The role of biotic interactions in shaping plant flowering phenology has long been controversial; plastic responses to the abiotic environment, limited precision of biological clocks and inconsistency of selection pressures have generally been emphasized to explain phenological variation. However, part of this variation is heritable and selection analyses show that biotic interactions can modulate selection on flowering phenology. Our review of the literature indicates that pollinators tend to favour peak or earlier flowering, whereas pre-dispersal seed predators tend to favour off-peak or later flowering. However, effects strongly vary among study systems. To understand such variation, future studies should address the impact of mutualist and antagonist dispersal ability, ecological specialization, and habitat and plant population characteristics. Here, we outline future directions to study how such interactions shape flowering phenology. IntroductionFor plant reproduction, timing is everything. An individual plant that flowers too early, before it has had time to accumulate sufficient material resources, will have a limited capacity for seed production. One that delays flowering might gain higher capacity, but might also run out of time to use it before the end of the season. Flowering phenology is affected by many environmental factors, among which temperature and photoperiod, which are reliable signals of seasons, are probably the best studied. Accurate detection of such environmental cues and the resulting plastic response of plants enable flowering to occur when climatic conditions are most suitable for reproduction. Thus, resources and conditions impose bottom-up selective forces on phenology.By contrast, top-down forces act on reproductive timing, particularly those imposed by mutualists (pollinators and seed dispersers) and antagonists (floral pathogens and predispersal seed predators). Here, we review recent progress in understanding some of the top-down selective forces that act on reproductive timing. We highlight what is known,
Summary• DNA methylation can cause heritable phenotypic modifications in the absence of changes in DNA sequence. Environmental stresses can trigger methylation changes and this may have evolutionary consequences, even in the absence of sequence variation. However, it remains largely unknown to what extent environmentally induced methylation changes are transmitted to offspring, and whether observed methylation variation is truly independent or a downstream consequence of genetic variation between individuals.• Genetically identical apomictic dandelion (Taraxacum officinale) plants were exposed to different ecological stresses, and apomictic offspring were raised in a common unstressed environment. We used methylation-sensitive amplified fragment length polymorphism markers to screen genome-wide methylation alterations triggered by stress treatments and to assess the heritability of induced changes.• Various stresses, most notably chemical induction of herbivore and pathogen defenses, triggered considerable methylation variation throughout the genome. Many modifications were faithfully transmitted to offspring. Stresses caused some epigenetic divergence between treatment and controls, but also increased epigenetic variation among plants within treatments.• These results show the following. First, stress-induced methylation changes are common and are mostly heritable. Second, sequence-independent, autonomous methylation variation is readily generated. This highlights the potential of epigenetic inheritance to play an independent role in evolutionary processes, which is superimposed on the system of genetic inheritance.
Many species are currently moving to higher latitudes and altitudes. However, little is known about the factors that influence the future performance of range-expanding species in their new habitats. Here we show that range-expanding plant species from a riverine area were better defended against shoot and root enemies than were related native plant species growing in the same area. We grew fifteen plant species with and without non-coevolved polyphagous locusts and cosmopolitan, polyphagous aphids. Contrary to our expectations, the locusts performed more poorly on the range-expanding plant species than on the congeneric native plant species, whereas the aphids showed no difference. The shoot herbivores reduced the biomass of the native plants more than they did that of the congeneric range expanders. Also, the range-expanding plants developed fewer pathogenic effects in their root-zone soil than did the related native species. Current predictions forecast biodiversity loss due to limitations in the ability of species to adjust to climate warming conditions in their range. Our results strongly suggest that the plants that shift ranges towards higher latitudes and altitudes may include potential invaders, as the successful range expanders may experience less control by above-ground or below-ground enemies than the natives.
When previously isolated populations meet and mix, the resulting admixed population can benefit from several genetic advantages, including increased genetic variation, the creation of novel genotypes and the masking of deleterious mutations. These admixture benefits are thought to play an important role in biological invasions. In contrast, populations in their native range often remain differentiated and frequently suffer from inbreeding depression owing to isolation. While the advantages of admixture are evident for introduced populations that experienced recent bottlenecks or that face novel selection pressures, it is less obvious why native range populations do not similarly benefit from admixture. Here we argue that a temporary loss of local adaptation in recent invaders fundamentally alters the fitness consequences of admixture. In native populations, selection against dilution of the locally adapted gene pool inhibits unconstrained admixture and reinforces population isolation, with some level of inbreeding depression as an expected consequence. We show that admixture is selected against despite significant inbreeding depression because the benefits of local adaptation are greater than the cost of inbreeding. In contrast, introduced populations that have not yet established a pattern of local adaptation can freely reap the benefits of admixture. There can be strong selection for admixture because it instantly lifts the inbreeding depression that had built up in isolated parental populations. Recent work in Silene suggests that reduced inbreeding depression associated with post-introduction admixture may contribute to enhanced fitness of invasive populations. We hypothesize that in locally adapted populations, the benefits of local adaptation are balanced against an inbreeding cost that could develop in part owing to the isolating effect of local adaptation itself. The inbreeding cost can be revealed in admixing populations during recent invasions.
Introduced exotic species encounter a wide range of non-coevolved enemies and competitors in their new range. Evolutionary novelty is a key aspect of these interactions, but who benefits from novelty: the exotic species or their new antagonists? Paradoxically, the novelty argument has been used to explain both the release from and the suppression by natural enemies. We argue that this paradox can be solved by considering underlying interaction mechanisms. Using plant defenses as a model, we argue that mismatches between plant and enemy interaction traits can enhance plant invasiveness in the case of toxin-based defenses, whereas invasiveness is counteracted by mismatches in recognition-based defenses and selective foraging of generalist herbivores on plants with rare toxins. We propose that a mechanistic understanding of ecological mismatches can help to explain and predict when evolutionary novelty will enhance or suppress exotic plant invasiveness. This knowledge may also enhance our understanding of plant abundance following range expansion, or during species replacements along successional stages.
One of the influential hypotheses invoked to explain why species become invasive following introduction is that release from natural enemies favours a shift in investment from defence to traits enhancing growth and reproduction. Silene latifolia was introduced from Europe (EU) to North America (NA) c. 200 years ago where it experiences lower damage by natural enemies. A common garden experiment in EU using seeds from 20 EU and 20 NA populations revealed (1) genetically-based differences in life history between plants from EU and NA; plants from NA have evolved a weedy phenotype that flowers earlier, and has a two-to threefold higher reproductive potential; (2) higher susceptibility of NA plants to fungal infection, fruit predation, and aphid infestation. These results suggest that the invasive NA phenotype has evolved at the expense of defensive abilities. Despite this increased susceptibility to enemies, NA populations still outperformed EU populations in this common garden.
The genus Silene, studied by Darwin, Mendel and other early scientists, is re-emerging as a system for studying interrelated questions in ecology, evolution and developmental biology. These questions include sex chromosome evolution, epigenetic control of sex expression, genomic conflict and speciation. Its well-studied interactions with the pathogen Microbotryum has made Silene a model for the evolution and dynamics of disease in natural systems, and its interactions with herbivores have increased our understanding of multi-trophic ecological processes and the evolution of invasiveness. Molecular tools are now providing new approaches to many of these classical yet unresolved problems, and new progress is being made through combining phylogenetic, genomic and molecular evolutionary studies with ecological and phenotypic data. The model role of a non-model organismThe genus Silene (Caryophyllaceae), with a tradition of genetical and ecological studies dating back to Mendel and Darwin, has remarkably many interesting features. First, the species in the genus vary widely in their breeding systems and ecology. Second, several members of this mainly holarctic genus can be easily bred, and have short life cycles, and are thus convenient for experimental and field studies. Genomic resources are now becoming increasingly available in Silene, making genetic, quantitative genetic and molecular studies possible. A strength of Silene as a model system, compared with many classical model organisms, is that researchers can rely on a large number of ecological studies encompassing biotic interactions with sexually transmitted fungi, pollinators and herbivores. It is the wealth of ecological and other earlier knowledge that makes the genus Silene important for studying many biological questions, including the suppression of recombination during sex chromosome evolution, sexually antagonistic selection in an organism that is not an animal, epigenetic processes in flower development, speciation and reproductive isolation, multi-trophic interactions, disease ecology and biological invasions.Thanks to the classical genetic and ecological work on Silene, new progress can now be made in studying some of these important unresolved questions in biology with the aid of modern molecular tools. That new model systems with accessible and well-studied ecology open fruitful avenues for investigation is illustrated also by Mimulus (Wu et al., 2008) and the ongoing efforts to develop genomic resources in an increasing number of different systems. In the following, we outline the unique features of the Silene system, and describe active research areas and future directions, highlighting new advances and work in progress. Evolution of sexual systemsPlants show remarkable diversity in their sexual and mating systems, ranging from hermaphroditism to dioecy, from self-incompatible hermaphroditism to hermaphroditism in which individuals possess a capacity to self-fertilize, but which often show complex mechanisms to promote outcrossing (Darwin, 18...
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