in the wildflower

Snow  A.A. and Spira  T.P. (1991) Pollen vigour and the potential for sexual selection in plants.

Snow  A.A. and Spira  T.P. (1996) Pollen-tube competition and male fitness in hibiscus moscheutos. PubMed

Tang  D., Chen  M., Huang  X., Zhang  G., Zeng  L., Zhang  G., et al. (2023) SRplot: a free online platform for data visualization and graphing. PubMed PMC

Taylor  M.L. and Williams  J.H. (2012) Pollen tube development in two species of PubMed

Tian  F., Yang  D.-C., Meng  Y.-Q., Jin  J. and Gao  G. (2019) PlantRegMap: charting functional regulatory maps in plants. PubMed PMC

Tonnabel  J., Cosette  P., Lehner  A., Mollet  J.-C., Amine Ben Mlouka  M., Grladinovic  L., et al. (2022) Rapid evolution of pollen and pistil traits as a response to sexual selection in the post-pollination phase of mating. PubMed

Tonnabel  J., David  P., Janicke  T., Lehner  A., Mollet  J.-C., Pannell  J.R., et al. (2021) The scope for postmating sexual selection in plants. PubMed

Tosto  N.M., Beasley  E.R., Wong  B.B.M., Mank  J.E. and Flanagan  S.P. (2023) The roles of sexual selection and sexual conflict in shaping patterns of genome and transcriptome variation. PubMed

Veltsos  P., Porcelli  D., Fang  Y., Cossins  A.R., Ritchie  M.G. and Snook  R.R. (2022) Experimental sexual selection reveals rapid evolutionary divergence in sex‐specific transcriptomes and their interactions following mating. PubMed PMC

Vuylsteke  M., van Eeuwijk  F., Van Hummelen  P., Kuiper  M. and Zabeau  M. (2005) Genetic analysis of variation in gene expression in PubMed PMC

Wang  H.-J., Huang  J.-C., Jauh  G.-Y. (2010) Pollen germination and tube growth.

Weng  X. and Wang  H. (2022) Apical vesicles: social networking at the pollen tube tip.

Wilkinson  G.S., Breden  F., Mank  J.E., Ritchie  M.G., Higginson  A.D., Radwan  J., et al. (2015) The locus of sexual selection: moving sexual selection studies into the post‐genomics era. PubMed

Willi  Y. and Määttänen  K. (2010) Evolutionary dynamics of mating system shifts in PubMed

Wright  S.I., Kalisz  S. and Slotte  T. (2013) Evolutionary consequences of self-fertilization in plants. PubMed PMC

Xiyan  L. (2011)

Xu  Y. and Huang  S. (2020) Control of the actin cytoskeleton within apical and subapical regions of pollen tubes. PubMed PMC

Zúñiga-Mayo  V.M., Gómez-Felipe  A., Herrera-Ubaldo  H. and de Folter  S. (2019) Gynoecium development: networks in PubMed

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