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Despite the economic, ecological, and scientific importance of the genera Salix L. (willows) and Populus L. (poplars, cottonwoods, and aspens) Salicaceae, we know little about the sources of differences in species diversity between the genera and of the phylogenetic conflict that often confounds estimating phylogenetic trees. Salix subgenera and sections, in particular, have been difficult to classify, with one recent attempt termed a “spectacular failure” due to a speculated radiation of the subgenera Vetrix and Chamaetia. Here, we use targeted sequence capture to understand the evolutionary history of this portion of the Salicaceae plant family. Our phylogenetic hypothesis was based on 787 gene regions and identified extensive phylogenetic conflict among genes. Our analysis supported some previously described subgeneric relationships and confirmed the polyphyly of others. Using an fbranch analysis, we identified several cases of hybridization in deep branches of the phylogeny, which likely contributed to discordance among gene trees. In addition, we identified a rapid increase in diversification rate near the origination of the Vetrix–Chamaetia clade in Salix. This region of the tree coincided with several nodes that lacked strong statistical support, indicating a possible increase in incomplete lineage sorting due to rapid diversification. The extraordinary level of both recent and ancient hybridization in both Salix and Populus have played important roles in the diversification and diversity in these two genera.

 

Secondary chemistry often differs between sexes in dioecious plant species, a pattern attributed to its possible role in the evolution and/or maintenance of dioecy. We used GC-MS to measure floral volatiles emitted from, and LC-MS to quantitate non-volatile secondary compounds contained in, female and male Salix purpurea willow catkins from an F2 family. Using the abundance of these chemicals, we then performed quantitative trait locus (QTL) mapping to locate them on the genome, identified biosynthetic candidate genes in the QTL intervals, and examined expression patterns of candidate genes using RNA-seq. Male flowers emitted more total terpenoids than females, but females produced more benzenoids. Male tissue contained greater amounts of phenolic glycosides, but females had more chalcones and flavonoids. A flavonoid pigment and a spermidine derivative were found only in males. Male catkins were almost twice the mass of females. Forty-two QTL were mapped for 25 chemical traits and catkin mass across 16 of the 19 S. purpurea chromosomes. Several candidate genes were identified, including a chalcone isomerase associated with seven compounds. A better understanding of the genetic basis of the sexually dimorphic chemistry of a dioecious species may shed light on how chemically mediated ecological interactions may have helped in the evolution and maintenance of dioecy.

 

All organisms experience fundamental conflicts between divergent metabolic processes. In plants, a pivotal conflict occurs between allocation to growth, which accelerates resource acquisition, and to defense, which protects existing tissue against herbivory. Trade-offs between growth and defense traits are not universally observed, and a central prediction of plant evolutionary ecology is that context-dependence of these trade-offs contributes to the maintenance of intraspecific variation in defense [Züst and Agrawal,Annu. Rev. Plant Biol., 68, 513–534 (2017)]. This prediction has rarely been tested, however, and the evolutionary consequences of growth–defense trade-offs in different environments are poorly understood, especially in long-lived species [Cipolliniet al.,Annual Plant Reviews(Wiley, 2014), pp. 263–307]. Here we show that intraspecific trait trade-offs, even when fixed across divergent environments, interact with competition to drive natural selection of tree genotypes corresponding to their growth–defense phenotypes. Our results show that a functional trait trade-off, when coupled with environmental variation, causes real-time divergence in the genetic architecture of tree populations in an experimental setting. Specifically, competitive selection for faster growth resulted in dominance by fast-growing tree genotypes that were poorly defended against natural enemies. This outcome is a signature example of eco-evolutionary dynamics: Competitive interactions affected microevolutionary trajectories on a timescale relevant to subsequent ecological interactions [Brunneret al.,Funct. Ecol.33, 7–12 (2019)]. Eco-evolutionary drivers of tree growth and defense are thus critical to stand-level trait variation, which structures communities and ecosystems over expansive spatiotemporal scales.

 

ABSTRACT Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems and which degrade the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus , the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria -dominant bacterial community present within fungus gardens. In this study, we investigated the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome P450 enzymes and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we showed that some of these degradation genes are expressed in situ . Most of the bacterial isolates grew unhindered in the presence of PSCs and, using gas chromatography-mass spectrometry (GC-MS), we determined that isolates from the genera Bacillus , Burkholderia , Enterobacter , Klebsiella , and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that subcolonies of fungus gardens reduced α-pinene and linalool over a 36-h period, while L. gongylophorus strains alone reduced only linalool. Overall, our results reveal that the bacterial communities in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system. IMPORTANCE Leaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut, composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their roles in the detoxification of plant secondary compounds. In this study, we assessed if the bacterial communities associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus . Our findings suggest that the fungus garden and its associated microbial community influence the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores. 

A paradigm in the plant defence literature is that defending against herbivores comes at a cost to growth, resulting in a growth–defence trade‐off. However, while there is strong evidence for growth–defence trade‐offs across species, evidence is mixed within species.

Several mechanisms can account for this equivocal support within species, but teasing them apart requires examining growth–defence relationships both within and among populations, an approach seldom employed.

We examined correlations between plant biomass (growth) and terpene production (defence) within and among populations ofMonarda fistulosa, a perennial herb. We sampled populations from Montana and Wisconsin, regions that differ in resource availability characterized by different summer precipitation and associated abiotic conditions that influence plant productivity.

We found negative, neutral and positive growth–defence correlations, depending on the scale examined. Negative correlations occurred across populations originating from divergent regions, positive correlations occurred across populations originating from within the high‐resource region and neutral correlations were found within single populations.

Collectively, these results challenge the general expectation of ubiquitous trade‐offs and support emerging views that resource availability (as it affects productivity) shapes the evolution of defence at different scales.

A freePlain Language Summarycan be found within the Supporting Information of this article.

 

Salix nigra(black willow) is a widespread tree that hosts many species of polylectic hymenopterans and oligolectic bees of the genusAndrena. The early flowering ofS. nigramakes it an important nutritive resource for arthropods emerging from hibernation. However, sinceS. nigrais dioecious, not all insect visits will lead to successful pollination. Using both visual observation and pan‐trapping, we characterized the community of arthropods that visitedS. nigraflowers and assessed differences among male and female trees as well as the chemical and visual drivers that influenced community composition across 3 years. We found that male trees consistently supported higher diversity of insects than female trees and only three insect species, allAndrenaspp., consistently visited both sexes. Additionally,Andrena nigrae, which was the only insect that occurred more on female than male flowers, correlated strongly to volatile cues. This suggests that cross‐pollinators cue into specific aspects of floral scent, but diversity of floral visitors is driven strongly by visual cues of yellow male pollen. Through time, the floral activity of twoAndrenaspecies remained stable, butA. nigraevisited less in 2017 when flowers bloomed earlier than other years. When native bee emergence does not synchronize with bloom, activity appears to be diminished which could threaten species that subsist on a single host. Despite the community diversity ofS. nigraflowers, its productivity depends on a small fraction of species that are not threatened by competition, but rather rapidly changing conditions that lead to host‐insect asynchrony.

 

Chiropterophily, or bat pollination, is typically considered a highly specialized pollination system that has evolved independently numerous times across the angiosperm phylogeny, with distinct lineages often converging on a similar suite of floral traits. The African baobab,Adansonia digitata, occurs widespread across continental Africa and introduced throughout much of the tropics, possesses floral traits classically associated with bat pollination, namely nocturnal anthesis, pendulous white flowers, and a “musky” fragrance. Despite this, our observations and pollination exclusion experiments in South African baobab populations suggested little if any role for bats, but instead showed that hawkmoths are the main pollinators. Hand pollination indicated strong self‐incompatibility and crossing experiments suggest minimal diurnal receptivity. Furthermore, our analyses of floral volatiles revealed not only sulfur‐containing compounds, commonly associated with bat pollination, but also a high concentration of the sesquiterpene β‐caryophyllene, a compound generally more typical of hawkmoth pollination. Comparing previous pollination studies and published floral scent profiles from West Africa suggests that the classic bat pollination system in baobabs may be more labile than previously thought. This study provides an empirical example of a species that most likely evolved due to bat pollination yet has some degree of generality and possible geographic variation in floral traits and pollinator visitation patterns across its range.

 

The ability to tolerate neighboring plants (i.e. degree of competitive response) is a key determinant of plant success in high‐competition environments. Plant genotypes adjust their functional trait expression under high levels of competition, which may help explain intra‐specific variation in competitive response. However, the relationships between traits and competitive response are not well understood, especially in trees. In this study, we investigated among‐genotype associations between tree trait plasticity and competitive response.

We manipulated competition intensity in experimental stands of trembling aspen (Populus tremuloides) to address the covariance between competition‐induced changes in functional trait expression and aspects of competitive ability at the genotype level.

Genotypic variation in the direction and magnitude of functional trait responses, especially those of crown foliar mass, phytochemistry, and leaf physiology, was associated with genotypic variation in competitive response. Traits exhibited distinct plastic responses to competition, with varying degrees of genotypic variation and covariance with other trait responses.

The combination of genotypic diversity and covariance among functional traits led to tree responses to competition that were coordinated among traits yet variable among genotypes. Such relationships between tree traits and competitive success have the potential to shape stand‐level trait distributions over space and time.

 

Plants employ a diverse set of defense mechanisms to mediate interactions with insects and fungi. These relationships can leave lasting impacts on host plant genome structure such as rapid expansion of gene families through tandem duplication. These genomic signatures provide important clues about the complexities of plant/biotic stress interactions and evolution. We used a pseudo‐backcross hybrid family to identify quantitative trait loci (QTL) controlling associations betweenPopulustrees and several commonPopulusdiseases and insects. Using whole‐genome sequences from each parent, we identified candidate genes that may mediate these interactions. Candidates were partially validated using mass spectrometry to identify corresponding QTL for defensive compounds. We detected significant QTL for two interacting fungal pathogens and three insects. The QTL intervals contained candidate genes potentially involved in physical and chemical mechanisms of host–plant resistance and susceptibility. In particular, we identified adjoining QTLs for a phenolic glycoside andPhyllocolpasawfly abundance. There was also significant enrichment of recent tandem duplications in the genomic intervals of the native parent, but not the exotic parent. Tandem gene duplication may be an important mechanism for rapid response to biotic stressors, enabling trees with long juvenile periods to reach maturity despite many coevolving biotic stressors.

 

Phylogenetic analysis is complicated by interspecific gene flow and the presence of shared ancestral polymorphisms, particularly those maintained by balancing selection. In this study, we aimed to examine the prevalence of these factors during the diversification ofPopulus, a model tree genus in the Northern Hemisphere.

We constructed phylogenetic trees of 29Populustaxa using 80 individuals based on re‐sequenced genomes. Our species tree analyses recovered four main clades in the genus based on consensus nuclear phylogenies, but in conflict with the plastome phylogeny. A few interspecific relationships remained unresolved within the multiple‐species clade because of inconsistent gene trees. Our results indicated that gene flow has been widespread within each clade and also occurred among the four clades during their early divergence.

We identified 45 candidate genes with ancient polymorphisms maintained by balancing selection. These genes were mainly associated with mating compatibility, growth and stress resistance.

Both gene flow and selection‐mediated ancient polymorphisms are prevalent in the genusPopulus. These are potentially important contributors to adaptive variation. Our results provide a framework for the diversification of model tree genus that will facilitate future comparative studies.