Biology subjects

Pannell, J.

Publications and source records attributed to Pannell, J..

12 recordsLinked to original sources

bioRxiv2026

Geographical gradients in leaky sex expression and reproductive effort in a dioecious plant are consistent with selection during range expansion

Range expansion involves repeated dispersal and the establishment of new populations through colonization. Natural selection is therefore expected to favour traits that enhance dispersal and enable uniparental reproduction when mates are scarce. It is known that range-edge populations may evolve increased dispersal and, in hermaphroditic species, an enhanced capacity for self-fertilization. Here, we report results from a large common-garden experiment showing that males and females of the dioecious annual herb Mercurialis annua are more likely to show leaky or inconstant sex expression towards the recently colonized edge of its geographical distribution in Europe than those from the eastern Mediterranean Basin, from where the species expanded its range. Range-edge populations also had greater reproductive effort (RE). Leaky sex expression allows otherwise unisexual individuals of M. annua to produce progeny by self-fertilization, a trait that may have been selected for reproductive assurance during the range expansion. High RE likely facilitated both colonization and subsequent population establishment. Our results show that selection during range expansions may modify reproductive traits towards range margins, extending this notion to the phenomenon of leaky sex expression in dioecious species. Previous work has shown that leaky sex expression in M. annua is strongly heritable; our results now further suggest that has been enhanced by selection for reproductive assurance towards range margins and confirm, in a natural setting, that the trait is not just an expression of developmental instability during floral development or a relic of an incomplete transition to dioecy.

evolutionary biology↗

bioRxiv2024

Replication of treatment effects and differences among populations during experimental evolution of sex allocation in an annual plant

Variation among replicates of experimental evolution studies that begin by sampling from a single source population can be attributed to measurement error or to random differences in the environment experienced by measured individuals. On the basis of measurements in a large common garden, Cossard et al. (2021: Current Biology 7, 1-7) reported rapid evolution of enhanced leaky sex allocation by females (which produced male flowers) in experimental populations of the dioecious herb Mercurialis annua from which males had been removed. Their study thus demonstrated the rapid dissolution of dioecy via changes in sex allocation in response to mate limitation and strong competition for siring success. But their study also found substantial variation among replicate populations. Here, we replicated their common garden, growing plants from the same populations but under different conditions and assaying the measured variables differently. The effects (significance, magnitude and direction) of selection treatment and generation on the sex expression of females with inconstant sex expression met five definitions for successful replication. Importantly, comparisons between the two studies revealed relatively consistent differences among the replicate populations, suggesting that the among-population variation reported by Cossard et al. cannot be attributed to random noise or local differences in growing conditions in the common garden. Our study represents a rare example of the replication of a common garden study and raises interesting questions about the nature of interpopulation divergence within treatment groups of studies using experimental evolution.

evolutionary biology↗

bioRxiv2024

The joint evolution of separate sexes and sexual dimorphism

Dioecious plants are frequently sexually dimorphic. Such dimorphism, which reflects responses to selection acting in opposite directions for male and female components of fitness, is commonly thought to emerge after separate sexes evolved from hermaphroditism. But associations between allocation to male and female function and traits under sexual conflict may well also develop in hermaphroditic ancestors. Here, we show that variation in sex allocation and a trait under sexual conflict inevitably generates an advantage to sexual specialisation, fueling the transition to dioecy. In the absence of constraints, this leads to the joint evolution of separate sexes and sexual dimorphism through the build-up of an association between sex allocation and the conflict trait, such that eventually the population consists of unisexuals expressing their sex-specific optima. We then investigate how such association might materialise genetically, either via recombination suppression or via sex-dependent expression, and show that the genetic architecture of sex allocation and the conflict trait readily evolves to produce the association favoured by selection. Finally and in agreement with previous theory, we demonstrate that limited dispersal and self-fertilisation, which are pervasive ecological characteristics of flowering plants, can offset the advantage of sexual specialisation generated by sexual conflict and thus maintain hermaphroditism. Taken together, our results indicate that advantages to sexual specialisation are inevitable when there is conflict between sexual functions in hermaphrodites, but these advantages can be counterbalanced by ecological benefits of hermaphroditism.

evolutionary biology↗

bioRxiv2024

Traits related to pollination and mating result in diverse reproductive strategies in angiosperms

O_LIFlowering plants have many modes of sexual reproduction, notably varying from selfing to outcrossing, and from bisexual flowers to individuals with separate sexes (dioecy). These reproductive modes are associated with floral and life-history traits that have evolved together, making it difficult to interpret correlations between traits. C_LIO_LIWe analysed variation in 21 traits related to flowers, pollination, mating, sexual systems and life history from 361 species representative of flowering plant diversity. C_LIO_LIOutcrossing was mainly found among long-lived, large-stature plants, but hermaphroditic outcrossers and dioecious species appeared as largely non-overlapping strategies in the trait space. Level of floral investment was the main difference between these strategies, with dioecious species having generally smaller, less rewarding flowers, a pattern that also occurred in biotically pollinated species. C_LIO_LIThis multi-trait study shows that pollination can be achieved in many, often contrasting, ways. Despite extensive variation in reproductive traits, dioecy stands out as being linked to floral traits primarily, while correlations with lifespan and dispersal traits appear spurious. We provide a conceptual framework based on lifespan, floral investment, and sexual separation that can be used to integrate pollination, reproduction and plant growth in future research on plant evolution and ecology. C_LI

evolutionary biology↗

bioRxiv2023

Pre-zygotic mate selection affects progeny fitness and is only partially correlated with the expression of NaS-like RNases

O_LINicotiana attenuata styles preferentially select pollen from accessions with corresponding expression patterns of NaS-like-RNases (SLRs), and the post-pollination ethylene burst (PPEB) is an accurate predictor of seed siring success. However, the ecological consequences of mate selection, its effect on the progeny, and the role of SLRs in the control of ethylene signaling are still not well understood. C_LIO_LIWe explored the link between the magnitude of the ethylene burst and transcript and protein abundance of the SLRs in a set of recombinant inbred lines (RILs) and investigated the fitness consequences of mate selection for the next generation. Genome Wide Association Study (GWAS) identified novel candidate genes potentially involved in the control of mate selection. C_LIO_LIWe found that high levels of PPEB are associated with the absence of SLR2 but not with the expression of SLR1 in most of the tested RILs. Maternal genotypes that favor certain pollen produce offspring with longer roots when pollinated with these donors, but the selection for beneficial traits is abolished when the maternal genotype selects only against certain pollen donors. C_LIO_LIWe conclude that mate selection mechanisms affect the offspring number and performance in ways that might be adaptive. C_LI

ecology↗

bioRxiv2021

Inferring the demographic history of tetraploid species from genomic data

Genomic patterns of diversity and divergence are impacted by certain life history traits, reproductive systems and demographic history. The latter is characterised by fluctuations in population sizes over time, as well as by temporal patterns of introgression. For a given organism, identifying a demographic history that deviates from the standard neutral model allows a better understanding of its evolution, but also helps to reduce the risk of false positives when screening for molecular targets of natural selection. Tetraploid organisms and beyond have demographic histories that are complicated by the mode of polyploidisation, the mode of inheritance and different scenarios of gene flow between subgenomes and diploid parental species. Here we provide guidelines for experimenters wishing to address these issues through a flexible statistical framework: approximate Bayesian computation (ABC). The emphasis is on the general philosophy of the approach to encourage future users to exploit the enormous flexibility of ABC beyond the limitations imposed by generalist data analysis pipelines.

genomics↗

bioRxiv2021

Rapid divergence in vegetative morphology of a wind-pollinated plant between populations at contrasting densities

Plant sexual dimorphism is thought to evolve in response to sex-specific selection associated with competition for access to mates or resources, both of which will often be density-dependent. In wind-pollinated plants in particular, vegetative traits can have an important influence on both resource acquisition and the pollen dispersal and receipt, with potential conflict between these two components of fitness. We evaluated the role of plant density in shaping plant traits by measuring evolutionary responses in experimental populations of the sexually dimorphic wind-pollinated plant Mercurialis annua. After three generations of evolution, we observed divergence between high- and low-density populations in several vegetative traits, whereas there was no divergence for reproductive traits. A reversal in the direction of sexually dimorphic traits expressed in young plants evolved in both low- and high-density populations compared to the original population (stored as seeds). Compared to the source population, males at high density evolved to be taller when young, whereas at low density young females tended to become smaller. These results demonstrate that a simple change in plant density can induce rapid, age-dependent and sex-specific evolution in the ontogeny of vegetative organs, and illustrates the power of experimental evolution for investigating plant trait evolution.

evolutionary biology↗

bioRxiv2021

Herbivory enhances leaky sex expression in the dioecious herb Mercurialis annua

Plant reproductive traits are widely understood to be responsive to the selective pressures exerted by pollinators, but there is also increasing evidence for an important role of antagonists such as herbivores in shaping these traits. Many dioecious species show leaky sex expression, with males and females occasionally producing flowers of the opposite sex. Here we show that leaky sex expression in both males and females of the wind-pollinated dioecious herb Mercurialis annua (Euphorbiaceae) is enhanced in response to simulated herbivory, increasing the probability and the degree of leakiness in both sexes. We also found that leakiness was greater in larger females but not in larger males. We discuss hypotheses for a possible functional link between herbivory and leaky sex expression, and consider what herbivory-induced leakiness might imply for the evolutionary ecology of plant reproductive systems, especially the breakdown of dioecy and the evolution of hermaphroditism.

ecology↗

bioRxiv2021

High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms

The males and females of many dioecious plants differ in morphological (Dawson and Geber 1999; Barrett and Hough 2013; Tonnabel et al. 2017), physiological (Juvany and Munne-Bosch 2015), life-history (Delph 1999), and defence traits (Cornelissen and Stiling 2005). Ultimately, such sexual dimorphism must largely be due to differential gene expression between the sexes (Ellegren and Parsch 2007), but little is known about how sex-biased genes are recruited and how their expression evolves over time. We measured gene expression in leaves of males and females of ten species sampled across the South African Cape genus Leucadendron, which shows repeated changes in sexual dimorphism and includes the most extreme differences between males and females in flowering plants (Midgley 2010; Barrett and Hough 2013; Tonnabel et al. 2014). Even in the most dimorphic species in our sample, fewer than 2% of genes showed sex-biased gene expression (SBGE) in vegetative tissue, with surprisingly little correspondence between SBGE and vegetative dimorphism across species. The identity of sex-biased genes in Leucadendron was highly species-specific, with a rapid turnover among species. In animals, sex-biased genes often evolve more quickly than unbiased genes in their sequences and expression levels (Ranz et al. 2003; Khaitovich et al. 2005; Ellegren and Parsch 2007; Voolstra et al. 2007; Harrison et al. 2015; Naqvi et al. 2019), consistent with hypotheses invoking rapid evolution due to sexual selection. Our phylogenetic analysis in Leucadendron, however, clearly indicates that sex-biased genes are recruited from a class of genes with ancestrally rapid rates of expression evolution, perhaps due to low evolutionary or pleiotropic constraints. Nevertheless, we also find evidence for adaptive evolution of expression levels once sex bias evolves. Thus, although the expression of sex-biased genes is ultimately responsive to selection, high rates of expression evolution might usually predate the evolution of sex bias.

evolutionary biology↗

bioRxiv2020

Sex allocation, inbreeding, and measures of population differentiation in hermaphroditic metapopulations

Selection in inbred populations is expected to favor female-biased sex ratios in dioecious populations as a result of local mate competition, a prediction that finds strong support in situations where females have control of the sex ratio. Local mate competition due to inbreeding should also promote female-biased sex allocation in hermaphrodites, with reduced emphasis on the production and dispersal of sperm or pollen relative to that of eggs, ovules or seeds. While inbreeding can be the direct result of the mating system in local populations, it can also be brought about by population turnover in metapopulations with frequent local extinction and recolonization. This effect of population turnover has previously been considered for species with separate sexes. Here, we use both formal analysis and individual-based simulations to explore the effect of population turnover on sex allocation in partially self-fertilizing hermaphroditic metapopulations. Using simulations, we also assess the extent to which different genetic measures of inbreeding and population differentiation predict the equilibrium sex allocation. We find that population turnover can select for strongly female-biased sex allocation in hermaphroditic metapopulations, particularly if amongdeme dispersal is low, even where local demes are fully outcrossing. In such situations, FST is a good predictor of the equilibrium sex allocation, and much better than the alternative differentiation measures GST and Josts D. Our study extends predictions for sex allocation in subdivided populations to hermaphroditic species, and draws attention in general to the power of Wrights hierarchical inbreeding statistics to predict the sex allocation in metapopulations at equilibrium.

evolutionary biology↗

bioRxiv2019

Rapid dissolution of dioecy by experimental evolution

Evolutionary transitions from hermaphroditism to dioecy have been frequent in flowering plants, but recent analysis indicates that reversions from dioecy to hermaphroditism have also been common. Here, we use experimental evolution to expose a mechanism for such reversions. We removed males from dioecious populations of the wind-pollinated plant Mercurialis annua and allowed natural selection to act on the remaining females that varied in their propensity for the occasional production of male flowers; such leaky sex expression is common in both males and females of dioecious plants. Over only four generations, females evolved a 23-fold increase in average male-flower production. The phenotypic masculinization of females was also sufficient to render them effective at siring progeny in the presence of males. Our study illustrates the rapid dissolution of dioecy and the evolution of functional hermaphroditism under conditions that may frequently occur during periods of low population density, repeated colonization, or range expansion. It thereby experimentally validates a mechanism for a major transition in plant sexual systems..

evolutionary biology↗

bioRxiv2018

A ghost of dioecy past and the legacy of sexual dimorphism: low siring success of hermaphrodites after the breakdown of dioecy

Evolutionary transitions from dioecy to hermaphroditism must overcome the inertia of sexual dimorphism because modified males or females will express the opposite sexual function for which their phenotypes have been optimized. We tested this prediction by comparing the siring success of female-derived hermaphrodites of the plant Mercurialis annua with males and hermaphrodites that present a male-like inflorescence. We found that pollen dispersed by female-derived hermaphrodites was about a third poorer at siring outcross offspring than that from hermaphrodites with male-like inflorescences, illustrating the notion that a ghost of dioecy past compromises the fitness of derived hermaphrodites in outcrossing populations. We conclude that whereas dioecy might evolve from hermaphroditism by conferring upon individuals certain benefits of sexual specialization, reversals from dioecy to hermaphroditism must often be limited to situations in which outcrossing cannot be maintained and inbreeding is favored. Our study provides novel empirical support for evolutionary models for the breakdown of dioecy.

evolutionary biology↗