Article Addendum: The paradox of clonality and the evolution of self-incompatibility

In the January issue of New Phytologist Vallejo-Marín and O’Brien documented that in the genus Solanum (Solanaceae) clonality and self-incompatibility, a common genetic mechanism enforcing cross-fertilization, co-occur more often than expected by chance. Using a phylogenetic approach the authors showed that the statistical association between clonality and self-incompatibility persists even after taking into account phylogenetic relationships among species, uncertainty in the phylogenetic reconstruction, and associations between clonality and life history (annual/perennial). Vallejo-Marín and O’Brien suggest that clonality and self-incompatibility tend to co-occur because clonality, by allowing the persistence and propagation of a genotype in environments with limited pollinator or mate availability, reduces the selective pressure favoring the breakdown of self-incompatibility. In addition to promoting the maintenance of self-incompatibility, when clonality results in the spatial aggregation of genetically identical individuals, clonality may promote its breakdown by restricting pollen transfer between different genotypes. Here I call attention to these contradictory predictions of the effects of clonality on the evolution of self-incompatibility, and suggest that the outcome of this paradox depend on both the extent to which clonal propagation compensates for limited seed production, and on the extent to which clonality reduces pollen transfer between genotypes

Neonicotinoid pesticide limits improvement in buzz pollination by bumblebees

Neonicotinoid pesticides have been linked to global declines of beneficial insects such as bumblebees. Exposure to trace levels of these chemicals causes sub-lethal effects, such as reduced learning and foraging efficiency. Complex behaviours may be particularly vulnerable to the neurotoxic effects of neonicotinoids. Such behaviours may include buzz pollination (sonication), in which pollinators, usually bees, use innate and learned behaviours to generate high-frequency vibrations to release pollen from flowers with specialised anther morphologies. This study assesses the effect of field-realistic, chronic exposure to the widely-used neonicotinoid thiamethoxam on the development of sonication buzz characteristics over time, as well as the collection of pollen from buzz-pollinated flowers. We found that the pollen collection of exposed bees improved less with increasing experience than that of unexposed bees, with exposed bees collecting between 47% and 56% less pollen by the end of 10 trials. We also found evidence of two distinct strategies for maximising pollen collection: (1) extensions to the duration of individual buzzes and (2) extensions of the overall time spent buzzing. We find new complexities in buzz pollination, and conclude that the impacts of field-realistic exposure to a neonicotinoid pesticide may seriously compromise this important ecosystem service

Simulated seed predation reveals a variety of germination responses of neotropical rain forest species

Seed predation, an omnipresent phenomenon in tropical rain forests, is an important determinant of plant recruitment and forest regeneration. Although seed predation destroys large amounts of the seed crop of numerous tropical species, in many cases individual seed damage is only partial. The extent to which partial seed predation affects the recruitment of new individuals in the population depends on the type and magnitude of alteration of the germination behavior of the damaged seeds. We analyzed the germination dynamics of 11 tropical woody species subject to increasing levels of simulated seed predation (0–10% seed mass removal). Germination response to seed damage varied considerably among species but could be grouped into four distinct types: (1) complete inability to germinate under damage ≥1%, (2) no effect on germination dynamics, (3) reduced germination with increasing damage, and (4) reduced final germination but faster germination with increasing damage. We conclude that partial seed predation is often nonlethal and argue that different responses to predation may represent different proximal mechanisms for coping with partial damage, with potential to shape, in the long run, morphological and physiological adaptations in tropical, large-seeded species

Strongly asymmetric hybridization barriers shape the origin of a new polyploid species and its hybrid ancestor

PREMISE OF THE STUDY: Hybridization between diploids and tetraploids can lead to new allopolyploid species, often via a triploid intermediate. Viable triploids are often produced asymmetrically, with greater success observed for maternal-excess crosses where the mother has a higher ploidy than the father. Here we investigated the evolutionary origins of Mimulus peregrinus, an allohexaploid recently derived from the triploid M. xrobertsii, to determine whether reproductive asymmetry has shaped the formation of this new species. METHODS: We used reciprocal crosses between the diploid (M. guttatus) and tetraploid (M. luteus) progenitors to determine the viability of triploid M. xrobertsii hybrids resulting from paternal-vs. maternal-excess crosses. To investigate whether experimental results predict patterns seen in the field, we performed parentage analyses comparing natural populations of M. peregrinus to its diploid, tetraploid, and triploid progenitors. Organellar sequences obtained from pre-existing genomic data, supplemented with additional genotyping was used to establish the maternal ancestry of multiple M. peregrinus and M. xrobertsii populations. KEY RESULTS: We found strong evidence for asymmetric origins of M. peregrinus, but opposite to the common pattern, with paternal-excess crosses significantly more successful than maternal-excess crosses. These results successfully predicted hybrid formation in nature: 111 of 114 M. xrobertsii individuals, and 27 of 27 M. peregrinus, had an M. guttatus maternal haplotype. CONCLUSION: This study, which includes the first Mimulus chloroplast genome assembly, demonstrates the utility of parentage analysis through genome skimming. We highlight the benefits of complementing genomic analyses with experimental approaches to understand asymmetry in allopolyploid speciation

Eukaryote hybrid genomes.

Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adaptation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve

Genetic variation and clonal diversity in introduced populations of Mimulus guttatus assessed by genotyping at 62 single nucleotide polymorphism loci

Background: Single nucleotide polymorphisms (SNPs) are increasingly being used to study non-native populations. SNPs are relatively information poor on a per locus basis, but allow genotyping more loci than others markers (e.g., microsatellites) and have the advantage of consistent allele calls between studies.Aims: We investigated the utility of a newly developed set of SNP markers, suitable for high throughput genotyping to characterise genotypic variation and population structure in non-native populations of the facultative clonal herb Mimulus guttatus in the United Kingdom (UK).Methods: We analysed 62 SNP markers and using a high throughput platform genotyped 383 individuals from 10 populations from the native range in North America and 14 populations in the UK.Results: We found wide variation in genotypic diversity within UK populations, indicating reproductive strategies that vary from mostly clonal to mostly sexual. All but one UK population were, on average, more closely related to each other than to North American populations, and the exceptional UK population showed strong affinity to native Alaskan plants.Conclusions: A small number of SNPs can detect patterns of clonality and broad-scale relationships between native and introduced populations. However, elucidating population structure at a finer scale will require genotyping individuals at greater depth

Variation in natural frequency of stamens with different morphologies and its relationship to bee vibrations

During buzz pollination, bees use vibrations to remove pollen from flowers. Vibrations at the natural frequency of pollencarrying stamens are amplified through resonance, resulting in higher amplitude vibrations. Because pollen release depends on vibration amplitude, bees could increase pollen removal by vibrating at the natural frequency of stamens. However, few studies have characterized the natural frequencies of stamens and compared them to the frequencies of buzzpollinating bees. We use laser Doppler vibrometry to characterize natural frequencies of stamens of six morphologically diverse, buzz-pollinated, heterantherous Solanum taxa and compare the frequency of bumblebee buzzes produced on two Solanum spp. with different natural frequencies. We found that stamen morphology and plant identity explain variation in their natural frequency. The natural frequencies of the stamens in the studied Solanum taxa fell between 45 and 295 Hz; in five out of six taxa the frequencies were < 190 Hz, which only partly overlaps floral vibrations of buzzpollinating bees. We show that captive bumblebees produce vibrations at a frequency of 345 Hz and do not change their floral vibrations to match the natural frequency of the visited flowers. Our results suggest that pollen release induced by vibrating stamens at their natural frequencies might only play a role in a subset of buzz pollination interactions

The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications

The duplication of an entire genome is no small affair. Whole genome duplication (WGD) is a dramatic mutation with long-lasting effects, yet it occurs repeatedly in all eukaryotic kingdoms. Plants are particularly rich in documented WGDs, with recent and ancient polyploidization events in all major extant lineages. However, challenges immediately following WGD, such as the maintenance of stable chromosome segregation or detrimental ecological interactions with diploid progenitors, commonly do not permit establishment of nascent polyploids. Despite these immediate issues some lineages nevertheless persist and thrive. In fact, ecological modeling commonly supports patterns of adaptive niche differentiation in polyploids, with young polyploids often invading new niches and leaving their diploid progenitors behind. In line with these observations of polyploid evolutionary success, recent work documents instant physiological consequences of WGD associated with increased dehydration stress tolerance in first-generation autotetraploids. Furthermore, population genetic theory predicts both short- and long-term benefits of polyploidy and new empirical data suggests that established polyploids may act as “sponges” accumulating adaptive allelic diversity. In addition to their increased genetic variability, introgression with other tetraploid lineages, diploid progenitors, or even other species, further increases the available pool of genetic variants to polyploids. Despite this, the evolutionary advantages of polyploidy are still questioned, and the debate over the idea of polyploidy as an evolutionary dead-end carries on. Here we broadly synthesize the newest empirical data moving this debate forward. Altogether, evidence suggests that if early barriers are overcome, WGD can offer instantaneous fitness advantages opening the way to a transformed fitness landscape by sampling a higher diversity of alleles, including some already preadapted to their local environment. This occurs in the context of intragenomic, population genomic, and physiological modifications that can, on occasion, offer an evolutionary edge. Yet in the long run, early advantages can turn into long-term hindrances, and without ecological drivers such as novel ecological niche availability or agricultural propagation, a restabilization of the genome via diploidization will begin the cycle anew

Correlations among Fertility Components Can Maintain Mixed Mating in Plants

Classical models studying the evolution of self-fertilization in plants conclude that only complete selfing and complete outcrossing are evolutionarily stable. In contrast with this prediction, 42% of seed-plant species are reported to have rates of self-fertilization between 0.2 and 0.8. We propose that many previous models fail to predict intermediate selfing rates because they do not allow for functional relationships among three components of reproductive fitness: self-fertilized ovules, outcrossed ovules, and ovules sired by successful pollen export. Because the optimal design for fertility components may differ, conflicts among the alternative pathways to fitness are possible, and the greatest fertility may be achieved with some self-fertilization. Here we develop and analyze a model to predict optimal selfing rates that includes a range of possible relationships among the three components of reproductive fitness, as well as the effects of evolving inbreeding depression caused by deleterious mutations and of selection on total seed number. We demonstrate that intermediate selfing is optimal for a wide variety of relationships among fitness components and that inbreeding depression is not a good predictor of selfing-rate evolution. Functional relationships subsume the myriad effects of individual plant traits and thus offer a more general and simpler perspective on mating system evolution

On the evolutionary costs of self-incompatibility: Incomplete reproductive compensation due to pollen limitation

Pollen limitation affects plants with diverse reproductive systems and ecologies. In self-incompatible (SI) species, pollen limitation may preclude full reproductive compensation for prezygotic rejection of pollen. We present a model designed to explore the effects of incomplete reproductive compensation on evolutionary changes at a modifier locus that regulates the level of SI expression. Our results indicate that incomplete reproductive compensation greatly increases the evolutionary costs of SI, particularly in populations with low S-allele diversity. The evolutionary fate of modifiers of SI expression depends on the rate at which they are transmitted to future generations as well as the effects of SI on offspring number and quality. Partial SI expression can represent a stable condition rather than an evolutionarily transient state between full expression and full suppression. This unanticipated result provides the first theoretical support for the evolutionary stability of such mixed mating systems, the existence of which has recently been documented