Biology subjects

Pannell, J. R.

Publications and source records attributed to Pannell, J. R..

16 recordsLinked to original sources

bioRxiv2026

The evolutionary interplay between self-fertilisation and sex allocation in flowering plants

Flowering plants vary in sex allocation (resource division between male and female function) and in selfing rate. These traits should evolve together: selfing changes fitness returns from pollen and ovules, whereas sex allocation changes the pollen available for selfing and export. Yet most models allow only one trait to evolve, leaving their evolutionary feedback unresolved. Here we model the joint evolution of sex allocation, pollen export and maternal control of competition between self- and cross-pollen. We show that selfing and sex allocation strongly influence one another, as selection favours associations between sex allocation and mating-system traits. When maternal control is fixed to recover classical mass-action, evolution can lead to the stable coexistence of selfing hermaphrodites and males specialised in pollen export. This androdioecy persists because hermaphrodites cannot prevent fertilisation by males. When maternal control of pollen competition also evolves, we find that where a mixed-mating equilibrium exists, selection again favours the emergence of androdioecy. As hermaphrodites evolve to favour their own pollen, however, they progressively exclude pollen from males, driving them extinct. The population may then return to mixed mating and repeat the process, or evolve complete selfing. We discuss these results with reference to known variation in the mating and sexual systems of plants.

evolutionary biology↗

bioRxiv2026

Evolution of recombination suppression and sex determination on Y chromosomes of the plant genus Mercurialis

Understanding why sex chromosomes repeatedly evolve recombination suppression, gene loss, and repeat accumulation remains a central challenge in evolutionary genomics. Plant sex chromosomes may be particularly informative, because they have often evolved recently from hermaphroditic ancestors. We studied the sex-linked region of the dioecious annual Mercurialis annua using new long-read genome assemblies of an XX female and a YY male, a published female assembly, linkage maps, and population-genomic data from several Mercurialis species. We identify two discrete nested evolutionary strata on the Y chromosome of diploid M. annua. A young stratum was generated by a large inversion and shows little degeneration, whereas an older stratum nested within it exhibits substantial gene loss, transposable-element accumulation, insertion of paralogous gene copies, and elevated X-Y sequence divergence. These findings indicate that recombination suppression evolved in at least two stages, with a recent inversion expanding an older non-recombining region. Comparative analyses among several Mercurialis species further show that the extent of sex-linked differentiation varies markedly among them. We also identify APRR7 as the only gene showing consistent male-specific inheritance across the genus; this gene is a strong candidate master sex-determination gene. Together, our results refine the structure and gene content of the sex-linked region in M. annua and contribute to our understanding of the diversity of sex chromosomes in plants.

evolutionary biology↗

bioRxiv2026

The evolution of condition-dependent self-fertilisation

Self-fertilisation is common in cosexuals, but selfing rates vary among species, among populations and among individuals within populations. Most evolutionary theory seeking to explain this variation assumes genetically determined selfing rates. Here we study the evolution and consequences of condition-dependent selfing, where individuals adjust their selfing rate in response to their deleterious mutation load. We analyse a two-locus population-genetic model in which one locus determines condition and the other is a modifier locus that determines condition-dependent selfing rates, and then extend the analysis to a polygenic background in which condition is determined by many loci. Our results show that selection favours positive condition dependence: high-condition individuals self-fertilise whereas low-condition individuals outcross. The resulting reaction norm generates stable within-population variation in realised selfing rates at evolutionary equilibrium and reduces the mutation load. We further show that it persists under environmental heterogeneity, and that pollen discounting favours a gradual increase in selfing with condition, leading to a continuum of selfing phenotypes. Altogether, our results indicate that condition-dependent selfing can generate substantial within-population variation in selfing rates. It may therefore contribute to mating-system diversity, and in particular to the maintenance of mixed mating.

evolutionary biology↗

bioRxiv2025

Dioecy in a wind-pollinated herb explained by disruptive selection on sex allocation

O_LIThe evolution of dioecy from hermaphroditism is widely thought to be a response to disruptive selection favouring males and females, driven by advantages of inbreeding avoidance, sexual specialization, or both. It has hitherto been difficult to uncouple the importance of these two hypotheses. C_LIO_LIWe use phenotypes produced by experimental evolution to test the inbreeding avoidance hypothesis in populations from which sexual specialization can be effectively ruled out. We estimate the selfing rate and the shape of fitness gain curves under scenarios with and without inbreeding depression in experimental populations of wind-pollinated Mercurialis annua with high variation in sex allocation. C_LIO_LIWe confirm a phenotypic trade-off between male and female allocation in M. annua. Individual selfing rates increased with pollen production. This dependence gave rise to strong disruptive selection on sex allocation due to its interaction with the mating system under the scenario of high inbreeding depression, especially for plants of medium and large sizes. C_LIO_LITaken together, we demonstrate that inbreeding avoidance on its own can lead to disruptive selection on sex allocation, favouring the selection and maintenance of dioecy under wind pollination without associated benefits of sexual specialization. C_LI

evolutionary biology↗

bioRxiv2024

Sex-allocation trade-offs and their genetic architecture revealed by experimental evolution

The theory of sex-allocation is hailed as one of evolutionary biologys great successes. But while it has successfully predicted strategies of resource allocation to sons versus daughters under a wide range of conditions in species with separate sexes, it has been difficult to apply to hermaphroditic species because of the repeated failure to verify the fundamental assumption of a direct genetic trade-off between male and female allocations made by hermaphrodites. This assumption supposes that mutations that increase an individuals male allocation reduce its female allocation in equal measure, yet there is almost no evidence for such trade-off loci in hermaphroditic populations. Here, we use experimental evolution to generate wide variation in hermaphroditic sex allocation in an annual plant and demonstrate a clear trade-off between the two sexual functions within populations as well as over time, with populations evolving both increased male and reduced female allocation. Quantitative trait locus (QTL) analysis performed on multiple crosses further reveals the segregation of allelic variation at trade-off loci. Taken together, our results demonstrate a phenotypic trade-off in sex allocation in hermaphrodites and provide compelling evidence for sex-allocation trade-off loci, verifying the fundamental assumption of sex-allocation theory and securing its general applicability to both dioecious and hermaphroditic species.

evolutionary biology↗

bioRxiv2024

Widespread male sterility and trioecy in androdioecious Mercurialis annua: an account of its distribution, its genetic basis, and estimates of its morph-specific fitness components

PremiseAngiosperms range from hermaphroditism through gynodioecy and androdioecy to dioecy. Trioecy, where females and males coexist with hermaphrodites, is rare. Recently, trioecy was documented in hexaploid populations of the wind-pollinated herb Mercurialis annua in Spain. MethodsWe surveyed the frequency of males, hermaphrodites and females in M. annua across its distribution in the Iberian Peninsula, tracked sex-ratio variation in several populations over consecutive generations, and assessed evidence for pollen limitation. In a common garden, we estimated male, female and hermaphrodite fitness. We used controlled crosses to infer the genetic basis of male sterility. Finally, we compared predictions of a deterministic model with the distribution of observed sex ratios in the field based on our fitness estimates and the inferred genetics of sex determination. Key resultsTrioecy is widespread in Spanish and Portuguese populations of M. annua. Males are determined by a dominant (Y-linked) allele, and female expression results from the interaction between cytoplasmic male sterility and multiple nuclear male sterility restorers partially linked to the male determiner. Male pollen production is approximately 12 times while female seed production is less than 1.12 times that of hermaphrodites. The distribution of sex ratios in natural populations conforms with predictions of our deterministic simulations. ConclusionsOur study documents and accounts for a clear case of trioecy in which sex is determined by both maternally and biparentally inherited genes.

plant biology↗

bioRxiv2024

Mapping fitness landscapes to interpret sex allocation in hermaphrodites

Sex allocation theory predicts sex ratios of dioecious organisms, but it has been poor at explaining sex allocation in hermaphrodites in which the assumed trade-off between male and female functions is often obscure. Here, we apply sex-allocation theory to hermaphrodites by mapping components of seasonal reproductive success onto a fitness landscape defined by potentially independent measures of allocation to male and female functions on orthogonal axes. We find that peaks of reproductive success in a perennial hermaphroditic plant reflect the interactive effect of both male and female allocations on self-fertilization and the effects of inbreeding depression. The rugged landscape corresponds well to the complex pattern of sex allocation observed in natural populations in which individuals produce a mix of male and bisexual flowers and express a type of gender diphasy. Our approach may help to interpret common complexities of sex allocation in hermaphroditic plants and animals.

evolutionary biology↗

bioRxiv2024

Effects of floral sex allocation and phenology on the within-flower selfing rate and female reproductive success in Pulsatilla alpina, a perennial herb with strong inbreeding depression

O_LIWithin-flower self-pollination should be the major source of self-fertilization in mixed-mating species presenting single or few flowers simultaneously. It is also an often unmeasured source of selfing in species with many flowers open simultaneously. In general, the rate of within-flower selfing is expected to depend on the number of pistils and stamens, the timing of flowering, and subsidiary floral traits in self-compatible species in which pistil and stamen numbers vary. Accordingly, the intensity and direction of selection on these traits should depend on the level of inbreeding depression. C_LIO_LIHere, we measured the dependence of the within-flower selfing rate on floral sex allocation, phenology, petal length, and floral stalk height in a population of the perennial herb Pulsatilla alpina (Ranunculaceae) in which most individuals had single flowers. We estimated inbreeding depression in the population by comparing inbreeding coefficients between parents and seed progeny using microsatellite markers. We then estimated selection on the measured traits via female reproductive success at the flower level and compared our estimates with a hypothetical scenario in which inbreeding depression was assumed to be absent. C_LIO_LIWe estimated inbreeding depression to be 0.93. The within-flower selfing rate varied widely among flowers and depended positively on stamen number and negatively on pistil number and flowering date, supporting the predictions of a mass-action model. The dependence of the selfing rate on the measured floral traits consistently predicted (non-linear) patterns of selection under high inbreeding depression that were distinct from those under a hypothetical scenario of no inbreeding depression. C_LIO_LISynthesis: While previous research has emphasized the importance of mass-action mating on selfing among flowers of plants with large floral displays, our results demonstrate its importance for selfing within individual flowers. They also demonstrate the importance of accounting for both the selfing rate and inbreeding depression when inferring selection on floral and other traits via female fitness. C_LI

evolutionary biology↗

bioRxiv2023

On the origins of Y and W chromosomes as an outcome of sex allocation evolution

In plants with separate sexes, the development of an individual as male or female is controlled by a dominant allele at a sex-determining locus - the fundamental basis of XY and ZW systems. The many independent transitions from hermaphroditism to dioecy that have taken place in flowering plants must therefore often have entailed the emergence of such a locus. One proposition is that this evolution occurs in two steps, with the initial invasion of a male-sterility mutation at one locus followed by mutations causing female sterility at a second closely linked locus. Here, we show how dioecy with heterogametic sex determination can also emerge in a gradual adaptive process, involving the co-evolution of resource allocation to different sexual functions jointly with its genetic architecture. Our model reveals that whether an XY or a ZW system evolves depends on the mating system of the ancestral hermaphrodites as well as the trade-off they face between allocation to male and female functions. In particular, the evolution of dioecy in response to selection to avoid selfing and inbreeding depression favours the emergence of XY systems, which characterise the vast majority of dioecious flowering plants. Selection favouring female specialisation also favours XY over ZW sex determination. Taken together, our results throw new light on the possible origins of dioecy from hermaphroditism by revealing a hitherto unrecognised link between the ecology and economics of sex allocation and the genetic basis of sex determination.

evolutionary biology↗

bioRxiv2023

Size-dependent sex allocation and the expression of andromonoecy in a protogynous perennial herb: both size and timing matter

The optimal life history and sex allocation of perennial hermaphrodites should depend on both their size and the relative costs and benefits of reproducing through male versus female functions. Theory predicts that insect-pollinated perennials should increase their allocation to female function with size, while the mating environment hypothesis predicts that allocation to male function should track mating opportunities over the course of flowering. We test these two predictions by inferring male and female reproductive success in the protogynous perennial herb Pulsatilla alpina by tracking the patterns and dynamics of sex allocation over time for marked individuals over a range of sizes. We found that small individuals tend to produce only male flowers and that both small and larger individuals produced male flowers at the beginning of the flowering season when mating opportunities were high. By considering within-population variation in life history and phenology jointly rather than separately, and by considering both the tradeoff costs and benefits of allocation to male versus female functions, our results provide new insights into the evolution of both gender diphasy and andromonoecy in perennial plants that are constrained by a dichogamous flowering strategy.

evolutionary biology↗

bioRxiv2022

Disruptive selection via pollinators and seed predators on the height of flowers in a wind-dispersed alpine herb

Premise of the studyFloral stalk height is known to affect pollination and seed dispersal in wind-dispersed grassland species, but it may also affect the attractiveness of flowers and fruits in animal-pollinated and animal-dispersed plants. Stalk height may thus be responsive to selection via interactions with both mutualist pollinators and seed dispersers, but also antagonist florivors and seed predators. In this study, we aimed to determine the effect of pollinators and seed predators on selection on floral stalk height in the insect-pollinated and wind-dispersed alpine andromonoecious herb Pulsatilla alpina, whose flowers also vary in their sex allocation and thus in the resources available to both mutualists and antagonists. MethodsWe measured the resource status of individuals in terms of their size and the height of the vegetation surrounding plants of P. alpina at eleven sites. In one population, we recorded the dynamics of floral stalk height over the course of an entire growing season and its association with floral morphology and floral sex allocation (pistil and stamen number), and we used leaf-removal manipulations to assess the effect of herbivory on floral stalk height. Finally, in four populations we studied phenotypic selection on floral stalk height in four female components of reproductive success before seed dispersal. Key resultsStalk height was positively associated with female allocation of the respective flower, the resource status of the individual, and the height of the surrounding vegetation, and negatively affected by leaf removal. Our results point to disruptive selection on stalk height in terms of both selection differentials and selection gradients for fertilization, seed predation, and seed maturation rates, and to positive selection on stalk height in terms of a selection differential for mature seed number. ConclusionsStalk height in P. alpina is a costly trait that affects female reproductive success via interactions with both mutualists and antagonists. We discuss the interplay between the resource status and selection imposed on female reproductive success and its likely role in the evolution of sex-allocation strategies, especially andromonoecy.

evolutionary biology↗

bioRxiv2021

Disentangling the effects of jasmonate and tissue loss on the sex allocation of an annual plant

Selection through pollinators plays a major role in the evolution of reproductive traits. However, herbivory can also induce changes in plant sexual expression and sexual systems, potentially influencing conditions governing transitions between sexual systems. Previous work has shown that herbivory has a strong effect on sex allocation in the wind-pollinated annual plant Mercurialis annua, likely mediated by resource loss. It is also known that many plants respond to herbivory by inducing signalling, and endogenous responses to it, via the plant hormone jasmonate. Here, we attempt to uncouple the effects of herbivory on sex allocation in M. annua through resource limitation (tissue loss) versus plant responses to jasmonate hormone signalling. We used a two-factorial experiment with four treatment combinations: control, herbivory (25% chronic tissue loss), jasmonate, and combined herbivory and jasmonate. We estimated the effects of tissue loss and defence-inducing hormones on reproductive allocation, male reproductive effort, and sex allocation. Tissue loss caused plants to reduce their male reproductive effort, resulting in changes in combined sex allocation. However, application of jasmonate after herbivory reversed its effect on male investment. Our results show that herbivory has consequences on plant sex expression and sex allocation, and that defence-related hormones such as jasmonate can buffer the impacts. We discuss the physiological mechanisms that might underpin the effects of herbivory on sex allocation, and their potential implications for the evolution of plant sexual systems.

evolutionary biology↗

bioRxiv2019

Enhanced leaky sex expression is an adaptive plastic response to pollen limitation in the dioecious plant Mercurialis annua

Phenotypic plasticity is almost ubiquitous across the tree of life, but clear demonstrations that it is adaptive are rare. In dioecious plants, males and females frequently show leaky sex expression, with individuals occasionally producing flowers of the opposite sex. Here, we demonstrate that leaky sex expression in the wind-pollinated dioecious herb Mercurialis annua is plastically responsive to its mating context. We compared experimental populations of females growing either with or without males. Females growing in the absence of males were leakier in their sex expression than controls with males, producing more than twice as many male flowers. Moreover, because greater leakiness was more highly represented in the populations progeny, we conclude that enhanced leakiness in sex expression is adaptive in M. annua. We discuss differences in the degree of plasticity between ploidal races of Mercurialis annua in terms of likely differences in the reliability of the signal plants may perceive for the presence of males in their populations. Our results provide a striking instance of adaptive plasticity in the reproductive behavior of plants and draw attention to possible constraints on plasticity when the environmental signals that individuals receive are unreliable.

evolutionary biology↗

bioRxiv2019

YY males of the dioecious plant Mercurialis annua are fully viable but produce largely infertile pollen

The suppression of recombination during sex-chromosome evolution is thought to be favoured by linkage between the sex-determining locus and sexually-antagonistic loci, and leads to the degeneration of the chromosome restricted to the heterogametic sex. Despite substantial evidence for genetic degeneration at the sequence level, the phenotypic effects of the earliest stages of sex-chromosome evolution are poorly known. Here, we compare the morphology, viability and fertility between XY and YY individuals produced by crossing seed-producing males in the dioecious plant Mercurialis annua L., which has young sex chromosomes with limited X-Y sequence divergence. We found no significant difference in viability or vegetative morphology between XY and YY males. However, electron microscopy revealed clear differences in pollen anatomy, and YY males were significantly poorer sires in competition with their XY counterparts. Our study suggests either that the X chromosome is required for full male fertility in M. annua, or that male fertility is sensitive to the dosage of relevant Y-linked genes. We discuss the possibility that the maintenance of male-fertility genes on the X chromosome might have been favoured in recent population expansions, which selected for the ability of females to produce pollen in the absence of males.

evolutionary biology↗

bioRxiv2017

Low Rate of Somatic Mutations in a Long-Lived Oak Tree

Because plants do not possess a proper germline, deleterious somatic mutations can be passed to gametes and a large number of cell divisions separating zygote from gamete formation in long-lived plants may lead to many mutations. We sequenced the genome of two terminal branches of a 234-year-old oak tree and found few fixed somatic single-nucleotide variants (SNVs), whose sequential appearance in the tree could be traced along nested sectors of younger branches. Our data suggest that stem cells of shoot meristems are robustly protected from accumulation of mutations in trees.

plant biology↗

bioRxiv2017

Hallmarks of early sex-chromosome evolution in the dioecious plant Mercurialis annua revealed by de novo genome assembly, genetic mapping and transcriptome analysis

Suppressed recombination around a sex-determining locus allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. Both genetic mapping and exome resequencing of individuals across the species range independently identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about a third of the Y chromosome has ceased recombining, a region containing 568 transcripts and spanning 22.3 cM in the corresponding female map. Patterns of gene expression hint at the possible role of sexually antagonistic selection in having favored suppressed recombination. In total, the genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. There was limited evidence of Y-chromosome degeneration in terms of gene loss and pseudogenization, but sequence divergence between the X and Y copies of many sex-linked genes was higher than between M. annua and its dioecious sister species M. huetii with which it shares a sex-determining region. The Mendelian inheritance of sex in interspecific crosses, combined with the other observed pattern, suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining about one million years ago. Article summaryPlants that evolved separate sexes (dioecy) recently are ideal models for studying the early stages of sex-chromosome evolution. Here, we use karyological, whole genome and transcriptome data to characterize the homomorphic sex chromosomes of the annual dioecious plant Mercurialis annua. Our analysis reveals many typical hallmarks of dioecy and sex-chromosome evolution, including sex-biased gene expression and high X/Y sequence divergence, yet few premature stop codons in Y-linked genes and very little outright gene loss, despite 1/3 of the sex chromosome having ceased recombination in males. Our results confirm that the M. annua species complex is a fertile system for probing early stages in the evolution of sex chromosomes.

genomics↗