Wind pollination may commonly evolve to provide reproductive assurance when pollinators are scarce. Evidence is presented that pollen limitation in wind-pollinated plants may not be as common as it is in animal-pollinated species. The studies of pollen capture in wind-pollinated herbs demonstrate that pollen transfer efficiency is not substantially lower than in animal-pollinated plants as is often assumed. These findings challenge the explanation that the evolution of few ovules in wind-pollinated flowers is associated with low pollen loads. Floral and inflorescence architecture is crucial to pollination and mating because of the aerodynamics of wind pollination. Evidence is provided for the importance of plant height, floral position, and stamen and stigma characteristics in promoting effective pollen dispersal and capture. Finally, it is proposed that geitonogamous selfing may alleviate pollen limitation in many wind-pollinated plants with unisexual flowers.
Organisms exhibit an incredible diversity of life history strategies as adaptive responses to environmental variation. The establishment of novel life history strategies involves multilocus polymorphisms, which will be challenging to establish in the face of gene flow and recombination. Theory predicts that adaptive allelic combinations may be maintained and spread if they occur in genomic regions of reduced recombination, such as chromosomal inversion polymorphisms, yet empirical support for this prediction is lacking. Here, we use genomic data to investigate the evolution of divergent adaptive ecotypes of the yellow monkey flower Mimulus guttatus. We show that a large chromosomal inversion polymorphism is the major region of divergence between geographically widespread annual and perennial ecotypes. In contrast, ∼40,000 single nucleotide polymorphisms in collinear regions of the genome show no signal of life history, revealing genomic patterns of diversity have been shaped by localized homogenizing gene flow and large‐scale Pleistocene range expansion. Our results provide evidence for an inversion capturing and protecting loci involved in local adaptation, while also explaining how adaptive divergence can occur with gene flow.
Flowering plants exhibit two principal life-history strategies: annuality (living and reproducing in one year) and perenniality (living more than one year). The advantages of either strategy depend on the relative benefits of immediate reproduction balanced against survivorship and future reproduction. This trade-off means that life-history strategies are associated with particular environments, with annuals being found more often in unpredictable habitats. Annuality and perenniality are the outcome of developmental genetic programs responding to their environment, with perennials being distinguished by their delayed competence to flower and reversion to growth after flowering. Evolutionary transitions between these strategies are frequent and have consequences for mating systems and genome evolution, with perennials being more likely to outcross with higher inbreeding depression and lower rates of molecular evolution. Integrating expectations from life-history theory with knowledge of the developmental genetics of flowering and seasonality is required to understand the mechanisms involved in the evolution of annual and perennial life histories. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 51 is November 2, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Wind pollination is predominantly a derived condition in angiosperms and is thought to evolve in response to ecological conditions that render animal pollination less advantageous. However, the specific ecological and evolutionary mechanisms responsible for transitions from animal to wind pollination are poorly understood in comparison with other major reproductive transitions in angiosperms, including the evolution of selfing from outcrossing and dioecy from hermaphroditism. To investigate correlations between wind pollination and a range of characters including habitat type, sexual system, floral display size, floral showiness, and ovule number, we used a large-scale molecular phylogeny of the angiosperms and maximum likelihood methods to infer historical patterns of evolution. This approach enabled us to detect correlated evolution and the order of trait acquisition between pollination mode and each of nine characters. Log likelihood ratio tests supported a model of correlated evolution for wind pollination and habitat type, floral sexuality, sexual system, flower size, flower showiness, presence versus absence of nectar, and ovule number. In contrast, wind pollination and geographical distribution and number of flowers per inflorescence evolve independently. We found that in wind-pollinated taxa, nectar is lost more often and ovule number is reduced to one. We also found that wind pollination evolves more frequently in lineages already possessing unisexual flowers and/or unisexual plants. An understanding of the ecological and life-history context in which wind pollination originates is fundamental to further investigation of the microevolutionary forces causing transitions from animal to wind pollination.
The maintenance of high outcrossing rates in colonizing populations of A. artemisiifolia is likely to be facilitated by the prodigious production of wind-borne pollen, high seed production and extended seed dormancy.
SummarySpecies with extensive ranges experience highly variable environments with respect to temperature, light and soil moisture. Synchronizing the transition from vegetative to floral growth is important to employ favorable conditions for reproduction. Optimal timing of this transition might be different for semelparous annual plants and iteroparous perennial plants.We studied variation in the critical photoperiod necessary for floral induction and the requirement for a period of cold-chilling (vernalization) in 46 populations of annuals and perennials in the Mimulus guttatus species complex. We then examined critical photoperiod and vernalization QTLs in growth chambers using F 2 progeny from annual and perennial parents that differed in their requirements for flowering.We identify extensive variation in critical photoperiod, with most annual populations requiring substantially shorter day lengths to initiate flowering than perennial populations. We discover a novel type of vernalization requirement in perennial populations that is contingent on plants experiencing short days first. QTL analyses identify two large-effect QTLs which influence critical photoperiod. In two separate vernalization experiments we discover each set of crosses contain different large-effect QTLs for vernalization.Mimulus guttatus harbors extensive variation in critical photoperiod and vernalization that may be a consequence of local adaptation.
Differential natural selection acting on populations in contrasting environments often results in adaptive divergence in multivariate phenotypes. Multivariate trait divergence across populations could be caused by selection on pleiotropic alleles or through many independent loci with trait-specific effects. Here, we assess patterns of association between a suite of traits contributing to life history divergence in the common monkey flower, Mimulus guttatus, and examine the genetic architecture underlying these correlations. A common garden survey of 74 populations representing annual and perennial strategies from across the native range revealed strong correlations between vegetative and reproductive traits. To determine whether these multitrait patterns arise from pleiotropic or independent loci, we mapped QTLs using an approach combining high-throughput sequencing with bulk segregant analysis on a cross between populations with divergent life histories. We find extensive pleiotropy for QTLs related to flowering time and stolon production, a key feature of the perennial strategy. Candidate genes related to axillary meristem development colocalize with the QTLs in a manner consistent with either pleiotropic or independent QTL effects. Further, these results are analogous to previous work showing pleiotropy-mediated genetic correlations within a single population of M. guttatus experiencing heterogeneous selection. Our findings of strong multivariate trait associations and pleiotropic QTLs suggest that patterns of genetic variation may determine the trajectory of adaptive divergence.
The proximity of mates can influence mating opportunities and the quantity and quality of offspring, especially in dioecious plant species. Progeny sex ratios modulated by environmental conditions is one of the most radical ways in which offspring quality may be influenced, yet it has rarely been reported in plants. A mechanism proposed to influence progeny sex ratios in dioecious plants involves competition between female-and male-determining microgametophytes (certation) as a result of variation in pollination intensity. However, the role of selective fertilization in dioecious plants is controversial and has not been demonstrated under field conditions. Here we investigate whether natural variation in the spatial arrangement of females and males influences pollination intensity and progeny sex ratios in the wind-pollinated herb Rumex nivalis. Based on previous experimental manipulation of pollination intensity in this species, we predicted that maternal parents in close proximity to males would produce more strongly female-biased progeny sex ratios. We tested this prediction in six alpine populations in Switzerland by measuring the distance between focal females and neighboring males and assessing pollen loads and seed sex ratios of maternal parents. In four of the six populations, females positioned in close proximity to males captured more pollen and exhibited more female-biased sex ratios. Our results demonstrate that demographic aspects of the maternal mating environment can influence progeny sex ratios. The most probable explanation for biased primary sex ratios in Rumex is selective fertilization resulting from pollen tube competition.female-biased sex ratios ͉ pollination intensity ͉ selective fertilization T he spatial context in which reproduction occurs is of critical importance for plants because of their sessile habit. Most plants mate and disperse offspring locally, so that mating success is context-dependent and influenced by plant density and the phenotypic composition of neighborhoods (1-3). Dioecious species are especially sensitive to spatial structure and composition because of the restricted number of mating groups within populations. Female reproductive success can be influenced by male flowering density, depending on the extent of pollen dispersal (4-6). Patch density and the local sex ratio may also affect parental fitness through their influence on pollination intensity. The amount of pollen captured by stigmas could potentially affect both the quality of offspring and progeny sex ratios through gametophytic competition (certation) and selective fertilization (7,8). However, the relative roles of genetic and environmental factors in governing primary sex ratios in dioecious populations are still poorly understood, and evidence for environmentally induced variation in primary sex ratios is limited despite considerable heterogeneity in seed sex ratios (9).Sex determination induced by the environment is one of the most direct ways in which progeny sex ratios can vary. Environmental sex de...
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