Modeling the two‐locus architecture of divergent pollinator adaptation: how variation in SAD paralogs affects fitness and evolutionary divergence in sexually deceptive orchids

Divergent selection by pollinators can bring about strong reproductive isolation via changes at few genes of large effect. This has recently been demonstrated in sexually deceptive orchids, where studies (1) quantified the strength of reproductive isolation in the field; (2) identified genes that appear to be causal for reproductive isolation; and (3) demonstrated selection by analysis of natural variation in gene sequence and expression. In a group of closely related Ophrys orchids, specific floral scent components, namely n‐alkenes, are the key floral traits that control specific pollinator attraction by chemical mimicry of insect sex pheromones. The genetic basis of species‐specific differences in alkene production mainly lies in two biosynthetic genes encoding stearoyl–acyl carrier protein desaturases (SAD) that are associated with floral scent variation and reproductive isolation between closely related species, and evolve under pollinator‐mediated selection. However, the implications of this genetic architecture of key floral traits on the evolutionary processes of pollinator adaptation and speciation in this plant group remain unclear. Here, we expand on these recent findings to model scenarios of adaptive evolutionary change at SAD2 and SAD5, their effects on plant fitness (i.e., offspring number), and the dynamics of speciation. Our model suggests that the two‐locus architecture of reproductive isolation allows for rapid sympatric speciation by pollinator shift; however, the likelihood of such pollinator‐mediated speciation is asymmetric between the two orchid species O. sphegodes and O. exaltata due to different fitness effects of their predominant SAD2 and SAD5 alleles. Our study not only provides insight into pollinator adaptation and speciation mechanisms of sexually deceptive orchids but also demonstrates the power of applying a modeling approach to the study of pollinator‐driven ecological speciation.     

POLLINATOR‐MEDIATED REPRODUCTIVE ISOLATION AMONG DIOECIOUS FIG SPECIES (FICUS,MORACEAE)

The extent of isolation among closely related sympatric plant species engaged in obligate pollination mutualisms depends on the fitness consequences of interspecies floral visitation. In figs (Ficus), interspecific gene flow may occur when pollinating wasps (Agaonidae) visit species other than their natal fig species. We studied reproductive isolation in a clade of six sympatric dioecious fig species in New Guinea. Microsatellite genotyping and Bayesian clustering analysis of the fig community indicated strong reproductive barriers among sympatric species. A total of 1–2% of fig populations consisted of hybrid individuals. A new experimental method of manipulating fig wasps investigated the reproductive consequences of conspecific and heterospecific pollinator visitation for both mutualists. Fig wasps introduced to Ficus hispidioides pollinated and oviposited in receptive figs. Seed development and seedling growth were largely comparable between conspecific and heterospecific crosses. Heterospecific pollinator fitness, however, was significantly less than that of conspecific pollinators. Heterospecific pollinators induced gall formation but offspring did not develop to maturity in the new host. Selection on pollinators maintaining host specificity appears to be an important mechanism of contemporary reproductive isolation among these taxa that could potentially influence their diversification.     

What makes a specialized endophyte special?

Fungal plant symbionts can be highly specialized on a limited range of host genotypes and species. Understanding the genetic basis of this specialization, the mechanisms governing its establishment and the relationship between specialization and speciation is a major challenge for evolutionary biologists (Timms & Read, 1999 ). A deeper knowledge of evolutionary plant–microbe interactions could be exploited to improve agricultural management, by bringing fungal biodiversity and fungal biomass under greater and more durable human control. Previous studies on pathogens have shown that effectors, that is, small secreted proteins that modulate plant physiology to favour host colonization, play a key role in infection of novel hosts (e.g., Inoue et al., 2017 ) or in host specialization (e.g., Liao et al. ( 2016 )). Like pathogens, endophytes also manipulate the physiology of their hosts and colonize novel hosts to which they specialize (Hardoim et al., 2015 ). These biological characteristics of endophytes raise the question of similarities in the protein arsenal contributing to the specialization of pathogens and endophytes. In this issue of Molecular Ecology, Schirrmann et al. ( 2018 ) used a combination of divergence genome scans and tests for positive selection to investigate the genetic basis of specialization of two subspecies of the symbiont Epichloë typhina occurring on two different grass hosts. Their analyses suggest a key role of effectors as determinants of host specialization. This study paves the way towards the comparative analysis of the genomics of speciation among plant symbionts.     

The role of individual variation in flowering and pollination in the reproductive success of a crepuscular buzz-pollinated plant

Background and AimsPlant individuals within a population differ in their phenology and interactions with pollinators. However, it is still unknown how individual differences affect the reproductive success of plants that have functionally specialized pollination systems. Here, we evaluated whether plant individual specialization in phenology (temporal specialization) and in pollination (pollinator specialization) affect the reproductive success of the crepuscular-bee-pollinated plant Trembleya laniflora (Melastomataceae).MethodsWe quantified flowering activity (amplitude, duration and overlap), plant–pollinator interactions (number of flowers visited by pollinators) and reproductive success (fruit set) of T. laniflora individuals from three distinct locations in rupestrian grasslands of southeastern Brazil. We estimated the degree of individual temporal specialization in flowering phenology and of individual specialization in plant–pollinator interactions, and tested their relationship with plant reproductive success.Key Results Trembleya laniflora presented overlapping flowering, a temporal generalization and specialized pollinator interactions. Flowering overlap among individuals and populations was higher than expected by chance but did not affect the individual interactions with pollinators and nor their reproductive success. In contrast, higher individual generalization in the interactions with pollinators was related to higher individual reproductive success.ConclusionsOur findings suggest that individual generalization in plant–pollinator interaction reduces the potential costs of specialization at the species level, ensuring reproductive success. Altogether, our results highlight the complexity of specialization/generalization of plant–pollinator interactions at distinct levels of organization, from individuals to populations, to species.     

Host specificity and reproductive success of yucca moths (Tegeticula spp. Lepidoptera: Prodoxidae) mirror patterns of gene flow between host plant varieties of the Joshua tree (Yucca brevifolia: Agavaceae)

Coevolution between flowering plants and their pollinators is thought to have generated much of the diversity of life on Earth, but the population processes that may have produced these macroevolutionary patterns remain unclear. Mathematical models of coevolution in obligate pollination mutualisms suggest that phenotype matching between plants and their pollinators can generate reproductive isolation. Here, we test this hypothesis using a natural experiment that examines the role of natural selection on phenotype matching between yuccas and yucca moths (Tegeticula spp.) in mediating reproductive isolation between two varieties of Joshua tree (Yucca brevifolia var. brevifolia and Y. brevifolia var. jaegeriana). Using passive monitoring techniques, DNA barcoding, microsatellite DNA genotyping, and sibship reconstruction, we track host specificity and the fitness consequences of host choice in a zone of sympatry. We show that the two moth species differ in their degree of host specificity and that oviposition on a foreign host plant results in the production of fewer offspring. This difference in host specificity between the two moth species mirrors patterns of chloroplast introgression from west to east between host varieties, suggesting that natural selection acting on pollinator phenotypes mediates gene flow and reproductive isolation between Joshua‐tree varieties.     

Asymmetric hybridization and gene flow between Joshua trees (Agavaceae: Yucca) reflect differences in pollinator host specificity

The angiosperms are by far the largest group of terrestrial plants. Their spectacular diversity is often attributed to specialized pollination. Obligate pollination mutualisms where both a plant and its pollinator are dependent upon one another for reproduction are thought to be prone to rapid diversification through co‐evolution and pollinator isolation. However, few studies have evaluated the degree to which pollinators actually mediate reproductive isolation in these systems. Here, we examine evidence for hybridization and gene flow between two subspecies of Joshua tree (Yucca brevifolia brevifolia and Yucca brevifolia jaegeriana) pollinated by two sister species of yucca moth. Previous work indicated that the pollinators differ in host specificity, and DNA sequence data suggested asymmetric introgression between the tree subspecies. Through intensive sampling in a zone of sympatry, a large number of morphologically intermediate trees were identified. These included trees with floral characters typical of Y. b. jaegeriana, but vegetative features typical of Y. b. brevifolia. The opposite combination—Y. b. brevifolia flowers with Y. b. jaegeriana vegetative morphology—never occurred. Microsatellite genotyping revealed a high frequency of genetically admixed, hybrid trees. Coalescent‐based estimates of migration indicated significant gene flow between the subspecies and that the direction of gene flow matches differences in pollinator host fidelity. The data suggest that pollinator behaviour determines the magnitude and direction of gene flow between the two subspecies, but that specialized pollination alone is not sufficient to maintain species boundaries. Natural selection may be required to maintain phenotypic differences in the face of ongoing gene flow.     

Divergent strategies in pre‐ and postzygotic reproductive isolation between two closely related Dianthus species

Quantifying the relative contribution of multiple isolation barriers to gene flow between recently diverged species is essential for understanding speciation processes. In parapatric populations, local adaptation is thought to be a major contributor to the evolution of reproductive isolation. However, extrinsic postzygotic barriers assessed in reciprocal transplant experiments are often neglected in empirical assessments of multiple isolation barriers. We analyzed multiple isolation barriers between two closely related species of the plant genus Dianthus, a genus characterized by the most rapid species diversification in plants reported so far. Although D. carthusianorum L. and D. sylvestris Wulf. can easily be hybridized in crossing experiments, natural hybrids are rare. We found that in parapatry, pollinator‐mediated prezygotic reproductive isolation barriers are important for both D. carthusianorum (0.761) and D. sylvestris (0.468). In contrast to D. carthusianorum, high hybrid viability in D. sylvestris (–0.491) was counteracted by strong extrinsic postzygotic isolation (0.900). Our study highlights the importance of including reciprocal transplant experiments for documenting extrinsic postzygotic isolation and demonstrates clearly divergent strategies and hence asymmetric pre‐ and postzygotic reproductive isolation between closely related species. It also suggests that pollinator‐mediated and ecological isolation could have interacted in synergistic ways, further stimulating rapid speciation in Dianthus.     

Predicting how pollinator behavior causes reproductive isolation

Pollinator behavior is an important contributor to plants speciation, yet how variation in pollinator behavior causes variation in reproductive isolation (RI) is largely uncharacterized. Here I present a model that predicts how two aspects of pollinator behavior, constancy and preference, contribute to a barrier to reproduction in plants. This model is motivated by two observations: most co‐occurring plants vary in frequency over space and time, and most plants have multiple pollinators that differ in behavior. Thus, my goal was to understand how relative frequencies of plants and pollinators in a community influence ethological RI between co‐occurring plants. I find that RI for a focal plant generally increases with increasing relative plant frequency, but the shape of this relationship is highly dependent on the strength of pollinator behavior (constancy and preference). Additionally, when multiple pollinators express different behavior, I find that pollinators with stronger preference disproportionately influence RI. But, I show that RI caused by constancy is the average RI predicted from constancy of each pollinator weighted by pollinator frequency. I apply this model to examples of pollinator‐mediated RI in Phlox and in Ipomopsis to predict the relationships between plant frequency and ethological RI in natural systems. This model provides new insights into how and why pollinator specialization causes RI, and how RI could change with changing biological communities.     

Genetic structure and hybridization in the species group of Ficus auriculata: can closely related sympatric Ficus species retain their genetic identity while sharing pollinators?

Obligate mutualistic nursery pollination systems between insects and plants have led to substantial codiversification involving at least some parallel cladogenesis, as documented in Yucca, Ficus and Phyllanthaceae. In such systems, pollinators are generally species specific thus limiting hybridization and introgression among interfertile host species. Nevertheless, in the three systems, cases of one insect pollinating several plant species are reported. In most cases, host plants sharing pollinators are allopatric. However, in the case of the species group of Ficus auriculata, forms may co‐occur over large parts of their range. We show here that the species group of F. auriculata is constituted by four well‐defined genetic entities that share pollinators. We detected hybrids in nature mainly when both parental forms were growing nearby. Controlled crosses showed that F1 offspring could be successfully backcrossed. Hence, despite sharing pollinators and despite hybrid viability, the different forms have preserved their genetic and morphological identity. We propose that ecological differentiation among forms coupled with limited overlap of reproductive season has facilitated the maintenance of these interfertile forms. As such, establishment of pollinator host specificity may not be a prerequisite for sympatric diversification in Ficus.     

Reproductive biology of the South American cycad Zamia boliviana,involving brood-site pollination

Brood-site pollination mutualisms represent extreme levels of reciprocal specialization between plants and insects. Several studies have revealed intimate associations between cycads and their insect pollinators across different continents. However, the reproductive biology of South American cycads is still poorly understood, with limited empirical data available. Here, we investigated the plant–pollinator interactions of Zamia boliviana (Cycadales, Zamiaceae), which is distributed on savanna patches in Brazil and Bolivia. Our aim was to examine reproductive biology (strobili development and their visitors) to identify potential pollinators from the perspective of dioecy and expectations of obligatory mutualism. We monitored reproductive cohorts and registered the strobiliʼs visitors. We classified the visitorsʼ activities and described the behavior of the most active and recurring ones in both reproductive structures to ascertain the potential pollinators and their relationship with the Z. boliviana. In situ experiments were used to demonstrate efficacy in seed production. Although other insects visit the strobili, only one Coleoptera (Erotylidae: Pharaxonotha) was present seasonally. Pharaxonotha cerradensis was the single species capable of transporting pollen and developing a life cycle associated with polleniferous strobili, while concomitantly visiting ovuliferous strobili. Experimental tests associated with observational evidence in the cycad indicated brood-site pollination mutualism with the Erotylidae beetle, a potential pollinator of Z. boliviana. Our investigation confirmed a new case of obligatory mutualism between cycads and P. cerradensis in the New World. Future research on Zamia from South America should address pollination systems of this genus to better understand the ecology and evolution of plant–pollinator interactions.     

Evolution of oviposition strategies and speciation in the globeflower flies Chiastocheta spp. (Anthomyiidae)

Trollius europaeus (Ranunculaceae) is involved in an intimate interaction with several species of Chiastocheta flies (Anthomyiidae) that are both seed predators and pollinators. In this paper, we analyse the oviposition strategy of the six Chiastocheta species found to coexist on T. europaeus in 19 populations from the French Alps. We show that the species are not equivalent in their oviposition behaviour: C. rotundiventris usually deposits no more than one egg per flower in first-day flowers whereas C. dentifera aggregates its eggs on fruits and thus does not contribute to pollination at all; the four remaining species deposit eggs sequentially during the flowering period from the 2nd to the 7th day. Hence, the outcomes of the interaction in terms of net seed production for the plant greatly depend on the Chiastocheta species visiting it, ranging from a mutualistic to a purely parasitic interaction. We assessed mitochondrial divergence between Chiastocheta spp. by sequencing a 1320-bp mitochondrial DNA fragment. The low divergence observed between species (0–4.15%) suggests that genus diversification took place recently. Unlike in other plant–insect systems where diversification is usually thought to be driven by cospeciation or host shifts, we propose that Chiastocheta speciation took place within the host plant. Basal separation of a particularly mutualistic species provided favourable conditions for plant specialization on this seed-parasite as a pollinator early in the evolution of the association. The parasitic species ovipositing on fruits derived from a species ovipositing on flowers. Diversification of the intermediate strategies probably occurred in relation with the Pleistocene climatic events, reproductive isolation between species being reinforced by niche partitioning for oviposition and/or sexual selection.     

Pollinator shifts between Ophrys sphegodes populations: might adaptation to different pollinators drive population divergence?

Local adaptation to different pollinators is considered one of the possible initial stages of ecological speciation as reproductive isolation is a by‐product of the divergence in pollination systems. However, pollinator‐mediated divergent selection will not necessarily result in complete reproductive isolation, because incipient speciation is often overcome by gene flow. We investigated the potential of pollinator shift in the sexually deceptive orchids Ophrys sphegodes and Ophrys exaltata and compared the levels of floral isolation vs. genetic distance among populations with contrasting predominant pollinators. We analysed floral hydrocarbons as a proxy for floral divergence between populations. Floral adoption of pollinators and their fidelity was tested using pollinator choice experiments. Interpopulation gene flow and population differentiation levels were estimated using AFLP markers. The Tyrrhenian O. sphegodes population preferentially attracted the pollinator bee Andrena bimaculata, whereas the Adriatic O. sphegodes population exclusively attracted A. nigroaenea. Significant differences in scent component proportions were identified in O. sphegodes populations that attracted different preferred pollinators. High interpopulation gene flow was detected, but populations were genetically structured at species level. The high interpopulation gene flow levels independent of preferred pollinators suggest that local adaptation to different pollinators has not (yet) generated detectable genome‐wide separation. Alternatively, despite extensive gene flow, few genes underlying floral isolation remain differentiated as a consequence of divergent selection. Different pollination ecotypes in O. sphegodes might represent a local selective response imposed by temporal variation in a geographical mosaic of pollinators as a consequence of the frequent disturbance regimes typical of Ophrys habitats.     

Non-additive effects of herbivores and pollinators on Erysimum mediohispanicum (Cruciferae) fitness

In this study, the non-additivity of effects of herbivores and pollinator on fitness of the plant Erysimum mediohispanicum (Cruciferae) has been experimentally tested. The abundance and diversity of the pollinator assemblage of plants excluded from and exposed to mammalian herbivores, and the combined effect of pollinators and herbivores on plant reproduction were determined over a period of 2 years. Pollinator abundance was higher and diversity was lower on plants excluded from herbivores. Furthermore, the experimental exclusions demonstrated that both pollinators and herbivores affected plant fitness, but their effects were not independent. Herbivores only had a detrimental effect on plant fitness when pollinators were present. Similarly, pollinators enhanced fitness only when herbivores were excluded. This outcome demonstrates that the importance of pollinators for plant fitness depends on the occurrence of herbivores, and suggests that herbivores may hamper pollinator-mediated adaptation in plants.     

Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity

Brood pollination mutualisms—interactions in which specialized insects are both the pollinators (as adults) and seed predators (as larvae) of their host plants—have been influential study systems for coevolutionary biology. These mutualisms include those between figs and fig wasps, yuccas and yucca moths, leafflowers and leafflower moths, globeflowers and globeflower flies, Silene plants and Hadena and Perizoma moths, saxifrages and Greya moths, and senita cacti and senita moths. The high reciprocal diversity and species‐specificity of some of these mutualisms have been cited as evidence that coevolution between plants and pollinators drives their mutual diversification. However, the mechanisms by which these mutualisms diversify have received less attention. In this paper, we review key hypotheses about how these mutualisms diversify and what role coevolution between plants and pollinators may play in this process. We find that most species‐rich brood pollination mutualisms show significant phylogenetic congruence at high taxonomic scales, but there is limited evidence for the processes of both cospeciation and duplication, and there are no unambiguous examples known of strict‐sense contemporaneous cospeciation. Allopatric speciation appears important across multiple systems, particularly in the insects. Host‐shifts appear to be common, and widespread host‐shifts by pollinators may displace other pollinator lineages. There is relatively little evidence for a “coevolution through cospeciation” model or that coevolution promotes speciation in these systems. Although we have made great progress in understanding the mechanisms by which brood pollination mutualisms diversify, many opportunities remain to use these intriguing symbioses to understand the role of biotic interactions in generating biological diversity.     

Multiple parapatric pollinators have radiated across a continental fig tree displaying clinal genetic variation

The ways that plant‐feeding insects have diversified are central to our understanding of terrestrial ecosystems. Obligate nursery pollination mutualisms provide highly relevant model systems of how plants and their insect associates have diversified and the over 800 species of fig trees (Ficus) allow comparative studies. Fig trees can have one or more pollinating fig wasp species (Agaonidae) that breed within their figs, but factors influencing their number remain to be established. In some widely distributed fig trees, the plants form populations isolated by large swathes of sea, and the different populations are pollinated by different wasp species. Other Ficus species with continuous distributions may present genetic signatures of isolation by distance, suggesting more limited pollinator dispersal, which may also facilitate pollinator speciation. We tested the hypothesis that Ficus hirta, a species for which preliminary data showed genetic isolation by distance, would support numerous pollinator species across its range. Our results show that across its range F. hirta displays clinal genetic variation and is pollinated by nine parapatric species of Valisia. This is the highest number of pollinators reported to date for any Ficus species, and it is the first demonstration of the occurrence of parapatric pollinator species on a fig host displaying continuous genetic structure. Future comparative studies across Ficus species should be able to establish the plant traits that have driven the evolution of pollinator dispersal behaviour, pollinator speciation and host plant spatial genetic structure.     

Selection to attract pollinators and to confuse antagonists specializes fig–pollinator chemical communications

Chemical communication is critical in establishing angiosperm–pollinator mutualisms. However, our understanding of how chemical communication shapes coevolution remains limited. Here, we integrated information theory to model three coevolutionary scenarios (I‒III), where the pollinator fitness is always optimized by the highest certainty of chemical information provided by plants, but plant fitness is determined by (I) the certainty of chemical information attracting pollinators, (II) the uncertainty of chemical information confusing antagonists, or (III) both aspects. We found that the statistical properties of empirical plant volatiles from 45 pairs of fig–pollinator mutualisms were best explained by the selection from both pollinators and antagonists (scenario III). Under this scenario, plant–pollinator mutualisms evolve to be specialized and as few as two volatile chemicals could supply sufficient information for pollinators’ host identification. Our study provides new insights into plant–pollinator coevolution and will facilitate further studies on the evolution and diversification in specialized plant–pollinator–herbivore systems.     

Seasonal and annual variations in the pollination efficiency of a pollinator community of Dictamnus albus L.

The interplay between insect and plant traits outlines the patterns of pollen transfer and the subsequent plant reproductive fitness. We studied the factors that affect the pollination efficiency of a pollinator community of Dictamnus albus L. by evaluating insect behaviour and morphological characteristics in relation to flowering phenology. In order to extrapolate the pollinator importance of single taxa and of the whole pollinator guild, we calculated an index distinguishing between potential (PPI) and realized (RPI) pollinator importance. Although the pollinator species spectrum appeared rather constant, we found high intra‐ and inter‐annual variability of pollinator frequency and importance within the insect community. Flower visitation rate strictly depended on insect abundance and on the overlap between their flying period and flower blooming. All the pollinators visited flowers from the bottom to the top of the racemes, excluding intra‐plant geitonogamous pollination, and most of them showed high pollen fidelity. Only medium large‐sized bees could contact the upward bending stiles while feeding on nectar, highlighting a specialisation of the plant towards bigger pollinators. Moreover, we found evidence of functional specialisation, since all pollinators were restricted to a single taxonomic group (order: Hymenoptera; superfamily: Apoidea). Both the PPI and RPI indices indicate Habropoda tarsata as the most important pollinator of D. albus. Following hand cross‐pollination experiments we revealed the presence of pollination limitation in 1 of the 3 years of field study. We discuss this result in relation to flowering abundance and to possible mismatches of phenological periods between plants and insects.     

Parallel chemical switches underlying pollinator isolation in Asian Mitella

Floral scents are among the key signals used by pollinators to navigate to specific flowers. Thus, evolutionary changes in scents should have strong impacts on plant diversification, although scent‐mediated plant speciation through pollinator shifts has rarely been demonstrated, despite being likely. To examine whether and how scent‐mediated plant speciation may have occurred, we investigated the Asimitellaria plant lineage using multidisciplinary approaches including pollinator observations, chemical analyses of the floral scents, electroantennographic analyses and behavioural bioassays with the pollinators. We also performed phylogenetically independent contrast analyses of the pollinator/floral scent associations. First, we confirmed that the pairs of the sympatric, cross‐fertile Asimitellaria species in three study sites consistently attract different pollinators, namely long‐tongued and short‐tongued fungus gnats. We also found that a stereoisomeric set of floral volatiles, the lilac aldehydes, could be responsible for the pollinator specificity. This is because the compounds consistently elicited responses in the antennae of the long‐tongued fungus gnats and had contrasting effects on the two pollinators, that is triggering the nectaring behaviour of long‐tongued fungus gnats while repelling short‐tongued fungus gnats in a laboratory experiment. Moreover, we discovered that volatile composition repeatedly switched in Asimitellaria between species adapted to long‐tongued and short‐tongued fungus gnats. Collectively, our results support the idea that recurrent scent‐mediated speciation has taken place in the Asimitellaria–fungus gnat system.     

The pollination niche and its role in the diversification and maintenance of the southern African flora

The flora of southern Africa has exceptional species richness and endemism, making it an ideal system for studying the patterns and processes of evolutionary diversification. Using a wealth of recent case studies, I examine the evidence for pollinator-driven diversification in this flora. Pollination systems, which represent available niches for ecological diversification, are characterized in southern Africa by a high level of ecological and evolutionary specialization on the part of plants, and, in some cases, by pollinators as well. These systems are asymmetric, with entire plant guilds commonly specialized for a particular pollinator species or functional type, resulting in obvious convergent floral evolution among guild members. Identified modes of plant lineage diversification involving adaptation to pollinators in these guilds include (i) shifts between pollination systems, (ii) divergent use of the same pollinator, (iii) coevolution, (iv) trait tracking, and (v) floral mimicry of different model species. Microevolutionary studies confirm that pollinator shifts can be precipitated when a plant species encounters a novel pollinator fauna on its range margin, and macroevolutionary studies confirm frequent pollinator shifts associated with lineage diversification. As Darwin first noted, evolutionary specialization for particular pollinators, when resulting in ecological dependency, may increase the risk of plant extinction. I thus also consider the evidence that disturbance provokes pollination failure in some southern African plants with specialized pollination systems.     

Digest: Plant‐pathogen coevolution extends to shifts in plant breeding systems*

Plants and their pathogens are in a coevolutionary arms race. Some pathogens, such as anther smuts, use their host plants’ pollinators for spore dispersal. In the plant Dianthus pavonius, gynodioecy (having female and hermaphroditic plants) has evolved to reduce flowering duration and therefore limit exposure to anther smut pathogens. Bruns et al. (2019) show that this shift in breeding system has evolved as a disease escape mechanism.